Preservational modes in the Ediacaran Gaojiashan Lagerstätte: Pyritization, aluminosilicification, and carbonaceous compression

This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright

Author's personal copy Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

Contents lists available at SciVerse ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology journal homepage: www.elsevier.com/locate/palaeo

Preservational modes in the Ediacaran Gaojiashan Lagerstätte: Pyritization, aluminosilicification, and carbonaceous compression Yaoping Cai a, James D. Schiffbauer b, c, Hong Hua a,⁎, Shuhai Xiao c,⁎ a

State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University, Xi'an, 710069, China Nanoscale Characterization and Fabrication Laboratory, Institute for Critical Technology and Applied Science, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA c Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA b

a r t i c l e

i n f o

Article history: Received 9 November 2011 Received in revised form 5 February 2012 Accepted 7 February 2012 Available online 15 February 2012 Keywords: Ediacaran Taphonomy South China Pyrite Aluminosilicate Carbonaceous compression

a b s t r a c t Burgess Shale-type (BST) fossils often are preserved as two-dimensional carbonaceous compressions, sometimes aided by two mineralization processes: pyritization and aluminosilicification, defined by a thin and sometimes localized coating of authigenic pyrite or aluminosilicate minerals on the carbonaceous materials. Here we report similar mineralization modes within the late Ediacaran Gaojiashan Lagerstätte of southern Shaanxi Province, South China. Examination of two common Gaojiashan fossils, Conotubus hemiannulatus and Gaojiashania cyclus (hereafter referred by generic names only), indicates that pervasive pyritization is the primary taphonomic pathway in this deposit, responsible for the preservation of ~80% of the collected fossils. Pervasive pyritization of Gaojiashan fossils results in their three-dimensional preservation, as opposed to two-dimensional carbonaceous compression with thin pyrite coatings seen in some BST Lagerstätte. However, microscale investigation using environmental scanning electron microscopy (ESEM) and energy dispersive Xray spectroscopy (EDS) shows that some flattened specimens of Conotubus and Gaojiashania are preserved as carbonaceous compressions, which are in some cases associated with aluminosilicate minerals. Rare compressed specimens of Conotubus are replicated by greenish clay minerals, which are interpreted as diagenetic products of aluminosilicate precursors. Our taphonomic analysis shows that pervasive authigenic pyritization tends to replicate more labile tissues than aluminosilicate-aided carbonaceous compression, but both pyritization and aluminosilicification processes can facilitate the replication and preservation of soft-bodied organisms in siliciclastic sediments. Building upon this conclusion, we propose that multiple taphonomic processes, including kerogenization (or polymerization of organic molecules), pyritization, and aluminosilicification, can contribute to the mode of BST preservation. Viewed in this light, various siliciclastic-hosted Lagerstätten that are facilitated by kerogenization, pyritization, and aluminosilicification can be plotted on a ternary diagram based on the relative importance of these taphonomic processes. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Exceptional fossil preservation, especially the preservation of soft tissues, is of particular importance to understanding the biosphere and evolutionary history of the Earth (Allison and Briggs, 1993; Bottjer et al., 2002). A global survey of exceptionally preserved fossil deposits indicates that the Cambrian and Jurassic periods are overrepresented in the temporal distribution of Konservat-Lagerstätten (Allison and Briggs, 1993). This finding implies that a distinct combination of palaeoenvironmental, sedimentological, and diagenetic conditions conducive to exceptional preservation may have driven the uneven distribution of Lagerstätten. To understand the taphonomic processes that contributed to the distribution of exceptional preservation in time, it is important to

⁎ Corresponding authors. E-mail addresses: [email protected] (H. Hua), [email protected] (S. Xiao). 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2012.02.009

demarcate environmental, sedimentological, and geochemical features of various Lagerstätten. This manner of investigation is especially useful for exceptionally preserved organisms of Ediacaran age, as taxonomic affinities of these organisms, taphonomic pathways responsible for their preservation, and their paleoecological systematics are often uncertain (Bottjer, 2002; Narbonne, 2005; Xiao and Laflamme, 2009). Previous taphonomic investigations have identified several preservational modes in the Ediacaran Period. The widespread Flinders-type ‘death mask’ preservation has been shown to be fundamentally facilitated by the colonization of microbial mats or biofilms following sediment burial; these microbial colonies prevented oxidizing agents from reaching the buried organisms and promoted three-dimensional casting and molding in siliciclastic sediments (Gehling, 1999; Narbonne, 2005; Laflamme et al., 2011). Doushantuo-type preservation (Butterfield, 2003), promoted by early diagenetic phosphate mineralization, captures threedimensional and cellular-level detail of genuine soft-tissues (Xiao et al., 1998; Xiao and Knoll, 1999; Xiao and Schiffbauer, 2009; Schiffbauer et

