Sponge Spicules from the Lower Cambrian in the Yanjiahe Formation, South China: the Earliest Biomineralizing Sponge Record

PALAEO-07880; No of Pages 9 Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record

Shan Chang a,b,QinglaiFenga,b,⁎, Sébastien Clausen c, Lei Zhang b a State Key Laboratory of Geological Processes and Mineral Resources, Faculty of Earth Sciences, China University of Geosciences, Wuhan 430074, China b School of Earth Science, China University of Geoscience, Wuhan 430074, China c Univ. Lille, CNRS, UMR 8198 - Evo-Eco-Paleo, F-59000 Lille, France article info abstract

Article history: Sponges are the earliest metazoans, and according to molecular-clocks, have a deep history back into the Received 17 February 2016 Cryogenian. However, the record of their biomineralized elements below the Ediacaran-Cambrian Boundary Received in revised form 10 June 2016 has been controversial. Here we present the first and earliest indisputable record of hexactinellid spicules in Accepted 21 June 2016 the lowest Cambrian, Terreneuvian, below the small shelly fossil Anabarites trisulcatus–Protohertzina anabarica Available online xxxx assemblage zone (Zone I). Spicules recovered from cherts of the lowest Yanjiahe Formation in the Yichang, Hubei province, South China, include monaxons, diaxons, triaxons, and that are all siliceous in composition. Keywords: fi Terreneuvian This earliest record of silica biomineralization by lter feeding metazoan suggests sponges have contributed to Hexactinellid spicules the cycling of silica in the oceanic system as early as the beginning of the Phanerozoic. These results, along Diversification with a review of previously reported sponge occurrences, suggest a two-step evolution on sponges of the early Biomineralization Cambrian. Evolution © 2016 Published by Elsevier B.V.

1. Introduction a matter of current controversy (Borchiellini et al., 2001; Medina et al., 2001; Muscente et al., 2015). During the last decades, increasing attention has been paid on the The ongoing work for a high-resolution chronostratigraphic and cor- origin and early biomineralization of sponges. The phylum Porifera relative scheme of the Cambrian System (e.g., Clausen et al., 2015 and (sponges) is widely acknowledged to be the most ancient and basal the references therein), is of great significance to decipher the exact se- group of multicellular animals, or Metazoa (Halanych, 2004; Taylor quence of appearance of fossils and the detailed bio-radiation process et al., 2007; Srivastava et al., 2010). Recent molecular clocks indicate a during the Neoproterozoic–Cambrian interval. It is undeniable that deep Precambrian origin of the Metazoa, with a divergence of sponge sponges are one of the main sessile suspension feeders and were quite classes at about 750 million years ago (Sperling et al., 2007, 2010; common and diversified in the Cambrian metazoan community from Erwin et al., 2011). Moreover, sponges are also one of the earliest ani- the Stage 3 upward, as argued by both complete exceptionally pre- mals to secrete a three dimensional, mineral skeletal-framework, al- served specimens and abundant isolated spicules. Numerous diversified though the timing of the earliest biomineralized sponges still remains and well-preserved sponges occur in the exceptional faunas from Cam- controversial (Muscente et al., 2015). brian Series 2 of the Yangtze Platform, China, such as the Chengjiang, the Even if biomarkers, paleontological and molecular clocks all con- Niutitang, the Sancha, the Zunyi, and the Hetang faunas (e.g., Zhang and verge to a probable Cryogenian origin of sponges, their fossil record re- Pratt, 1994; Yuan et al., 2002; Xiao et al., 2005; Wu et al., 2014). Along mains controversial until the Cambrian. Consequently, it is not clearly with comparable coeval sponge faunas from South Australia and Siberia established yet if there is a bias in the fossil record of sponge biominer- (e.g., Shabanov et al., 1987; Bengtson, 1990; Rozanov and Zhuravlev, alization or if they evolved biomineralization long after their divergence 1992), they suggest that sponge groups diversified quickly during the (Muscente et al., 2015). Moreover, whether the molecular data support Cambrian Series 2. On the opposite, Terreneuvian sponge fossils are a demosponge + hexactinellid grouping to form a monophyletic silica is conspicuously rare and poorly-substantiated, and even appear to be rare to absent in the earliest Cambrian (Terreneuvian) as well as the late Neoproterozoic (Debrenne and Reitner, 2001; Xiao et al., 2005; Antcliffe et al., 2014). To date, the oldest known reliable sponge spicules ⁎ Corresponding author at: State Key Laboratory of Geological Processes and Mineral came from the Fortunian small shelly fossil Protohertzina anabarica Zone Resources, Faculty of Earth Sciences, China University of Geosciences, Wuhan 430074, China. of the Soltanieh Formation, Iran (Antcliffe et al., 2014). In South China, E-mail address: [email protected] (Q. Feng). the oldest convincing sponge spicules were reported from the lower

