- Email: [email protected]
Euendoliths versus ambient inclusion trails from Early Cambrian Kuanchuanpu Formation, South China
Accepted Manuscript Euendoliths versus ambient inclusion trails from Early Cambrian Kuanchuanpu Formation, South China
Xiao-guang Yang, Jian Han, Xing Wang, James D. Schiffbauer, Kentaro Uesugi, Osamu Sasaki, Tsuyoshi Komiya PII: DOI: Reference:
S0031-0182(16)30465-5 doi: 10.1016/j.palaeo.2017.03.028 PALAEO 8251
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
13 September 2016 28 March 2017 30 March 2017
Please cite this article as: Xiao-guang Yang, Jian Han, Xing Wang, James D. Schiffbauer, Kentaro Uesugi, Osamu Sasaki, Tsuyoshi Komiya , Euendoliths versus ambient inclusion trails from Early Cambrian Kuanchuanpu Formation, South China. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Palaeo(2017), doi: 10.1016/j.palaeo.2017.03.028
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Euendoliths versus Ambient Inclusion Trails from Early Cambrian Kuanchuanpu Formation, South China
PT
Xiao-guang Yanga, Jian Hana*, Xing Wanga, James D. Schiffbauerb, Kentaro Uesugic,
RI
Osamu Sasakid, Tsuyoshi Komiyae a
SC
State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University, 229 Taibai Road, Xi'an 710069, P.R. China ([email protected])
b
MA
Columbia 65211, Missouri, USA
NU
Department of Geological Sciences, University of Missouri, 101 Geology Building,
c
PT E
Sayo-gun, Hyogo, Japan
D
Japan Synchrotron Radiation Research Institute (JASRI), 1-1-1 Kouto, Sayo-cho,
d
Tohoku University Museum, Tohoku University, 6-3 Aoba, Aramaki, Aoba-ku, Sendai,
e
CE
Japan
Department of Earth Science and Astronomy, Graduate School of Arts and Sciences,
AC
The University of Tokyo, Tokyo 153-8902, Japan
* To whom correspondence should be addressed. E-mail: [email protected]
Abstract: Abundant microstructures have been discovered in small skeletal fossils (SSFs) and embryo-like fossils collected from the Lower Cambrian Kuanchuanpu Formation (ca. 535 Ma) in Xixiang County, Shaanxi Province, China. These involve
ACCEPTED MANUSCRIPT two co-occurring structures: (1) long, unbranched cylindrical filaments, which are comparable to phosphatic casts of microborings constructed by euendolithic cyanobacteria (Endoconchia lata) in morphology and preservation pathway; and (2) meandering micro-tubes or grooves on fossil moulds (and steinkerns) of a wide range
PT
of sizes and morphological diversities, perceived as ambient inclusion trails (AITs).
RI
Herein, we also report a new occurrence of organic carbon spherules as
SC
AIT-propelled material, which is rare in comparable fossils. From direct comparison of endolithic traces and AITs, we propose a mechanism to account for their notably
NU
different preservation, and further attempt to offer an explanation for their
MA
co-occurrence. Their differential preservation suggests a chronological, taphonomic sequence of their formation. We interpret that E. lata microborings formed prior to
D
phosphate sedimentation, whereas AITs are likely generated in a later phase of (or
PT E
after) phosphorite precipitation but before calcareous re-cementation. Dissecting the sequence of formation of these structures, in conjunction with detailed morphological
CE
observations, assists in distinguishing true biologically produced endoliths from
AC
otherwise abiogenically produced microstructures.