Author's personal copy 110

Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

al., 2012). Burgess Shale-type (BST) preservation, a taphonomic mode defined by the exceptional preservation of non-mineralizing organisms as two-dimensional carbonaceous compressions in fully marine finegrained sediments (Butterfield, 1995; Gaines et al., 2008), is also present in Ediacaran deposits (Xiao et al., 2002; Tang et al., 2008; Zhu et al., 2008; Anderson et al., 2011). Taphonomic investigations of Phanerozoic examples of BST preservation emphasized the importance of such factors as dysoxia or anoxia (Allison and Brett, 1995; Gaines et al., 2012), the lack of bioturbation (Allison and Briggs, 1993; Orr et al., 2003), inhibition of autolytic decay by clay minerals (Butterfield, 1995), and early diagenetic carbonate cementation (Gaines et al., 2005). These factors are not mutually exclusive, and they all focus on mechanisms responsible for delaying degradation or destruction. These factors can be viewed as “distal” environmental and diagenetic conditions that facilitate but do not guarantee BST preservation. In other words, delaying destruction is not sufficient for BST preservation, and constructive processes to stabilize or replicate the organic tissues through some sort of mineralization (Briggs, 2003) are additionally necessary for the fossils to survive long geological periods. These constructive processes can be viewed as “proximal” causes, and they include kerogenization (polymerization of organic carbon to form geologically stable kerogen; Stankiewicz et al., 2000; Gaines et al., 2008), aluminosilicification (formation of authigenic clay templates; Orr et al., 1998), and authigenic pyritization (Gabbott et al., 2004; Hu, 2005; Zhu et al., 2005). In previous analyses of BST preservation, there is a clear discrepancy in the role that clay minerals play in soft-tissue preservation. The model proposed by Orr et al. (1998) posits that authigenic clays acted as constructive replication agents, to form a template around carcasses during early diagenesis and prior to substantial decay. This model opposes the hypothesis of Butterfield (1995), in which detrital clays were suggested to be anti-degradation agents, to suppress enzymatic activity and thus autolytic degradation. Other researchers, however, have questioned any taphonomic role of clays in BST preservation, instead suggesting a metamorphic origin of clays in association with BST fossils (Butterfield et al., 2007; Gaines et al., 2008; Page et al., 2008). The late Ediacaran (ca. 551–541 Ma) Gaojiashan Lagerstätte in the southern Shaanxi Province of South China can provide new insights into the role of mineralization in exceptional preservation, because multiple preservational modes—pyritization, carbonaceous compression, and association with aluminosilicate minerals—are simultaneously present in this Lagerstätte. Using environmental scanning electron microscopy (ESEM) and integrated energy dispersive X-ray spectroscopy (EDS), we investigated the microchemistry and taphonomy of two non-mineralizing fossils known only from the Gaojiashan biota: Conotubus hemiannulatus—a conotubular fossil consisting of a series of nested cylinders (Cai et al., 2011), and Gaojiashania cyclus—a cylindrical fossil consisting of a series of couplets of rings and annuli (Cai and Hua, 2011). While potentially related to some of the earliest known biomineralizing organisms from the Nama assemblage (Cai et al., 2011), the phylogenetic positions of Conotubus and Gaojiashania remain uncertain. Their paleontological significance, however, should not be overlooked. Geochronologically, the Gaojiashan biota is positioned within the last 10 million years of the Ediacaran Period. With possible phylogenetic ties to other tubular forms found in Ediacaran and early Cambrian deposits, Conotubus and Gaojiashania have the potential to elucidate the evolutionary history of many problematic forms across the Ediacaran– Cambrian transition. Perhaps more importantly, the Gaojiashan fossils also provide taphonomic insights into other Lagerstätten where phylogenetically important forms are preserved. Thus, our focus in this study to dissect the complex taphonomic histories of Conotubus and Gaojiashania can contribute to a better understanding of soft-tissue preservation during this important interval of evolutionary history. 2. Materials and methods The investigated fossils were collected from the middle Gaojiashan Member of the Dengying Formation, along a fresh roadcut (see Fig. 3A

in Cai et al., 2010) at the Gaojiashan section. Specifically, the fossils were sampled from beds 26–35 m above the base of the Gaojiashan Member, stratigraphically above the enigmatic fossil Shaanxilithes from the lower Gaojiashan Member (Meyer et al., in press). The host rocks consist of normally graded siltstone (typically 3–5 mm thick) capped by mudstone (typically 1–3 mm thick); these couplets have been interpreted as marine obrution deposits below storm wave base (Cai et al., 2010). In order to explore the taphonomic modes and reconstruct the diagenetic history of the Gaojiashan Lagerstätte, we microchemically analyzed representative specimens of Conotubus and Gaojiashania preserved on bedding planes. A total of 16 fossil specimens were analyzed, including pervasively and three-dimensionally pyritized specimens, compressed specimens preserved as carbonaceous films, and specimens replicated by greenish minerals. Exposed specimens were first examined with reflected light microscopy. Selected specimens were prepared for thin sectioning (perpendicular to bedding planes) and optical petrographic observation. Additional exposed specimens were prepared for electron microscopic analysis on an FEI Quanta 600 field-emission ESEM equipped with an integrated high-speed silicon drift detector (Bruker AXS QUANTAX 400 EDS system). A range of beam accelerating voltages (5–20 keV) were used for imaging purposes, but consistent operating conditions (20 keV, 5.0 spot size [unitless approximation of beam current and probe diameter], 11.5 mm working distance) were maintained for EDS analyses. The greenish minerals present on some Conotubus specimens were also analyzed using Raman spectroscopy (Renishaw 514 nm Ar laser at room temperature and atmospheric pressure). 3. Results The Gaojiashan fossils found in the event sediments can easily be identified under reflected light on the basis of both color and grain size contrasts. The majority of the fossils are pyritized, displaying a rusty color from pyrite oxidation, and are preferentially embedded in siltstone rather than mudstone beds (Cai et al., 2010), facilitating their identification. The three preservational styles identified in the Gaojiashan Lagerstätte—(1) pyritization (Fig. 1A–B), as previously documented by Cai and Hua (2007); (2) dark gray carbonaceous compression (Fig. 1C–D); and (3) replication by greenish minerals (Fig. 1E)—are often intermixed and can occur in the same specimen (Fig. 1F–H). 3.1. Pyritization A large majority of the Conotubus and Gaojiashania material (~80%, based on quantitative assessment of a collection with more than 10,000 specimens) is pyritized, easily recognizable not only by their characteristic color but also by their three-dimensional preservation as compared to the greenish-to-gray compressed specimens. As would be expected, elemental X-ray mapping of lightly weathered specimens documented localizations of both Fe and S (Cai and Hua, 2007). Most specimens are pervasively pyritized, with little to no organic carbon remains. Their three-dimensional preservation is sharply contrasted to two-dimensional soft-tissue preservation in the Chengjiang and Fezouata biotas where pyrite precipitation (or iron oxide pseudomorphs from chemical weathering) is localized to certain anatomical structures, likely reflecting variability in tissue susceptibility to decay (Gabbott et al., 2004; Hu, 2005; Lin and Briggs, 2010; Van Roy et al., 2010). The pervasive pyritization observed here preserves anatomies unseen in other preservational styles of Gaojiashan fossils. This is exemplified by the preservation of Gaojiashania, where pyritization captured annuli (thin membranous structures between much thicker rings; Fig. 1F left) that are absent in carbonaceous compressions (Fig. 1D; F right).