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 2 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx

Cambrian Yangjiaping Formation in Hunan (Ding and Qian, 1988)and basal dolomitic conglomerates, mostly consists of dolostone to sandy the Gezhongwu Formation in Guizhou (Yang et al., 2004). The paucity dolostone and banded black cherts. Bed 2 is dominated by siliceous of biomineralizing sponge fossils in the Precambrian and their abun- phosphatic dolostone with flat pebble conglomerates. It is followed by dance in the early Cambrian have been considered to reflect an impor- a thick succession of alternation of shale, in which siliceous- tant evolutionary process that closely linked to the major geologic, phosphatic nodules are common, and limestone (Bed 3). Bed 4 com- geomorphic and geochemical changes in the oceanic realm of the prises carbonaceous limestones. The uppermost Bed 5 is characterized Precambrian-Phanerozoic transition (Brasier, 1992; Bengtson, 1994). by cherts and siliceous phosphatic dolostone with flat pebble However, new data is required to assess this assertion and to fill the conglomerates. gap between fossil record and biomarkers or molecular data, to reveal The sponge spicules described here were obtained from the upper the early biomineralization history of sponges and its possible environ- dark cherts of Bed 1 (sample: ljc-1-2; Fig. 2). Occurrence of the acritarch mental controls. Micrhystridium regulare has been reported from the black cherts of Bed 1 In this paper we report the oldest sponge spicules from cherts of the (Ding et al., 1992). Other SSFs, including Anabarites trisulcatus, first basal Yanjiahe Formation, in Luojiacun section, Yichang, Hubei Province, occur in Bed 2 (sample ljc-2-2), suggesting that Bed 1 is earlier than South China. They occur below the small shelly fossil Anabarites SSFs Zone 1. The SSFs zone 1 has been provisionally dated from 537 to trisulcatus–Protohertzina anabarica assemblage zone (Zone I, early 532 Ma (Fortunian; Peng et al., 2012). Furthermore, a negative excur- Fortunian). The paleontological data on the Precambrian-Cambrian ap- sion of δ13Ccarb was detected from the base of the Yanjiahe Formation, pearance of sponges are summarized and discussed in the light of this which reaches its nadir (−7‰) below the SSF Zone I (Ishikawa et al., new discovery in order to understand their diversification and biomin- 2008). This excursion can be correlated with the Basal Cambrian Carbon eralization during the Cambrian explosion. Isotope Excursion (‘BACE’)(Peng et al., 2012). The Bed 1 sponge spicules therefore are confidently referred to as Fortunian in age. 2. Geological setting and stratigraphy Fossil assemblage from Bed 2 includes tubular microfossils Megathrix longus and poorly preserved acritarchs (observed in thin sec- The studied section crops out in a quarry (30°47′40.95″N, 110°54′ tion of phosphatic nodules). Radiolarians have been recovered from the 49.81″E) closed to the Luojiacun village, western of Yichang, Hubei limestone nodules of Bed 3. Megascopic algae are very abundant in Bed Province, China (Fig. 1). The Ediacaran to lower Cambrian succession 4. Bed 5 contains a new SSF assemblage, which is currently under study. is well exposed. It includes, in ascending order, the Dengying, the Yanjiahe, the Shuijingtuo, and the Shipai formations. The basal Cam- brian Yanjiahe Formation, disconformably overlies the Baimatuo Mem- 3. Material and methods ber of the Ediacaran Dengying Formation. There is also a remarkable sedimentary hiatus between the Yanjiahe and the Shuijingtuo forma- About 10 Kg of dark cherts were collected from the basal Yanjiahe tions (Fig. 2). Formation. Samples were processed following the long known method The current definition of the Precambrian–Cambrian boundary, for extracting radiolaria from cherts (Pessagno and Newport, 1972). based on the first appearance datum (FAD) of ichnospecies Trichophycus They were crushed into 1 to 2 cm pieces and then etched in 5% pedum, is not applicable in Yangtze Platform due to facies restriction hydrofluoric acid solution at room temperature. Subsequently, the resi- (Babcock et al., 2014; Yang et al., 2014). Alternatively, Small Shelly Fos- due was sieved (0.054 mm in diameter), dried at room temperature and sils (SSFs) have been proved widely useful for lower Cambrian biostra- then hand-picked under a binocular microscope. As for radiolaria, it is tigraphy (Steiner et al., 2007). Guo et al. (2014) identified three Small assumed that the silica comprising the sponge spicules is somewhat Shelly Fossils (SSFs) assemblage zones from the Yanjiahe Formation, more stable and dissolve more slowly than the including matrix, proba- namely: the Anabarites trisulcatus–Protohertzina anabarica assemblage bly due to a difference in crystal-size between spicules and matrix zone (Zone I), the Purella antiqua assemblage zone (Zone II), and the (Pessagno and Newport, 1972). The isolated specimens obtained were Aldanella yanjiaheensis assemblage zone (Zone III), suggesting an early mounted on stubs with latex, then sputter coated with gold and exam- to mid-Meishucunian age for the formation (Fortunian-early Stage 2; ined on Stereoscan Electron Microscope (SEM) equipped with Energy Guo et al., 2014). In the studied area, the sampled succession of the Dispersive X-ray (EDX) and Energy Dispersive Spectrometer (EDS) at Yanjiahe Formation can be subdivided into 5. Bed 1, characterized by the State Key Laboratory of Geological Process and Mineral Resources