Keywords: cyanobacteria; Endoconchia lata; microborings; small skeletal fossils; phosphatized fossils
1. Introduction
Microtubular structures recorded in rocks have been reported broadly through
ACCEPTED MANUSCRIPT geologic time, from the Archean through the Palaeozoic, and in various matrices, such as chert, sandstone, or phosphorite. (Tyler and Barghoorn, 1963; Knoll and Barghoorn, 1974; Grey, 1986; Xiao and Knoll, 1999; Brasier et al., 2006; Wacey et al., 2006, 2008a, b; McLoughlin et al., 2007). Such structures are often termed “ambient
PT
inclusion trails” (AITs), and a recent summary of AIT studies suggests that AITs are
RI
predominantly generated by migration of mineral crystals, often pyrite, through a
SC
lithified fine-grained substrate (Wacey et al., 2008b). So far, most AITs are known from thin sections of Archean and Proterozoic rocks, although AITs have additionally been
NU
identified from Palaeozoic fossils (Olempska and Wacey, 2016). While analogous
MA
Palaeozoic tubular structures are more often surmised as traces of boring animals or endolithic micro-organisms (Hinz-Schallreuter et al., 1998; Stockfors and Peel, 2005b;
D
Conway Morris et al., 1994; Zhang and Pratt, 2008). Mircoborings made by endoliths
PT E
(Knoll et al., 1986; Campbell, 1982; Golubic, 1969; Zhang and Golubic, 1987; Golubic et al., 1984, 2000; Furnes et al., 2004; Stockfors and Peel, 2005a) or possibly by
CE
predatory animals (Bengtson et al., 1992; Hua et al., 2003) are widespread through at
AC
least the Phanaerozoic record, yet the recognition of AIT is still somehow equivocal, especially with regarding to the bioturbation in Palaeozoic.
Herein, we describe a co-occurrence of AITs and euendolithic traces from phosphatized microfossils of the Lower Cambrian Kuanchuanpu Formation in Xixiang County, Shaanxi Province, China, and report a new occurrence of organic carbon spherules as AIT-propelled material (or terminal grains).
Previous studies on either AITs or euendoliths tend to treat these structures
ACCEPTED MANUSCRIPT separately. Their co-occurrence in phosphatized microfossils from the Kuanchuanpu Formation, however, permits direct comparison from a single unit. Recognition of chronological ordering of these structures during the taphonomic sequence of the fossils thus enables us to conceptualize a preservational model to explain their
PT
co-occurrence and help us to recognize the diagenetic stage of AIT formation in this
NU
SC
morphology between AITs and euendolith traces.
RI
case. As we describe here, there are distinctions in the formation, preservation, and
MA
2. Geological Setting
All specimens described herein were collected from the Lower Cambrian
D
Kuanchuanpu Formation in Xixiang County, Shaanxi Province. This fossil locality
PT E
belongs to the northern margin of the Yangtze Block and was first reported by Li (1984) as the Zhangjiagou Section, named after the nearby village about 55 km to the
CE
southwest of the administrative center of Xixiang (Fig. 1A).
AC
The Kuanchuanpu Formation is well exposed at this section, with a total thickness of ca. 21 m. It disconformably underlies the black shale of the Lower Cambrian Guojiaba Formation, and conformably overlies the Neoproterozoic Upper Dolomite Member of the Dengying Formation. From lower to upper, the Kuanchuanpu Formation can be subdivided into 4 units as follows: (1) grey blocks of microsparitic limestone (0.8 m); (2) grey and white blocks of phosphorus limestone (2.2 m); (3) thick-bedded dark grey microsparitic limestone (17.4 m); (4) thin-bedded light grey
ACCEPTED MANUSCRIPT silty-fine dolomitic limestone (0.6 m) (Fig. 1B).
In contrast to the sparsely fossiliferous units 1 and 4, units 2 and 3 contain a high abundance of various small shelly fossils (SSFs), including Protohertzina anabarica, Canopoconus calvatus, Conotheca subcurvata, Olivooides multisulcatus, and
PT
Olivooides mirabilis. Preliminary taxon counts show that Conotheca is the dominant
et
al.
2012),
with
SSF
taxa
comparable
to
the
Anabarites
SC
(Peng
RI
genus. The fossiliferous horizon belongs to the Fortunian Stage, Terreneuvian Series
NU
trisulcatus-Protohertzina anabarica assemblage zone (Steiner et al. 2007). The assemblage can be correlated with that in the Meishucun section, Yunnan Province,
MA
South China, which, from U–Pb dating, has been assigned an age of ca. 536.5±2.5 Ma (Sawaki et al. 2008). From additional comparisons of SSF assemblages and other
D
radiometric dating results, Steiner et al. (2014) estimated the age of comparable fossil
CE
PT E
horizons to be approximately 535 Ma.
