Late Tremadocian (Early Ordovician) reefs on the Yangtze Platform, South China, and their geobiological implications: a synthesis

This study provides an overview and discussion of controls on the distribution of organic reefs during the Early Ordovican Period, in the Yangtze Platform, a region of epicontinental sedimentary rocks in South China. The Yangtze Platform was located in low latitudes during the Early Ordovician and recorded rich and diverse reefs through that time. During the late Tremadocian Epoch, dolomitic and stratiform stromatolites were common in supratidal to intertidal zones of the western Yangtze Platform, while columnar stromatolites formed in deeper waters of the eastern Yangtze Platform. Skeletal-dominated reefs occurred in upper subtidal settings of the central Yangtze Platform. A transition from microbial-dominated to metazoan-dominated reefs with shallowing-upward cycles was evident, indicating that the composition of the main reef-builders was driven mainly by water depth. Increasing metazoan competition during the Great Ordovician Biodiversification Event reduced the abundance of microbial reefs. Sufficient nutrient supply is interpreted to have promoted development of skeletal-dominated reefs locally in shallow settings in the central Yangtze Platform, especially represented by the expansion of abundant solitary fossils of lithistid sponges and Calathium. High salinity environmental settings facilitated the bloom of stromatolites in near-shore locations. Low oxygen content in deep subtidal settings may have led to the absence of skeletal reefs in these habitats, so the mass occurrences of stromatolites was located in the shallower-water central and eastern platform. No keratose sponge-bearing stromatolite can be confirmed across the platform during this interval.

In the last decade, much progress has been achieved in understanding the nature and environments of Early Ordovician reefs on the Yangtze Platform of South China Block (e.g., Adachi et al. 2012a;Li et al. 2015Li et al. , 2017. Early Tremadocian reefs on the Yangtze Platform are characterized by microbialites with low abundance of lithistid sponges and Calathium Zhang et al. 2016). The oldest bryozoan reefs occurred in the late Tremadocian; while microbialites and bryozoan reefs dramatically declined with the expansion of hypercalcified sponges (e.g., Calathium, Pulchrilamina) on the platform during the Floian (Zhu et al. 2006;Adachi et al. 2011Adachi et al. , 2012aAdachi et al. , 2013Xiao et al. 2011;Zhang et al. 2016;Li et al. 2017). Thus, the late Tremadocian reefs on the Yangtze Platform showcase one of the most diverse shallow marine ecosystems in the world at that time (Li et al. 2004;Zhu et al. 2006;Xiao et al. 2011;Adachi et al. 2011Adachi et al. , 2013Wang et al. 2012;Li et al. 2015).
It has been proposed that variation of water depth, bioturbation (Liu 2009;Liu and Zhan 2009), temperature (Trotter et al. 2008), oxygen level (Edwards et al. 2017) and nutrient conditions (Martin 1995(Martin , 1996 may have had strong influence on reef developments during the Early Ordovician. In this paper, we re-examine the late Tremadocian reefs on the Yangtze Platform. Based on published data and our own collections, we discuss how environmental factors affected the spatial differentiations, which provide insight into the paleoecology of Early Ordovician reefs and their geobiological implications. We therefore aim to provide an overview of the depositional settings and environmental controls on the development of Early Ordovician reefs on the Yangtze Platform.

