The Ediacaran-Cambrian rise of siliceous sponges and development of modern oceanic ecosystems

Precambrian Research 333 (2019) 105438

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The Ediacaran-Cambrian rise of siliceous sponges and development of modern oceanic ecosystems Shan Changa,b, Lei Zhanga,b, Sébastien Clausenc, David J. Bottjerd, Qinglai Fenga,b,

T

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a

School of Earth Sciences, China University of Geosciences, Wuhan 430074, China State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences, Wuhan 430074, China c Université de Lille, UMR CNRS 8198-Evo-Eco-Paleo, F-59000 Lille, France d Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089, USA b

A R T I C LE I N FO

A B S T R A C T

Keywords: Ediacaran Chert Sponge spicules Ecosystem engineers Ecological trigger Cambrian explosion

The lack of unequivocal sponge fossils before the Cambrian despite their probable deep origin during the Cryogenian period has been a conundrum to geologists. Their impact on the dramatic evolution of ecosystems and the seawater silica cycle during the Ediacaran-Cambrian (E-C) transition is also speculative. In this study, abundant sponge spicules and spicule-like structures that probably represent original sponge fossils were recovered from four sections of the E-C boundary interval in the Yangtze Gorges, South China. The paleontological and geochemical data presented herein provides evidence for a continuous distribution of relatively abundant sponge spicules, some even forming spiculites, as well as the earliest biogenic deposition of silica by metazoans in the Ediacaran-Cambrian boundary interval. These results further confirm that a biological takeover of oceanic dissolved Si co-occurred with the evolution of silica biomineralization in the E-C interval, resulting in the widespread deposition of biogenic chert. Hydrothermal input in spicule-bearing cherts is also observed. Such hydrothermal activity might have favored the blooming of sponges through significant nutrient supply. These results provide the first conjunction of geochemical and paleontological proxies in support of previous models considering that sponges, by ventilation, filtration and oxygenation of seawater, were important ecosystem engineers of the E-C bioradiation event and of the related establishment of modern-type ecosystems.

1. Introduction

last common ancestor of animals (Taylor et al., 2007). In addition, different models suggest sponges played a key role in the evolution of geobiological cycles and ecosystem diversification during the Cambrian explosion, which lack the support from an incomplete fossil record. As filter feeders and bioeroders (Bell, 2008), sponges undoubtedly contributed to the formation of the typical Phanerozoic, well-mixed, clear oceanic water column and to its oxygenation through ventilation (Erwin and Tweedt, 2012; Tatzel et al., 2017). They therefore acted as one of the earliest major ecosystem engineers (sensu Jones et al., 1994). It has even been suggested that oceanic ventilation by siliceous sponges might have engendered the conspicuous geochemical perturbations which occurred during the Neoproterozoic–Paleozoic transition, including a progressive deepening of the oxygen minimum zone (Lenton et al., 2014; Tatzel et al., 2017). The latter would accordingly be better interpreted as consequences rather than the cause of metazoan evolution. The E-C interval further records a shift in the marine silica cycle, a

Porifera are among the earliest-branching metazoan taxa. Although their relationships to the other non-bilaterian animals and the exact branching pattern of their main clades (Wörheide et al., 2012) have been debated, recent phylogenetic analyses based on genes tend to agree on the monophyly of the demosponges as the sister-group of the hexactinellids, forming the Silicea clade (Gray, 1867). Molecular divergence estimates date the origin of the Silicea well within the Cryogenian (692 Ma in Sperling et al., 2010; 704 Ma in Ma and Yang, 2015), consistent with the biomarker record (713–635 Ma, Love et al., 2009; Zumberge et al., 2018; but see Nettersheim et al., 2019). They would have been a major component of shallow to deep marine ecosystems some time since the Neoproterozoic and are still significant in modern aquatic environments (Muir et al., 2017). To elucidate the phylogeny and time of divergence of sponges is definitely instrumental to understand early animal evolution and to decipher the paleogenomics of the

⁎ Corresponding author at: Room 202, State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences, No. 388 Lumo Road, Wuhan, Hubei, China. E-mail address: [email protected] (Q. Feng).

https://doi.org/10.1016/j.precamres.2019.105438 Received 24 April 2019; Received in revised form 11 August 2019; Accepted 23 August 2019 Available online 24 August 2019 0301-9268/ © 2019 Published by Elsevier B.V.

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Fig. 1. Paleogeographic map of the Yangtze Block and the studied area (A) (after Wang J. et al., 2012) and location of the studied four sections (B).

cycles is somewhat unresolved. Four chert-rich sections of the E-C boundary interval from the Three Gorges area, South China, spanning depositional conditions from the tidal zone to offshore basin, were sampled in high resolution and analysed herein for paleontological and geochemical purposes. Relatively highly abundant sponge spicules and spicule-like structures that represent possible original sponge spicules, were determined from both chert and carbonate deposits through observation of hand samples, thin sections, and acid-etching. Quantitative data on spicule and spicule-like structure abundance (individuals/g) and size (length and diameter) were obtained from specimens extracted through acid maceration. Geochemical analyses (major elements, trace elements) were processed in parallel to paleontological studies, which indicate most of the cherts of the Yanjiahe Formation are of biogenic origin, most probably influenced by sponges. A geochemical signature of hydrothermal activity suggests the related input of silica-rich fluids and nutrients might have contributed to the flourishing of sponges. Finally, the rise of siliceous sponges during the Ediacaran to Cambrian transitional interval might have favored the burial of organic carbon (Tatzel et al., 2017), accelerated the ventilation of seawater (Butterfield, 2011), as well as increased the structural complexity of habitats and biodiversity of metazoans (Beazley et al., 2015). Such engineering effects might have eventually contributed to the first establishment of modern-type ocean ecosystems and the triggering of the Cambrian explosion.

biogeochemical transition difficult to elucidate through a uniformitarian approach. In today’s oceans, dissolved Si concentrations are largely biologically controlled, while the Precambrian Si cycle was dominated by inorganic reactions and diagenetic silicification (Maliva et al., 1989, 2005; Conley et al., 2017). A biological takeover of dissolved oceanic Si occurred with the evolution and expansion of silica biomineralizing eukaryotes, which have contributed to the subsequent deposition of biogenic Si, resulting in stepwise drops in ocean dissolved Si concentrations (Conley et al., 2017). Biological use of silica occurs in different marine protists such as diatoms, testate amoebae, radiolarians and their relatives (Knoll, 2014; Morais et al., 2017), while siliceous sponges are the only significant silica-biomineralizing metazoans. Biosilicification by siliceous organisms may have been the mechanism for the formation of the widely-distributed cherts from the E-C interval (Guo et al., 2007). However, this is debated, alternative hypotheses including hydrothermal origin and diagenetic silica replacement (e.g. Chen et al., 2009; Wen et al., 2016). To date, no paleontological evidence has been provided in support of the biogenic origin of the abundant E-C cherts. Except for a few Neoproterozoic, siliceous vase-shaped microfossils, the earliest record of siliceous protists, assigned to the radiolarians is from the Cambrian Age 2 (Cao et al., 2014; Aitchison et al., 2017). A sponge-grade microfossil from the Doushantuo Formation in Weng’an is preserved at cellular resolution (Yin et al., 2015), while its phosphatized body provides little information on its biomineralization. The first appearance date of siliceous sponges, which are otherwise abundantly preserved as disarticulated spicules in Cambrian sediments, and when they became ecologically significant enough to influence the Si cycle, are still debated. Recently, demosponge biomarker 26-methylstigmastane was detected, along with 24-isopropylcholestane, in abundance in Neoproterozoic-Cambrian strata, suggesting that demosponges first achieved ecological prominence in Neoproterozoic marine environments, at least between 660 and 635 Ma (Zumberge et al., 2018; but see Nettersheim et al., 2019). However, it still remains to be reconciled from the fossil record when spiculate sponges first occurred and what their spicules looked like. Even if spicules are considered the most easily identifiable and most commonly preserved remains of crown-group sponges, they are not unequivocally reported before the Cambrian (Antcliffe et al., 2014 and references cited therein; Muscente et al., 2015; Botting and Muir, 2018). This may reflect an evolutionary pattern, as silica biomineralization by sponges may not have evolved or may have remained weak; or on the other hand, an ecological trend, as spiculate sponges may have stayed ecologically restricted until the early Cambrian (Muscente et al., 2015). As a consequence, the precise process, extent and timing of significant changes in the silica and oxygen geobiological