Author's personal copy Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

111

Fig. 1. Reflected light photographs (except SEM photomicrograph in B) showing various preservational styles of the two common Gaojiashan taxa, Gaojiashania cyclus (D and F) and Conotubus hemiannulatus (all others). (A, B) Pyritization. A is a fracture surface with a transverse cross section view of a pyritized Conotubus hemiannulatus specimen, and B shows framboidal pyrite on exterior surface of a pyritized Conotubus hemiannulatus tube. (C–D) Dark gray carbonaceous compressions. (E) Replication by greenish minerals. (F) Transition from pyritization (black arrowed area) to dark gray carbonaceous compression (white arrows). (G) Dark gray carbonaceous compression with greenish mineral replication in the middle part of the tube. (H) Transition from pyritization (black arrowed area) to dark gray carbonaceous compression and greenish mineral replication (white arrowed area). Rectangles in C, D, and F indicate areas analyzed via ESEM EDS shown respectively in Figs. 4A, 2A–F, and Fig. 3, with white arrows (beside rectangles) indicate top side.

3.2. Carbonaceous compression and association with aluminosilicates Apart from pyritized specimens, the remainder of the Gaojiashan biota is preserved as compressed fossils with two different colors. Dark gray compressions (Fig. 1C–D) represent ~15% of the total assessed specimens, and those replicated by greenish minerals with a greasy luster (Fig. 1E) constitute the remaining ~ 5%. Backscattered z-contrast (atomic number contrast) imaging and EDS elemental mapping of a dark gray-colored Gaojiashania specimen (Fig. 1D) revealed a sharp compositional distinction between the fossil and matrix, and indicated preservation of carbonaceous material or organic remains (Fig. 2A–F). The body rings of this specimen are clearly defined in EDS elemental maps by stronger localization of carbon and

complementary lowered abundances of other elements (Fig. 2C–F). While topography plays a role in elemental mapping, this observed trend of carbon concentration in the body rings of Gaojiashania is supported by EDS point analyses, which are less influenced by topographic variation due to careful selection of points on locally flat surfaces (i.e., maintaining a consistent take-off angle with no large topographic highs nearby to obscure X-ray signal). From numerous point spectra comparing Gaojiashania body rings to the host rock matrix, carbon clearly showed greater abundance on the fossil, with a normalized range of 3.5–5.0 wt.% versus a maximum carbon concentration of b1.0 wt.% in host rock point analyses. In addition, several dark graycolored Conotubus specimens (e.g., Fig. 2G) were longitudinally sectioned and petrographically analyzed. Petrographic observations show

Author's personal copy 112

Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

Fig. 2. Secondary electron (SE) and backscattered electron (BSE) images, energy dispersive X-ray spectroscopic (EDS) elemental maps, and light photomicrographs illustrating preservation of Gaojiashania cyclus and Conotubus hemiannulatus as carbonaceous compression. (A) SE image of a Gaojiashania cyclus specimen (rectangle in Fig. 1D). (B) BSE photomicrograph of A. (C–F) C, O, Si, and Al maps of A. Color intensity corresponds to relative elemental abundance. (G) Reflected light photomicrograph of a Conotubus hemiannulatus specimen preserved as carbonaceous compression. Arrows mark location of thin sections shown in H–J. (H–J) Transmitted light photomicrographs of longitudinal sections cut perpendicular to bedding plane. Note thin (20–50 μm thick in H and J; b 100 μm in I) carbonaceous films (black arrows) defining the fossil and detrital quartz grains (white arrows in I) in host rock matrix.

that, instead of continuous carbonaceous films, the morphological outline of Conotubus is roughly defined by discontinuous kerogen material (Fig. 2H–J). Carbonaceous compressions of Conotubus and Gaojiashania are sometimes associated with localized pyrite and aluminosilicate minerals (Figs. 3, 4A–C, 5A), although this association is not present in all specimens (e.g., Fig. 2A–F). The identification of pyrite is based on the localization of Fe and S, whereas aluminosilicate identification is based on localization of Al and K.

Secondary electron microscopy of Gaojiashan fossils replicated by dark greenish minerals (Fig. 4D) revealed 1–2 μm-sized spheroidal aggregates in an amorphous material (Fig. 4E–F). EDS analysis showed that both the spheroidal aggregates and the amorphous material consist of aluminosilicate minerals, but the aggregates show higher concentrations of Fe (Fig. 5B). The spheroidal aggregates are too small to be analyzed individually using conventional Raman spectroscopy, but Raman spectroscopic analysis of areas that include both aggregates and amorphous material yielded Raman shift peaks (e.g.,

Author's personal copy Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

113

Fig. 3. Backscattered electron (BSE) image and energy dispersive X-ray spectroscopic (EDS) elemental maps illustrating preservation of Gaojiashania cyclus as pyrite molds but with carbonaceous residue and associated aluminosilicates. (A) BSE image of mapped area (rectangle in Fig. 1F). The arcuate bright area corresponds to a ring of Gaojiashania cyclus that is molded by densely packed framboidal pyrite crystals. (B–H) Fe, C, Si, Al, K, O, and Ca maps. Color intensity corresponds to relative elemental abundance. The presence of aluminosilicates is inferred from the co-occurrence of Si, Al, and K, whereas the presence of carbonaceous material from the presence of C independent of Ca.

