Gondwana Research 28 (2015) 432–450

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Mass-occurrence of oncoids at the Cambrian Series 2–Series 3 transition: Implications for microbial resurgence following an Early Cambrian extinction

Wenhao Zhang a,b, Xiaoying Shi a,b,⁎, Ganqing Jiang c, Dongjie Tang a,b, Xinqiang Wang a,b a State Key Laboratory of Biogeology and Environmental Geology, Beijing 100083, China b School of Geoscience and Resources, China University of Geosciences, Beijing 100083, China c Department of Geoscience, University of Nevada, Las Vegas, NV 89154-4010, USA article info abstract

Article history: The traditional Lower–Middle Cambrian transition (Cambrian Series 2–Series 3 transition) is marked by the Received 22 October 2013 first major biotic extinction of the Phanerozoic Eon. This biotic crisis has been arguably linked to changes in ocean Received in revised form 21 March 2014 chemistry and/or marine environments but their casual relationships remain controversial. To better understand Accepted 22 March 2014 the microbial responses to paleoceanographic changes across this critical transition, we have studied the environ- Available online 18 April 2014 mental conditions for mass–occurrence of oncoids in the western North China Platform. Oncoids at the Lower–Mid- – Handling Editor: G.C. Zhao dle Cambrian transition form 1 to 3-m-thick massive beds, show spherical subspherical morphology, and contain 8–14 light–dark cortical laminar couplets. The light laminae are thicker and contain densely intertwined filamentous Keywords: cyanobacteria that have calcified sheaths and a prostrate growth pattern. The dark laminae are thinner and rich in Oncoids organic matter relics, pyrite framboids, and heterotrophic bacteria. In most oncoids, cortical laminae show the same Organomineralization growth orientation for more than five light–dark laminar couplets, suggesting much less frequent grain overturning Extinction than generally thought. Both light and dark laminae contain well-preserved organomineralization fabrics/textures Anoxic event including extracellular polymeric substances (EPSs), nanoglobules, polyhedrons, and micropeloids, suggesting Early Cambrian oncoid formation in shallow-marine environments with high alkalinity and active sulfate reduction. The presence of pyrite framboids and heterotrophic bacterial relics implies anoxic/dysoxic bottom-water conditions. Stratigraphic correlation indicates that time-equivalent oncolites and other microbialites are widespread not only in North China, but also in other Early Cambrian successions globally. The mass-occurrence of oncoids coincides with the Kalkarindji large igneous province of Australia, a prominent negative δ13C excursion (ROECE or Redlichiid–Olenellid Extinction Carbon isotope Excursion), a significant increase in 87Sr/86Sr, and a large positive shift in δ34S. The coincidence of these events suggests that the Early Cambrian biotic crisis may have been caused by an ocean anoxic event resulting

from enhanced volcanic release of CO2, global warming, and increased continental weathering. Preservation of mas- sive oncolites is likely related to decreased metazoan grazing following an Early Cambrian biotic crisis, during which archaeocyathids and many Early Cambrian trilobite taxa went to extinction. The oncoid mass-occurrence provides evidence for the resurgence of microbial life in anoxic/dysoxic marine shelf environments concomitant with the Early Cambrian extinction event. © 2014 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

1. Introduction depth, temperature, carbonate saturation and redox state (e.g., Woods and Baud, 2008; Kershaw et al., 2012; Mata and Bottjer, 2012; Tang The abundance and distribution of microbialites in geological record et al., 2013a, 2013b). Particularly during the Phanerozoic, when the provide information on the responses of microbial community to envi- preservation of microbialites has greatly reduced due to metazoan graz- ronmental and ecological changes (Riding and Liang, 2005; Wood, ing and ecological competition (Grotzinger and Knoll, 1999; Riding 2004; Dupraz et al., 2009; Harwood and Sumner, 2011). Numerous and Liang, 2005), the mass-occurrence of microbialites is commonly studies have demonstrated that the composition, microfabrics and interpreted as recording rapid colonization and ecological expansion organomineralization features of microbialites can be used to analyze of microbes in highly stressed environments where benthic metazoans the environmental conditions of microbial ecosystems, such as water were largely depressed (Schubert and Bottjer, 1992; Wood, 2000; Whalen et al., 2002; Wang et al., 2005; Kershaw et al., 2007, 2012; Lee et al., 2012). ⁎ Corresponding author at: School of Geoscience and Resources, China University of Geosciences, Beijing 100083, China. Oncoids are coated grains larger than 2 mm in diameter that exhibit E-mail address: [email protected] (X. Shi). irregularly concentric laminae (i.e., coatings or cortex) surrounding a

http://dx.doi.org/10.1016/j.gr.2014.03.015 1342-937X/© 2014 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved. W. Zhang et al. / Gondwana Research 28 (2015) 432–450 433 nucleus of detrital origin (Tucker and Wright, 1990; Flügel, 2010). They In this paper we report a comprehensive micro-texture study of were once called as “spheroidal stromatolites” or “algal balls” (Riding the spectacular oncoids from the marine carbonate succession at the and Voronova, 1982). In general, the formation of oncoids involves micro- Cambrian Series 2–Series 3 transition of the western North China bial encrusting (e.g., Peryt, 1981; Jones and Renaut, 1997; Hägele et al., Platform. We mainly focus on the microfabrics and organominerals 2006). Thus, oncolites are generally regarded as a type of microbialites recognized in oncoid cortices at micro- to nano-meter scales using (Tucker and Wright, 1990; Riding, 2000; Shapiro et al., 2009). Oncoids petrographic microscope, FESEM, EDS and XRF analyses. Micro-texture have been recorded in shallow-marine strata from the Paleoproterozoic variations are used to interpret the organomineralization processes to Cenozoic (e.g., Li et al., 2000; Schaefer et al., 2001; Shi and Chen, and microbe–environmental interactions during oncoid formation. 2006; Reolid and Nieto, 2010; Lazăretal.,2013). They are also known Through a global correlation, we also discuss the casual link between in a variety of modern depositional environments, such as peritidal the mass occurrence of oncoids and a possible anoxic event following beach (e.g., Peryt, 1981; Alshuaibi et al., 2012), fresh-water lakes and riv- the biotic extinction event at the Cambrian Series 2–Series 3 transition, ers (e.g., Davaud and Girardclos, 2001; Hägele et al., 2006), salt lakes with emphasis on the responses of microbial community to changes in (Jones and Renaut, 1994), soil pockets (Jones, 2011), hot springs (e.g., ocean chemistry. Renaut et al., 1996; Jones et al., 1999a, 1999b), and deep-marine environ- ments below photic zone (Wang et al., 2012b), where environmental 2. Geological background conditions are commonly less favorable for benthic metazoans (e.g., Renaut et al., 1996; Hägele et al., 2006). During the Cambrian, the North China Platform was a flat-topped car- It is commonly thought that turbulent hydraulics and frequent grain bonate platform (Fig. 1A) developed after a long period of weathering overturning are required for developing the spherical morphology and since its uplift at ca. 850 Ma (e.g., Meng et al., 1997; Xiang et al., 1999; syn-axial laminations in the cortex of oncoids (e.g., Tucker and Wang et al., 2000; Cheng et al., 2009). In paleogeographical reconstruc- Wright, 1990; Shi and Chen, 2006; Flügel, 2010; Zatoń et al., 2012). tion, the North China Platform belongs to the Sino-Korean plate (Wang Therefore, in facies analyses the presence of oncoids in marine carbon- and Mo, 1995; Wang et al., 2000) that was located in the northern ate strata has often been taken as an indicator for shallow and agitated Gondwana continent, close to Australia (Wotte et al., 2007; Fig. 1B). depositional environments (e.g., Lanés and Palma, 1998; Shi and Chen, Following the breaking-up of the supercontinent Rodinia since the 2006; Flügel, 2010). Many studies, however, indicated that oncoids late Neoproterozoic, the North China Platform started to subside and can form by in situ microbial accretion, not necessarily requiring turbu- receive sediments during the late Early Cambrian (Shi et al., 1997, lent hydraulic condition and grain overturning (e.g., Dahanayake et al., 1999; Xiang et al., 1999; Wang et al., 2000). In most areas of the 1985; Leinfelder and Hartkopf-Fröder, 1990; Hägele et al., 2006; platform, the Cambrian Series 1 (i.e., the Terreneuvian) and parts of Shapiro et al., 2009; Jones, 2011; Zatoń et al., 2012). For example, the Cambrian Series 2 strata are absent. Lithostratigraphic units for some polymetallic (Fe, Mn, Co, and Ni) nodules on modern ocean sea- rest of the Cambrian are dominated by shallow-water carbonate rocks floor are considered as a kind of oncoids resulted from biogeochemical and are widespread across the platform (e.g., Xiang et al., 1981, 1999; processes in deep, quiet environments below the photic zone (e.g., Wang et al., 2000; Peng, 2009). For a given time interval, the major Chen et al., 1997; Préat et al., 2011; Wang et al., 2012b). In Mesozoic ma- components of benthic fauna and sequence stratigraphic framework rine environments of the western Tethys Ocean, ferromanganese are highly comparable across the platform (Zhang et al., 1980; Wang macro-oncoids are known to have formed along hardground surfaces et al., 2000; Cheng et al., 2009). and condensed intervals. Some of them were formed far below fair- The Wuhai area of the Inner Mongolia (Fig. 1A) is located in the weather wave base without frequent bottom-water agitation (e.g., western margin of the North China Platform. In this area, the Lower Gradziński et al., 2004; Védrine et al., 2007; Reolid and Nieto, 2010; Cambrian to Middle Ordovician strata are dominated by shallow- Préat et al., 2011; Zatoń et al., 2012; Lazăr et al., 2013). The occurrence marine carbonates that show an overall shallowing-upward trend of oncoids in a wide spectrum of environments, their morphological (e.g., Shi et al., 1999; Xiang et al., 1999; Wang et al., 2000). A major facies variability, and diverse mineral compositions likely imply that microbes change happened during the latest Middle Ordovician when extension and chemical conditions in waters may have played more important and subsidence occurred along the platform margin (Wang et al., roles in oncoid formation than previously thought (e.g., Hägele et al., 2000; Cheng et al., 2009). Late Ordovician strata in this area are charac- 2006; Préat et al., 2011). terized by deep-water dark graptolite shale and thick terrigenous slope An intriguing phenomenon in the geological record that has not deposits containing abundant slump blocks and turbidites (Wang et al., been adequately studied is the global occurrence of massive oncolites 2000; Cheng et al., 2009). and other microbialites at the traditional Lower–Middle Cambrian tran- In Wuhai area, the Cambrian strata start with the Maozhuang For- sition (or Cambrian Series 2–Series 3 transition in the new Geological mation that unconformably overlies the Mesoproterozoic dolostone Time Table) (e.g., Youngs, 1978; Shi et al., 1997, 1999; Álvaro et al., with locally abundant chert bands and columnar stromatolites (Wang 2000; Elicki et al., 2002; Sundberg, 2005; Powell et al., 2006; Yang et al., 2000; Cheng et al., 2009). In this formation, two depositional et al., 2011, 2013; Perejón et al., 2012). Paleontological evidence has sequences can be recognized (Fig. 1C). The first sequence starts with shown that a major biotic extinction occurred at this time interval, limestone and silty shale and ends with fine- to medium-grained, during which many trilobite taxa and archaeocyathids disappeared cross-bedded quartz sandstone. The second sequence consists of green- (e.g., Zhuravlev and Wood, 1996; Palmer, 1998; Erwin, 2001; Yuan ish shale–wackestone in the lower part and wackestone–packstone in et al., 2002; Hallam, 2005; Peng et al., 2012). Associated with this the upper part. Thick oncolite beds (about 8 m thick) occur in its upper- extinction are prominent changes in seawater carbon, sulfur isotope most part. The top of the second sequence is marked by a type-I se- compositions and 87Sr/86Sr ratios (e.g., Montañez et al., 2000; Hough quence boundary characterized by exposure features and minor karst et al., 2006; Zhu et al., 2006). Although there are persistent debates on breccias (Fig. 1C). The Maozhaung Formation is overlain by the the bio- and chemostratigraphic correlations and on the precise position Xuzhuang Formation, which is dominated by bioturbated, micritic lime- of the Cambrian Series 2–Series 3 boundary (e.g., Gaines et al., 2011; stone and yellowish green shale, with some grainstone and flat-pebble Geyer and Peel, 2011; Peng et al., 2012; Álvaro et al., 2013; Gozalo conglomerate interbeds. In the Xuzhuang Formation, two depositional et al., 2013; Landing et al., 2013), the temporal proximity of biological sequences are also recognizable (Fig. 1C), and oncolite beds are restrict- and geochemical events suggests a major paleoceanographic change. ed to the lowermost part, less than 3 m thick. Oncoids from this part A detailed study of the massive oncolites may provide valuable informa- are commonly smaller (mean diameter of 13 mm) in size than those tion on the microbial responses to ecosystem changes and help to eluci- (average diameter of 15 mm) from the underlying Maozhuang Forma- date the cause of the Early Cambrian biotic extinction. tion (Fig. 1C). 434 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Earlier studies demonstrated that trilobite fossils are reasonably di- correlation with those from other areas of the platform, four versified in the upper Lower to Middle Cambrian strata of the Wuhai assemblage zones (i.e., in ascending order, Ruichengella, Sunaspis, area. About 22 species of 16 genera have been documented from the Poriagraulos,andBailiella) of the Xuzhuang Formation and one Xuzhuang Formation (Zhang et al., 1980; Geological Bureau of Inner zone (Shantungaspis) of the upper Maozhuang Formation were Mongolia Autonomous Region, 1991); among them the genera Bailiella, established for the area (Zhang et al., 1980; Geological Bureau of Poriagraulos, Inouyops, Metagraulos, Sunaspis, Pagetia, Solenoparia, Inner Mongolia Autonomous Region, 1991), which are correlatable Ruichengaspis, Luaspides and Ruichengella are broadly known across with those established in other areas of the North China Platform the North China Platform (Zhang et al., 1980). In contrast, fossils from (Xiang et al., 1981, 1999; Wang et al., 2000; Peng, 2009). With the the Maozhuang Formation are much less common, including only a constraints from these trilobite fossils (Fig. 1C), the four depositional few species of Shantungaspis, Probowmania,andPerriomma (Zhang sequences recognized in the study area can be correlated across the et al., 1980; Geological Bureau of Inner Mongolia Autonomous Region, entire North China Platform (Meng et al., 1997; Shi et al., 1997, 1991). Based on a comprehensive study of the trilobites and their 1999; Wang et al., 2000).