2. Geological setting 2.1. Lithology of the four studied sections The Precambrian-Cambrian stratigraphic succession is well exposed in numerous complete and continuous sections, including many significant lagerstätten, in the eastern Yangtze Gorges area of southern China. This area is therefore key for high resolution analysis of the Ediacaran-Cambrian boundary, which is particularly well-exposed in the Yanjiahe Formation (Wang et al., 2002; Zhu et al., 2003). Outcrops of the Yanjiahe Formation are mostly distributed around the southern and western flanks of the Huangling anticline as well as in the core of the Changyang anticline (Fig. 1). The Yanjiahe Formation was defined by Chen (1984) at Yanjiahe village near the town of Sandouping as 38.7 m in thickness. However, this original definition made the boundary between the Yanjiahe Formation and the underlying Dengying Formation difficult to distinguish. Wang et al. (2002) therefore revised the definition of the Yanjiahe Formation, moving the boundary downwards by about 15.3 m. The Yanjiahe Formation as revised by Wang et al. (2002), a concept 2

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Fig. 2. Lithological columns showing positions of samples in the four studied sections and paleoenvironmental reconstruction of these studied sections. Reconstruction on the Songlinpo section (the Tianzhushan Member) and the Gunshi’ao section (the Yanjiahe Formation) is based on Wang et al. (2001) and Zhu (2010), respectively. δ13C isotope profiles are based on Wang D. et al. (2012) and Ishikawa et al. (2008) study of Gunshi’ao section and close-by drilled core respectively.

in thickness in the Gunshi’ao section and 20 m in the Qiaojiaping section. In the Luojiacun section, cherts are far thinner (less than 1 m) than in the Gunshi’ao and Qiaojiaping sections. The Tainzhushan Member at the Songlinpo section is about 2.5 m in thickness and can be divided into two parts: the lower part is dominated by micritic dolostone and the upper part is composed of dolostone with siliceous-phosphate intraclastic dolostone. From the Songlinpo section to the Gunshi’ao section, paleogeographical studies show it represents foreshore (Tianzhushan Member, Wang et al., 2001) to restricted offshore environments (Yanjiahe Formation, Zhu, 2010) (Fig. 2).

followed herein, is 54 m in thickness. Its lower boundary is now well characterized by the interbedding of chert and dolostone, contrasting with the thick-bedded dolostone of the uppermost Dengying Formation. The Yanjiahe Formation disconformably overlies the Dengying Formation and is overlain by the trilobite-bearing Shuijingtuo Formation. In the eastern flank of the Huangling anticline, a synchronous depositional unit was named the Tianzhushan Member. The Tianzhushan Member disconformably overlies the Baimatuo Member and is overlain by the Shuijingtuo Formation. Four sections have been studied herein (Fig. 1B). They are, from west to east, the Luojiacun (Chang et al., 2017), the Qiaojiaping, the Gunshi’ao and Sunglinpo sections. The chert deposits of the Yanjiahe Formation are thinner on the western flank of the Huangling anticline (the Luojiacun section) and get more abundant and thicker southward (in the Gunshi’ao and Qiaojiaping sections) Among these section, the Gunshi’ao section is the thickest, with well-developed chert levels, and the most representative of the Yanjiahe Formation, It has therefore been the most studied and is well stratigraphically constrained (see following section). The Yanjiahe Formation in the Gunshi’ao section is 54.4 m thick and can be divided into 8 beds (Fig. 2). Bed 1 is about 2.2 m thick and consists of sandy dolostones and shales. The overlying 6.6 m-thick Bed 2 consists of dolostones intercalated with banded cherts and shales. Bed 3 is 19 m thick and consists of cherts interbedded with silty shales. Bed 4 is 2.65 m in thickness and is dominated by siliceous to phosphatic, intraclastic dolostones. The 1.84 m-thick Bed 5 consists of cherts alternating with carbonaceous shales. Bed 6 is about 15 m thick and is composed of limestones interbedded with silty shales containing siliceous nodules. The 4.7 m-thick Bed 7 mainly consists of carbonaceous limestone. Finally, the topmost Bed 8 is about 2.2 m thick and consists of siliceous to phosphatic, intraclastic limestone. The Yanjiahe Formation in the Qiaojiaping section is similar to that of the Gunshi’ao section, although its lowermost part is covered. The cherts are about 32 m

2.2. Stratigraphy of the Ediacaran-Cambrian boundary interval in the four studied sections of the Three Gorges area, South China The Cambrian GSSP (Global Boundary Stratotype Section and Point) of the Ediacaran–Cambrian boundary is defined at the lowest occurrence of the ichnofossil Treptichnus pedum or the base of the T. pedum Ichnozone at Fortune Head, Southeast Newfoundland, Canada (Brasier et al., 1994; Landing et al., 2013). However, due to problems associated with facies restriction, preservation and taxonomy, the utility of T. pedum in many areas other than Avalonia and Baltica has been questioned (Peng and Babcock, 2011; Babcock et al., 2014). In South China, the lowest occurrence of T. pedum is up to 12 m higher above the lowest occurrence of typical Terreneuvian small shelly fossils (SSFs) (Zhu, 1997; Zhu et al., 2001; Babcock et al., 2014). Therefore, it is difficult to use T. pedum and the associated ichnofossil assemblage as a correlation tool for the Ediacaran–Cambrian transition in South China. Instead, the regional correlation of this interval is largely dependent on SSFs or acritarchs (Moczydłowska, 1991; Vidal and Moczydłowska-Vidal, 1997; Moczydłowska et al., 2011), along with the record of the worldwide Basal Cambrian Carbon isotope Excursion (BACE; Li et al., 2009, 2013; Maloof et al., 2010; Peng et al., 2012; Babcock et al., 2014). This δ13C 3