AC
3. Materials and Methods
The majority of our collected samples came from the top of Kuanchuanpu Formation unit 2. Fossil material was extracted from rock samples using acid maceration with an 8% acetic acid solution. The residuals were examined using standard binocular microscopy. After optical inspection, selected specimens were coated with gold and examined using a FEI Quanta 400F scanning electron microscope (SEM), equipped with an Oxford Instruments energy dispersive X-ray
ACCEPTED MANUSCRIPT spectrometer (EDS). Related thin sections were additionally examined using crossed polarizing microscopy and cathodoluminescence microscopy (CL). Spot analysis by laser micro-Raman spectroscopy was additionally utilized for clarification of the chemical composition of some enigmatic, spherical AIT terminal grains. We
PT
deliberately crushed one phosphatic fossil to retrieve such terminal grains distributed
RI
on different sides of the host specimen. These grains, together with another terminal
SC
particle found from thin section, were spotted with a 50× objective and a 20 μm diameter pinhole in a Renishaw inVia confocal Raman microscope equipped with a
NU
514.5nm laser. After Raman analysis, the spherical grains were subsequently coated
MA
with gold and imaged via SEM. Select specimens were additionally investigated with a ScanXmate-D160TSS105/11000 X-ray microcomputed tomographic microscope
D
(µCT) in Tohoku University, Japan (110 KeV, 0.812 μm3/pixel), as well as synchrotron
PT E
radiation X-ray tomographic microscopy (SRXTM) of SPring-8 in Hyogo, Japan (20 KeV, 0.37 μm3/pixel). All µCT and SRXTM data were processed with VG Studio 2.2
CE
Max software for tomographic analysis and 3D visualization. All analyzed specimens
AC
are housed in the Early Life Institute, Northwest University, Xi'an, Shaanxi, China.
4. Description
4.1 Euendoliths
The euendoliths observed here are preserved as phosphatic casts on the surface of steinkerns or moulds of tube-like SSFs, such as Conotheca. Conotheca is a
ACCEPTED MANUSCRIPT millimeter-sized, cone-shaped, tubular SSF that occurs widely in deposits of Siberia, China, India, and France, and ranges from the Lower to Middle Tommotian Stage of the Cambrian Period. The tube of Conotheca is straight to curved, with a closed and somewhat blunt base, and a straight aperture. It is circular in transverse section and
PT
shows no indication of internal septa (Steiner et al., 2004). Most Conotheca samples
RI
examined here exhibit a multi-layered cone-in-cone construction, although the
SC
skeletal carbonate is not preserved (Fig. 2C–D). In these samples, the euendolith casts are always oriented parallel or sub-parallel to each layer and they never cross
NU
different layers.
MA
The euendolith casts appear as long, non-branched, cylindrical filaments (Fig. 2A–C), with a mean diameter of 6.9 μm (range = 5.5 to 7.5 μm), and an observed
D
length of up to approximately 300 μm. A clear moniliform shape can be observed in
PT E
some of our specimens, consisting of isodiametric spheroidal expansions, with consistent diameters of about 9 μm.
Some parts of the filaments bear a distinctive
CE
oblique decoration (Fig. 2F), appearing as tiny threads on the surface of the
AC
phosphatic infill. These threads, or micro-filaments, are typically separate, with some interlacing and appearing to form pseudo-branches. The joints of these pseudo-branches show that the filaments are actually in different planes, indicating overlap of independent microfilaments (Fig. 2B).