Fig. 1. Geological background and stratigraphy of the study area. (A) Early Cambrian paleogeography of the North China Platform (modified after Feng, 1990). 1 — Tongxin, southern Ningxia Autonomous Region; 2 — Longxian, Shaanxi Province. (B) Early–Middle Cambrian reconstruction of the North China Platform in eastern Gondwana (modified after Wotte et al., 2007). Red triangle marks the location of the study area and red star marks the Kalkarindji igneous province (Australia). (C) Early to Middle Cambrian stratigraphy in the study area (trilobite fossils are adapted from Zhang et al., 1980). Sb refers to sequence boundary. W. Zhang et al. / Gondwana Research 28 (2015) 432–450 435

The division of the Cambrian strata of the North China Platform and 3. Materials and study methods their correlation with those of South China and globally are provided in Fig. 2. In the North China Platform, two benthic trilobite zones, Samples studied in this paper were primarily collected from the Yaojiayuella in the lower part and Shantungaspis in the upper part, are carbonates of the upper Maozhaung Formation and lower Xuzhuang commonly used as index fossils (Xiang et al., 1999; Wang et al., 2000; Formation of the Wuhai area, Inner Mongolia, North China (Fig. 1A, C). Peng, 2009) of the Maozhuang Formation (Fig. 2). The Xuzhuang For- Additional samples are from time-equivalent stratigraphic units of south- mation contains four trilobite zones (Fig. 2) including, in ascending ern Ningxia and central Shaanxi (Fig. 1A). Morphology and macro- order, Hsuchuangia, Sunaspis, Priagraulosa and Bailiella (e.g., Xiang structures of the oncoids were observed in outcrops and on polished et al., 1999; Wang et al., 2000; Peng, 2009). In the North China Platform, slabs. Micro-textures were mainly studied on thin sections using a Zeiss the traditional Early–Middle Cambrian boundary was placed at the base Axio Scope A1 microscope. Ultra-fabrics and organominerals in oncoid of the Shantungaspis/Yaojiayuella zone, roughly coincident with the cortices were studied using a Supra 55 Field Emission Scanning Electron boundary between the Maozhuang Formation and the Mantou Forma- Microscopy (FESEM). Elemental concentration and spatial variation of tion (Fig. 2). According to Peng (2009), the two benthic trilobite zones micron-sized spots were determined using an Oxford Energy Dispersive of the Maozhuang Formation can be approximately correlated to the X-ray Spectroscopy (EDS) connected to FESEM and an X-ray Fluores- pelagic trilobite zones of Ovatoryctocara granulata (the uppermost cence Spectroscopy (XRF). For better results, both thin sections and Duyunian Stage) and Oryctocephalus indicus (the lowermost Taijiangian freshly broken fragments were used; some of them were coated with Stage) in South China (Fig. 2; Peng, 2009). These two Chinese stages platinum prior to observation. (Duyunian and Taijiangian) are roughly equivalent to the undefined FESEM study was operated at 10 or 15 kV with a working distance of Cambrian Stage 4 and Stage 5 of the International Cambrian 3.0 mm to 9.4 mm. An in-Lens detector for secondary electron imaging Chronostratigraphy (Fig. 2; Peng et al., 2012). The Bailiella zone of the (nano-topography of samples) and an Angle selective Backscattered uppermost Xuzhuang Formation approximately correlates to the pelag- (AsB) detector for low-angle backscattered electrons were used. Some ic zones of Ptychagnostus atavus of the uppermost Taijiangian stage FESEM studies of nanofacies were also performed using a Hitachi (equivalent to Stage 5; Peng, 2009)andPtychagnostus punctuosus in 3400N and operating in 20 kV with a working distance of 15.1 mm. All the lowermost Wangcunian stage of South China (Fig. 2; coeval to the laboratory analyses are conducted at the State Key Laboratory of Drumian; Peng, 2009; Peng et al., 2012). The base of the Wangcunian Biogeology and Environmental Geology, China University of stage is possibly at ca. 504.5 Ma (Haq and Schutter, 2008; Walker and Geosciences, Beijing. Morphologic measurements and terms used in Geissman, 2009), although additional radiometric ages and high- the description of oncoids are illustrated in Fig. 3AandB. resolution biostratigraphy are still needed to define the stage bound- aries. Thus, the oncoid-bearing strata in the study area are most likely 4. Characteristics of the oncoids within an interval from the O. granulata zone to the lower Peronopsis taijiagnensis zone (Fig. 2; Peng, 2009), straddling the boundary pro- 4.1. Morphology and macro-structures posed for the Cambrian Series 2–Series 3, if the FAD of O. indicus will be formally ratified as the marker for the base of Cambrian Series 3 The oncolites from the Maozhuang and Xuzhuang formations form and Stage 5 (Peng et al., 2012; Landing et al., 2013). 3-m- to 6-m-thick wackestone–packstone beds. Most oncoids are

Fig. 2. Cambrian lithostratigraphic subdivisions (part) and trilobite zones of the North China Platform and their correlation with those of South China. Stages, Series and pelagic trilobite zones of South China are from Peng (2009). The lithostratigraphic subdivisions and benthic trilobite zones of the North China Platform are summarized from Xiang et al. (1999) and Wang et al. (2000). Stages of Siberia and Laurentia are from Peng et al. (2012). 436 W. Zhang et al. / Gondwana Research 28 (2015) 432–450 spherical to subspherical in shape (Fig. 3C, D), without noticeable defor- Morphologically, fossil microbes observed in oncoids can be grouped mation. Individual oncoids are commonly 10 mm to 24 mm in diameter into three morphotypes: (1) tangled filaments (Figs. 4C, 5A, B, 6A). Fil- (Fig. 3B), with an average of 15 mm and a maximum up to 30 mm. aments of ~20 μm wide and 0.5–2 mm long intertwine together and Oncoids consist of a clear nucleus and cortex (coatings) (Fig. 3C, D). form densely packed clusters in light laminae; (2) branching calcified The nuclei are subcircular, 4 mm to 9 mm (mean 6.5 mm) in diameter, microbes (Fig. 4B). Individual filaments up to 50 μm wide form radiating and composed of a mixture of micrite, bioclasts, organic remains, and clusters of 1–2 mm in size, lining along the lower portion of light lami- minor terrigenous grains (Fig. 3E, F). In some samples, bioclasts in nuclei nae; (3) tiny filamentous bacteria (Fig. 5C, E, F). Small filaments of canbeashighas15–25% in volume. The cortices of oncoids commonly 2–5 μm in diameter and ~15 μm long are unevenly distributed in the have 8–14 concentric bands composed of alternating dark and light dark laminae. The first morphotype is similar to Girvanella identified laminae (Fig. 3E–H). These cortical bands are uneven in thickness, from Late Neoproterozoic carbonates (Pratt, 2001)andfromsome devoid of terrigenous particles, and follow the outline of the nuclei modern microbialites (e.g., Défarge et al., 1994, 1996). The second (Fig. 3E–H). The cortex–nucleus thickness ratio varies between 0.7 morphotype resembles Renalcis or Epithyton, both of which have been and 1.5, with a mean value of approximately 1.0. interpreted as autotrophic bacteria colonies (Woo et al., 2008; Hicks and Rowland, 2009). The third morphotype is reminiscent of 4.2. Micro-textures and fossil microbes in oncoids heterotrophic bacteria (cf. Défarge et al., 1996). It is important to note that large and sheathed filamentous Microbial fossils are abundant in the oncoids (Fig. 4A–D), especially cyanobacteria (Girvanella-like) are common in light laminae, but rare in their cortices. Densely packed, calcified microbial clumps (Fig. 4A) or in the dark laminae. In fact, many light laminae are almost entirely sub-spheroidal clumps of micrite and organic remains (Fig. 4D) are ob- built of densely intertwined filamentous cyanobacteria (Figs. 5A, B, 6A, served in some oncoid nuclei. Microbial remnants in oncoid cortices B). These cyanobacteria appear as one of the four colonial patterns: mainly appear as filaments (Fig. 4B–D), with some coccoid forms or (1) connected clumps, where filamentous bacteria aggregate into their fragments (Fig. 4C, D). Microbial fossils (Fig. 4E) and bioclasts irregular clumps that connected laterally along the lamination, growing (Fig. 4F) are also found in the matrix between oncoids, but they are outwards; (2) isopachous sheet, where interweaved or aggregated fila- less abundant. The outermost lamina of individual oncoids is commonly ments grow into isopachous meshwork (e.g., Fig. 6A, B); (3) connected thicker than all the other laminae in the cortex (Fig. 4F), in which sparse cones, where bacterial colonies grow upwards and form minute cones filaments and micropeloids are identifiable. that are horizontally separated by microsparitic pillars (e.g., Fig. 6F) Alternation of dark and light laminae is obvious in oncoid cortex and overlain by filament meshwork; and (4) branching complex, (Fig. 3E–H), but the boundary between laminae is commonly transition- where microbial colonies grow upwards with branches and inter- al and sometimes, blurry (Fig. 5A, B). The dark laminae are 50–200 μm branch spaces are filled with microspars (e.g., Fig. 6G). These patterns thick (100 μm in average) and consist mainly of micrite and organic may not have been formed by different types of microbial groups; matter. Their contact with the underlying light laminae is commonly instead, they are more likely resulted from varying mineralization well-defined, but their contact to the overlying light laminae is often processes. transitional, with dark “flames” protruding into the overlying light lam- Tiny bacteria filaments have also been observed in cyanobacteria- inae (Fig. 5A). Dark laminae show strong orange-red autofluorescence enriched light laminae (e.g., Fig. 5C), but they are uncommon. In con- (Fig. 5D) under fluorescence microscope, suggesting the presence of trast, dark laminae contain a much higher proportion of tiny bacteria concentrated organic matter (Tang et al., 2013a, 2013b). Identifiable mi- relics (Fig. 5E, F), pyrite framboids (Fig. 5G–J) and residual organic mat- crobial fossils in the dark laminae are rare, except for some randomly ter (Fig. 5D). Occasionally, filamentous cyanobacteria are seen at the distributed, small filaments that are likely remains of heterotrophic bac- margins of dark laminae, extending from their underlying light laminae teria (Fig. 5E, F). Minute pyrite framboids are common in the dark lam- (Fig. 5B, L), but overall, they are not common in the dark laminae. inae (Fig. 5G–J) and they are seen to be associated with organic material relics (Fig. 5I) or entombed in amorphous silica (Fig. 5J). In cross section, 4.3. Ultra-fabrics in cortical laminae individual pyrite microcrystals in framboids show growth rings (Fig. 5H). Relics of extracellular polymeric substances (EPSs) are com- FESEM observations reveal amorphous, platy or sheet-like structures mon in the dark laminae. Under FESEM, they appear as honeycomb- that are interpreted as extracellular polymeric substances (EPSs) like textures (Fig. 5K), identical to those recognized in some modern and other organomineralization products including nanoglobules, microbialites (e.g., Défarge et al., 1994, 1996; Dupraz et al., 2004, polyhedrons, and micropeloids in oncoid cortices. These micron- to 2009; Spadafora et al., 2010). Voids in the dark laminae are variable in nanometer-scale organomineral features are closely associated with shape and often filled with residual organic matter (Fig. 5B, K). filamentous bacterial relics and framboidal pyrites, highlighting the role Light laminae in oncoid cortex are commonly thicker (200–1000 μm; of sulfate reduction in organomineralization during oncoid formation. ~500 μm in average) than dark laminae. They are composed primarily of microsparites (Fig. 5A, B). In comparison with the dark laminae, voids in 4.3.1. EPS light laminae are smaller in size but more abundant, and they are com- EPSs in cortical laminae of oncoids are commonly present as amorphous monly filled with microspars instead of organic remains (Figs. 4C, D, flats, irregular strips or mucus-like matrix (Fig. 7A–C). They are seen in 5A, B). The most important feature of the light laminae is the abundance walls surrounding micro-pores that form alveolar structures. Some EPS of calcified filamentous cyanobacteria (predominantly Girvanella-like; relics appear as twisted strips (Fig. 7D) that were possiblyformedbydehy- Figs. 4C, D, 5A, B) that show prostrate growth pattern (Fig. 5L). Many dration during early diagenesis. Bacterial filaments of 2–5-μm wide and 30- light laminae in the studied samples are virtually composed of calcified μm long are seen to be closely associated with or embedded in EPS relics bacterial filaments. Filaments are entangled together, either as thin (e.g., Fig. 7A, C, and E). Some filaments are covered with nanoglobules on meshwork roughly parallel to the lamination (Figs. 5L, 6A, B) or as vari- their surfaces (Figs. 7A, 8C) and show nanometer-scale internal fibers ably shaped colonies surrounded by obscured microsparite rims (Fig. 7F) that have been interpreted as resulting from partial dissolution of (Fig. 4B–D). Some coccoid forms are also recognizable in the vicinity of mineralized bacteria during early diagenesis (Défarge et al., 1996; filaments, partially entombed in EPS relics (Fig. 4C, D). FESEM observa- Sprachta et al., 2001; Planavsky and Ginsburg, 2009). tion reveals that many of the larger bacterial filaments are segmented (Fig. 6C, D) and have ultrathin walls (i.e., calcified sheaths). In cross sec- 4.3.2. Organominerals tion, the filaments display tube-like texture, with a solid center and an Nanoglobules of 40–200 nm in size are common in cortical laminae encasing rim composed of bladed calcite (Fig. 6E). of oncoids (Fig. 8A–D). They are closely associated with EPS relics and W. Zhang et al. / Gondwana Research 28 (2015) 432–450 437