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nadir has been regarded as a proxy for the global Ediacaran–Cambrian boundary (e.g., Brasier et al., 1992, 1996; Strauss et al., 1992; Grotzinger et al., 1995; Babcock et al., 2014; Landing et al., 2013). However, there is no agreement yet whether the onset of the BACE excursion, its nadir, or its demise is most practicable to define the boundary (Peng and Babcock, 2014; Zhu et al., 2019 and reference therein), so here it is better considered as characterizing the EdiacaranCambrian boundary-interval. The most recent discovery of fossil assemblages dominated by typical Ediacaran taxa (Cai et al., 2019) from the Beiwan Member of the Dengying Formation (Northern Yangtze Block, South China), at the onset of the BACE excursion supports the use of the nadir or the demise (as in Cai et al., 2019) of this excursion as the marker of the Ediacaran-Cambrian boundary. This would extend the Ediacaran system to the lower Yanjiahe Formation in the studied area (see below). SSFs, acritarchs and carbon isotope data have been reported from the Yanjiahe Formation in the Yangtze Gorges area, representing one of the best stratigraphic sequences across the Ediacaran–Cambrian boundary interval in South China (Wang et al., 2002; Zhu et al., 2003; Ishikawa et al., 2008; Wang D. et al., 2012). High-resolution δ13C chemostratigraphy has been reported based on a drill core nearby the herein studied Gunshi’ao section, one of the reference sections of the southern and western flanks of the Huangling anticline. There, the BACE peak is recognized at a horizon 13.8 m above the Dengying–Yanjiahe boundary and has been considered as marking the Ediacaran-Cambrian boundary (Ishikawa et al., 2008); later the position was revised by Wang D. et al. (2012) as 27 m above the Dengying–Yanjiahe boundary in the Gunshi’ao section. The Asteridium–Heliosphaeridium–Comasphaeridium acritarchs assemblage zone (AHC), which is widely recorded (Yin, 1987; Ding et al., 1992; Palacios and Vidal, 1992; Vidal and Moczydłowska-Vidal, 1997; Tiwari, 1999; Yao et al., 2005; Moczydłowska and Zang, 2006; Dong et al., 2009; Palacios et al., 2011; Ahn and Zhu, 2017), has been used in South China as indicating the Ediacaran-Cambrian boundary (Ahn and Zhu, 2017), by correlation with Poland, where it starts just below the lowest occurrence of T. pedum and just above Ediacaran fossils Harlaniella podolica and Palaeopascichnus delicatus (Moczydłowska, 1991; Moczydłowska et al., 2011). Ahn and Zhu (2017) confirmed the AHC indicates the upper part of the BACE excursion, and can be used instead when carbon isotope data are not available. The AHC ranges 22.2–31.0 m above the Dengying–Yanjiahe boundary in the Gunshi’ao section (Fig. 3). This congruent with the identification of the BACE peak at ca. 27 m above the boundary of the Yanjiahe Formation by Wang et al. (2012). It is therefore used herein to characterize the Ediacaran-Cambrian boundary interval. SSFs belonging to the Anabarites trisulcatus–Protohertzina anabarica zone (Cambrian SSF Zone I of South China) are reported from the phosphatic clasts of Bed 4 of the Yanjiahe Formation in the Gunshi’ao section, at the uppermost part of the AHC. This Bed 4 is therefore correlated with the lower Zhongyicun Member of Yunnan, with the lower Nemakit–Daldynian of Siberia and with the base of the global Fortunian (Chen, 1984; Wang D. et al., 2012). Purella antiqua (SSF zone II of South China) and other SSFs are reported from the phosphatic chert nodules of Bed 6 of the Yanjiahe Formation in the Gunshi’ao section (corresponding to Bed 3 in Guo et al., 2014), which can be correlated with the upper Zhongyicun Member in eastern Yunnan and the upper Nemakit–Daldynian of Siberia, upper Fortunian (Yang et al., 2014). The Aldanella yanjiaheensis assemblage zone is reported from Bed 8, which can be correlated with international provisional Stage 2 (Guo et al., 2014; Steiner et al., 2007). As Bed 7 is barren, the exact position of the Fortunian-Stage 2 boundary is however unclear. To conclude, the stratigraphy of the Gunshi’ao section has been deeply studied and, even though there has been some discussion (Jiang et al., 2012), chemostratigraphic and biostratigraphic data converge to place the Ediacaran-Cambrian boundary within the first meters of the Yanjiahe Formation, although sometimes it is considered at the base of the latter (Zhao et al., 2018). In the Luojiacun section, less than 10 km away

Fig. 3. Thin-section photomicrographs of Cambrian acanthomorphic acritarchs from the Yanjiahe Formation in the Gunshi’ao section. A. Asteridium tornatum; B-C. Heliosphaeridium ampliatum; D. Comasphaeridium annulare. Scale bar: 10 µm.

from the Gunshi’ao section, the Anabarites trisulcatus–Protohertzina anabarica zone (SSF Zone I of South China) occurs just a few meters above the base of the Yanjiahe Fm. (Liu et al., 2018). In the Qiaojiaping section, the base of the Yanjiahe Fm. is covered. In absence of further biostratigraphic information, the complete outcrop there is considered herein as Cambrian. In the Songlinpo section, located on the eastern flank of the Huangling anticline, the Tianzhushan Member of the Dengying Formation is equivalent to the upper part of the thicker Yanjiahe Formation outcropping on the south-western flank of the anticline (Qian et al., 1979). This member overlies a major depositional hiatus affecting the Ediacaran-Cambrian interval and belongs to the SSFs Circotheca-Anabarites-Protoherzina-Paragloborilus-Siphogonouchites Assemblage Zone (Qian et al., 1979), which is Terreneuvian in age (Chen, 1984; Steiner et al., 2007; Yang et al., 2014; Dong et al., 2019). The exact position of the Ediacaran/Cambrian boundary is highly debatable (Babcock et al., 2014; Zhu et al., 2019), and requires more research on the correlation of carbon isotope excursion with biostratigraphy. Based on the stratigraphic tools mentioned above, the Yanjiahe Formation is generally considered to straddle the Ediacaran/Cambrian boundary (Ishikawa et al., 2008; Wang D. et al., 2012; Tian and Luo, 2017). Although the exact position of the latter remains unclear, biostratigraphic (SSF, acritarchs) and chemiostratigraphic (carbon isotope curve) data indicate the Ediacaran-Cambrian boundary straddles the Yanjiahe Formation and might be located in the Bed 3 of the Yanjiahe Formation in the Gunshi’ao section, whereas the exposed parts of the Yanjiahe Formation in the Luojiacun and the Qiaojiaping sections are considered Cambrian. 3. Materials and methods Samples were taken with high-resolution from the Yanjiahe Formation in the Gunshi’ao, Qiaojiaping and Luojiacun sections and the coeval Tianzhushan Mbr. in the Songlinpo section in the Three Gorges area. The abundance of spicules and their size range were analysed in chert, dolomite and limestone from the Ediacaran-Cambrian transition. Isolated sponge spicules were extracted by acid maceration of 129 samples (see Fig. 2 for sampling). A total of 69 chert samples were processed using a technique 4

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pointed ends are finely tapered, and axial canals can be observed (Fig. 4), thus possibilities of mineral origin can be ruled out. The first triaxon spicules, mostly preserved as fragments, occur in the upper Bed 3 of the Yanjiahe Formation in different studied sections (Fig. 5). We document the abundance of spicules thorough the Yanjiahe Formation in the Gunshi’ao section (Fig. 6), which is the most continuous among the studied sections. It should be noticed that spiculelike structures are difficult to distinguish from regular monaxon spicules under the binocular microscope, thus the quantitive value on abundance is only referential. However, there is still a trend that maximum size of recovered spicules tends to increase through the Yanjiahe Formation, with carbonate beds always yielding larger, mostly broken spicules compared with underlying and overlying cherts, probably due to taphonomic bias. The first occurrences of spiculites were identified at about 10 m above the base of the Yanjiahe Formation in the Gunshi’ao section. According to carbon isotope chemostratigraphy, SSFs and acritarch biostratigraphy, these oldest spicules are from the Ediacaran-Cambrian boundary interval. Although not as widespread and laterally continuous as those reported from younger strata, these spiculites represent the earliest metazoan biogenic deposits. They show flaser bedding with lateral transitions from dark brown spiculites to lighter chert (Fig. 7F-I). Similar spiculites composed of simple monaxons have been reported from the Mississipian Cowley Formation of southern Kansas (Mazzullo et al., 2009), and high silica and nutrient contents may have favored the flourishing of sponges and the formation of such spiculites (Mazzullo et al., 2009).