Fig. 5C) characteristic of chlorite (Wang et al., 2002). We therefore infer that the spheroidal aggregates consist of Fe-rich chloritic minerals. Unlike fossils preserved as dark gray-colored compressions (Figs. 1C–D, 2G), those replicated with greenish minerals contain little or no carbonaceous material. 4. Discussion 4.1. Taphonomic modes A key challenge in our taphonomic analysis relates to the uncertainty of the original composition of Conotubus and Gaojiashania. Although it has been shown that these Gaojiashan fossils likely

represent non-biomineralizing tubular organisms (Cai et al., 2011), the chemical composition and taphonomic lability of the tubes are unknown, hindering a detailed taphonomic comparison with their Phanerozoic counterparts. Nonetheless, certain taphonomic attributes can be inferred from the morphologies of these Gaojiashan fossils. For example, the rings of Gaojiashania are often better preserved and show more three-dimensionality than the annuli that connect the rings (Cai and Hua, 2011), indicating that the former are more recalcitrant than the latter. This distinction provides a basis for our analysis of tissue-specific mineralization processes. The primary mode of mineralization in the Gaojiashan biota is pyritization, a taphonomic process that is responsible, to varying degrees, for soft tissue preservation in a number of Phanerozoic Lagerstätte,

Author's personal copy 114

Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

Fig. 4. Reflected light photomicrograph (D) and secondary electron photomicrographs (A–C, E–F) illustrating the presence of clay minerals in Conotubus hemiannulatus. (A) Secondary electron photomicrograph of a Conotubus hemiannulatus specimen (rectangle in Fig. 1C; the fossil is identified by transverse ornaments marked by black arrows) preserved as carbonaceous compression but associated with clay minerals. (B–C) Close-up views (labeled white arrows in A), showing aluminosilicate minerals identified by EDS analysis (result shown in Fig. 5A). (D) Conotubus hemiannulatus tube preserved as greenish minerals. Labeled arrow marks approximate location of secondary electron photomicrographs shown in E–F. (E–F) Spherical aggregates of possible chlorite and other aluminosilicate minerals (as identified by EDS and Raman data shown in Fig. 5B–C), which are probably diagenetic product of aluminosilicate precursors. Labeled diamonds in E mark locations of EDS point analysis (results shown in Fig. 5B).

including the early Cambrian Chengjiang biota (Gabbott et al., 2004; Hu, 2005; Zhu et al., 2005), the Late Ordovician Beecher's Trilobite Bed (Cisne, 1973; Briggs et al., 1991; Raiswell et al., 2008; Farrell et al., 2009), the Late Ordovician Llanfawr Mudstones biota (Botting et al., 2011), and the Late Devonian Hunsrück Slate biota (Briggs et al., 1996; Raiswell et al., 2008). These biotas show varying degrees of pyritization. Some exhibit thin coatings of pyrite on two-dimensionally compressed fossils or, as is observed in the Chengjiang fossils, pyrite framboids restricted to more labile tissues that supported bacterial sulfate reduction and pyrite precipitation (Gabbott et al., 2004; Hu, 2005; Lin and Briggs, 2010). Others, such as Beecher's Trilobite Bed, display wholesale and pervasive three-dimensional pyritization likely reflecting rapid burial and focused bacterial sulfate reduction on degrading carcasses surrounded by sediments rich in reactive iron but poor in organic carbon (Farrell et al., 2009). Pyritization in the Gaojiashan biota fits with the latter, sharing taphonomic similarities to Beecher's Trilobite Bed, as pervasive pyritization preserves three-dimensional aspects of the organisms. The three dimensionality of pyritized Gaojiashan tubular fossils in conjunction with observed framboidal pyrite crystals

(Fig. 1B) indicates that pyrite precipitation occurred relatively rapidly, prior to both degradational collapse and sediment compaction, furthermore exemplifying the role of early diagenetic pyritization in the replication of the most labile tissues in the Gaojiashan biota. Our analysis also shows that carbonaceous compressions of Conotubus and Gaojiashania are sometimes associated with clay minerals. Similar associations have been reported from other carbonaceous compression fossils (Orr et al., 1998; Anderson et al., 2011), but debate continues on the role that clays play in soft tissue preservation (Butterfield et al., 2007; Page et al., 2008). From currently published taphonomic data, clay minerals have been found in association with soft-tissue preservation in numerous deposits of varying ages, including the Late Ordovician Soom Shale (Gabbott, 1998), Burgess Shale biota (Orr et al., 1998), and organic-walled microfossils from the Ediacaran Doushantuo Formation (Anderson et al., 2011). Several taphonomic hypotheses have been proposed to account for these clay mineral associations, including (1) binding to enzymes to impede autolytic decay (Butterfield, 1995); (2) binding to organic materials (Petrovich, 2001) to promote organic preservation; and (2) authigenic precipitation of

Author's personal copy Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

A

Mg

Al

Si

K

Ca

Fe

O

Fig. 4B

2.8

10.7

25.7

7.6

7.6

7.6

45.5

Fig. 4C

2.8

10.7

27.1

7.1

0.4

5.1

46.3

Mg

Al

Si

K

Ca

Fe

O

Spheroid

1.4

9.6

17.1

2.8

0.7

27.1

41.4

Amorphous material

2.2

10.4

26.1

7.0

/

8.1

45.8

B

Intensity

C

545 396

0

703

500

1000

1500

2000 3900 4000 4100

Raman shift (cm-1)

Fig. 5. Energy dispersive X-ray spectroscopic (EDS) and Raman analyses of clay minerals on Conotubus hemiannulatus specimens. (A–B) EDS point analysis of dark greenish material marked in Fig. 4B–C and E, respectively. Elemental compositions of the analyzed materials are shown in normalized weight percentage. (C) A representative Raman spectrum of greenish material (+spheroidal aggregates) on a Conotubus hemiannulatus specimen. No peaks were identified between wave number 2000 and 3900 cm− 1.