Fig. 1. Geological map of Zigui, Yichang, South China and location of studied area.

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx 3

and State Key Laboratory of Biogeology and Environmental Geology at China University of Geosciences (Wuhan).

4. Morphological notes of sponge spicules

Depending on the numbers of rays and axes, four forms are identified and described here: monaxons; tetractines; pentactines and hexactines. The nomenclature used here follows Butler (1961) and Ding and Qian (1988). They possess typical cylindrical shape and rounded cross sections, axial canals are often preserved. They are smooth and no small spines are observed. Most of them are preserved as silica; only 4 specimens (Fig. 3G–J) are preserved as pyrite. Monaxons: They have a single, straight or curved axe, making up the majority of the collected spicules. Siciform monaxons (Fig. 3N–T): The outline resembles a knife or a blade, all are siliceous in composition; ray appears to be smooth, 0.3– 0.6 mm long, and the diameter varies from 20 μmto70μm; axe is generally straight to slightly curved with rounded to elliptical cross sections; one end of the ray is rounded, stubby, and the other end tapers into pointed; axial canal sometimes can be observed (Fig. 3N, T). This morphology is rarely reported in the early Cambrian and was only documented from the Yanjiehe Formation in Hubei and the Yangjiaping Formation in Hunan, South China (Ding and Qian, 1988, plate IV.11–12). Specimens illustrated in Fig. 3R–T can be well correlated with those reported from Hunan, while specimens shown in Fig. 3N–Q provide a transitional type to the diactinal monaxons. Diactinal monaxons (Fig. 3U–AE): Compared to siciform monaxons, they are highly symmetrical in the outline; all are siliceous in composition, the ray is smooth, 0.3–0.6 mm long, and the diameter varies from 20 μmto80μm; axe is straight to curved with two similar pointed (Fig. 3L) to rounded (Fig. 3M) ends. Diaxons: They possess two axes, bearing similar rays at right angle. Tetractines or stauractines (Fig. 3B, G, H): They possess 4 smooth and regular rays; axial canal is often preserved (Fig. 3B). Two specimens are replaced by pyrite (Fig. 3G, H), as also commonly seen in the shale and limestone of the overlying Shuijingtuo Fm. in the studied area (pers. obs). Pyrite replacement would generally obscure the morphology of spicules (as shown in Fig. 3I, J), although the morphology of the specimens recovered herein, from cherts beds of the Yanjiahe Formation, is less altered. Triaxons: They possess three axes and five (pentactine) or six (hexactine) rays which extending at right angle from a central point. These spicules are restricted to the class Hexactinellida (Butler, 1961). Pentactinal triaxons (Fig. 3A, C–F): They have five rays, four of which lie in a single plane; rays are 0.1 mm to 0.5 mm long, 12 μmto25μmin diameter, rays are generally straight, smooth, with strongylote (Fig. 3C– F) to pointed (Fig. 3A) ends; cross section is generally rounded (Fig. 3C). Pentactines are widely distributed in the early Cambrian. Morphol- ogy of recovered pentactines are similar to those reported from the Fortunian Soltanieh Formation in Iran (Antcliffe et al., 2014), the early Cambrian Yangjiapin Formation in Hunan (Ding and Qian, 1988) and the Series 2 Shuijingtuo Formation in Hubei and Shaanxi province (e.g., Zhao and Li, 2006; Zheng et al., 2012). Pentactines in the Qiongzhusian (Series 2) possess knobs or small spines that ornamented in the rays, while the Meishucunian (Terreneuvian) are characterized by smooth rays. The smooth rays might represent an original character. Hexactinal triaxon (Fig. 3G, K): They have three axes and six, slender and irregular rays radiates from a central point (two longer and straight rays along one axe, and four shorter and slightly curved rays); axial canal is visible on broken ray (Fig. 3K1). Length of each ray varies from 0.03 mm to 0.3 mm, or longer, diameter varies from 5 μmto 24 μm. The recovered hexactines are morphologically similar to those reported from the Yangjiapin Formation in Hunan (Ding and Qian, 1988), the Shuijingtuo Formation in Hubei and Shaanxi (e.g., Zhao and Fig. 2. Stratigraphic column of the Yanjiahe Formation in Luojiacun section with sampled levels. (DY represents the Dengying Formation; YJH represents the Yanjiahe Formation; Li, 2006; Zheng et al., 2012), while spicule assemblages from the SJT represents the Shuijingtuo Formation.) Shuijingtuo Formation display much higher diversity.

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 4 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx

Fig. 3. Sponge spicules from dark cherts of the Yanjiahe Formation. A, C–F: pentactines; B, H, tetractines; I–J, poorly-preserved spicules preserved as pyrite, dashed rectangular area shows coarse pyrite crystals; G, K, hexactine, detail of the central area of K is shown in K1, axial canal is shown in K2; L, monaxons with pointed ends; M, monaxons with tapered ends and circular cross section; N–T, siciform monaxons; U–AE, diactinal monaxons. Arrows show the axial canals of the sponge spicules. Scale bar: 20 μm for K1 and 100 μmfortherestspecimens.