introduced by Pessagno and Newport (Pessagno and Newport, 1972), where 200 g samples were immersed in buffered 3% hydrofluoric acid for 8 h and then rinsed. After repetition of this process for 2 weeks the residues were sieved (diameter = 0.030 mm and 2 mm) and dried. A total of 60 limestone and dolomite samples, each of 1000 g, were immersed in a 9% solution of acetic acid. The diluted acetic acid was changed every 5 days and repeated for 2 months, then the residues were sieved (diameter = 0.030 mm and 2 mm) and dried. The calcareous dolomite from the Tianzhushan Mbr. is not easily dissolved, just a few residues were obtained in sample SLP-5, with only a few spicules observed both in residues and thin section in SLP-5. The abundances of spicules were calculated from 500 fields of view under a stereoscopic microscope. Sizes of spicules were measured from 50 fields under a Leica DVM6 microscope for average length and diameter. Isolated specimens were hand-picked under a binocular microscope and were mounted on stubs with latex, then examined with a Stereoscan Electron Microscope (SEM) in the State Key Laboratory of Geological Process and Mineral Resources. Geochemical analyses of 50 samples (including 42 chert samples and 8 siliceous carbonate samples, see Supplementary Table S1 for data) on major elements and trace elements were done by the State Key Laboratory of Geological Process and Mineral Resources. Rare earth elements have been normalized by PAAS (Taylor and McLennan, 1985), and Eu/Eu*, Ce/Ce* and Y/Y* were calculated using the formulae Ce/ Ce* = 2 × CeN/(LaN + PrN), Eu/Eu* = 2 × EuN/(SmN + GdN) and Y/Y* = 2 × YN/(DyN + HoN). 4. Spicules recovered from the studied sections 4.1. Distribution and abundance of spicules

4.2. Description of recovered spicules and comparison with similar structures

In this study, spicules were recovered from four laterally deposited successions of the Yangtze Gorges area and complete the first recent data obtained from the Luojiacun section (Chang et al., 2017). They were observed in cherts, limestones and dolostones from the whole Yanjiahe Formation and the middle Tianzhushan Member of the Dengying Formation, and were observed as isolated spicules, as well as on hand-samples and in thin sections. The spicules analysed here include sponge spicules and spicule-like structures (see description below). According to our observations, spicule-like structures massively occur in Bed 1 to Bed 3 (Table 1), the first occurrence for such structures is 1.6 m above the Dengying/Yanjiahe boundary. There are three explanations for their origin: minerals, void-filling structures, and original sponge spicules. Regular monaxons (oxea) first occurred in lowermost Bed 3 (GY3-1, 8.98 m above the Dengying/Yanjiehe boundary), which is slightly earlier than stauracines and triaxons. The monaxons recovered herein, described as siliceous sponge remains, include diactinal monaxons (oxea and stongyle); monactinal monaxons including drop-form, tylostyle and siciform, all of which have a fossil record and/ or modern analogues. In outline they are cylindrical in cross section and sometimes are finely curved, with rounded or pointed ends, and those

Diactinal monaxon: Oxea (Fig. 8A): axes straight or slightly curved, ends pointed. 150–400 µm in length. Oxea is a regular type of diactinal monaxon that can commonly be seen in living and fossil sponges. The surface can be smooth or rough due to dissolution. Strongyle (Fig. 8B): axes straight or slightly curved, ends rounded. 250–400 µm in length. The surface can be smooth or rough. Monactinal monaxons: Tylostyle (Fig. 8C): one end rounded with enlarged knob, one end pointed, axes slightly curved. Their length is 150–300 µm, diameter varies from 20 to 50 µm. Tylostyle spicules are common in many demosponges (Boury-Esnault and Rützler, 1997). The surface can be smooth or rough. Siciform (Fig. 8D): outline resembles a knife or a blade; axes are generally straight to slightly curved with rounded to elliptical cross sections. Their length is 150–300 µm and maximum diameter within the spicule is 40–80 µm. For a similar morphotype see Chang et al. (2017) and Ding and Qian (1988). The surface can be smooth or rough. Drop-form (Fig. 8E): outline resembles a drop of water with one end chubby and the other end pointed, axes straight or slightly curved.

Table 1 Distribution of spicules through the studied sections. Studied sections Gunshi’ao section

Qiaojiaping section Luojiacun section Songlinpo section

Bed Bed Bed Bed Bed Bed Bed Bed

1 2 3 4 5 6 7 8

Spicule-like structure

Modified spicules

√ √ √

√

√ √

Oxea

√ √ √ √

√ √ √ √

√

5

Drop-form

Tylostyle

Siciform

Stauractine

Triaxon

√

√

√

√ √ √

√ √ √ √

√ √

√

√ √ √

√ √ √

√

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Fig. 4. Sponge spicules show different condition of axial canal. A. monaxon with rounded ends, G-Y3-10; B. monaxon with pointed, tapered ends, close-up photo is shown in right rectangle, G-Y3-1; C. axial canal shown in broken end, a close-up photo is shown in D, L-Y2-1; E. oxea showing enlarged axial canal due to dissolution, G-Y3-1; F. axial canal filled with recrystallized quartz, dashed line shows quartz crystals, L-Y2-2, the same specimen with Fig. 3.W in Chang et al. (2017); G. monaxon cluster shows tapered ends and cylindrical cross section, axial canal was not preserved, L-Y2-1; H. triaxon spicule with both solid and enlarged canal, L-Y3-1; I. triaxon with concentric structure of axial canal, a close-up photo is shown in J, G-YC6-2. Scale bar: 100 µm except 20 µm in J.

Fig. 5. Stauractines, triaxons and broken sponge spicules from the Yanjiahe Formation. A. G-Y3-25; B. G-Y3-26; C-E: G-YC4; F-K. G-YC6-2; L. G-YC6-4; M-O. L-Y3-1; M-Q: L-4Y-12. N and O are from Fig. 3 A and C, respectively, in Chang et al. (2017). Scale bar: 200 µm except 50 µm in A, M-Q.