Fig. 3. Morphologic features of oncoids from the Maozhuang and Xuzhuang formations. (A) Schematic diagram showing general textures of an oncoid and terminology used in the study. (B) Size distribution of measured oncoids. (C) Oncolite from the upper Maozhuang Formation. (D) Oncolite from the lowermost Xuzhuang Formation. (E) Spherical oncoid with clearly defined nucleus and cortex. Bacterial colonies (a) and biotic detritus (b) are visible in the nucleus. The cortex consists of alternating light and dark laminae, with interweaving filamentous bacteria (i) in light laminae. (F) Subspherical oncoid with a large nucleus containing multiple biotic detritus and an indention in the cortex (lower left). (G–H) Microtextures of oncoid cortex showing consistent growth orientation of light–dark laminar couplets. (C–D) Field photographs; (E–H) thin section microphotographs, plane-polarized light. All samples are from the Wuhai area, Inner Mongolia. 438 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Fig. 4. Micro-textures and microbial fossils in oncoids. (A) Entangled filamentous microbes (Girvanella-like) at the nucleus center. (B) Calcified filamentous bacteria (center) and vague clumps formed of bacterial aggregates (lower left) in a light lamina. (C) Meshwork of filamentous bacteria (Girvanella-like) in a light lamina, with coccoid forms visible on the left and patchy sparry calcite of possibly diagenetic origin. (D) A clumped cluster composed of microbes and microspars in light lamina, with microspar-filled voids in the center and filaments near the margins. (E) Putative Epiphyton (bacterial colony?) in the matrix between oncoids. Calcified filaments are visible on the upper left and microbial colony is recognizable on the upper right. (F) Calcified filaments (b) and their aggregates in the matrix; the outermost layer (i) of oncoid cortex contains dense filaments. All are thin section microphotographs, plane-polarized light. clustered on EPS surfaces (Fig. 8A, D), implying their likely origin nanoglobules (Fig. 8C). These nanoparticles represent the smallest from anaerobic degradation of EPS (Aloisi et al., 2006; Sánchez- components observable in oncoid cortices. Similar nanoparticles Román et al., 2008; Perri et al., 2012). Nanoglobules are seen to ag- were thought to be probably formed by mixed organic macro- gregate or fuse into variably shaped polyhedrons (Fig. 8C, D) that molecules and carbonate minerals (Young and Martel, 2010), re- in turn coalesce into larger aggregates or micropeloids (Fig. 8A, B). cording the initial stage of carbonate nucleation in modern calcified Occasionally, smaller nanoparticles are seen on the surfaces of microbial mats (Visscher and Stolz, 2005; Aloisi et al., 2006;

Fig. 5. Microfabrics of oncoid cortical laminae. (A)–(B) Alternation of light (LL) and dark (DL) laminae in oncoid cortex. Dark laminae are thin and porous, rich in organic matter and pyrites (Py). Light laminae are thick, containing abundant filamentous cyanobacteria (AuB). (C) Close view of the boxed area in (B), showing tiny filaments associated with organic remains. (D) Fluorescence microphotograph of a dark lamina sandwiched between light laminae. Strong orange-red autofluorescence (excited by ultra-violet light) suggests the presence of concentrated organic matter. (E) Tiny filaments (arrows) dispersed in the dark lamina (putative heterotrophic bacteria), associated with film-like EPS relics (light flats, upper left). (F) Close view of tiny filaments (arrows) in the dark lamina. (G) Pyrite framboids in the dark lamina, associated with organic matter. (H) Close view of a framboid in (G) (arrow). Individual pyrite microcrystals within the framboid display a dark core and growth rings. (I) Pyrite framboids associated with bacterial filaments (between arrows). (J) Pyrite framboids entombed in amorphous silica matrix. (K) Platy EPS relics in the dark lamina showing honeycomb-like features under FESEM, with unfilled voids. (L) Schematic diagram summarizing the main features observed in dark and light laminae. Prostrate cyanobacterial filaments in light lamina occasionally protrude into the overlying dark lamina. SRB refers to sulfate reducing bacteria. (I–K) FESEM images; others are thin section photomicrographs under plane-polarized light. Scale bar in (E), (F), and (H–J) is 1 μm, and in (G) is 10 μm. W. Zhang et al. / Gondwana Research 28 (2015) 432–450 439

Dupraz et al., 2009; Obst et al., 2009). The polyhedrons formed by 4.3.3. Micropeloids nanoglobules may have served as primary sites or nuclei for subse- Subspheroidal micropeloids in oncoid cortices are closely asso- quentcarbonatecrystalgrowth(Sánchez-Román et al., 2008; ciated with organic remains (Fig. 9A–D). They are larger in light Spadafora et al., 2010; Perri et al., 2011; Tang et al., 2013a). laminae (60–120 μm; a few up to 200 μm) than in the dark laminae 440 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Fig. 6. Microbial fossils in oncoid cortical laminae. (A) Intertwined cyanobacterial filaments showing prostrate growth pattern in light lamina. (B) Enlarged view of the boxed area in (A), showing suberect growth style of filaments at their initial stage (lower right). (C) SEM image showing segmented bacterial filament (circled in dot-line) with recognizable sheath (furrows on two sides), and many filament relics (arrows). Micro-particles are possibly fragments of mineralized filaments. (D) Close view of a segmented filament. Particles around the filament are similar to the filament segments in both color and size. (E) Transverse section of a filament showing that the core likely represents mineralized bacterial cells and the rim constructed by bladed microcrystals is possibly calcified bacterial sheath. (F) Clumps (arrows) aligned along the lower part of a light lamina. Clumps are separated by microsparitic pillars. Entangled bacterial filaments in clumps remain upward growth orientation. (G) Large microbial colony with branches (dark color), voids (or interstices) and crystalline microspars between the branches. (C–E) FESEM images; others are thin section photomicrographs under plane-polarized light.

(20–60 μm). In some samples, micropeloids constitute the main experiments, however, demonstrated that similar micropeloids texture of calcified filaments (Fig. 9A, C, D). They consist of a vague- could also be formed from inorganic chemical processes (Bosak ly defined granular core and an encasing rim composed of bladed et al., 2004b; Meister et al., 2011). crystals (Fig. 9B, C). FESEM observation shows that the core of micropeloids consists of polyhedron aggregates (Fig. 8B). Under 4.3.4. Pyrite framboids high magnification, submicron-sized micropores are observed in Pyrite framboids are common in organic-rich dark laminae (Fig. 5G–J). the rims of micropeloids (Fig. 9B). Similar micropores in modern They are embedded in platy or amorphous, partially silicified EPS microbialites have been interpreted as molds of decomposed bac- (Figs. 5J, 10A, B). Framboids appear as 3–12 μm spherical aggregates teria (e.g., Défarge et al., 1996) and their presence was considered composed of euhedral microcrystals of 0.5–1.5 μm in diameter as evidence for microbial activities (e.g., Bosak et al., 2004a; Tang (Fig. 10C, D). Microcrystals in framboids have silicified cores and accre- et al., 2013b). In both modern and ancient microbialites, tionary rims in cross section (Fig. 10D); their surfaces are seen to be micropeloids are common and have been interpreted as biogenic covered with ultrathin films composed of nanometer-scale fibers or origin (Chafetz, 1986; Chafetz and Buczynski, 1992; Défarge et al., particles (Fig. 10F, G). EDS analysis of pyrite framboids embedded in 1996; Dupraz et al., 2004, 2009; Spadafora et al., 2010; Power EPS matrix (Fig. 10H) reveals C, S, Fe, O, Ca, and Si in pyrite microcrystals et al., 2011; Tang et al., 2013a, 2013b). Some laboratory (Fig. 10I, upper panel), while the compositions of EPS matrix are mainly W. Zhang et al. / Gondwana Research 28 (2015) 432–450 441

Fig. 7. Ultra-fabrics in cortical laminae. (A) Filamentous bacteria (Ba) interweaved with EPS relics, with nanoglobules scattered on platy or amorphous EPS. (B) Micro-pores (Mh) walled by mucus-like EPS. EPS is also visible on the surface of micropeloid (Pe) (upper left). (C) Micro-pores (Mh) and mucus-like EPS together form alveolar structures. Nanoglobules are visible on EPS surfaces. (D) Extremely fine fibers on twisted EPS strips, likely resulting from EPS dehydration in very early diagenesis. (E) Numerous nanoglobules (Ns) visible on EPS flats. They coalesced into polyhedrons (Po) that aggregated into micropeloids (Pe). (F) Calcified sheath remnants (Bs, between arrows), with very fine fibers on inner surfaces, probably resulting from dissolution in early diagenesis. Micropeloid (Pe) is visible at the lower left and many fine fibers can be seen at the upper left. All are FESEM images.