5. Discussion spicules” might be bacterial filaments or acicular crystals molded by organic matter (Muscente et al., 2015). These “mineralized spicules” 5.1. Nature of “Mineralized spicules” and other sponge remains from the therefore are still problematic. Ediacaran-Cambrian transition Most spicules reported herein are siliceous, with rounded cross section and preserved a reminiscent to obvious axial canal. However, some Spiculate sponges and sponge spicules form the majority of Phanero- “mineralized spicule-like structures”, etched from Bed 2 of the Yanjiahe zoic sponge fossils, since they have the best potential to be preserved and Formation (Fig. 4), lack such features, although their morphology is very recognized in the fossil record. However, the Precambrian fossil record in- similar to Hexactinellida spicules. In these pseudo-spicules, the rays are cludes only dubious and equivocal occurrences, and the interpretation to rectangular in cross-section, longitudinally striated (Fig. 4C1). Rays sponges has been questioned (Yin et al., 2001; Antcliffe et al., 2014; form at least two bunches: the larger ones are about 75–100 μm long, Muscente et al., 2015).Amongthem,theonceoldest,widelyacceptedsi- andupto15μm in diameter at their base; on the top of the larger liceous sponge spicules, from the Tsagaan Oloom Formation in Mongolia, bunch radiates the shorter rays, which are less than 10 μm long, and about 545 Ma (Brasier et al., 1997), were shown to be cruciform arseno- up to 5 μm in diameter. Rays aggregate in more or less irregular angles pyrite crystals by EDX analysis (Antcliffe et al., 2014). Zhou et al. (1998) from the central part, and the smaller rays are often covered by silicon reported very similar clusters of spicule-like structures from the Ediacaran crystals. EDS and EDX analysis both revealed their P and Ca composition Doushantuo Formation in Weng'an, South China and pointed out that (Figs.5,6). These structures therefore differ from definite spicules such these arsenopyrite crystals preserved in some sedimentary rocks would as those described above, but share the P-Ca composition and striated easily be misidentified as Hexactinellida spicules. rays with the putative spicules described from the Doushantuo Forma- One putative Precambrian sponges that preserved with “mineralized tion (Yin et al., 2001, Fig. 1). Due to their morphological features and spicules” from the Doushantuo Formation at Weng'an, South China mineralogical composition, we are confident these pseudo-spicules were originally interpreted as the oldest and only Ediacaran are not related to sponges, although their biological or diagenetic origin demosponges in the fossil record (Li et al., 1998). However, Zhang cannot be assessed without further analysis. However, a formation et al. (1998) considered these “mineralized spicules” might be aggre- through phosphatic replacement of originally siliceous spicules seems gates of broken spines of collapsed acanthomorphic acritarchs that are unlikely as none of the other, indisputable, spicule