Comparison between these possibilities is developed below. Hollow tubes have also been described in radiolarians, with sponges being the oldest silicon biomineralizers (Afanasieva and Amon, 2013). However, as noted by Afanasieva and Amon (2013), such hollow structures rarely occur but seem to have been repeatedly developed by radiolarians during their evolution. The presence of an axial canal is therefore not considered an apomorphy of the group. The oldest reported radiolarians with hollow spines are from the middle Cambrian of Australia (Won and Below, 1999), and one specimen of undescribed genus and species from the upper Cambrian of Newfoundland (Won and Iams, 2002). Their spines are fused and none of these taxa show monaxon spicules like those described herein. There is a possibility that these spicules might be a main spine of some Spumellaria that lost its spherical shell (Feng et al., 2001), and such structures are commonly seen in the Triassic, although they have never been reported in the Cambrian. An inorganic origin of recovered spicules would be very difficult to support. Indeed, such structures with tapered ends, with axial canal (or hollow tube), sometimes curved, are never seen in any minerals. Some spicules are preserved as clusters (Fig. 9B), suggesting that such structures cannot be formed simply by filling of a void. Arsenopyrite crytals have been misidentified as monaxons and hexactins (Brasier et al., 1997; Zhou et al., 1998; Antcliffe, et al., 2014; Muscente et al., 2015). The tricrystal of arsenopyrite shows a fused centre, while all spicules recovered herein are isolated, even when preserved as cluster. They further differ from those pseudofossils described by Chang et al. (2017) in that they show a cylindrical cross section and in that they possess a hollow axial canal. To conclude, these spicule-like structures are probably remains of siliceous sponges, such small, stubby and unstable outline may represent an original character of siliceous

Their length is 120–300 µm; diameter for the chubby end is 20–60 µm; for a similar morphotype from the sponge fossil record of the Terreneuvian see Fig. 2f-g in Luo and Reitner (2019). The surface can be smooth or rough. Modified spicules (Fig. 8F): The outline is irregular, their two ends are asymmetrical showing inflated and, or bulging cross section in the middle or one end. Their length is 150–300 µm and maximum diameter within the spicule is 50–200 µm. The surface can be smooth or rough. Modified, obese sponge spicules are also known to occur worldwide from the Cambrian Series 2 to Series 3 (Peel, 2017; somewhat similar to inflated spicules reported herein). As shown by Uriz et al. (2003), inflated siliceous spicules can be produced by sponges through their hypersilification. However, the modified spicules described here are poorly preserved without any more details, there is insufficient information to definitely conclude about their sponge origin. Other possibilities include unknown organism or inorganic void-filling structure. Spicule-like structures (Fig. 9): Stubby or regular, needle-like (Fig. 9A-B) or fusiform (Fig. 9D) in outline, axial can be curved (Fig. 9C), sometimes with a hollow axial canal, ends pointed or rounded, 50–250 µm in length and the maximum diameter observed is about 50 µm. Some are preserved as clusters (Fig. 9B). All are siliceous in composition (Fig. 10). The surface can be smooth or rough, which might be a result of severe dissolution and recrystallization of quartz. In outline they resemble some living sponge spicules that have been described as club-shaped spicules and fusiform spicules (e.g., Fig. 2Q in Łukowiak et al., 2013; fig. 31B-F in Łukowiak, 2015). However, they are poorly preserved, and information on their axial canal is missing. Other possible interpretations of such structures include radiolarians, filing of void and pseudomorph of minerals. 6

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Fig. 6. Abundance and size of monaxon spicules and spicule-like structures from the Yanjiahe Formation in the Gunshi’ao section. Length from carbonates was not measured due to poor preservation. Note that the abundance of spicules is only referential for it includes both sponges and spicule-like structures. BACE: Basal Cambrian Carbon isotope Excursion, based on Ishikawa et al. (2008), AHC: acritarchs Asteridium–Heliosphaeridium–Comasphaeridium Zone.

spicules as observed herein. Similar empty sponge spicules have also been reported from the middle Cambrian by Chen and Dong (2008, Fig. 3d). Presence among recovered spicules of triaxons with both regular and enlarged canals (Fig. 4F) further supports interpretation of the later as a result of early diagenetic process. Dissolution during diagenesis may have completely altered the thinnest spicules from the lowest part of the section from where they are not reported. The rough surface of the spicule-like structures described above (Fig. 9), which are interpreted as sponge spicules here, may be caused by dissolution and recrystallization during diagenesis. The inflated, fusiform spicules (Fig. 9D) disappeared in upper Bed 3, and their inflated morphology might be produced by sponges through their hypersilification. These spicules being easily dissolved especially in shallow water may explain their scarcity in the fossil record during the Precambrian. If correct, the succession, in all studied sections, of assemblages made of monaxons only, followed by more diverse assemblages including fragmentary stauractine and triaxon spicules (from upper Bed 3 of the Yanjiahe Formation), most probably reflects an evolutionary pattern.

biomineralization by sponges.

4.3. Taphonomic condition may have affected morphology of sponge spicules Due to preservational conditions, morphology of surface and axial canals of sponge spicules can be varied. Poorly preserved sponge spicules always show a rough surface as a result of dissolution. This phenomenon can be observed in both monaxons and triaxons (e.g., Fig. 5A), especially in Bed 2 to Bed 3. Sponge spicules from above Bed 3 are smoother in outline. Another difference between sponge spicules from the lower and upper parts of the succession is the way the axial canal is preserved, sponge spicules from Bed 2 to Bed 3 always show an enlarged axial canal (Fig. 4E). We analyzed sponge spicules from siliceous nodules in Bed 6, where the axial canal with concentric structure is preserved (Fig. 4I-J). Both enlarged and solid axial canals can be observed in the rays of some triaxon specimens (Fig. 4H). Also in thin sections both solid axial canals filled by silica recrystallization or enlarged empty canals caused by dissolution can be observed (Fig. 11, marked by arrows). In field experiments Bertolino et al. (2017) demonstrated that silica dissolution can lead to significant enlargement of the axial canal of sponge spicules, sometimes resulting in empty 7

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Fig. 7. A-I. Spiculite from the Yanjiahe Formation in the Gunshi’ao section. A. hand specimen of sample G-Y3-2; B. thin section of sample G-Y3-5; C-E. SEM photo of sample G-Y3-22 showing bundles of monaxons; F. polished slab showing flaser bedding with lateral transitions form dark brown spiculite to lighter chert (sample GY3-22); G-H. microphotography of area marked by the left rectangle in F, under plane-polarized light in G and cross-polarized light in H; I. microphotography of area marked by the right rectangle in F, under plane-polarized light; J. diaxons and monaxons preserved in dolostone sample of g-yc4; K-L. Thin section of sample L-Y412, showing monaxons from limestone; M. hand specimens of spiculite from the Qiaojiaping section, Q-Y3; N. thin section of sample Q-Y15, showing diaxons; O. thin section from the Tianzhushan Member in the Songlinpo section. Scale bar: 200 µm except 1 cm in F and J.

Fig. 8. Monaxon morphotypes and modified spicules from the Yanjiahe Formation. Scale bar: 100 µm except 50 µm in F. 8

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Fig. 9. Spicule-like structure from Bed 1 to Bed 3 of the Yanjiahe Formation. A. needle-shape; B. clusters of spicules; C. curved spicules; D. fusiform-shape. Scale bar: 50 µm.