Geological setting
South China Block was interpreted to be dominated by a low-gradient basinward epeiric platform (Yangtze Platform) (Torsvik and Cocks 2013), deepening from shallow areas in the west towards the southeastern Jiangnan Slope and Zhujiang Basin during the Early Ordovician (Li et al. 2004) (Fig. 1). Except for localized input of terrigenous sediments in the western and northwestern near-shore belts, most of the Yangtze Platform is carbonate-dominated (Chen et al. 1995;Zhan and Jin 2007). Gradual transgression from the beginning of the Ordovician triggered a lithological changeover from the dolostone-dominated Furongian (Series 4 of the Cambrian) to the limestone-dominated Tremadocian Series (Zhang et al. 2016). The reef-bearing units of the late Tremadocian Tungtzu (or Tongzi), Fenhsiang (or Fenxiang) and Lunshan formations are arranged approximately from west to east, shown in Fig. 2. Fig. 1 Localities of the late Tremadocian reef sections of South China (modified from Zhan and Jin 2007). Note that three sections from western Yangtze Platform: Wudang (section 1), Kuaizishan (section 2) and Honghuayuan (section 3) sections in Guizhou Province; three sections from central Yangtze Platform: Taiping (section 4), Huanghuachang (section 5) and Liujiachang (section 6) sections in the Three Gorges Area; and two sections from eastern Yangtze Platform: Shitai (section 7) and Beigong (section 8) sections in Anhui Province Tungtzu Formation is confined to a very shallow belt covering the main part of the western Yangtze Platform; coeval shales of the Luohanpo and Tangchi formations occur along the westernmost near-shore belts (Zhan and Jin 2007). Contemporary reef-bearing units to the east are the Nantsinkuan and Fenhsiang formations in ascending order, which comprise offshore facies in the central platform region, and the Lunshan Formation in eastern Yangtze Platform, representing another offshore area (Li et al. 2004). The overlying Hunghuayuan Formation (latest Tremadocian to early Floian) with fossil-rich bioclastic limestones developed almost synchronously across the most part of Yangtze Platform, although its base is stratigraphically slightly older in the western platform than elsewhere (Zhen et al. 2009).
Lithological sequences of the Tungtzu Formation are characterized by medium-to thick-bedded dolomites and bioclastic limestones intercalated with pebble, oolitic and oncolitic dolomites, and shale interbeds are common in the top and lower part (Zhan and Jin 2007). Wang et al. (1996) reported Tremadocian conodont biozonations of Acanthodus costatus, Glyptoconus quadraplicatus, and Scolopodus barbatus in ascending order. Fenhsiang Formation is composed of medium-bedded bioclastic and oolitic packstones in the lower part; and thin-to thick-bedded bioclastic limestones rich in crinoidal and brachiopodal fragments with less shales in the upper part. Wang et al. (1987) dated the sequence as belonging to the Tripodus proteus (=Paltodus deltifer) conodont biozone, and the top reaches the Paroistodus proteus conodont biozone. Lithologies in the Lunshan Formation change from dolomite-dominated facies in the lower part to thick-bedded micritic limestonedominated strata with stromatolites (tens of meters thick) in the upper part. The Drepanodus deltifer-Scandodus proteus conodont biozone in the upper part of the Lunshan Formation (BGMRAP 1987) is equivalent to the Tripodus proteus biozone of the Fenhsiang Formation (Fig. 2).

Spatial distribution and succession of the late Tremadocian reefs
Late Tremadocian reefs are abundant in the central platform, but they are relatively rare in the western and eastern part of the Yangtze Platform. Eight reef-bearing sections are used to illustrate facies differentiation: 1) western platform: Wudang, Kuaizishan and Honghuayuan sections in Guizhou Province; 2) central platform: Taiping, Huanghuachang and Liujiachang sections in the Three Gorges Area; and, 3) eastern platform: Shitai and Beigong sections in Anhui Province (see Fig. 1). Lithology and reef horizons of these sections are shown in Figs. 3 and 4.

Western platform
Late Tremadocian stromatolites occur mostly near the top of the Tungtzu Formation in the western platform. The stromatolites in the Wudang section are 40 cm thick and flat column shaped, but strongly dolomitized (Figs. 3,5a). Stromatolite laminae are recognizable in outcrop due to surface weathering (Fig. 5a, b), but are not visible in thin sections. The reef is covered by wellbedded dolostones. In contrast to the reefs of the Wudang section, the laminar stromatolites in two layers of 1.5 m and 2 m in thickness at the Honghuayuan section ( Fig. 5c, d) are both dolomitized (Zhang et al. 2016) and are covered by oolitic limestones (Fig. 5c, d). At the Kuaizishan section, small low dome-shaped stromatolites ( Fig. 5e) are surrounded by flat-pebble beds and thinbedded grainstones (Fig. 5f), indicating a wave/stormdominated carbonate tidal setting (Myrow et al. 2004).