morphotypes de- common in the Doushantuo Formation. Similarly, Yin et al. (2001) scribed herein are found to illustrate such a diagenetic pattern. showed that these spicules were not siliceous as claimed by Li et al. (1998) but, instead, were mainly composed of Ca and P and might be 5.2. Early Cambrian fossil record and the sponge diversification diagenetic in origin. Yin et al. (2001) also questioned the presence of axial canals in the structures described by Li et al. (1998). Moreover, It has been widely accepted that sponges exhibit a dramatic diversi- in situ nanoscale analytical techniques showed that the “mineralized fication during the early Cambrian. However, we suggest herein, based

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx 5

Fig. 4. Problematic “pseudo-spicules” from Bed 2 of the Yanjiahe Formation, preserved as phosphatic minerals. C1 is magniﬁed picture of the rectangular area in C, showing rectangular cross section and multiple longitudinal striae on rays; arrow in D shows ﬂattened spine without cylindrical cross-section.

mostly on the sponge fossil-record from Siberia and South China, that morphology and different biominerals. A diverse assemblage of isolated before the great diversification of the “Cambrian explosion” in the Series spicules, including monaxons, T-form diaxons, tumour-shaped triaxons 2, the sponges may have undergone a quiet and gradual development in has been described from the lower Cambrian Yangjiaping Formation in their skeletons during the Terreneuvian (Fig. 7). Hunan, South China (Fig. 7E; Ding and Qian, 1988). Even if this interval Fortunian sponge fossils are rare, poorly-substantiated and low di- lacks detailed biozonation, it can be tentatively assigned to the late versified. In addition to the assemblage reported herein, reliable youn- Fortunian-early Stage 2 (Steiner et al., 2007). ger spicules were reported from Iran (Fig. 7B; Antcliffe et al., 2014), Material from the Hetang Formation of Anhui (e.g., Hu et al., 2002; and from Guizhou, South China (Fig. 7C; Yang et al., 2004). An assem- Yuan et al., 2002) and the Niutitang black shales of Hunan (Steiner blage of hexactinellid spicules has also been reported from the Purella et al., 1993), illustrating the earliest well-preserved complete antiqua Zone of the upper Ust'-Yudoma Formation, Siberia (upper Hexactinellid body fossils, were documented from relatively deep set- Fortunian Stage, Fig. 7D; Khomentovsky et al., 1990; Brasier et al., tings of the Yangtze platform. The occurrence in the Hetang Formation 1993; Khomentovsky and Karlova, 1993; Khomentovsky and Karlova, in Anhui was between the Small Shelly Fossils Anabarites-Protohertzina 2005). zone and the trilobite Hunanocephalus-Hupeidiscus-Hsuaspis assem- Based on fossil record, skeletons of sponges begun to develop grad- blage zone (Fig. 7L; Yuan et al., 2002). This occurrence can be broadly ually during the Terreneuvian Age 2, leading to more diversified correlated with the Terreneuvian to Epoch 2, but the exact stratigraphic