clay minerals that replicates fossils (Orr et al., 1998). It has been argued, however, that these clay mineral associations may have resulted from metamorphic replacement of, or overgrowth on, carbonaceous material, and thus may not have played a constructive role in fossil preservation (Butterfield et al., 2007; Page et al., 2008). Our combined EDS and petrographic observations demonstrate the presence of organic carbon and clay minerals in some Conotubus and Gaojiashania fossils, although our data are insufficient to determine whether these clays are authigenic (Gabbott, 1998; Orr et al., 1998) or detrital in origin. However, as demonstrated by taphonomic experiments, both authigenic and detrital clays may aid in replicating the decaying organisms (Martin et al., 2004; Darroch et al., in press). Replication by greenish minerals may not be unique to Conotubus and Gaojiashania in the Gaojiashan biota. A taphonomic analysis of the problematic fossil Shaanxilithes from the lower Gaojiashan Member also found a preferential presence of greenish clay minerals in the fossils (Meyer et al., in press). The greenish minerals shown in Fig. 1E and Fig. 4D-F may be late diagenetic or metamorphic products. This interpretation is supported by three primary lines of evidence. First, fossils replicated by the greenish minerals are typically preserved with limited morphological details. This morphological ambiguity is strikingly different from fossils preserved as dark gray compressions, which show biological details such as cylinder rims of Conotubus and body rings of Gaojiashania. Second, transitional colors from dark gray to green can be observed on some specimens with intermixed preservational styles (Fig. 1G–H). Third, unlike the Gaojiashan fossils preserved as dark gray carbonaceous compressions in association with aluminosilicates (Figs. 2–3), organic remains have not been detected in association with greenish minerals in our EDS analysis (Fig. 5B). The presence of spheroidal aggregates of possibly chlorite (Figs. 4E–F, 5B–C) indicates that the greenish minerals are likely a

115

product of chloritization; thus, although their precursors may have played a role in fossil preservation, the greenish minerals themselves played no constructive role. Comparison of the different preservational modes within the Gaojiashan biota shows that authigenic pyritization can preserve more labile tissues, whereas carbonaceous compression (with or without clay association) tend to preserve more recalcitrant tissues. In other literature describing the taphonomy of BST fossils, it has been suggested that tissues preserved as carbonaceous compressions represent remains of recalcitrant structures, such as the carapaces of arthropods (Butterfield, 2003). Early authigenic pyritization, on the other hand, can capture intricate details of delicate and easily degradable features, such as the antennae and appendages of arthropods (Briggs et al., 1991; Briggs et al., 1996; Gabbott et al., 2004; Farrell et al., 2009). Investigation of the early Cambrian Chengjiang biota also illustrates that more labile tissues were often preserved through pyritization resulting from localized degradation by sulfate reduction bacteria, whereas recalcitrant tissues are preserved as carbonaceous compression (Gabbott et al., 2004; Hou et al., 2004; Zhu et al., 2005). Similarly, in the Gaojiashan fossils, carbonaceous-aluminosilicate compressions are found to preserve presumably recalcitrant anatomies (such as the rings of Gaojiashania) in two dimensions, whereas pyritization preserves features interpreted to be more labile, including the annuli of Gaojiashania, sometimes in three dimensions. There is an obvious but important distinction in the pervasiveness of pyritization between the Chengjiang and Gaojiashan biotas: Chengjiang fossils are two-dimensionally preserved and characterized by highly localized, tissue-specific, pyritization, whereas Gaojiashan fossils are fully pyritized in three dimensions. A potential explanation for this difference may stem from biostratinomic limitations: unlike Chengjiang fossils that are preserved in finer-grained mudstones/claystones, Gaojiashan fossils are preferentially embedded in siltstones (Cai et al., 2010). As siltstones contain coarser grains than those of mudstones and therefore have comparatively higher permeability, it is likely that, with greater accessibility to seawater sulfate, more extensive degradation through bacterial sulfate reduction may have occurred during the preservation of Gaojiashan fossils. Other important factors in threedimensional pyritization include (1) a relatively low organic content in matrix sediments so that sulfate reduction can be focused on metabolizable tissues of the degrading organism (Briggs et al., 1991) and (2) availability of reactive iron to trap H2S resulting from bacterial sulfate reduction and to precipitate pyrite in direct proximity to the degrading organism before its collapse (Xiao et al., 2010). In contrast, twodimensional carbonaceous compression can be facilitated by pyrite formation only if bacterial sulfate reduction is terminated early so that only sporadic pyrite is formed to replicate soft tissues. The early termination could be due to the sulfate limitation in the sediments, potentially resulting from the low permeability of fine-grained sediments (thus limited accessibility to seawater sulfate) or the consumption of sulfate by organic carbon in matrix sediments. Thus, pyritization can be a double-edged taphonomic sword. On one hand, authigenic pyrite can replicate labile tissues if there are mechanisms to form a thin pyrite coat on soft tissues. On the other hand, pyritization depends on bacterial sulfate reduction which is itself a destructive process, and extensive sulfate reduction can lead to complete loss of anatomical details. Furthermore, recrystallization and overgrowth of authigenic pyrite can also limit preservational resolution. In other words, the taphonomic resolution of the pyritization window depends on a delicate balance between sulfate reduction and mineralization. It is also important to point out that three-dimensional pyritization may be size selective. After all, wholesale pyritization of volumetrically larger organisms would require greater availability of degradable organic carbon, sulfate, and reactive iron to precipitate pyrite. Thus, the two-dimensional preservation of some Chengjiang fossils, with light and localized pyritization, might be in part related to a balance between their relatively large size and the capacity of pyrite precipitation.

Author's personal copy 116

Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

Although the Gaojiashan fossils Conotubus and Gaojiashania can reach 18 cm in length, they are volumetrically small because they are typically just a few mm in diameter. Their conotubular and cylindrical shape, with small surface area to volume ratios, is particularly conducive to the containment of H2S by reactive iron from the ambient sediments (Xiao et al., 2010). It would be a profitable line of research to estimate the theoretical size limit on three-dimensional pyritization and to explore the empirical data to see whether (and why) there is a secular trend in the size of pervasively pyritized fossils.