Central platform
As the first occurrence of the metazoan-bearing reefs in the Yangtze Platform, Calathium-lithistid spongemicrobial and bryozoan reefs were reported respectively in the early Tremadocian Nantsinkuan Formation in Wentang, Hunan Province Zhang et al. 2016) and Liujiachang, Hunan Province (Cuffey et al. 2013). Small-scale reefs expanded in the late Tremadocian Fenhsiang Formation, with various metazoan builders throughout the central platform. Five types had been distinguished: lithistid sponge-microbial, lithistid sponge-bryozoan, bryozoan, lithistid sponge-Calathiummicrobial reefs and stromatolites (Zhu et al. 2006;Xiao et al. 2011;Wang et al. 2012;Adachi et al. 2013;Zhang et al. 2016). Although small in size (mostly 1-5 m in length and 0.3-2 m in height), such reefs are quite common in the central part of the Yangtze Platform, especially in the Three Gorges Area. The shapes of those reefs vary from lenticular to irregular dome-shaped.
Apart from the bryozoan reefs in the Liujiachang section, lithistid sponge-microbial reefs are widespread in the Three Gorges Area, as pioneer communities. The reefs in the Huanghuachang and Taiping sections grew on skeletal hard grounds (Fig. 6a, b), or unconsolidated sediments (Fig. 6e), and the reef cores are dominated by sponge bafflestones (Fig. 6c) with a few crinoids (holdfasts) (Fig. 6d). Encrustations of microbes were common with laminar texture in most cases ( Fig. 6 c, d, Fig. 7 a), and Girvanella appears uncommonly (Fig. 7b, c). Adachi et al. (2013) also reported small stromatolites in one of the lithistid sponge-microbial reefs in the Fenhsiang Formation at the Chenjiahe section, which is close to the Huanghuachang site.
The oldest bryozoan Prophyllodictya simplex was discovered from the Nantsinkuan Formation by Ma et al. (2015) at the Liujiachang section, but it is not a reefbuilder. In contrast, the colonial and encrusting Nekhorosheviella was the main framework builder of the oldest bryozoan reefs in the Fenhsiang Formation (Adachi et al. 2012a). In the Huanghuachang and Liujiachang sections, bryozoans show two different growth patterns in reefs: 1) lithistid sponges firstly settled on the skeletal substrate acting as framebuilders, then bryozoans encrusted the sponges with downward growth, forming a lithistid sponge-bryozoan reef (Fig. 8a, c, e); and, 2) stacked bryozoans directly grew on the skeletal hard ground to develop bryozoan reefs (Fig. 8b, d, f). Adachi et al. (2013) also reported that bryozoans used pelmatozoans as scaffolds to build a skeletal framework in the Fenhsiang Formation at Chenjiahe, similar to the growth pattern of the lithistid sponge-bryozoan reefs. Also, the hypercalcified sponge Pulchrilamina was found in the reefs in the Fenhsiang Formation, encrusting lithistid sponges and bryozoans (Zhu et al. 1993;Adachi et al. 2012b).
As a baffler, Calathium played a minor role in the community when it first occurred in the Calathiumlithistid sponge-microbial reef in Unit 3 of the Fenhsiang Formation in the Huanghuachang section (Fig. 4). On average, Calathium occupied less than 5% of the reefs. In terms of reef construction, however, the Calathiumlithistid sponge-microbial reef is not much different from the lithistid sponge-microbial reef, except for the occurrence of Calathium. Calathium became a main reef-builder in the lithistid sponge-Calathium-microbial reefs nearing the boundary between the Fenhsiang and Hunghuayuan formations. These reefs are surrounded by shale (Fig. 9a) and are characterized by occurrences of rich Calathium (making up 20%-30%) and a few lithistid sponges (about 5%) (Fig. 9b). Calathids and lithistid sponges encrusted upon each other (Fig. 7d) in some cases.
The stromatolites of the upper Fenhsiang Formation in the Liujiachang section are rare (Fig. 4), but they represent one of a few microbial reefs in the central platform (Adachi et al. 2013). The stromatolite-bearing beds of up to 5-m-thick are surrounded by 10-m-thick shales interbedded with thick-bedded bioclastic limestones (Fig. 9c, d). Cross-bedded limestones are distinct in the outcrop, suggesting a high energy environment.

Eastern platform
Stromatolites of the Lunshan Formation in the Shitai section, Anhui Province, were firstly reported by Li et al. (2004), and were subsequently re-measured and described by Jiang et al. (2014). The stromatolites are about 23 m thick, with columnar to conical shapes (Fig. 10). The reefs are sporadic in the outcrops, with relatively higher abundance in the lower and middle parts. Macrofossils are rare in the reef, including sparse nautiloids, trilobites and crinoids in the space between stromatolitic columns. However, organic burrows commonly disturbed the laminae of the stromatolites. The top of the stromatolites is capped by bioclastic limestones. In contrast, the stromatolites of the Lunshan Formation in the Beigong section, Jiangxi Province, are characterized by stratiform and dome-shaped laminations (Fig. 11a, c). Girvanella filaments are ubiquitous in thin sections (Fig. 11b, d). Crinoids grew on the surfaces of the microbialites (Yu et al. 2020).