Fig. 5. EDX elemental mapping of a real monaxon (A) and the problematic “pseudo-spicule” (B). Scale bar: 50 μm.

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 6 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx

Fig. 6. EDS element maps of a “pseudo-spicules”.

position of these strata remains unclear since the sponge-bearing hori- slow, gradual evolution of their skeletal framework, leading, at the zon is poorly fossiliferous. Isolated siliceous stauracts and pentactines end of the epoch, to still relatively low-diversified spicule assem- have been reported from the Nochoroicyathus sunnaginicus Zone blages, which, nonetheless, feature different biominerals. By con- (upper Stage 2) of the Siberian Platform (Fig. 7F; Sokolov and trast, Series 2 illustrates an explosive diversification of sponges, Zhuravleva, 1983; Rozanov and Sokolov, 1984; Pel'man et al., 1990). both in morphospaces and ecological neaches. Oldest archaeocyathans are also reported from Siberia within the The late Neoproterozoic–Cambrian has been described as a critical Tommotian (N. sunnaginicus Zone, Stage 2, Fig. 7G; Rozanov et al., time interval for chert deposition and silica cycle, since it started to be 1969; Kruse et al., 1995; Varlamov et al., 2008). influenced by silica biomineralizing organisms, such as the During Epoch 2 (particularly during Age 3), sponge groups experi- Hexactinellida Sponges and polycystine Radiolaria (Maliva et al., 1989; enced explosive radiation both in morphospace and ecospace. Racki and Cordey, 2000; Braun et al., 2007; Zhang et al., 2013). The pres- On the Siberian platform, calcareous sponge spicules with triradiate ence of siliceous sedimentary rocks, including organic-rich black sili- symmetry and demosponge spicules were present in the Atdabanian ceous shales and cherts, is widely distributed in the lower Cambrian (lower Stage 3, Fig. 7I; Shabanov et al., 1987;Fig.14a–binRozanov sequences of South China. Although the depositional settings of these and Zhuravlev, 1992). In the Botoman (Stage 4), pentactines were successions have been largely discussed (e.g., Zhou and Jiang, 2009; found together with hexactines and they formed spongolites (Fedorov Zhang et al., 2013; Cremonese et al., 2014; Dong et al., 2015), no agree- and Pereladov, 1987). ment has been reached so far and more studies regarding the On the Yangtze platform there has been numerous diversified and paleoenvironmental reconstructions and in particular the redox- well-preserved sponge faunas described in the Qiongzhucian (Stage conditions are required to better understand whether the low–oxygen 3), such as the Chengjiang Fauna, the Niutitang Sponge Fauna, the requiring Hexactinellida sponges originated from shallow water or Sancha Sponge Fauna, the Zunyi Fauna, the Hetang Sponge Fauna deep water. (Fig. 7; Xiao et al., 2005; Wu et al., 2014; Zheng et al., 2012) and the It is hypothesized that during the Neoproterozoic, sponges may pro- Shuijingtuo sponge fauna (e.g., Zhang and Pratt, 1994; Yuan et al., duce ostensibly small and weak spicules in the absence of predatory an- 2002; Zhao and Li, 2006). These fossils, along with a comparable coeval imals, the evolution of sponges with larger, more easily-preserved fauna from South Australia and Siberia (e.g., Bengtson, 1990; Rozanov spicules may have been promoted by secular change in nutrient avail- and Zhuravlev, 1992), have remarkably diversified skeletons, indicating ability, oxygen, and stress from predatory animals through the that sponge groups established quickly during the Cambrian Epoch 2 as Cryogenian-Cambrian interval (Muscente et al., 2015). The spicules re- a part of the “Cambrian Explosion”. Besides, sponges were presented ported here are already relatively large with strong silica composition. both in deep-water and shallow water environments and the epifaunal It's therefore still possible to date the origin of mineralized (or siliceous) tiering have been well developed into different levels (some sponges spicules back to the Pre-Cambrian, although such undisputable fossils reach the 50 cm tier according to Yuan et al., 2002), indicating that are still to be found. sponges have successfully evolved into important ecological actors of bottom-level suspension feeding communities. 6. Conclusions Morphologically, spicules from the early Terreneuvian (Fortunian) are low-diversified and consist of simple forms such as monaxons, (1) The sponge fossils reported here include monaxons, diaxons and stauractines, triaxons and tetraxons, no small spine or desma was devel- triaxons. They occur near the base of the Cambrian succession oped. During the late Terreneuvian (Age 2), skeletons of sponges begin (below the Anabarites trisulcatus–Protohertzina anabarica assem- to develop gradually with different biominerals. Finally, during the early blage zone). Epoch 2, sponge groups experienced explosive radiation and success- (2) These remains provide the earliest clear evidence for organisms fully broadened their ecological niches. that can be assigned without question to biomineralizing Porifera, To conclude, it is considered herein, that early Cambrian sponge evo- and the first firm evidence for filter feeding and metazoan silica lution might be divided into two steps. Terreneuvian was a period of biomineralization in the fossil record, indicating that sponges