4.2. Taphonomic processes Our taphonomic data show that soft-tissue preservation in siliciclastic rocks can be driven by several diagenetic processes. These endmembers, including kerogenization or polymerization of organic compounds (Stankiewicz et al., 2000; Gupta et al., 2007; Gupta and Briggs, 2011), clay mineral replication or aluminosilicification (Orr et al., 1998), and pyritization (Briggs et al., 1991), can occur within the same deposit or even the same specimen, as exemplified by the Gaojiashan fossils. We have devised a ternary diagram to visualize the contribution of these three taphonomic processes to the preservation of soft-bodied organisms (Fig. 6). Other mineralization processes, such as calcification, phosphatization and silicification, are not included in the ternary diagram because we have focused only on the preservation of soft tissues within siliciclastic rocks based on our case study of the Gaojiashan biota, where these processes are unimportant and do not form a gradient with kerogenization, aluminosilicification, and pyritization. Future research can of course extend this approach to include other mineralization processes (e.g., phosphatization; Butterfield, 2002) if they are found to also contribute to soft-tissue preservation in siliciclastic facies.

BST preservation mode

Sh al e

Kerogenization

en gj ia ng

n

tio

iza

rit

eu se ium in ca osil tio ici n f

Py

Beecher's Trilobite Bed

Al

Hunsrück

m

So

om

ao jia sh an

Fe r

G

Bu

Ch

rg es s

Miaohe

To illustrate the gradient between kerogenization, aluminosilicification, and pyritization, we have plotted some important examples of soft-tissue preservation (by no means an exhaustive list) in the ternary diagram (Fig. 6). Kerogenization is a significant taphonomic process in carbonaceous compression of Ediacaran and Cambrian BST preservation (Gaines et al., 2008). Preservation of soft-bodied fossils through aluminosilicification or clay mineral association is best seen in the Ediacaran Fermeuse-style preservation (Narbonne, 2005; Laflamme et al., 2011), the Late Ordovician Soom Shale (Gabbott, 1998), Shaanxilithes fossils from the lower Gaojiashan Member (Meyer et al., in press), and some carbonaceous compression fossils (Orr et al., 1998; Zhu et al., 2005; Anderson et al., 2011). Soft-tissue preservation dominated by pyritization is well documented in the Late Ordovician Beecher's Trilobite Bed (Cisne, 1973; Briggs et al., 1991; Raiswell et al., 2008; Farrell et al., 2009), the Late Ordovician Llanfawr Mudstones biota (Botting et al., 2011), and the Late Devonian Hunsrück Slate (Briggs et al., 1996; Bartels et al., 1998; Raiswell et al., 2008). The Gaojiashan case study indicates that preservation of soft tissues in siliciclastic facies through these taphonomic pathways can occur in the same fossil assemblage, as is also supported by taphonomic analysis of the Cambrian Chengjiang and Kaili biotas (Gabbott et al., 2004; Zhu et al., 2005; Lin and Briggs, 2010). The dashed circle in Fig. 6 denotes the realm of the BST preservational mode. The original definition of BST preservation is one of taphonomic mode (i.e., carbonaceous compressions) (Butterfield, 1995; Gaines et al., 2008). A number of proximal taphonomic processes (e.g., kerogenization, clay template formation, pyrite formation) and distal biostratinomic conditions (e.g., delay of degradation through clay-enzyme bonding, dysoxia or anoxia, lack of bioturbation, and early diagenetic carbonate cementation) have been proposed to explain the BST preservational mode. We propose that these factors are not mutually exclusive, and they may all contribute to BST preservation. The ternary diagram in Fig. 6 emphasizes the constructive processes that contribute to the geological stability of BST preservation; after all, for BST preservation to be successful, the fossils need to be preserved or replicated by geologically stable material (e.g., minerals or kerogen). Thus, our analysis supports the view that some form of mineralization plays a proximal and constructive role in the preservation of soft-bodied fossils (Briggs, 2003). If so, then the predominance of Cambrian and Jurassic Konservat-Lagerstätten (Allison and Briggs, 1993) should find more distal explanations among factors that promote these constructive processes, as well as factors that inhibit destructive processes. Bioturbation is certainly such a factor, because it impacts sulfur recycling and remineralization of organic material (Canfield and Farquhar, 2009). Other distal factors include, but are not limited to, ocean redox conditions, seawater sulfate concentrations, seawater silica concentration, and pH–Eh conditions that influence authigenic mineralization. Tests of these controls require more geochemical data to quantify ancient sedimentary and diagenetic environments.

Fig. 6. Ternary diagram showing three interrelated taphonomic processes (kerogenization, pyritization, and aluminosilicification, as represented in the corners) that can potentially contribute to the taphonomic mode of BST preservation (represented by the dashed circle). This ternary diagram illustrates that some sort of mineralization or stabilization is needed in BST preservation, that multiple processes can fulfill this role, and that there may exist a continuous gradient between various preservation modes depending on the varying levels of influence of different taphonomic processes. Exemplary Lagerstätten are plotted in the ternary diagram based on our preliminary and qualitative evaluation of their taphonomy.

5. Conclusions The late Ediacaran Gaojiashan Lagerstätte is characterized by several taphonomic modes—primarily authigenic pyritization and auxiliarily carbonaceous compression and aluminosilicification. These taphonomic modes and their underlying processes can sometimes be found in a single specimen, indicating that conditions conducive to a specific taphonomic pathway can be highly localized. The lack of predators, scavengers, or deep bioturbators in Ediacaran oceans, together with ocean redox conditions in the Ediacaran Period, may have distally contributed to the exceptional preservation of the Gaojiashan biota, but the proximal and constructive processes—such as early authigenic mineralization and kerogenization—are directly responsible for fossil preservation. Because many Palaeozoic Lagerstätten