C, Ca, O, and Si, without detectable Fe and S. This is consistent with the organomineralization provided sufficient pyrite nucleation sites for EDS element mapping of framboids (Fig. 10I, lower panel). framboid formation (e.g., Konhauser, 1998; Maclean et al., 2008; Pyrite framboids with diameters less than 10 μm are commonly Cavalazzi et al., 2012). In comparison with the pyrite framboids report- taken as evidence for pyrite precipitation from euxinic water column ed from black shales and some other microbialites (e.g., Wilkin and (e.g., Wilkin et al., 1996; Wilkin and Barnes, 1997; Wignall et al., Barnes, 1997; Wignall et al., 2005; Liao et al., 2011; Cavalazzi et al., 2005; Liao et al., 2011; Wang et al., 2012). Some studies proposed that 2012; Wang et al., 2012), framboids in oncoid cortical laminae have pyrite framboids may represent pyritized microbial colonies (e.g., smaller sizes but larger and fewer internal microcrystals. These features Popa et al., 2004; Folk, 2005; Gong et al., 2008), but others have were thought to be characteristic of biogenic pyrite framboids such as suggested that the formation of pyrite framboids occurs mostly in pyritized bacterial colonies (e.g., Popa et al., 2004; Folk, 2005; Ohfuji

H2S-rich water column where pyrite nucleation exceeds pyrite crystal and Rickard, 2005). growth (e.g., Konhauser, 1998; Butler and Rickard, 2000; Gabbott et al., 2004; Maclean et al., 2008). In micro-environments such as micro- 5. Discussion bial mounds (e.g., Cavalazzi et al., 2012), minute pyrite particles formed through EPS degradation and organomineralization could serve as 5.1. Formation of oncoid cortical laminae preferential sites for pyrite nucleation. The formation of framboidal pyrites in oncoid cortical laminae may be similar to those in microbial The alternations of light and dark laminae in microbialites including mounds and other microbial mats where sulfate-reduction and stromatolites, biolaminites, and some siliceous oncoids have been 442 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Fig. 8. Organominerals in oncoid cortex. (A) Nanoglobules (Ns) coalesced into aggregates (Ag) or polyhedrons. Mucus-like EPS strips are visible between aggregates. (B) Two micropeloids (dot line circles) consist of polyhedron (Po) aggregates and interweaving EPS remnants. (C) Polyhedrons (Po) and their aggregates, with minute nanoglobules on surfaces. A filament (Fil) made up of polyhedrons is also visible. (D) Nanoglobules (Ns) coalesced into sub-hexagonal polyhedrons (Po). Some nanoglobules with vague rims are not completely fused together yet. Amorphous EPS films are visible on the left side. All are FESEM images. ascribed to (1) variations in microbial groups and their relative abun- them are seen to have erect growth orientation at the base of the lami- dance (e.g., Freytet and Plet, 1996; Jones et al., 1998), (2) variations in nae (Fig. 6B). Organic relics (e.g., EPS) and grainy pyrites are present, growth pattern or arrangement style of microbial filaments (e.g., but no pyrite framboids are observed. These features suggest that mi- Janssen et al., 1999; Jones et al., 2005), (3) changes in mineral composi- crobial filaments in light laminae were calcified when microbial colo- tion and/or texture in response to microbial–environmental interac- nies were still alive or freshly buried. In vivo filament calcification tions (e.g., Jones and Renaut, 1994; Jones and Renaut, 1997), and (4) may have been controlled by high microbial growth rate that resulted imbalance between mineral precipitation and organic matter decompo- in low aqueous CO2 and high alkalinity in ambient microenvironments sition (e.g., Renaut et al., 1996; Konhauser et al., 2001; Kano et al., 2003). (e.g., Jones and Renaut, 1994; Arp et al., 2010), but whether this early These interpretations are based on variations in laminar microbial fossil calcification was related to metabolism of a particular cyanobacterial contents (e.g., mineralized filaments), mineral compositions and community (e.g., Arp et al., 2001, 2010; Pratt, 2001; Obst et al., 2009) organomineral fabrics/textures. is uncertain. Post-mortem organomineralization must have also hap- Except for their spherical morphology, the Cambrian oncoids show pened during the formation of the light laminae, as evidenced by the alternating laminar composition and texture similar to those of the presence of micropeloids, their aggregates (Fig. 9A, B) and larger other microbialites. The dark laminae primarily consist of micrite microsparitic crystals. (Fig. 5A) and subordinate amorphous silica (Fig. 10B, I). Platy or amor- The formation processes of oncoid cortical laminae seem to be phous EPS relics (Figs. 5K, 10H) and framboidal pyrites (Fig. 5G–J) are identical to those recognized in many modern microbialites (e.g., common, but filamentous cyanobacteria are rare, except for a small Konhauser, 1998; Jones et al., 1999a, 1999b; Dupraz et al., 2009; Perri amount of scattered, minute filaments that are reminiscent of hetero- et al., 2011). In modern microbialites, two major organomineralization trophic bacteria (Fig. 5E, F). The presence of framboidal pyrites indicates processes have been documented: (1) impregnation or replacement of sulfidic or suboxic microenvironments where sulfate reduction oc- organic materials and (2) encrustation on microbial filaments. The curred in the water column or close to sediment/seawater interface former occurs when organic matter has been largely degraded and (e.g., Wilkin and Barnes, 1997; Ohfuji and Rickard, 2005; Maclean organominerals start to form and replace organic remains after the mi- et al., 2008). In such microenvironments in vivo cyanobacterial calcifica- croenvironments become dysoxic or anoxic (e.g., Dupraz et al., 2009; tion may have been hindered by slow bacterial growth rate, relatively Spadafora et al., 2010; Perri et al., 2011). During this process, mineral 2+ 2+ high ambient water-column CO2, and absorption of Ca ,Mg by precipitation happened after significant decomposition of organic EPS during the early stages of mineralization (e.g., Bartley, 1996; matter so that morphologically distinguishable microbial filaments are Dupraz et al., 2004, 2009; Braissant et al., 2007). This explains the over- rarely preserved (e.g., Bartley, 1996). Encrustation of microbial all scarcity of bacterial filaments in the dark laminae. filaments is facilitated by increased alkalinity through photosynthetic

In contrast to the dark laminae, light laminae in oncoid cortices are removal of CO2 from the ambient waters (e.g., Jones and Renaut, characterized by densely intertwined filamentous cyanobacteria, with 1994; Arp et al., 2001, 2010; Obst et al., 2009) and by carbon concentrat- − some coccoid forms (Fig. 4C, D). Most of the filaments are wrapped ing mechanisms (CCMs) that involves active cellular uptake of HCO3 , − by thin microsparitic crusts (Fig. 6C–E). Although the majority of release of CO2 and OH , and increase of pH, promoting carbonate nucle- cyanobacterial filaments are preserved in a reclining pattern, some of ation in microbial sheath (Riding, 2006; Kah and Riding, 2007). In W. Zhang et al. / Gondwana Research 28 (2015) 432–450 443

Fig. 9. Micropeloids and their fabrics. (A) Micropeloids at the dark laminar margin. They are associated with residual organic matter (darker color) and commonly crystallized with vague denticulate rims. (B) Micropeloids encased with denticulate rim and surrounded by organic matter (dark color). EPS relics are visible in micropeloids, particularly between microcrystals. (C) Organic-rich clump surrounded by discrete crystalline sparitic patches. Abundant filaments in the clump (right) and micropeloids in sparitic patches (left). (D) Close view of the filaments in (C), showing filaments interweaving with microsparitic particles.

siliceous microbialites of hot springs, encrustation of microbial fila- 1000 μm(Figs. 3E–H, 5A, B), similar to the thickness of the annual lam- ments is enhanced by supersaturated opal-A in the ambient waters inar couplets in modern and Holocene tufas (500–2000 μm; Janssen (Renaut et al., 1996; Jones and Renaut, 1997; Jones et al., 1998, 1999a, et al., 1999; Kano et al., 2003; Kawai et al., 2009) but larger than the b; Konhauser et al., 2001, 2004). In this case, the major role that mi- thickness of biomineralization crust during a 12-day-incubation of crobes have played is to provide a template for silica nucleation and pre- cyanobacteria (~5 μm; Phoenix et al., 2000). Thus, we interpret that cipitation (Renaut et al., 1996; Konhauser et al., 2001, 2004). Because the light–dark laminar couplets in oncoid cortices may record seasonal encrustation occurs prior to significant microbial organic matter decom- variations, similar to those in the Mesoproterozoic stromatolites (Tang position, microbial filaments have much better chances to be preserved et al., 2013b) and in modern calcified microbial mats (Visscher et al., in their primary growth pattern (Bartley, 1996; Renaut et al., 1996; 1998; Spadafora et al., 2010). Konhauser et al., 2001). The dark laminae in oncoid cortices may have A schematic interpretation on the formation of oncoid cortical lami- been calcified mainly through impregnation or replacement of organic nar couplets is given in Fig. 11. The dark laminae were possibly formed materials, while the light laminae with abundant filaments were most during relatively cold and dry periods from late autumn to winter, while likely calcified through in vivo encrustation, followed by impregnation the light laminae were likely formed during warm and wet periods from after burial. late spring to early autumn (Fig. 11). The discrepancies in fabrics, com- The amount of time required to form a light–dark laminar couplet in position, and textures between dark and light laminae may record modern and ancient microbialites is debatable. Some alternating micro- variations in microbial growth rates, carbonate precipitation and bial laminae such as those in recent tufas are interpreted as recording decomposition of microbial organic matter in oncoid-forming microen- seasonal variations (Freytet and Verrecchia, 1998; Janssen et al., 1999; vironments. Although different microbial groups may have developed Kano et al., 2003; Kawai et al., 2009), but laminar alternations in modern during seasonal environmental changes, their impact on the laminar aragonite travertines (Okumura et al., 2011, 2012) and siliceous thickness and structure is difficult to evaluate due to the paucity of stromatolites (Berelson et al., 2011; Mata et al., 2012) are believed to recognizable microbial filaments in the dark laminae. record daily variations. In the latter case, the dark laminae that contain reclining microbial filaments are interpreted to have formed at night, 5.2. Water-energy conditions for oncoid formation while the porous light laminae containing vertically-oriented filaments were formed during daytime. Laboratory experiments have shown that The spherical morphology of oncoids is generally interpreted as encrustation of cyanobacterial filaments could form a 5-μm-thick crust having formed in agitated environments where oncoids experienced within a few weeks when microbes were still alive or shortly after frequent overturn (e.g., Hender and Dix, 2008; Flügel, 2010). Some of their death (Phoenix et al., 2000). The thickness of the light–dark lami- the subspherical–spherical oncoids, however, were also seen to form nar couplets from the Cambrian oncoid cortices varies from 200 μmto by in situ microbial accretion, not necessarily requiring turbulent 444 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Fig. 10. Pyrite framboids and ultra-fabrics in cortical laminae. (A) Abundant pyrite framboids present in the dark lamina, often entombed in the matrix. (B) Organic remains visible around framboids. Some filamentous relics are attached to (lower left) or on surfaces of (lower right) the framboids. Micro-holes are visible in micritic particles (midright). (C) Framboid composed of equidimensional pyrite microcrystals, with partially degraded EPS strip between microcrystals. (D) Individual pyrite microcrystals showing dark finely granular core and clear accretionary ringsincrosssection.(E)Nanoglobulesobservablein a pyrite mould in amorphous matrix. (F) Decomposed EPS films on pyrite microcrystals, showing as numerous fine and short fibers. (G) Close view of decomposed EPS relics in (C) (arrows). Densely packed fibers are present on remnant EPS surface. (H) Abundant EPS relics (arrows) present in the dark laminae. They tend to form honey-comb structures that wrap micrite particles. (I) EDS spectrum of pyrite microcrystal (in C, “+” marks the position of the tested spot). The upper right inset shows the relative concentration of elements (in atm %; element Pt resulting from platinum coating). Three images in the lower panel show element mappings of a framboid (EDS areal scanning). Elements S and Fe are dominated in the framboid but Ca is more abundant in the surrounding matrix without detectable S and Fe. Scale bar in (I) is 1 μm. All pictures are FESEM images. W. Zhang et al. / Gondwana Research 28 (2015) 432–450 445