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx 7

Fig. 7. Illustration of the early sponge diversiﬁcation during the Terreneuvian to Cambrian Series 3 (the biostratigraphic time scale was revised after Steiner et al., 2007 and Yang et al., 2014). Dashed lines and arrows represent uncertain age. A, this paper. B, Antcliffe et al. (2014).C,Yang et al. (2004).D,Khomentovsky et al. (1990), Brasier et al. (1993), Khomentovsky and Karlova (1993), Khomentovsky and Karlova (2005).E,Ding and Qian (1988).F,Sokolov and Zhuravleva (1983), Pel'man et al. (1990).G,Rozanov et al. (1969), Varlamov et al. (2008).H,Kruse et al. (1995).I,Shabanov et al. (1987), Rozanov and Zhuravlev (1992). J, Siberian records, e.g. Sokolov and Zhuravleva (1983), Pel'man et al. (1990), Kruse et al. (1995), Shabanov et al. (2008).K,Steiner et al. (1993).L,Yuan et al. (2002).M,Hu et al. (2002).

have contributed to the cycling of silica in the oceanic system as Zhang Mingliang, Liu Kai and Guo Wei for help in the ﬁeldwork; sup- early as the beginning of the Phanerozoic. ports and experimental assistance by Li Jiangyan, Ngnyen Minh Quyen (3) Before the great diversiﬁcation of the “Cambrian explosion” in the and Wei Rong are greatly appreciated. Martial Caridroit and Taniel Series 2, the sponges may have undergone a quiet and gradual de- Danelian are acknowledged for constructive discussions during prepa- velopment in their skeletons in the Terreneuvian. ration of this manuscript. Special thanks are due to Brian Pratt, one anonymous reviewer and the Guest Editor Prof. Z.Q. Chen for their constructive remarks on the manuscript. Acknowledgments

This research is supported by NSFC (Grant No. 41430101), NSFC References (Grant No. 41502014), project CGL2013-48877-P from Spanish Antcliffe, J.B., Callow, R.H., Brasier, M.D., 2014. Giving the early fossil record of sponges a MINECO and Feder. We express our sincere thanks to Zhang Yan, squeeze. Biol. Rev. 89, 972–1004.

Please cite this article as: Chang, S., et al., Sponge spicules from the lower Cambrian in the Yanjiahe Formation, South China: The earliest biomineralizing sponge record, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2016), http://dx.doi.org/10.1016/j.palaeo.2016.06.032 8 S. Chang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2016) xxx–xxx

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