supporting their evolution through simplification from a ctenophorelike or cnidarian-like ancestor (Dunn et al., 2015; Botting and Muir, 2018). The most recent studies on modelling of compositional heterogeneity suggest that trees placing the comb jellies at the root of the animals are artifactual (Feuda et al., 2017); besides, the newly discovered fossil forms related to ctenophores exhibit anatomies that trace ctenophores to a sessile, polypoid stem lineage, indicating that coelenterate (ctenophore + cnidarian) might be monophyletic or that such a body plan might be due to convergent evolution (Zhao et al., 2019). As a consequence, the discovery of earliest stem-group sponge fossils and sponge-grade organisms is important for the understanding of basal animal evolution as well as early sponge diversification. Preservation of articulated, early sponges is usually limited to sites with exceptional preservation, while mineralized spicules have the best preservation potential and are generally easily identified. However, spicules remain rare in Precambrian deposits. This scarcity and its causes have been widely discussed. Preservational bias has been suggested to have controlled the absence of an Ediacaran sponge record (e.g., Sperling et al., 2010). However, as noticed by Botting and Muir (2018), taphonomic environments that lead to different Cambrian exceptional sponge preservation outcomes are also described from the Ediacaran, and intrinsic factors may better explain the absence of Ediacaran fossils. It is for example possible that Precambrian sponges were aspiculate (Muscente et al., 2015; but see Botting and Muir, 2018). Monaxon spicules and spicule-like structures in the lower Yanjiahe Formation might putatively be interpreted as demosponge remains. This interpretation would be fully congruent with recent genomic studies suggesting ancestral characters of the demosponge skeleton are monaxon diactines and spongin fibers (Cárdenas et al., 2012) and molecular estimates of an early Ediacaran diversification of demosponges (Sperling et al., 2010). On the opposite, this interpretation would be incongruent with the paleontological model of sponge evolution that skeletons of the last common ancestor is hexactines-based (Botting and Muir, 2018). However, the preservation of reported spicules (obliterating important details) precludes their definite assignment to any sponge clade. In addition, disarticulated spicules, as recovered herein, can hardly be implied in evolutionary model, and we agree with Botting and Muir (2018) that more material of articulated spiculate sponges is needed to improve or test the diverse phylogenetic

Fig. 10. Scanning Electronic Microscopy (SEM) image (A, D, G) and their corresponding backscattered image (B, E, H) of spicule-like structure (sample G-Y3-2), the Energy Dispersive Spectrometer (EDS) results (C, F, I) show the composition of quartz. Scale bar: 50 µm.

4.4. Evolutionary implications Recently Fortunato et al. (2015) demonstrated the last common ancestor of sponges might possess a much more diverse repertoire of developmental transcription factors than extant sponges. The presence among sponge larvae of traits and complexity shared with eumetazoans suggests the simple sedentary adult lifestyle of sponges probably reflects some degree of secondary simplification (Wörheide et al., 2012). Moreover, while recent studies tend to support the monophyly of the sponges (Simion et al., 2017) after a long debate about their possible paraphyly (Wörheide et al., 2012), paleontological and molecular research has challenged their most basal position among the metazoans, 9

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200um

A

B

C

D

E

F

G

H

I

J

K

L

M

N

O

Fig. 11. Thin sections of spicules of the Yanjiahe Formation. A-O are from the Gunshi’ao section: A. stubby, spicule-like structure (G-Y1-1); B-E. spiculite composed of monaxons. B. G-Y3-2. C. G-Y3-5, D-E. G-Y3-6. F-O. monaxons and stauractins with enlarged or solid axial canal. F-G. G-Y4-2; H-I. G-Y3-24; J-K. G-Y3-26; L-O. G-Y41. Arrows in B, F-G, L-O show spicules end up with a siliceous outer wall that was caused by dissolution, their axial canals were enlarged; arrows in H-K show spicules where their axial canal was filled by recrystallized quartz; arrow in D shows cross section of axial canals. Photomicrography in B, D-E, G, I, K, M, O were taken under plain-polarized light and others were under cross-polarized light. Scale bar: 500 µm, except 200 µm in A-I.

This is consistent with the fossil record as updated herein. Spicules remain simple in morphology and small in the lowermost Yanjiahe Formation. They then diversified quickly with larger, more resistant spicules of different biominerals, and more complex construction (Chang et al., 2017). The lack of spicules during the Precambrian might therefore be better explained as the result of a massive taphonomic bias (as suggested by Muscente et al., 2015), possibly due to the small size of earliest spicules, which would therefore easily dissolve during diagenetic processes. However, the biomineralization may also have remained weak or evolved late after sponge divergence (Muscente et al., 2015; Tang et al., 2019).

hypotheses advanced based on molecular or paleontological record. Absence of such data from Ediacaran and lower Precambrian deposits may come from collection, or more probably (and as further discussed below) from taphonomic artifact. Molecular paleobiology results show that metazoan siliceous biomineralization has Precambrian roots, and spicules might be small and easily dissolved. Furthermore, molecular paleobiology data suggest that siliceous spicules arose well before the origin of gut-bearing eumetazoans, so that the original function of spicules was for structural support and that defence against predators represents an exaptation that occurred during the Cambrian explosion (Sperling et al., 2010). 10

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Fig. 12. Geochemical analysis on chert samples from the Yanjiahe Formation in Gunshi’ao (GSA), Qiaojiaping (QJP) and Luojiacun (LJC). A. Al-Fe-Mn ternary plot (after Adachi et al., 1986), samples gy3-4, gy4-4, gy4-5, ly3-3 and qy-4 fall out of non-hydrothermal origin field. B. values of Ge/Si ratio (expressed in µg/g) (after Tribovillard et al., 2011).

of Precambrian Si biomineralization by eukaryotes is scant, and there is no further direct evidence that any organisms precipitated silica in the Precambrian in sufficient quantity to affect the silica cycle. We provide herein the first close conjunction of direct paleontological and geochemical evidence of biogenicity of Ediacaran-Cambrian cherts from the Yanjiahe Formation, South China. During the Ediacaran-Cambrian transitional interval, bedded chert successions are widespread in slope to deep-water basin environments around both the northern and the southern margins of the Yangtze Platform in South China as well as in many other continents (e.g., Chen et al., 2009; Stolper et al., 2017). Recent studies of chert occurrences along the Yangtze platform through observation of silica chimneys and analyses of silicon isotopes as well as of major and trace elements, indicate that hydrothermal activities provided abundant silica fluids resulting in cherts of hydrothermal origin especially in deep water successions, with the estimated area of the vent field at 50,000–120,000 km2 (Chen et al., 2009). It has even been hypothesised that hydrothermal activities during the E-C transition may have global significance as a possible alternative trigger of the observed changes in climate, ocean environmental chemistry and evolution of metazoans (Chen et al., 2009). However, abundance of spicules recovered from the Yanjiahe Formation suggests a biogenicity of related cherts. In order to decipher paleoenvironmental settings and origin of the cherts from the Yanjiahe Formation, their content in major, minor and trace elements along with rare earth elements (REE) were analysed herein (see “material and methods”). A ternary Fe-Al-Mn plot has been used to test the possible hydrothermal origins of the studied cherts (Boström et al., 1973; Murray, 1994). Approximately 90% of the tested chert samples fall in the nonhydrothermal origin field on the resulting ternary plot; only three samples (gy3-4, gy4-5, ly3-3) fall in the hydrothermal origin field (Fig. 12A). Ge/Si ratio, which is commonly used to distinguish the different sources of silica in cherts (Tribovillard et al., 2011), was calculated (Fig. 12B; see Fig. 13 for stratigraphic plot). Although the preservation of the Ge/Si ratio during diagenesis has been discussed, multiproxy analyses indicated that Ge/Si in chert is a robust proxy for origin of silica (Kolodny and Halicz, 1988; Tribovillard, 2013). Ge and Si share similar geochemical characters and are closely related in oceanic cycling. The Ge/Si ratio in modern seawater is 0.72 μmol/mol, far lower than that of land-derived and hydrothermal fluids (about 5 μmol/mol), while it is 0.45–0.78 μmol/mol in diatoms, 0.62–1.57 μmol/mol in radiolarians (radiolarites), and 0.08–0.38 μmol/ mol in modern and fossil sponges (Froelich et al., 1989; Mortlock et al., 1993; Tribovillard et al., 2011; Tribovillard, 2013). Tribovillard (2013,

Even if they illustrate simple morphologies, the recovered spicules are relatively abundant, even forming spiculites as early as the Ediacaran (Fig. 7). This high abundance suggests they were a significant component of benthic ecosystems during the Ediacaran-Cambrian transition interval. Moreover, spicules have been recovered from sections recording different parts of a Cambrian basin, from tidal shoreface to restricted offshore. During the earliest Cambrian, sponges might have therefore been widely distributed from both shallow to deep water environments.