Fig. 11. Schematic diagram explaining microbial growth and mineralization processes of the Cambrian oncoids. (A–C) Suggested formation process of oncoid nucleus. (D–F) Suggested formation process of oncoid cortex. (G) Possible mineralization process of microbial filaments. hydraulic conditions or frequent grain overturning (e.g., Dahanayake (e.g., Calner, 2005), widespread microbialites and anachronistic facies et al., 1985; Leinfelder and Hartkopf-Fröder, 1990; Hägele et al., 2006). in the aftermath of Late Devonian (Frasnian–Fammenian boundary) These in situ oncoids were commonly associated with microbial mats and end-Permian mass extinctions (e.g., Whalen et al., 2002; Shen and (Dahanayake et al., 1985) and their spherical morphology was interpreted Webb, 2004; Wood, 2004; Xie et al., 2005, 2010; Pruss et al., 2006; as having formed by fast microbial occupation of the entire available space Woods and Baud, 2008; Ezaki et al., 2012; Kershaw et al., 2012), and surrounding a nucleus (Leinfelder and Hartkopf-Fröder, 1990). abundance of microbialites after the Miocene Messinian Salinity Event Most oncoids from the Maozhuang and Xuzhuang formations show (e.g., Martıń et al., 1993; Arenas and Pomar, 2010). spherical or subspherical morphology (Fig. 3C–F). Some of them have a Massive oncolite layers across the Cambrian Series 2–Series 3 transi- small depression or indention at the base but their cortical laminae are tion are widespread in the North China Platform and in other continents laterally continuous surrounding the nuclei (Fig. 3F). Although the globally. In the North China Platform, oncoids were predominantly thickness of some laminae varies laterally, in most cases the cortical formed by Girvanella-like microbes. They roughly occur at the same laminae show the same growth orientation for more than 5 light–dark stratigraphic interval covering the uppermost Maozhuang Formation laminar couplets (e.g., Fig. 3G, H). No microbial mats were observed in and lowermost Xuzhuang Formation (Fig. 1C). Although no detailed the matrix of oncolite layers but oncoid cortical laminae contain calci- study has been focused on oncolites in many cases, massive oncolite fied bacterial filaments and/or abundant organomineral features includ- layers/units have been reported from a number of Chinese localities in ing EPS, nanoglobules, polyhedrons, and micropeloids (Figs. 5–8), Shandong (Shi et al., 1999; Yang et al., 2011, 2013), Shanxi (Gao and recording active microbial accretion during oncoid formation. If the Zhu, 1998; Xiang et al., 1999), the suburb of Beijing, Hebei, and Liaoning light–dark laminar couplets represent seasonal cycles, it implies that, provinces (Meng et al., 1997; Shi et al., 1997; Wang et al., 2000). Similar at least for the studied examples, oncoids may have grown in situ for a oncoids are also reported from time-equivalent strata in South China significant amount of time (for examples, a few years) before their over- (e.g., Liu and Zhang, 2012) and northwestern China, including Shaanxi, turn. Thus, the spherical morphology of oncoids may have been largely Ningxia, Gansu (Fig. 1A) and Xinjiang (Wang et al., 2011). Globally, formed by three-dimensional microbial colonization on the nuclei and massive oncolites and/or other microbialites have been reported across subsequent cortical surface (cf., Leinfelder and Hartkopf-Fröder, 1990). the traditional Early–Middle Cambrian transition in North America and Frequent wave or tidal activities may not be required; instead, storm Australia (e.g., Youngs, 1978; Sundberg, 2005; Powell et al., 2006), events that episodically agitated the substrate may have helped to Jordan (Elicki et al., 2002), Spain (Álvaro et al., 2000; Perejón et al., shape the final size and morphology of oncoids. 2012), and Argentina (Gomez et al., 2007). Although there are uncer- tainties related to the trilobite biostratigraphy that prevent a precise 5.3. Mass-occurrence of Cambrian oncoids: linked to an ocean anoxic global correlation, mass-occurrence of oncolites and other microbialites event? in different continents all appears around the stratigraphic interval that contains O. indicus (or its correlatives), a potential candidate fossil rec- The resurgence of microbialites after mass extinction events in ommended to define the GSSP for the base of Cambrian Series 3/Stage Phanerozoic marine successions has been taken as evidence for highly 5(Figs. 2 and 12; Babcock and Peng, 2007; Peng, 2009; Wotte et al., stressed, possibly dysoxic–anoxic bottom-water conditions unfavorable 2011; Sundberg et al., 2011; Peng et al., 2012; Gozalo et al., 2013; for grazing metazoans (e.g., Riding, 2000; Woods and Baud, 2008; Mata Landing et al., 2013). and Bottjer, 2012). Examples include the resurgence of stromatolite/ The mass-occurrence of oncoids is also coincident with an Early thrombolite/dendrolite after the Late Ordovician mass extinction (e.g., Cambrian extinction event and a negative δ13C excursion (Redlichiid– Sheehan and Harris, 2004), mass-occurrence of oncoids, stromatolites Olenellid Extinction Carbon isotope Excursion or ROECE; Zhu et al., and wrinkle structures following the Late Silurian extinction event 2006). In the study area and across the North China Platform, oncoid- 446 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Fig. 12. Proposed correlation of oncoid mass-occurrence with other geological and geochemical events across the Cambrian Series 2–Series 3 transition. A pronounced positive δ34S shift is present approximately at Series 2–Series 3 transition with a peak around 512–508 Ma. A negative carbon isotope excursion (ROECE) coincides with the biotic extinction, eruption of Kalkarindji igneous province, 87Sr/86Sr rise, and sea-level rise. Data source: sea-level change curve: Haq and Schutter (2008); δ34Scurve:Hough et al. (2006) and Gill et al. (2007, 2011); δ13Ccurve:Zhu et al. (2006); biotic extinction data: Zhu et al. (2006) and Erwin (2001); Kalkarindji igneous province data: Glass and Phillips (2006) and Evins et al. (2009); 87Sr/86Sr data: Montañez et al. (2000) and Peng et al. (2012). bearing strata are constrained by benthic trilobite zones of Shantungaspis the Cambrian Stage 4–Stage 5 boundary (e.g., Zhu et al., 2006; Guo et al., to lower Ruichengaspis (Figs. 1Cand2), which have been correlated 2010; Wotte et al., 2011; Peng et al., 2012; Gozalo et al., 2013; Landing with the pelagic trilobite zones of O. granulata and O. indicus recognized et al., 2013). in slope facies of South China (Peng, 2009; Fig. 2). The O. granulata and The latest Early Cambrian biotic crisis has been ascribed to wide- O. indicus intervals are temporally coincident with the well-known biot- spread anoxia in shallow marine environments (Zhuravlev and Wood, ic crisis at the latest Early Cambrian (Palmer, 1998; Erwin, 2001; Yuan 1996; Palmer, 1998; Erwin, 2001; Hallam, 2005; Zhu et al., 2006; Mata et al., 2002; Hallam, 2005; Zhu et al., 2006; Peng et al., 2012). During and Bottjer, 2012), possibly resulting from the upwelling of 13C- this biotic crisis (Fig. 12), some benthic trilobites that characterize the depleted anoxic deep-water to shallow-marine shelves (Wignall, Early Cambrian worldwide (e.g., redlichiids in eastern Gondwana, 2001; Hough et al., 2006; Dilliard et al., 2007; Wotte et al., 2007; Guo olenellids in Laurentia, and protolenids in Siberia) demised completely et al., 2010; Gozalo et al., 2013). Coincident with this biotic crisis and (e.g., Palmer, 1998; Yuan et al., 2002; Zhu et al., 2006; Peng et al., 2012; the ROECE is a notable rise in 87Sr/86Sr ratio that has been reported Gozalo et al., 2013). Archaeocyathids, the earliest Phanerozoic calcare- from several Early Cambrian successions (Fig. 12) (e.g., Montañez ous reef-building metazoan group that was common during the Early et al., 2000; Mazumdar and Strauss, 2006; Wotte et al., 2007; Wang Cambrian, disappeared entirely around the O. granulata zone (Álvaro et al., 2011; Wotte et al., 2011). The increase of 87Sr/86Sr was interpreted et al., 2000; Hallam, 2005; Wotte et al., 2011; Perejón et al., 2012; as recording enhanced terrestrial weathering in response to Early Pruss et al., 2012; Gozalo et al., 2013). Accompanied with this biotic cri- Cambrian tectonic uplift (Montañez et al., 2000; Evins et al., 2009). Re- sis is a profound change in the style of carbonate deposition in continen- cently a large igneous province (Kalkarindji igneous province) of Early– tal shelves (e.g., Álvaro et al., 2000; Gozalo et al., 2013)anda Middle Cambrian transition age (Fig. 12) has been documented in pronounced negative δ13C excursion with a shift down to −4‰ to Australia (Glass and Phillips, 2006) and dated as 513–505 Ma (Hanley −6‰ (ROECE; Zhu et al., 2006), followed by a sharp positive rise in and Wingate, 2000; Glass and Phillips, 2006; Evins et al., 2009). The δ13C that may have been resulted from enhanced burial of organic car- Kalkarindji igneous province occupies an area of 2.1 × 106 km2 and is bon and pyrite (e.g., Guo et al., 2010; Gill et al., 2011; Saltzman et al., regarded as one of the largest igneous provinces of the Phanerozoic, in 2011; Fig. 12). The ROECE and the subsequent positive δ13C shift have addition to the Siberian trap basalts (at P/T transition), the Central At- been documented in several Early Cambrian successions including lantic Magmatic Province (CAMP, at T/J transition), and the Deccan those in South China (Zhu et al., 2004, 2006; Guo et al., 2010), North traps (at K/T transition) (cf. Wignall, 2001). In addition, a large positive China (Zhu et al., 2004), the Tarim basin (Wang et al., 2011), North sulfur isotope shift with maximum values up to +50‰ (Fig. 12)isalso America (e.g., Montañez et al., 2000; Howley and Jiang, 2010), Canada reported around ca. 510 Ma (Hough et al., 2006). This δ34S shift was (Dilliard et al., 2007), Spain (Wotte et al., 2007, 2012; Gozalo et al., interpreted as recording enhanced burial of pyrites, low sulfate concen- 2013), France (Wotte et al., 2007, 2011, 2012), Argentina (Gomez tration, and widespread ocean anoxia (Hough et al., 2006; Hurtgen et al., 34 et al., 2007), and Siberia (Brasier et al., 1994; Dilliard et al., 2007; 2009; Thompson and Kah, 2012). A similar δ SCAS shift has been recent- Wotte et al., 2011). The ROECE and its overlying positive δ13Cshift ly documented from multiple sections in South China (Guo et al., 34 13 have also been suggested to be used as additional markers for defining 2014) and the parallel δ SCAS–δ C trends suggest seawater isotope W. Zhang et al. / Gondwana Research 28 (2015) 432–450 447 signature. Sulfur isotope data from time equivalent strata of Siberia and Natural Science Foundation of China (nos. 41272039, 40972022). Laurentia, however, display large temporal and spatial variations Thanks are given to Mr. Liu Dianbo and Mr. Li Bin for their field assis- (Wotte et al., 2011, 2012) that call attention for using the positive tance. We are grateful to Drs. T. Wotte, G.C. Zhao and M. Santosh for 34 δ SCAS excursion as a global seawater isotope signature. their constructive suggestions and critical comments that greatly The coincidence of the Early Cambrian extinction event with a large helped to improve the paper. igneous province, ROECE, 87Sr/86Sr increase and a positive δ34S excur- sion supports the interpretation that the biotic crisis at the Cambrian Se- Appendix A. Supplementary data ries 2–Series 3 transition was likely caused by an ocean anoxic/dysoxic event. The oncoid mass-occurrence at the same stratigraphic interval Supplementary data associated with this article can be found in the provides additional support for the resurgence of microbial ecosystem online version, at http://dx.doi.org/10.1016/j.gr.2014.03.015. These in anoxic/dysoxic shelf environments concomitant with the biotic crisis, data include Google map of the most important areas described in this likely due to reduced metazoan grazing capacity and high alkalinity that article. promote carbonate nucleation and precipitation in oncoid-forming mi- croenvironments. Shallow-water anoxia/dysoxia could be triggered by Appendix A. Supplementary data global warming induced by release of voluminous CO2 and other vola- tiles associated with the activity of Kalkarindji igneous province. Global Supplementary data to this article can be found online at http://dx. warming and reduced thermalhaline circulation would lower dissolved doi.org/10.1016/j.gr.2014.03.015. oxygenlevelinseawater(Evins et al., 2009; Elrick et al., 2011), leading to bottom-water anoxia/dysoxia in shelf environments. Although more References direct geochemical and sedimentological evidence are still needed, the mass-occurrence of oncoids following the Early Cambrian extinction Aloisi, G., Gloter, A., Krüger, M., Wallmann, K., Guyot, F., Zuddas, P., 2006. Nucleation of event is consistent with many of the Phanerozoic examples that demon- calcium carbonate on bacterial nanoglobules. Geology 34, 1017–1020. Alshuaibi, A., Duane, M.J., Mahmoud, H., 2012. Microbial-activated sediment traps associ- strated a causal link between mass extinction, microbial resurgence, and ated with oncolite formation along a Peritidal Beach, Northern Arabian (Persian) Gulf, isotope excursions. Kuwait. Geomicrobiology Journal 29, 679–696. Álvaro, J.J., Vennin, E., Moreno-Eiris, E., Perejón, A., Bechstädt, T., 2000. Sedimentary pat- – 6. Conclusion terns across the Lower Middle Cambrian transition in the Esla nappe (Cantabrian Mountains, northern Spain). Sedimentary Geology 137, 43–61. Álvaro, J.J., Ahlberg, P., Babcock, L.E., Bordonaro, O.L., Choi, D.K., Cooper, R.A., Ergaliev, G.K., Well-preserved oncolites across the Cambrian Series 2–Series 3 Gapp, I.W., Pour, M.G., Hughes, N.C., 2013. Global Cambrian trilobite palaeobiogeography transition are documented from the western margin of the North assessed using parsimony analysis of endemicity. Geological Society, London, Memoirs 38, 273–296. China Platform. The oncoid-bearing strata are widespread across the Arenas, C., Pomar, L., 2010. Microbial deposits in upper Miocene carbonates, Mallorca, North China Platform and in many other time-equivalent successions Spain. Palaeogeography, Palaeoclimatology, Palaeoecology 297, 465–485. globally. Stratigraphic correlation indicates the concomitant occurrence Arp, G., Reimer, A., Reitner, J., 2001. Photosynthesis-induced biofilm calcification and – – calcium concentrations in Phanerozoic oceans. Science 292, 1701 1704. of a few geological and geochemical events at the Cambrian Series 2 Arp, G., Bissett, A., Brinkmann, N., Cousin, S., De Beer, D., Friedl, T., Mohr, K.I., Neu, T.R., Series 3 transition (close to the traditional Early–Middle Cambrian Reimer, A., Shiraishi, F., 2010. Tufa-forming biofilms of German karstwater streams: boundary), including the mass-occurrence of oncoids, the large igneous microorganisms, exopolymers, hydrochemistry and calcification. Geological Society, London, Special Publications 336, 83–118. province (Kalkarindji igneous province) in Australia, the prominent Babcock, L.E., Peng, S., 2007. Cambrian chronostratigraphy: current and future plans. 13 87 86 negative δ C excursion (ROECE), the large positive shift in Sr/ Sr Palaeogeography, Palaeoclimatology, Palaeoecology 254, 62–66. and δ34S, and the extinction of archaeocyathids and many trilobite Bartley, J.K., 1996. Actualistic taphonomy of cyanobacteria: implications for the Precam- brian fossil record. Palaios 11, 571–586. taxa. The coincidence of these events implies a causal link between Berelson, W.M., Corsetti, F.A., Pepe-Ranney, C., Hammond, D.E., Beaumont, W., Spear, J.R., seemly unrelated phenomena, possibly anchored to an ocean anoxic 2011. Hot spring siliceous stromatolites from Yellowstone National Park: assessing event. The anoxic event may be triggered by global warming and seawa- growth rate and laminae formation. Geobiology 9, 411–424. ter transgression resulted from CO release associated with the Bosak, T., Souza-Egipsy, V., Corsetti, F.A., Newman, D.K., 2004a. Micrometer-scale porosity 2 as a biosignature in carbonate crusts. Geology 32, 781–784. Kalkarindji igneous province. The mass-occurrence of oncoids may re- Bosak, T., Souza-Egipsy, V., Newmanne, D.K., 2004b. A laboratory model of abiotic peloid cord a microbial resurgence following the Early Cambrian extinction formation. Geobiology 2, 189–198. event that reduced the metazoan grazing capacity in anoxic/dysoxic Braissant, O., Decho, A.W., Dupraz, C., Glunk, C., Przekop, K.M., Visscher, P.T., 2007. Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at shelf environments. alkaline pH and implication for formation of carbonate minerals. Geobiology 5, The oncoids from the Early Cambrian strata display well-preserved 401–411. 13 cortical light–dark laminar couplets. Light laminae contain abundant Brasier, M., Corfield, R., Derry, L., Rozanov, A.Y., Zhuravlev, A.Y., 1994. Multiple δ C fi fi excursions spanning the Cambrian explosion to the Botomian crisis in Siberia. cyanobacterial laments; their preservation requires in vivo calci ca- Geology 22, 455–458. tion. Dark laminae contain organic relics, framboidal pyrites and abun- Butler, I.B., Rickard, D., 2000. Framboidal pyrite formation via the oxidation of iron (II) dant organomineralization fabrics; they may have been calcified monosulfide by hydrogen sulphide. Geochimica et Cosmochimica Acta 64, 2665–2672. mainly through post-mortem impregnation. The cortical laminae in Calner, M., 2005. A Late Silurian extinction event and anachronistic period. Geology 33, oncoids are laterally continuous surrounding the nuclei and show the 305–308. same growth orientation for a few light–dark laminar couplets, suggest- Cavalazzi, B., Barbieri, R., Candy, S., George, A., Gennaro, S., Westall, F., Lui, A., Canteri, R., fi Rossi, A., Ori, G., Taj-Eddinei, K., 2012. Iron-framboids in the hydrocarbon-related ing that oncoid remained in situ for a signi cant amount time (e.g., a Middle Devonian Hollard Mound of the Anti-Atlas mountain range in Morocco: few years) and their spherical morphology was largely formed by evidence of potential microbial biosignatures. Sedimentary Geology 263, 183–193. three-dimensional microbial colonization on the nuclei and subse- Chafetz, H.S., 1986. Marine peloids—a product bacterially induced precipitation of calcite. – quent cortical surface. Frequent grain overturning in wave- or tide- Sedimentary Petrology 56, 812 817. Chafetz, H.S., Buczynski, C., 1992. Bacterially induced lithification of microbial mats. agitated environments may not be required for the sphericity of Palaios 7, 277–293. oncoids but episodic storm events capable of agitating the substrate Chen, J., Zhang, F., Bian, L., 1997. Ultra-microbes are the minerogenetic constructors of – are necessary. oceanic polymetallic nodules. Chinese Science Bulletin 42, 617 624. Cheng, Y.Q., Wang, Z.J., Huang, Z.G., 2009. Stratigraphic Lexicon of China—General Introduction. Geological Publishing House, Beijing pp. 1–411 (in Chinese). Acknowledgements Dahanayake, K., Gerdes, G., Krumbein, W.E., 1985. Stromatolites, oncolites and oolites biogenically formed in situ. Naturwissenschaften 7, 513–518. Davaud, E., Girardclos, S., 2001. Recent freshwater ooids and oncoids from western Lake The study was supported by the Ministry of Science and Technology Geneva (Switzerland): indications of a common organically mediated origin. Journal of the People's Republic of China (no. 2011CB808806) and the National of Sedimentary Research 71, 423–429. 448 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Défarge, C., Trichet, J., Coute, A., 1994. On the appearance of cyanobacterial calcification in Series 3, Kaili area, Yangtze Platform: evidence from biogenic sulfur and degree of modern stromatolites. Sedimentary Geology 94, 11–19. pyritization. Palaeogeography, Palaeoclimatology, Palaeoecology 398, 144–153. Défarge, C., Trichet, J., Jaunet, A.M., Robert, M., Tribble, J., Sansone, F.J., 1996. Texture of Hägele, D., Leinfelder, R., Grau, J., Burmeister, E.G., Struck, U., 2006. Oncoids from the river microbial sediments revealed by cryo-scanning electron microscopy. Journal of Alz (southern Germany): tiny ecosystems in a phosphorus-limited environment. Sedimentary Research 66, 935–947. Palaeogeography, Palaeoclimatology, Palaeoecology 237, 378–395. Dilliard, K.A., Pope, M.C., Coniglio, M., Hasiotis, S.T., Lieberman, B.S., 2007. Stable isotope Hallam, T., 2005. Catastrophes and Lesser Calamities: The Causes of Mass Extinctions. geochemistry of the lower Cambrian Sekwi Formation, Northwest Territories, Oxford University Press, USA pp. 1–274. Canada: implications for ocean chemistry and secular curve generation. Hanley, L.M., Wingate, M.T.D., 2000. SHRIMP zircon age for an Early Cambrian dolerite Palaeogeography, Palaeoclimatology, Palaeoecology 256, 174–194. dyke: an intrusive phase of the Antrim Plateau Volcanics of northern Australia. Dupraz, C., Visscher, P., Baumgartner, L., Reid, R., 2004. Microbe–mineral interactions: Australian Journal of Earth Sciences 47, 1029–1040. early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas). Haq, B.U., Schutter, S.R., 2008. A chronology of Paleozoic sea-level changes. Science 322, Sedimentology 51, 745–765. 64–68. Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S., Visscher, P.T., 2009. Process- Harwood, C.L., Sumner, D.Y., 2011. Microbialites of the Neoproterozoic Beck Spring es of carbonate precipitation in modern microbial mats. Earth-Science Reviews 96, Dolomite, Southern California. Sedimentology 58, 1648–1673. 141–162. Hender, K.L.B., Dix, G.R., 2008. Facies development of a late Ordovician mixed carbonate- Elicki, O., Schneider, J., Shinaq, R., 2002. Prominent facies from the Lower/Middle siliciclastic ramp proximal to the developing taconic orogen: Lourdes formation, Cambrian of the Dead Sea area (Jordan) and their palaeodepositional significance. Newfoundland, Canada. Facies 54, 121–149. Bulletin de la Societe Geologique de France 173, 547–552. Hicks, M., Rowland, S.M., 2009. Early Cambrian microbial reefs, archaeocyathan inter-reef Elrick, M., Rieboldt, S., Saltzman, M., McKay, R.M., 2011. Oxygen-isotope trends and communities, and associated facies of the Yangtze Platform. Palaeogeography, seawater temperature changes across the Late Cambrian Steptoean positive carbon- Palaeoclimatology, Palaeoecology 281, 137–153. isotope excursion (SPICE event). Geology 39, 987–990. Hough, M., Shields, G., Evins, L., Strauss, H., Henderson, R., Mackenzie, S., 2006. Amajor Erwin, D.H., 2001. Lessons from the past: biotic recoveries from mass extinctions. sulphur isotope event at c. 510 Ma: a possible anoxia–extinction–volcanism connec- Proceedings of the National Academy of Sciences 98, 5399–5403. tion during the Early–Middle Cambrian transition? Terra Nova 18, 257–263. Evins, L.Z., Jourdan, F., Phillips, D., 2009. The Cambrian Kalkarindji Large Igneous Province: Howley, R.A., Jiang, G., 2010. The Cambrian Drumian carbon isotope excursion (DICE) in extent and characteristics based on new 40Ar/39Ar and geochemical data. Lithos 110, the Great Basin, western United States. Palaeogeography, Palaeoclimatology, Palaeo- 294–304. ecology 296, 138–150. Ezaki, Y., Liu, J., Adachi, N., 2012. Lower Triassic stromatolites in Luodian County, Guizhou Hurtgen, M.T., Pruss, S.B., Knoll, A.H., 2009. Evaluating the relationship between the Province, South China: evidence for the protracted devastation of the marine envi- carbon and sulfur cycles in the later Cambrian ocean: an example from the Port au ronments. Geobiology 10, 48–59. Port Group, western Newfoundland, Canada. Earth and Planetary Science Letters Feng, Z.Z., 1990. Lithologic Paleogeography of Early Paleozoic of the North China Platform. 281, 288–297. Geological Publishing House, Beijing (270 pp. (in Chinese with English abstract)). Janssen, A., Swennen, R., Podoor, N., Keppens, E., 1999. Biological and diagenetic influence Flügel, E., 2010. Microfacies of Carbonate Rocks: Analysis, Interpretation and Application, in recent and fossil tufa deposits from Belgium. Sedimentary Geology 126, 75–95. 2nd ed. Springer, Berlin pp. 1–984. Jones, B., 2011. Biogenicity of terrestrial oncoids formed in soil pockets, Cayman Brac, Folk, R.L., 2005. Nannobacteria and the formation of framboidal pyrite: textural evidence. British West Indies. Sedimentary Geology 236, 95–108. Journal of Earth System Science 114, 369–374. Jones, B., Renaut, R.W., 1994. Crystal fabrics and microbiota in large pisoliths from Laguna Freytet, P., Plet, A., 1996. Modern freshwater microbial carbonates: the Phormidium Pastos Grandes, Bolivia. Sedimentology 41, 1171–1202. stromatolites (tufa-travertine) of southeastern Burgundy (Paris Basin, France). Facies Jones, B., Renaut, R.W., 1997. Formation of silica oncoids around geysers and hot springs 34, 219–237. at El Tatio, Chile. Sedimentology 44, 287–304. Freytet, P., Verrecchia, E.P., 1998. Freshwater organisms that build stromatolites: a Jones, B., Renaut, R.W., Rosen, M.R., 1998. Microbial biofacies in hot-spring sinters: a synopsis of biocrystallization by prokaryotic and eukaryotic algae. Sedimentology model based on Ohaaki Pool, North Island, New Zealand. Journal of Sedimentary 45, 535–563. Research 68, 413–434. Gabbott, S.E., Hou, X.G., Norry, M.J., Siveter, D.J., 2004. Preservation of Early Cambrian Jones, B., Renaut, R.W., Rosen, M.R., 1999a. Actively growing siliceous oncoids in the animals of the Chengjiang biota. Geology 32, 901–904. Waiotapu geothermal area, North Island, New Zealand. Journal of Geological Society, Gaines, R.R., Mering, J.A., Zhao, Y., Peng, J., 2011. Stratigraphic and microfacies analysis of London 156, 89–103. the Kaili Formation, a candidate GSSP for the Cambrian Series 2–Series 3 boundary. Jones, B., Renaut, R.W., Rosen, M.R., 1999b. Role of fungi in the formation of siliceous coat- Palaeogeography, Palaeoclimatology, Palaeoecology 311, 171–183. ed grains, Waiotapu geothermal area, North Island, New Zealand. Palaios 14, Gao, J.P., Zhu, S.X., 1998. Cambrian microbialites from the northeastern Shanxi Province 475–492. and their relation to sedimentary environments. Acta Micropalaeontologica Sinica Jones, B., Renaut, R.W., Konhauser, K.O., 2005. Genesis of large siliceous stromatolites at 15, 166–177 (in Chinese, with English abstract). Frying Pan Lake, Waimangu geothermal field, North Island, New Zealand. Sedimen- Geological Bureau of Inner Mongolia Autonomous Region, 1991. Regional Geology of the tology 52, 1229–1252. Inner Mongolia Autonomous Region. Geological Publishing House, Beijing pp. 72–84 Kah, L.C., Riding, R., 2007. Mesoproterozoic carbon dioxide levels inferred from calcified (in Chinese). cyanobacteria. Geology 35, 799–802. Geyer, G., Peel, J.S., 2011. The Henson Gletscher Formation, North Greenland, and its Kano,A.,Matsuoka,J.,Kojo,T.,Fujii,H.,2003.Origin of annual laminations in tufa de- bearing on the global Cambrian Series 2–Series 3 boundary. Bulletin of Geosciences posits, southwest Japan. Palaeogeography, Palaeoclimatology, Palaeoecology 86, 465–534. 191, 243–262. Gill, B.C., Lyons, T.W., Saltzman, M.R., 2007. Parallel, high-resolution carbon and sulfur iso- Kawai, T., Kano, A., Hori, M., 2009. Geochemical and hydrological controls on biannual tope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeography, lamination of tufa deposits. Sedimentary Geology 213, 41–50. Palaeoclimatology, Palaeoecology 256, 156–173. Kershaw, S., Li, Y., Crasquin-Soleau, S., Feng, Q., Mu, X., Collin, P.Y., Reynolds, A., Guo, L., Gill, B.C., Lyons, T.W., Young, S.A., Kump, L.R., Knoll, A.H., Saltzman, M.R., 2011. Geochem- 2007. Earliest Triassic microbialites in the South China block and other areas: controls ical evidence for widespread euxinia in the Later Cambrian ocean. Nature 469, 80–83. on their growth and distribution. Facies 53, 409–425. Glass, L.M., Phillips, D., 2006. The Kalkarindji continental flood basalt province: a new Kershaw, S., Crasquin, S., Li, Y., Collin, P.Y., Forel, M.B., Mu, X., Baud, A., Wang, Y., Xie, S., Cambrian large igneous province in Australia with possible links to faunal extinctions. Maurer, F., 2012. Microbialites and global environmental change across the Geology 34, 461–464. Permian–Triassic boundary: a synthesis. Geobiology 10, 25–47. Gomez, F.J., Ogle, N., Astini, R.A., Kalin, R.M., 2007. Paleoenvironmental and carbon– Konhauser, K.O., 1998. Diversity of bacterial iron mineralization. Earth-Science Reviews oxygen isotope record of Middle CambrianCarbonates (La Laja Formation) in the 43, 91–121. Argentine Precordillera. Journal of Sedimentary Research 77, 826–842. Konhauser, K.O., Phoenix, V.R., Bottrell, S.H., Adams, D.G., Head, I.M., 2001. Microbial– Gong, Y., Shi, G.R., Weldon, E.A., Du, Y., Xu, R., 2008. Pyrite framboids interpreted as micro- silica interactions in Icelandic hot spring sinter: possible analogues for some bial colonies within the Permian Zoophycos spreiten from southeastern Australia. Precambrian siliceous stromatolites. Sedimentology 48, 415–433. Geological Magazine 145, 95–107. Konhauser, K.O., Jones, B., Phoenix, V.R., Ferris, G., Renaut, R.W., 2004. The microbial Gozalo, R., Álvarez, M.E.D., Vintaned, J.Z.G., Zhuravlev, A.Y., Bauluz, B., 2013. Proposal of a role in hot spring silicification. AMBIO: A Journal of the Human Environment 33, reference section and point for the Cambrian Series 2–3 boundary in the Mediterra- 552–558. nean subprovince in Murero (NE Spain) and its intercontinental correlation. Geolog- Landing, E., Geyer, G., Brasier, M.D., Bowring, S.A., 2013. Cambrian evolutionary radiation: ical Journal 48, 142–155. context, correlation, and chronostratigraphy—overcoming deficiencies of the first Gradziński, M., Tyszka, J., Uchman, A., Jach, R., 2004. Large microbial–foraminiferal appearance datum (FAD) concept. Earth-Science Review 123, 133–172. oncoids from condensed Lower–Middle Jurassic deposits: a case study from the Lanés, S., Palma, R.M., 1998. Environmental implications of oncoids and associated Tatra Mountains, Poland. Palaeogeography, Palaeoclimatology, Palaeoecology 213, sediments from the Remoredo Formation (Lower Jurassic) Mendoza, Argentina. 133–151. Palaeogeography, Palaeoclimatology, Palaeoecology 140, 357–366. Grotzinger, J.P., Knoll, A.H., 1999. Stromatolites in Precambrian carbonates: evolutionary Lazăr, I., Grădinaru, M., Petrescu, L., 2013. Ferruginous microstromatolites related to mileposts or environmental dipsticks? Annual Review of Earth and Planetary Sci- Middle Jurassic condensed sequences and hardgrounds (Bucegi Mountains, Southern ences 27, 313–358. Carpathians, Romania). Facies 59, 359–390. Guo, Q., Strauss, H., Liu, C., Zhao, Y., Yang, X., Peng, J., Yang, H., 2010. A negative carbon Lee, J.H., Chen, J., Chough, S.K., 2012. Demise of an extensive biostromal microbialite in the isotope excursion defines the boundary from Cambrian Series 2 to Cambrian Series Furongian (late Cambrian) Chaomidian Formation, Shandong Province, China. 3 on the Yangtze Platform, South China. Palaeogeography, Palaeoclimatology, Palaeo- Geosciences Journal 16, 275–287. ecology 285, 143–151. Leinfelder, R.R., Hartkopf-Fröder, C., 1990. In situ accretion mechanism of concavo‐convex Guo, Q., Strauss, H., Zhao, Y., Yang, X., Peng, J., Yang, Y., Deng, Y., 2014. Reconstructing lacustrine oncoids (‘swallow nests’) from the Oligocene of the Mainz Basin, Rhine- marine redox conditions for the transition between Cambrian Series 2 and Cambrian land, FRG. Sedimentology 37, 287–301. W. Zhang et al. / Gondwana Research 28 (2015) 432–450 449