Author's personal copy Y. Cai et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 109–117

share taphonomic modes with the Gaojiashan biota, the uneven distribution of exceptional preservation in geologic history may be related to factors that ultimately influence the constructive and destructive taphonomic processes. Acknowledgments We thank Hujun Gong for help with SEM analyses, Xingliang Zhang and Maoyan Zhu for valuable discussion, and two anonymous reviewers for critical comments. ESEM and EDS analyses were conducted at the State Key Laboratory of Continental Dynamics and Virginia Tech Institute of Critical Technology and Applied Science Nanoscale Characterization and Fabrication Laboratory. This work was supported by the National Natural Science Foundation of China (nos. 40872021, 41030209, 41028002), Program for New Century Excellent Talents in Universities, NASA Exobiology and Evolutionary Biology Program, State Key Laboratory of Continental Dynamics Research Project, and Northwest University Doctoral Dissertation Funds (no. 09YYB01). References Allison, P.A., Brett, C.E., 1995. In situ benthos and paleo-oxygenation in the Middle Cambrian Burgess Shale, British Columbia, Canada. Geology 23, 1079–1082. Allison, P.A., Briggs, D.E.G., 1993. Exceptional fossil record: distribution of soft-tissue preservation through the Phanerozoic. Geology 21, 527–530. Anderson, E.P., Schiffbauer, J.D., Xiao, S., 2011. Taphonomic study of Ediacaran organicwalled fossils confirms the importance of clay minerals and pyrite in Burgess Shale-type preservation. Geology 39, 643–646. Bartels, C., Briggs, D.E.G., Brassel, G., 1998. The Fossils of the Hunsrück Slate: Marine Life in the Devonian. Cambridge University Press, Cambridge. 309 pp. Botting, J.P., Muir, L.A., Sutton, M.D., Barnie, T., 2011. Welsh gold: a new exceptionally preserved pyritized Ordovician biota. Geology 39, 879–882. Bottjer, D., 2002. Enigmatic Ediacara fossils: ancestors or aliens? In: Bottjer, D., Etter, W., Hagadorn, J.W., Tang, C.M. (Eds.), Exceptional Fossil Preservation: A Unique View on the Evolution of Marine Life. Columbia University Press, New York, pp. 11–33. Bottjer, D.J., Etter, W., Hagadorn, J.M., Tang, C.M., 2002. Fossil-Lagerstätten: jewels of the fossil record. In: Bottjer, D.J., Etter, W., Hagadorn, J.M., Tang, C.M. (Eds.), Exceptional Fossil Preservation: A Unique View on the Evolution of Marine Life. Columbia University Press, New York, pp. 1–10. Briggs, D.E.G., 2003. The role of decay and mineralization in the preservation of softbodied fossils. Annual Review of Earth and Planetary Sciences 31, 275–301. doi:10.1146/annurev.earth.31.100901.144746. Briggs, D.E.G., Bottrell, S.H., Raiswell, R., 1991. Pyritization of soft-bodied fossils: Beecher's Trilobite Bed, Upper Ordovician, New York State. Geology 19, 1221–1224. Briggs, D.E.G., Raiswell, R., Bottrell, S.H., Hatfield, D., Bartels, C., 1996. Controls on the pyritization of exceptionally preserved fossils: an analysis of the Lower Devonian Hunsrück Slate of Germany. American Journal of Science 296, 633–663. Butterfield, N.J., 1995. Secular distribution of Burgess Shale-type preservation. Lethaia 28, 1–13. Butterfield, N.J., 2002. Leanchoilia guts and the interpretation of three-dimensional structures in Burgess Shale-type fossils. Paleobiology 28, 155–171. Butterfield, N.J., 2003. Exceptional fossil preservation and the Cambrian Explosion. Integrative and Comparative Biology 43, 166–177. Butterfield, N.J., Balthasar, U., Wilson, L.A., 2007. Fossil diagenesis in the Burgess Shale. Palaeontology 50, 537–543. Cai, Y., Hua, H., 2007. Pyritization in the Gaojiashan Biota. Chinese Science Bulletin 52, 645–650. Cai, Y., Hua, H., 2011. Discussion of ‘First finds of problematic Ediacaran fossil Gaojiashania in Siberia and its origin’. Geological Magazine 148, 329–333. Cai, Y., Hua, H., Xiao, S., Schiffbauer, J.D., Li, P., 2010. Biostratinomy of the late Ediacaran pyritized Gaojiashan Lagerstätte from southern Shaanxi, South China: importance of event deposits. Palaios 25, 487–506. Cai, Y., Schiffbauer, J.D., Hua, H., Xiao, S., 2011. Morphology and paleoecology of the late Ediacaran tubular fossil Conotubus hemiannulatus from the Gaojiashan Lagerstätte of southern Shaanxi Province, South China. Precambrian Research 191, 46–57. Canfield, D.E., Farquhar, J., 2009. Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proceedings of the National Academy of Sciences of the United States of America 106, 8123–8127. Cisne, J.L., 1973. Beecher's Trilobite Bed revisited: ecology of an Ordovician deepwater fauna. Postilla 160, 1–25. Darroch, S.A.F., Laflamme, M., Schiffbauer, J.D., Briggs, D.E.G., in press. Experimental formation of a microbial death mask. Palaios. Farrell, Ú.C., Martin, M.J., Hagadorn, J.W., Whiteley, T., Briggs, D.E.G., 2009. Beyond Beecher's Trilobite Bed: widespread pyritization of soft tissues in the Late Ordovician Taconic foreland basin. Geology 37, 907–910. Gabbott, S.E., 1998. Taphonomy of the Upper Ordovician Soom Shale Lagerstätte: a unique example of soft tissue preservation in clay minerals. Palaeontology 41, 631–637.