Summary of reef pattern and water depth correlation
The spatial distribution of late Tremadocian reefs shows the occurrence of stromatolites throughout the Yangtze Platform, however skeletal reefs occur only in the central platform (Fig. 12). Centimeter-scale stromatolites also occur in those skeletal reefs, which may have developed in upper subtidal zones based on faunal and depositional characters in the Huanghuachang section (Chen and Qiu 1986). The skeletal reefs at Taiping and Liujiachang sections shared similar habitats of shallow subtidal environment. Stromatolites tend to be better developed in intertidal and deep subtidal settings. Evaporative and high salinity settings were recorded in the stromatolites in the western platform . In contrast, the high aspect ratio of the stromatolites and associated fine-grained clastics are consistent with deep subtidal habitats, which might be deeper than fair-weather wave base (Grotzinger 1989). There is no evidence of any keratose sponge-bearing (e.g. Li et al. 2017) stromatolite on the platform during this time. During late Tremadocian, the reef successions in the central platform were driven mainly by sea level fluctuation (Zhu et al. 2006;Xiao et al. 2011): lithistid spongemicrobial reefs were replaced by bryozoan reefs or lithistid sponge-Calathium-microbial reefs in shallowing upward cycles in the Unit 3 and Unit 5 of Huanghuachang section. Transition from lithistid sponge-bryozoan reefs to stromatolites in the Liujiachang section is attributed to increasing water depth, due to the reduction of metazoan builders and rise of microbialites. Overall, in terms of faunal composition, the waxing and waning of reef communities on the Yangtze Platform indicate that different reef types had different construction ability in relation to water depth (Fig. 13).