Li, X.Z., Guan, S.R., Xie, Q.B., Wang, Z.C., 2000. The oncoids genesis in the Middle Member Riding, R., 2000. Microbial carbonates: the geological record of calcified bacterial–algal of the Guanzhuang Formation of Eocene in Pingyi Basin. Acta Petrologica Sinica 16, mats and biofilms. Sedimentology 47, 179–214. 261–268 (in Chinese with English abstract). Riding, R., 2006. Cyanobacterial calcification, carbon dioxide concentrating mechanisms, Liao, W., Wang, Y.B., Kershaw, S., Weng, Z.T., Yang, H., 2011. Shallow-marine dysoxia and Proterozoic–Cambrian changes in atmospheric composition. Geobiology 4, across the Permian–Triassic boundary: evidence from pyrite framboids in the 299–316. microbialite in South China. Sedimentary Geology 232, 77–83. Riding, R., Liang, L., 2005. Geobiology of microbial carbonates: metazoan and seawater Liu, W., Zhang, X., 2012. Girvanella-coated grains from Cambrian oolitic limestone. Facies saturation state influences on secular trends during the Phanerozoic. 58, 779–787. Palaeogeography, Palaeoclimatology, Palaeoecology 219, 101–115. Maclean, L., Tyliszczak, T., Gilbert, P., Zhou, D., Pray, T.J., Onstott, T.C., Southam, G., 2008. A Riding, R., Voronova, L., 1982. Recent freshwater oscillatoriacean analogue of the Lower high-resolution chemical and structural study of framboidal pyrite formed within a Palaeozoic calcareous alga Angulocellularia. Lethaia 15, 105–114. low‐temperature bacterial biofilm. Geobiology 6, 471–480. Saltzman, M.R., Young, S.A., Kump, L.R., Gill, B.C., Lyons, T.W., Runnegar, B., 2011. Pulse of Martın,́ J.M., Braga, J.C., Riding, R., 1993. Siliciclastic stromatolites and thrombolites, late atmospheric oxygen during the late Cambrian. Proceedings of the National Academy Miocene, S.E. Spain. Journal of Sedimentary Research (SEPM) 63, 131–139. of Sciences 108, 3876–3881. Mata, S.A., Bottjer, D.J., 2012. Microbes and mass extinctions: paleoenvironmental Sánchez-Román, M., Vasconcelos, C., Schmid, T., Dittrich, M., McKenzie, J.A., Zenobi, R., distribution of microbialites during times of biotic crisis. Geobiology 10, 3–24. Rivadeneyra, M.A., 2008. Aerobic microbial dolomite at the nanometer scale: implica- Mata, S.A., Harwood, C.L., Corsetti, F.A., Stork, N.J., Eilers, K., Berelson, W., Spear, J.R., 2012. tions for the geologic record. Geology 36, 879–882. Influence of gas production and filament orientation on stromatolite microfabric. Schaefer, M.O., Gutzmer, J., Beukes, N.J., 2001. Late Paleoproterozoic Mn-rich oncoids: Palaios 27, 206–217. earliest evidence for microbially mediated Mn precipitation. Geology 29, 835–838. Mazumdar, A., Strauss, H., 2006. Sulfur and strontium isotopic compositions of carbonate Schubert, J.K., Bottjer, D.J., 1992. Early Triassic stromatolites as post-mass extinction and evaporite rocks from the late Neoproterozoic-early Cambrian Bilara Group disaster forms. Geology 20, 883–886. (Nagaur-Ganganagar Basin, India): Constraints on intrabasinal correlation and global Shapiro, R.S., Fricke, H.C., Fox, K., 2009. Dinosaur-bearing oncoids from ephemeral lakes of sulfur cycle. Precambrian Research 149, 217–230. the Lower Cretaceous Cedar Mountain Formation, Utah. Palaios 24, 51–58. Meister, P., Johnson, O., Corsetti, F., Nealson, K., 2011. Magnesium inhibition controls Sheehan, P.M., Harris, M.T., 2004. Microbialite resurgence after the Late Ordovician spherical carbonate precipitation in ultrabasic springwater (Cedars, California) and extinction. Nature 430, 75–78. culture experiments. Advances in Stromatolite Geobiology 131, 101–121. Shen, J., Webb, G., 2004. Famennian (Upper Devonian) stromatolite reefs at Shatang, Meng, X., Ge, M., Tucker, M.E., 1997. Sequence stratigraphy, sea-level changes and Guilin, Guangxi, South China. Sedimentary Geology 170, 63–84. depositional systems in the Cambro-Ordovician of the North China carbonate Shi, G.R., Chen, Z.Q., 2006. Lower Permian oncolites from South China: implications for platform. Sedimentary Geology 114, 189–222. equatorial sea-level responses to Late Palaeozoic Gondwanan glaciation. Journal of Montañez, I.P., Osleger, D.A., Banner, J.L., Mack, L.E., Musgrove, M., 2000. Evolution of the Asian Earth Sciences 26, 424–436. Sr and C isotope composition of Cambrian oceans. GSA Today 10, 1–7. Shi, X.Y., Chen, J.Q., Mei, S.L., 1997. Cambrian sequence chronostratigraphic framework of