117

Gabbott, S.E., Hou, X.G., Norry, M.J., Siveter, D.J., 2004. Preservation of Early Cambrian animals of the Chengjiang biota. Geology 32, 901–904. Gaines, R.R., Kennedy, M.J., Droser, M.L., 2005. A new hypothesis for organic preservation of Burgess Shale taxa in the Middle Cambrian Wheeler Formation, House Range, Utah. Palaeogeography, Palaeoclimatology, Palaeoecology 220, 193–205. Gaines, R.R., Briggs, D.E.G., Zhao, Y.L., 2008. Cambrian Burgess Shale-type deposits share a common mode of fossilization. Geology 36, 755–758. Gaines, R.R., Droser, M.L., Orr, P.J., Garson, D., Hammarlund, E., Qi, C., Canfield, D.E., 2012. Burgess shale-type biotas were not entirely burrowed away. Geology 40. doi:10.1130/G32555.1. Gehling, J.G., 1999. Microbial mats in terminal Proterozoic siliciclastics: Ediacaran death masks. Palaios 14, 40–57. Gupta, N.S., Briggs, D.E.G., 2011. Taphonomy of animal organic skeletons through time. In: Allison, P.A., Bottjer, D.J. (Eds.), Taphonomy: Process and Bias Through Time. Springer, Dordrecht. Gupta, N.S., Briggs, D.E.G., Collinson, M.E., Evershed, R.P., Michels, R., Jack, K.S., Pancost, R.D., 2007. Evidence for the in situ polymerisation of labile aliphatic organic compounds during the preservation of fossil leaves: implications for organic matter preservation. Organic Geochemistry 38, 499–522. Hou, X., Aldridge, R.J., Bergström, J., Siveter, D.J., Siveter, D.J., Wang, H., 2004. The Cambrian Fossils of Chengjiang, China: The Flowering of Early Animal Life. Blackwell Science, Oxford, UK. 233 pp. Hu, S., 2005. Taphonomy and paleoecology of the Early Cambrian Chengjiang Biota from Eastern Yunnan, China, Band 7. Berliner Paläobiologische Abhandlungen, Berliner. 197 pp. Laflamme, M., Schiffbauer, J.D., Narbonne, G.M., Briggs, D.E.G., 2011. Microbial biofilms and the preservation of the Ediacara biota. Lethaia 44, 203–213. Lin, J.P., Briggs, D.E.G., 2010. Burgess Shale-type preservation: a comparison of naraoiids (Arthropoda) from three Cambrian localities. Palaios 25, 463–467. Martin, D., Briggs, D.E.G., Parkes, R.J., 2004. Experimental attachment of sediment particles to invertebrate eggs and the preservation of soft-bodied fossils. Journal of the Geological Society of London 161, 735–738. Meyer, M., Schiffbauer, J.D., Xiao, S., Cai, Y., Hua, H., in press. Taphonomy of the late Ediacaran enigmatic ribbon-like fossil Shaanxilithes. Narbonne, G.M., 2005. The Ediacara Biota: Neoproterozoic origin of animals and their ecosystems. Annual Review of Earth and Planetary Sciences 33, 421–442. Orr, P.J., Briggs, D.E.G., Kearns, S.L., 1998. Cambrian Burgess Shale animals replicated in clay minerals. Science 281, 1173–1175. Orr, P.J., Benton, M.J., Briggs, D.E.G., 2003. Post-Cambrian closure of the deep-water slope-basin taphonomic window. Geology 31, 769–772. Page, A., Gabbott, S.E., Wilby, P.R., Zalasiewicz, J.A., 2008. Ubiquitous Burgess Shalestyle “clay templates” in low-grade metamorphic mudrocks. Geology 36, 855–858. Petrovich, R., 2001. Mechanisms of fossilization of the soft-bodied and lightly armored faunas of the Burgess Shale and of some other classical localities. American Journal of Science 301, 683–726. Raiswell, R., Newton, R.J., Bottrell, S.H., Coburn, P.M., Briggs, D.E.G., Bond, D.P.G., Poulton, S.W., 2008. Turbidite depositional influences on the diagenesis of Beecher's Trilobite bed and the Hunsrück Slate: site of soft tissue pyritization. American Journal of Science 308, 105–129. Schiffbauer, J.D., Xiao, S., Sen Sharma, K., Wang, G., 2012. The origin of intracellular structures in Ediacaran metazoan embryos. Geology 40, 223–226. Stankiewicz, B.A., Briggs, D.E.G., Michels, R., Collinson, M.E., Flannery, M.B., Evershed, R.P., 2000. Alternative origin of aliphatic polymer in kerogen. Geology 28, 559–562. Tang, F., Yin, C., Bengtson, S., Liu, P., Wang, Z., Gao, L., 2008. Octoradiate spiral organisms in the Ediacaran of South China. Acta Geologica Sinica 82, 27–34. Van Roy, P., Orr, P.J., Botting, J.P., Muir, L.A., Vinther, J., Lefebvre, B., Hariri, K., Briggs, D.E.G., 2010. Ordovician faunas of Burgess Shale type. Nature 465, 215–218. Wang, A., Freeman, J., Kuebler, K.E., 2002. Raman spectroscopic characterization of phyllosilicates. 33rd Annual Lunar and Planetary Science Conference, Houston, Texas, pp. 1–2. Xiao, S., Knoll, A.H., 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32, 219–240. Xiao, S., Laflamme, M., 2009. On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends in Ecology & Evolution 24, 31–40. Xiao, S., Schiffbauer, J.D., 2009. Fossil preservation through phosphatization and its astrobiological implications. In: Seckbach, J., Walsh, M. (Eds.), From Fossils to Astrobiology. Springer, New York. Xiao, S., Zhang, Y., Knoll, A.H., 1998. Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite. Nature 391, 553–558. Xiao, S., Yuan, X., Steiner, M., Knoll, A.H., 2002. Macroscopic carbonaceous compressions in a terminal Proterozoic shale: a systematic reassessment of the Miaohe biota, South China. Journal of Paleontology 76, 347–376. Xiao, S., Schiffbauer, J.D., McFadden, K.A., Hunter, J., 2010. Petrographic and SIMS pyrite sulfur isotope analyses of Ediacaran chert nodules: implications for microbial processes in pyrite rim formation, silicification, and exceptional fossil preservation. Earth and Planetary Science Letters 297, 481–495. Zhu, M., Babcock, L.E., Steiner, M., 2005. Fossilization modes in the Chengjiang Lagerstätte (Cambrian of China): testing the roles of organic preservation and diagenetic alteration in exceptional preservation. Palaeogeography, Palaeoclimatology, Palaeoecology 220, 31–46. Zhu, M., Gehling, J.G., Xiao, S., Zhao, Y., Droser, M.L., 2008. Eight-armed Ediacara fossil preserved in contrasting taphonomic windows from China and Australia. Geology 36, 867–870.