5. Sponge bearing cherts from the Yanjiahe Formation: Implications for the Ediacaran-Cambrian evolution of the geobiological Si cycle and related decrease in marine dissolved Si Silicon is the second most abundant element on Earth, and it has been hypothesized that dissolved silica in the Precambrian ocean, depleted of eukaryote silica-biomineralizers, was roughly 10 times higher than today (Racki and Cordey, 2000; Perry and Lefticariu, 2014). However, Conley et al. (2017), by combining genomic and geological data, produced a new narrative for biologically triggered, stepwise reduction of dissolved Si starting with the appearance of oxygenic photosynthesis in the Archean. This model also assumes, based on genomics, that eukaryotic Si metabolism already occurred in the Neoproterozoic and reaffirmed the important role of late Neoproterozoic evolution of biosilicification across different eukaryotic groups including sponges. Indeed, paleogenomic studies have determined that gene families of active Si transporters are present in multiple eukaryotic supergroups, and phylogenetic analyses of these genes suggest that they have an origin in the Precambrian, possibly 1.7 Ga (Parfrey et al., 2011). Although the widespread Precambrian cherts have mostly been interpreted as inorganic in origin (Maliva et al., 1989, 2005), organic influence on the Precambrian Si cycle (from indirect to biosilicification) and related deposits (e.g. iron formations) since the Proterozoic or even late Archean has been increasingly supported (Fischer and Knoll, 2009; Marron et al., 2016; Ding et al., 2017). However, late Archean cherts are generally depleted in microfossil preservation in contrast with the younger Proterozoic peritidal chert (Fischer and Knoll, 2009 and reference therein). Late diagenetic carbonate silicification is common in these Proterozoic successions, with typical chert occurrences as discrete nodules or layers within limestone or dolomite formations. Such early diagenetic peritidal cherts formed in Meso- and Neoproterozoic successions are of particular interest because they contain extraordinarily preserved microfossil assemblages, providing a crucial record of Proterozoic life (e.g. Knoll, 2014). Nevertheless, confirmed fossil evidence 11

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Fig. 13. Plots of spicule and spicule-like structure abundance and the values Ge/Si, Ce/Ce*, Eu/Eu*, Y/Y* and Y/Ho along the column of the Yanjiahe Formation in the Gunshi’ao section.

from the Qiaojiaping section reveal a slight positive Eu anomaly with Eu/Eu* being 1.0–2.4 (average is 1.42), while both analysis of the FeAl-Mn plot and Ge/Si ratio (Supplementary Table S1) shows that cherts from this section are of sponge origin. A possible explanation for this is that a hydrothermal imprint was imparted to the silica within the water column which subsequently was the initial source of some of the silica precipitated by siliceous sponges (cf. Guo et al., 2007). It has been demonstrated that hypersiliceous domains and intervals, brought by volcano-hydrothermal activity during major plate-boundary reconfigurations, favoured siliceous biotas acme, their skeletal remains accumulation and preservation (Racki, 1999; Racki and Cordey, 2000). A higher rate of input of silica and other nutrients by hydrothermal activities would prompt eutrophication pulses, increase zooplankton biomass (Racki and Cordey, 2000), and also contribute to the flourishing of demosponges (Tarasov et al., 1999). Previous studies of Si isotopes and geochemical analyses conducted herein suggest an overall influence of hydrothermal activity (e.g., plumes from spreading ridge volcanism) on chert formation, which might have also contributed to the first bloom of siliceous sponges in the Ediacaran-Cambrian interval by providing silica-rich fluids and other nutrients to the marine ecosystems. However, the abundant spicules or even spiculites recorded through the Yanjiahe Formation, along with the sponge geochemical signature on deposited Si, further indicate an early diagenetic solution of biosiliceous particles was most probably the major source of silicification in the Yanjiahe Formation. Siliceous sponges might have been important contributors to the Ediacaran-earliest Cambrian benthic ecosystems. They might have further significantly influenced the cycling of silica, by acting as a principle sink for oceanic dissolved silica, resulting in its decrease since the latest Ediacaran. New discoveries reported herein, along with geochemical analyses, reduce the incongruence between the fossil record and the recent assumptions regarding

Fig. 2) also provides detailed comparison between Ge/Si ratio of biosilica with ratios in various lithologies (e.g. basalt, granite, clays) and with estimated ratios of oceanic and continental crusts which all exceed 3 μmol/mol. The Ge/Si ratio obtained from all except one (G-Y3-1, 2.30 μmol/mol) of the chert samples from the Yanjiahe Formation ranges between 0.15 and 0.66 μmol/mol, and the average value is 0.31 μmol/mol. The average value of Ge/Si ratios analysed herein is slightly lower than values reported from the Ediacaran chert of the Doushantuo and Laobao-Liuchapo formations (Shen et al., 2011; Dong et al., 2015), the latter have been regarded as of seawater origin (Dong et al., 2015; Wen et al., 2016). In our samples Ge/Si ratios are congruent with a sponge origin of the silica in these cherts, while a contribution from radiolarians cannot be excluded for the few samples with highest value. In the analysed samples, the value of SiO2 (ωB/%) shows a low relationship with Al2O3 and TiO2, and no systematic relationships of Pr/YbN, Y/Ho, Ce/Ce* and Eu/Eu* with TiO2 (Fig. 14) indicating a low influence of terrigenous input on REE-pattern. The samples from the Yanjiahe Formation exhibit a seawater-REE pattern (see Fig. 15 for REE + Y distribution spectra) with a negative Ce anomaly (0.3–0.87, average is 0.61), positive Y/Y* (1.05–2.16, average is 1.46), high Y/Ho ratio (30.97–56.98, average is 40.90), and very low Mn concentrations (Supplementary Table S1). Europium is enriched in highly reducing hydrothermal fluids (Michard and Albarede, 1986) and positive Eu anomalies are very common in marine hydrothermal sediments (Murray et al., 1991). The value of Eu/Eu* confirms the results from the Fe-Al-Mn plot, indicating a probable hydrothermal influence at some levels of the formation, which is variously recorded in the different studied sections. Three samples (gy3-9, gy3-18, gy3-19) in the Gunshi’ao section show slight positive Eu anomalies, indicating there might have been some hydrothermal input in some levels of Bed 3. Samples 12

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Fig. 14. Relationship of SiO2 (ωB/%) with Al2O3 and TiO2, and TiO2 with Pr/YbN, Y/Ho, Ce/Ce* and Eu/Eu* in the analyzed samples.