Obst, M., Wehrli, B., Dittrich, M., 2009. CaCO3 nucleation by cyanobacteria: laboratory the North China Platform. Earth Science Frontiers 4, 161–173 (in Chinese with evidence for a passive, surface-induced mechanism. Geobiology 7, 324–347. English abstract). Ohfuji, H., Rickard, D., 2005. Experimental syntheses of framboids—a review. Earth- Shi, X.Y., Mei, S.L., Chen, J.Q., Yang, X.D., 1999. Cambrian sequence stratigraphy and sea Science Reviews 71, 147–170. level cycles of the North China Platform. Journal of China University of Geosciences Okumura, T., Takashima, C., Shiraishi, F., Nishida, S., Yukimura, K., Naganuma, T., Koike, H., 10, 110–118. Arp, G., Kano, A., 2011. Microbial processes forming daily lamination in an aragonite Spadafora, A., Perri, E., McKenzie, J.A., Vasconcelos, C.G., 2010. Microbial biomineralization travertine, Nagano-yu Hot Spring, Southwest Japan. Geomicrobiology Journal 28, processes forming modern Ca:Mg carbonate stromatolites. Sedimentology 57, 27–40. 135–148. Sprachta, S., Camoina, G., Golubicc, S., Campiond, T.L., 2001. Microbialites in a modern la- Okumura, T., Takashima, C., Shiraishi, F., Akmaluddin, Kano, A., 2012. Textural transition goonal environment: nature and distribution, Tikehau atoll (French Polynesia). in an aragonite travertine formed under various flow conditions at Pancuran Pitu, Palaeogeography, Palaeoclimatology, Palaeoecology 175, 103–125. Central Java, Indonesia. Sedimentary Geology 265–266, 195–209. Sundberg, F.A., 2005. The Topazan Stage, a new Laurentian stage (Lincolnian series— Palmer, A.R., 1998. Terminal Early Cambrian extinction of the Olenellina: documentation “Middle” Cambrian). Journal of Paleontology 79, 63–71. from the Pioche Formation, Nevada. Journal of Paleontology 72, 650–672. Sundberg, F.A., Zhao, Y.L., Yuan, J.L., Lin, J.P., 2011. Detailed trilobite biostratigraphy across Peng, S.C., 2009. The newly-developed Cambrian biostratigraphic succession and chrono- the proposed GSSP for Stage 5 (“Middle Cambrian” boundary) at the Wuliu– stratigraphic scheme for South China. Chinese Science Bulletin 54, 4161–4170. Zengjiayan section, Guizhou, China. Bulletin of Geosciences 86, 423–464. Peng, S., Babcock, L.E., Cooper, R.A., 2012. The Cambrian Period. In: Gradstein, F.M., Ogg, J. Tang, D.J., Shi, X.Y., Jiang, G.Q., 2013a. Mesoproterozoic biogenic thrombolites from the G., Schmitz, M., Ogg, G. (Eds.), The Geologic Time Scale 2012. Elsevier, London, North China Platform. International Journal of Earth Science 102, 401–413. Heidelberg, pp. 437–488. Tang, D.J., Shi, X.Y., Jiang, G.Q., Zhang, W.H., 2013b. Microfabrics in Mesoproterozoic Perejón, A., Moreno-Eiris, E., Bechstädt, T., Menéndez, S., Rodríguez-Martínez, M., 2012. microdigitate stromatolites: evidence of biogenicity and organomineralization at New Bilbilian (Early Cambrian) archaeocyath-rich thrombolitic microbialite from micron and nanometer scales. Palaios 28, 178–194. the Láncara Formation (Cantabrian Mts., northern Spain). Journal of Iberian Geology Thompson, C.K., Kah, L.C., 2012. Sulfur isotope evidence for widespread euxinia and a fluc- 38, 313–330. tuating oxycline in Early to Middle Ordovician greenhouse oceans. Palaeogeography, Perri, E., Manzo, E., Tucker, M.E., 2011. Multi-scale study of the role of the biofilm in the Palaeoclimatology, Palaeoecology 313–314, 189–214. formation of minerals and fabrics in calcareous tufa. Sedimentary Geology 263–264, Tucker, M.E., Wright, V.P., 1990. Carbonate Sedimentology. Wiley-Blackwell, Oxford pp. 16–29. 1–482. Perri, E., Tucker, M.E., Spadafora, A., 2012. Carbonate organo-mineral micro- and Védrine, S., Strasser, A., Hug, W., 2007. Oncoid growth and distribution controlled by sea- ultrastructures in sub-fossil stromatolites: Marion Lake, South Australia. Geobiology level fluctuations and climate (Late Oxfordian, Swiss Jura Mountains). Facies 53, 10, 105–117. 535–552. Peryt, T.M., 1981. Phanerozoic oncoids—an overview. Facies 4, 197–213. Visscher, P.T., Stolz, J.F., 2005. Microbial mats as bioreactors: populations, processes, and Phoenix, V.R., Adams, D.G., Konhauser, K.O., 2000. Cyanobacterial viability during products. Palaeogeography, Palaeoclimatology, Palaeoecology 219, 87–100. hydrothermal biomineralization. Chemical Geology 169, 329–338. Visscher, P.T., Reid, R.P., Bebout, B.M., Hoeft, S.E., Macintyre, I.G., Thompson, J.A., 1998. Planavsky, N., Ginsburg, R.N., 2009. Taphonomy of modern marine Bahamian Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): microbialites. Palaios 24, 5–17. the role of sulfur cycling. American Mineralogist 83, 1482–1493. Popa, R., Kinkle, B.K., Badescu, A., 2004. Pyrite framboids as biomarkers for iron–sulfur Walker, J., Geissman, J., 2009. GSA geologic time scale. GSA Today 19, 60–61. system. Geomicrobiology Journal 21, 193–206. Wang, H.Z., Mo, X.X., 1995. An outline of the tectonic evolution of China. Episodes 18, Powell, W.G., Johnston, P.A., Collom, C.J., Johnston, K.J., 2006. Middle Cambrian brine seeps 6–16. on the Kicking Horse Rim and their relationship to talc and magnesite mineralization Wang, H.Z., Shi, X.Y., Wang, X.L., Yin, H.F., Qiao, X.F., 2000. Research on the Sequence and associated dolomitization, British Columbia, Canada. Economic Geology 101, Stratigraphy of China. Guangdong Science and Technology Press, Guangzhou pp. 431–451. 1–457 (in Chinese). Power, I.M., Wilson, S.A., Dipple, G.M., Southam, G., 2011. Modern carbonate microbialites Wang, Y.B., Tong, J.N., Wang, J.S., Zhou, X.G., 2005. Calcimicrobialite after end-Permian from an asbestos open pit pond, Yukon, Canada. Geobiology 9, 180–195. mass extinction in South China and its palaeoenvironmental significance. Chinese Pratt, B.R., 2001. Calcification of cyanobacterial filaments: Girvanella and the origin of Science Bulletin 50, 665–671. lower Paleozoic lime mud. Geology 29, 763–766. Wang, X.L., Hu, W.X., Yao, S.P., Chen, Q., Xie, X.M., 2011. Carbon and strontium isotopes Préat, A., Mamet, B., Di Stefano, P., Martire, L., Kolo, K., 2011. Microbially-induced Fe and and global correlation of Cambrian Series 2–Series 3 carbonate rocks in the Keping Mn oxides in condensed pelagic sediments (Middle–Upper Jurassic, Western Sicily). area of the northwestern Tarim Basin, NW China. Marine and Petroleum Geology Sedimentary Geology 237, 179–188. 28, 992–1008. Pruss, S.B., Bottjer, D.J., Corsetti, F.A., Baud, A., 2006. A global marine sedimentary response Wang, L., Shi, X.Y., Jiang, G.Q., 2012a. Pyrite morphology and redox fluctuations recorded to the end-Permian mass extinction: examples from southern Turkey and the west- in the Ediacaran Doushantuo Formation. Palaeogeography, Palaeoclimatology, ern United States. Earth-Science Reviews 78, 193–206. Palaeoecology 333, 218–227. Pruss, S.B., Clemente, H., Laflamme, M., 2012. Early (Series 2) Cambrian archaeocyathan Wang, X.H., Gan, L., Wiens, M., Schlossmacher, U., Schröder, H.C., Müller, W.E., 2012b. reefs of southern Labrador as a locus for skeletal carbonate production. Lethaia 45, Distribution of microfossils within polymetallic nodules: biogenic clusters within 401–410. manganese layers. Marine Biotechnology 14, 96–105. Renaut, R.W., Jones, B., Rosen, M.R., 1996. Primary silica oncoids from Orakeikorako hot Whalen, M.T., Day, J., Eberli, G.P., Homewood, P.W., 2002. Microbial carbonates as indica- springs, North Island, New Zealand. Palaios 11, 446–458. tors of environmental change and biotic crises in carbonate systems: examples from Reolid, M., Nieto, L.M., 2010. Jurassic Fe–Mn macro-oncoids from pelagic swells of the the Late Devonian, Alberta basin, Canada. Palaeogeography, Palaeoclimatology, External Subbetic (Spain): evidences of microbial origin. Geologica Acta 8, 151–168. Palaeoecology 181, 127–151. 450 W. Zhang et al. / Gondwana Research 28 (2015) 432–450