Discussion: geobiological implications for Early Ordovician reef systems
According to Webby (2002) and new data from Early Ordovician strata (e.g., Federov 2003;Adachi et al. 2009;Choh et al. 2013;Li et al. 2019), some sixty reefs are recorded globally. Almost 70% of them are microbial reefs and only four cases are colonial skeletal reefs (Toomey 1970;Toomey and Nitecki 1979;Adachi et al. 2009;Cuffey et al. 2013). The distribution and characters of the reefs in South China are consistent with those in some other areas of the world. In southeastern USA, supratidal stromatolites occurred in the lower Ordovician Jefferson City Dolomite in the Missouri River floodplain (Ethington 1977), while subtidal microbial-lithistid sponge-Calathium reefs were found in the Mckelligon Canyon Formation in West Texas and the Kindblade Formation of Oklahoma (Toomey and Nitecki 1979). In northern Canada and Greenland, thriving microbial reefs were characterized by their occurrence in restricted inner shelf to outer shelf positions, whereas a few lithistid sponges encrusted stromatolites occurred in the outer shelf (de Freitas and Mayr 1995). Microbiallithistid sponge-Calathium reefs mostly occurred in subtidal settings in Korea and in Utah of USA (Hintze 1973;Church 1974;Choh et al. 2013).
With mat colonization reducing through time by metazoan grazing and competition for space on the shallow seafloor (Riding 2006;Fischer 1965), increasing bioturbation during the Great Ordovician Biodiversification Event (Liu 2009;Liu and Zhan 2009) altered primary microbialite fabrics, leading to the survival of stromatolites mainly in low bioturbation settings. The observed ecological antagonism between stromatolites and benthic animals on the Yangtze Platform is consistent with this hypothesis. Cluster growth of the solitary skeletal reefbuilders, such as lithistid sponges and Calathium, would provide habitats for growth of reefal microbial carbonates to avoid predation (Forsythe 2003;Mallela 2007); they also provided hard substrates and shelters (e.g. cavities) which further promoted the diversification of reef communities on the Yangtze Platform (Li et al. 2017).
Biomass of animals is interpreted to have increased during the Ordovician (Payne and Finnegan 2006), a view supported by the sustained growth of skeletal components in Tremadocian reefs as we show above. The available habitat area expanded in the epeiric sea of the Yangtze Platform as sea level rose (Chen et al. 1995;Zhu et al. 2006;Xiao et al. 2011). Lithistid sponges and Calathium likely preferred eutrophic or rich nutrient environments (Church 2009(Church , 2017, contrasting with modern nutrient-independent scleractinian corals (Wood 1993). In addition, bryozoan-rich deposits may have been promoted by high trophic levels in the Ordovician (Taylor and Sendino 2010). Although the Cambrian-Ordovician seas have been demonstrated in extremely low nutrient conditions (e.g. Martin 1995Martin , 1996Servais et al. 2010), metazoan reef-builders gradually returned in nutrient-rich habitats interpreted with the sea level rise on the platform during late Tremadocian.
The scarcity of metazoan reefs in the western Yangtze Platform may be related to evaporative and high salinity conditions  in the nearshore areas, in an arid climate (Boucot et al. 2009) influenced by high temperatures (Fischer 1984;Trotter et al. 2008). Similar cases were reported in the Jefferson City Dolomite with abundant stromatolites (Ethington 1977). In addition,  various microbial reefs were recorded in the Early Ordovician evaporites from North and South Laurentia, and Siberia (Witzke 1990;Boucot et al. 2009).
In the Liujiachang and Shitai sections, stromatolites in deep subtidal settings might have suffered from hypoxia. With the sea-level rise, decreasing oxygen content was indicated by the Ce anomalies of conodont apatite from the Huanghuachang section, and the Unit 4 of the Fenhsiang Formation even showed anoxic conditions (Chen et al. 2012). Thick yellow-green shales in the Liujiachang section and scarce metazoan fossils in the Shitai section both indicate a similar redox condition to the Unit 4 of  the Fenhsiang Formation at Huanghuachang section. A case study from the Survey Peak Formation in Alberta (Pratt 1995) also revealed lithistid sponges, which might have survived below fair-weather wave base, representing the deepest position of lithistid-bearing reef distribution in the water column. These are evidence of limited oxygen in some deep subtidal settings, leading to scarcity of skeletal reefs there.
As described above, a similar pattern of reef systems on the central Yangtze Platform was reported in the McKelligon Canyon Formation of west Texas (Toomey 1970) and in the Fillmore Formation of Utah (Church 1974). At the dawn of the Ordovician Radiation, these metazoan-bearing reefs thus represent the initial rebound of metazoan-dominated reefs after the Cambrian archaeocyath reef crisis (Li et al. 2015). With a high tolerance to hypoxia (Lee and Riding 2018), lithistid sponges are interpreted to have wider distribution than other skeletal reef-builders and act as pioneers in most skeletal reefs on the Yangtze Platform. The availability of silica might promote the expansion of orchoclad lithistids in shallow environments (Carrera and Botting 2008), however, there is no direct evidence in the material studied here that confirms this hypothesis.
With a subtle difference of environmental preference from anthaspidellids, solitary Calathium and encrustingdomical bryozoans as well as Pulchrilamina replaced lithistid sponges as the main reef-builders when the amelioration in habitat occurred in the upper part of the shallowing upward cycles, which was showed by the examples from the Yangtze Platform of China, Texas and Utah of USA. In the Kindblade Formation in Oklahoma of USA, the hypercalcified sponge Pulchrilamina was a main reef-builder in upper subtidal settings (Toomey and Nitecki 1979), indicating they had competitive superiority for space in these settings, compared with solitary (or low integration) metazoan (e.g. lithistid sponges and Calathium) (Wood 1999).
It is noteworthy that shallow subtidal settings in eastern USA yielded the oldest coral Lichenaria in the widely distributed microbial reefs in ramp settings in Virginia (Bova and Read 1987). As a reef builder, the oldest occurrence of coralomorph Amsassia has reported in the Tremadocian strata from Precordillera of western Argentina (Carrera et al. 2017). Although Amsassia has been described in the Middle-Upper Ordovician from South China and Korea (Lee et al. 2016), there is no reliable record of any reef-building corals on the Yangtze Platform during the Early Ordovician. It is also worth noting that the latest morphological comparisons indicate that Lichenaria actually belong to Amsassia, and Amsassia may represent a calcareous alga, instead of a tabulate (Elias et al. 2020). More work needs to be done to confirm this new insight of origin and evolutionary history of reef-building corals.

Conclusions
1) The late Tremadocian stromatolites on the Yangtze Platform tend to occur in evaporative facies and deep subtidal settings, while metazoan-dominated reefs are found in the shallow subtidal settings of the central platform. There is no evidence of any keratose spongebearing stromatolite on the platform during this time. 2) Reef communities were observed in the Huanghuachang section of the central platform: a trend from microbial-dominated to metazoan-dominated with shallowing upward cycles was evident, indicating that the composition of the most reef-builders was mainly driven by water depth.
3) Increasing metazoan competition during the Great Ordovician Biodiversification Event hindered the development of microbial reefs. Sufficient nutrient supply promoted local flourishing of skeletal-dominated reefs in shallow-water settings in the central platform, indicated by the expansion of solitary lithistid sponges and Calathium.