progress has been made in deciphering the mechanisms of these abiotic perturbations and more precisely in correlating with biotic patterns recorded in the fossil record. However, some of the triggers might be the results of expansion of ecosystem engineering, which is a consequence of the Cambrian explosion rather than a cause, falling into the trap of a chicken and egg problem (Zhang et al., 2014). Ecosystem engineering is likely a pivotal ecological prerequisite for the ecological success of bilaterian clades and biological innovations during the Ediacaran-Cambrian interval (Zhang et al., 2014). However, ecological engineering during the Ediacaran-Cambrian interval is poorly understood. Most Ediacaran fauna are problematic both in affinity and ecology due to the lack of analogous body plans today. The Cambrian substrate revolution is a part of the most important allogenic

the evolution of the biogeochemical cycle of Si in the oceans during Neoproterozoic-Cambrian times (Conley et al., 2017). 6. Sponges as ecological engineers of the Cambrian explosion The Ediacaran-Cambrian transition is one of the most important intervals during Earth history for it records an unprecedented bioradiation event, commonly named the “Cambrian explosion”. This event introduced the first establishment of complex, often called modern-type ocean ecosystems. Triggers for the Cambrian explosion have long been discussed, including external environmental perturbations as well as intrinsic genomic novelties and ecological engineers (Zhang et al., 2014; Paps and Holland, 2018; Wood and Erwin, 2018). Considerable

Fig. 15. Shale-normalized REE + Y distribution spectra of the cherts and limestone from the Yanjiahe Formation. A-B. Samples from the Gunshi’ao section (gy3-8, gy3-20, gy3-21, gy7-1 are siliceous carbonate); C. samples from the Luojiacun section (ly3-2, ly6-1 and ly8-1 are limestone); D. samples from the Qiaojiaping section. 13

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Older sponges were likely around prior to the Late Ediacaran, but related siliceous spicules might not be preserved due to dissolution during diagenesis. The reported Ediacaran spicules suggest Precambrian sponge spicules might have been significantly smaller and simple in morphology. As a consequence they might have been easily dissolved or morphologically affected by diagenesis. (4) Older Precambrian sponge spicules might be difficult to recognise due to taphonomic artefact, but also due to environmental influence on their original morphology. Environmental conditions have been demonstrated to affect the morphology of spicules secreted by extant sponges. Resulting abnormal morphotypes (such as inflated spicules produced through hypersilicification) are difficult to identify. Such abnormal spicule-like structures should be taken given careful attention especially in Ediacaran succession. Indeed, in sea-water environments that were different from the Phanerozoic, Ediacaran sponges may have produced abnormal spicules which don’t have modern analogue, hampering their identification. (5) Sponge biosilicification has been considered as a main driver for the decline of oceanic dissolved Si during the Ediacaran-Cambrian transition and concurrent bottom seawater oxygenation. Geochemical analyses in this study demonstrates that even if hydrothermal activity was regionally important during the studied interval, sponges were most probably the main silicon-source for the formation of abundant reported cherts. Hydrothermal activity might have however played an indirect key-role through Si input to sea-water favouring Si biomineralizers by sponges. By delivering nutrients, hydrothermal activity might have further enhanced the productivity of water column ecosystems and as a consequence the organic material in suspension available for feeding sponge community. We thus provide the first joint geochemical and paleontological evidence of abundant sponges involved in a significant silicon-takeover during the Ediacaran-Cambrian transition. These results confirm ecosystem engineering by sponges was probably an important trigger for the first establishment of modern-type ecosystems.

ecosystem engineering by metazoans, which contributed to mixgrounds, ventilation of the sediments and change in redox gradients by bioturbators, resulting in the introduction of infaunal habits and adaptive strategies of benthic fauna to newly emerging bioturbated mixgrounds (Bottjer et al., 2000). Siliceous sponges might be an important autogenic ecosystem engineer during the Ediacaran-Cambrian interval. In modern seas, sponge grounds contribute to increasing the structural complexity of habitats, attracting a larger variety of organisms and locally enhancing biodiversity (Maldonado et al., 2015). Of the five extinction events during geological history, siliceous sponges have been shown to have flourished after some mass extinctions, facilitating the recovery of ecosystems during the aftermath (Racki, 1999; Vishnevskaya et al., 2002; Delecat et al., 2011; Ritterbush et al., 2015; Botting et al., 2017). During the Ediacaran and earliest Cambrian interval, some of the major changes in seawater geochemistry are in accordance with a functional effect by sponges. Specifically, studies have shown that sponges are capable of stabilizing the seafloor (Beazley et al., 2015), turning over many thousands of liters of water per day (Reiswig, 1974), and are significant sinks for particulate organic material and for dissolved organic carbon by effectively feeding on picoplankton (Perea-Blazquez et al., 2012), and thus might have clarified turbid Ediacaran-Cambrian cyanobacteria-dominated conditions (Erwin and Tweedt, 2012) by redistributing organic carbon oxidation. It has been assumed that without abundant suspension feeding animals, there would have been no mechanisms for tipping the system out of a stratified, bacterially dominated condition, irrespective of the ambient oxygen (Butterfield, 2011). Based on geochemistry and silicon isotope analysis, Tatzel et al. (2017) calculated the relative abundance of sponges during the Ediacaran-Cambrian interval, indicating that organic carbon transfer rates increased at the same time as siliceous sponges became more abundant, thus sponges might have oxygenated the Neoproterozoic ocean. But to date, the absolute abundance of sponges indicated directly by fossils has not been recorded in the Ediacaran-Cambrian interval, thus hampering our understanding of their engineering effect. In this research, by study of thin sections, hand specimens and abundance of isolated spicules from four sections in the Three Gorges area, we show that siliceous sponges might be well established in the late Ediacaran, given the high abundance in the lowermost Cambrian, and with their rise in the late Ediacaran, their engineering effects may have fundamentally changed the geochemical conditions of the ocean and contributed to the first establishment of modern-type ocean ecosystems. Besides the widely discussed environmental triggers, genomic innovations and cell stemness (Hammarlund et al., 2018), sponges might have acted as an essential ecological trigger for the Cambrian explosion.

Acknowledgements This research was supported by funding from the National Natural Science Foundation of China Grant 41430101. L. Zhang was supported by the National Natural Science Foundation of China Grant 41502014. S. Clausen was supported by a grant from the Spanish Ministry of Economics, Finance and Competitiveness CGL2017-87631-P. D.J. Bottjer was supported by US National Science Foundation Grant EAR1338329. We express our sincere thanks to Guo Wei and Hu Jiabo for assistance in the geochemistry experiments and thin sections, as well as to Zhang Ke, Ye Yan, Gan Zhengqin and Chen Can for help in the field work. Anonymous reviewers are acknowledged for their detailed commons which have greatly improved the manuscript.

7. Conclusions (1) Sponge spicules and spicule-like structures were reported form four sections of E-C boundary interval sections from the Three Gorges area, South China, we made quantitive analysis on the abundance and size of these spicules. Comparison of these spicule-like structures with other organic or inorganic structures as well as taphonomic analysis showed that they probably represent original character or abnormal morphotype of monaxon spicules of siliceous sponges. (2) The occurrence of spiculite and relatively abundant sponge spicules spanning depositional conditions from the tidal zone to offshore basin indicate sponges may have flourished during the EdiacaranCambrian transitional interval in different environmental setting, and that current palaeontological data may not appropriately illustrate the evolutionary history of sponges. (3) Taphonomy have influenced the morphology of recovered spicules, especially in shallow settings, where previous studies demonstrated spicules are easily influenced by dissolution during diagenesis.

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