Wignall, P.B., 2001. Large igneous provinces and mass extinctions. Earth-Science Reviews Xie, S.C., Pancost, R.D., Yin, H., Wang, H., Evershed, R.P., 2005. Two episodes of microbial 53, 1–33. change coupled with Permo/Triassic faunal mass extinction. Nature 434, 494–497. Wignall, P.B., Newton, R., Brookfield, M.E., 2005. Pyrite framboid evidence for oxygen poor Xie, S.C., Pancost, R.D., Wang, Y.B., Yang, H., Wignall, P.B., Luo, G.M., Jia, C.L., Chen, L., 2010. deposition during the Permian–Triassic crisis in Kashmir. Palaeogeography, Cyanobacterial blooms tied to volcanism during the 5 m.y. Permo-Triassic biotic cri- Palaeoclimatology, Palaeoecology 216, 183–188. sis. Geology 38, 447–450. Wilkin, R., Barnes, H.L., 1997. Formation processes of framboidal pyrite. Geochimica et Yang, R.C., Fan, A.P., Han, Z.Z., Chi, N.J., 2011. Status and prospect of studies on oncoid. Cosmochimica Acta 61, 323–339. Advances in Earth Science 26, 465–474. Wilkin, R.T., Barnes, H.L., Brantley, S.L., 1996. The size distribution of framboidal pyrite in Yang, R.C., Fan, A.P., Han, Z.Z., Chi, N.J., 2013. Characteristics and genesis of microbial modern sediments: an indicator of redox conditions. Geochimica et Cosmochimica lumps in the Maozhuang Stage (Cambrian Series 2), Shandong Province, China. Acta 60, 3897–3912. Science China Earth Sciences 56, 494–503. Woo, J., Chough, S.K., Han, Z., 2008. Chambers of Epiphyton thalli in microbial buildups, Young, J.D., Martel, J., 2010. The rise and fall of nanobacteria. Scientific American Zhangxia Formation (Middle Cambrian), Shandong Province, China. Palaios 23, Magazine 302, 52–59. 55–64. Youngs, B.C., 1978. The petrology and depositional environments of the Middle Cambrian Wood, R., 2000. Novel paleoecology of a postextinction reef: Famennian (Late Devonian) Wirrealpa and Aroona Creek limestones (South Australia). Journal of Sedimentary of the Canning basin, northwestern Australia. Geology 28, 987–990. Petrology 48, 63–74. Wood, R., 2004. Palaeoecology of a post-extinction reef: Famennian (Late Devonian) of Yuan, J.L., Zhao, Y.L., Li, Y., Huang, Y.Z., 2002. Trilobite Fauna of the Kaili Formation the Canning Basin, north-western Australia. Palaeontology 47, 415–445. (Uppermost Lower Cambrian–Lower Middle Cambrian) from Southeastern Guizhou, Woods, A.D., Baud, A., 2008. Anachronistic facies from a drowned Lower Triassic carbon- South China. Shanghai Science and Technology Publishing House, Shanghai pp. 1–422 ate platform: lower member of the Alwa Formation (Ba'id Exotic), Oman Mountains. (in Chinese with English summary). Sedimentary Geology 209, 1–14. Zatoń, M., Kremer, B., Marynowski, L., Wilson, M.A., Krawczyński, W., 2012. Middle Wotte, T., Álvaro, J.J., Shields, G.A., Brown, B., Brasier, M.D., Veizer, J., 2007. C-, O- and Sr- Jurassic (Bathonian) encrusted oncoids from the Polish Jura, southern Poland. Facies isotope stratigraphy across the Lower–Middle Cambrian transition of the Cantabrian 58, 57–77. Zone (Spain) and the Montagne Noire (France), West Gondwana. Palaeogeography, Zhang, W.T., Zhu, Z.L., Wu, H.J., Yuan, J.L., Shen, H., Yao, B.Q., Luo, K.Q., Wang, X.P., 1980. Palaeoclimatology, Palaeoecology 256, 47–70. The Cambrian strata at southern and western margins of the Ordos platform. Journal Wotte, T., Strauss, H., Sundberg, F.A., 2011. Carbon and sulphur isotopes from the Cambri- of Stratigraphy 4, 106–119 (in Chinese). an Series 2–Cambrian Series 3 of Laurentia and Siberia. Museum of Northern Arizona Zhu, M.Y., Zhang, J.M., Li, G.X., Yang, A.H., 2004. Evolution of C isotopes in the Cambrian of Bulletin 67, 47–63. China: implications for Cambrian subdivision and trilobite mass extinctions. Geobios Wotte, T., Strauss, H., Fugmann, A., Garbe-Schönberg, D., 2012. Paired δ34S data from car- 37, 287–301. bonate associated sulfate and chromium–reducible sulfur across the traditional Zhu, M.Y., Babcock, L.E., Peng, S.C., 2006. Advances in Cambrian stratigraphy and Lower–Middle Cambrian boundary of W-Gondwana. Geochimica et Cosmochimica paleontology: integrating correlation techniques, paleobiology, taphonomy and Acta 85, 228–253. paleoenvironmental reconstruction. Palaeoworld 15, 217–222. Xiang, L.W., Li, S.J., Nan, R.S., 1981. The Cambrian System of China. Geological Publishing Zhuravlev, A.Y., Wood, R.A., 1996. Anoxia as the cause of the mid–Early Cambrian House, Beijing pp. 1–193 (in Chinese). (Botomian) extinction event. Geology 24, 311–314. Xiang, L.W., Zhu, M.L., Li, S.J., 1999. Stratigraphical Lexicon of China–Cambrian. Geological Publishing House, Beijing pp. 1–95 (in Chinese).