4.2 Ambient Inclusion Trails
The AITs are present as meandering micro-grooves or tubes with longitudinal wall
ACCEPTED MANUSCRIPT striations on various types of phosphatized fossils, including the internal moulds or steinkerns of SSFs, unknown fragments, and rounded fossils (Fig. 3, 6). The Kuanchuanpu Formation in the sampled region is famous for rounded embryo fossils, such as Olivooides; the rounded fossils examined here, although similar in size, lack
PT
both characteristic surface ornaments and internal structures, and thus we
RI
conservatively refer to them as embryo-like fossils. The AITs occur singly, or
SC
sometimes form various assemblages. The AITs predominantly appear gently curved, while some have sharp changes in direction (Fig. 3B, 4C–D). These features are
NU
highly comparable to those AITs described by Knoll and Barghoorn (1974), Xiao and
MA
Knoll (1999), Wacey et al. (2008b), and Olempska and Wacey (2016). The distribution of AITs is random, they can be found almost everywhere within the fossils, regardless
D
of taxonomy or different biological tissues.
PT E
Detailed observations of the copious AIT-hosting specimens reveal that the morphology of AITs in microscale is extremely irregular in several respects: (1) The
CE
size of AITs from our materials ranges from a minimum of 2.5 µm (Fig. 4B) to 75 µm
AC
(Fig. 4C), while those with a diameter of 10–20 µm being the most common. Starting or ending points are difficult to determine in the current specimens, and so an approximation of length would be tenuous. (2) The shapes of the AIT cross-sections were usually thought to be polygonal or rectangular, but some distinctively rounded ones can be found, along with some that host spherical, organic carbon terminal grains (Fig. 6). The margins of the AITs match closely with the edge of grains (Fig. 4A, 6B–C). Lateral study prove that the spherical terminal grains are primarily composed
ACCEPTED MANUSCRIPT of organic carbon (Fig. 6). (3) Most of the AITs are characterized by longitudinal fluting. This surface decoration is formed by non-intersecting, concave-sided ridges running parallel to each other. These features are also variable, with some arranged neatly with a relatively uniform size (Fig. 3A, 4B), and others showing varied widths and
PT
intervals within a single trail, especially in the larger ones (Fig. 4C, 7). In yet other
RI
specimens, these wall striations are faint, giving the appearance of smooth inner walls
SC
and perhaps suggesting that they may have been altered to varying degrees (Fig. 4D, F). Additional perforations were observed along the sidewall in many instances (Fig.
NU
4D).
MA
The assemblages of AITs also show irregular patterns, mainly divided into two types: (1) dense concentrations of single tubes, intercrossing and cutting through
PT E
surface (Fig. 3D).
D
each other (Fig. 3C,4E); and (2) numerous congested micro-tubes, forming a ragged
CE
From µCT and SRXTM techniques, we generated a three-dimensional reconstruction of one specimen with well-developed AITs (ELIXX29-22). The irregular
AC
cross-sections (Fig. 5C) and the randomly oriented AITs with dramatic change in size (Fig. 5D) are well displayed by the tomographic image and 3D visualized model.
5. Discussion
5.1 Euendolithic identity
The genus Endoconchia was established by Runnegar (in Bengtson et al., 1990)
ACCEPTED MANUSCRIPT with two species described: E. lata and E. angusta. E.lata is characterized by a constant diameter of 10 μm while E.angusta is much thinner (about 3 μm) with some distinct bulbous chambers in the ends and some points along the filaments, which could expand to 5 μm and were similar with the structures of heterocysts. The
PT
morphology of those micro-filaments described here corresponds well with the genus
RI
Endoconchia, and their consistent parallel arrangement along the original shell
SC
material also suggests an euendolithic identity (Fig. 10 in Bengtson et al., 1990, pp
NU
22–24).
The filaments in our materials, however, present a slightly smaller diameter than
MA
E. lata (Runnegar, 1985a, b; in Bengtson et al., 1990) and show more continuous and well-developed spheroidal swellings (Fig. 1B). Such a smaller diameter could also be
D
seen from E. lata in Maidiping Formation of Sichuan, China, which is about 2.5–5 μm
PT E
(Qian et al., 2007). Spheroidal expansions are more common in the other species E. angusta, but the diameter of these bulbs or bead structures as described in E.
CE
angusta can reach twice the size of ordinary filaments (Runnegar 1985a; Bengtson et
AC
al., 1990; Li, 1997). This much variability is not observed in E.lata, and is not observed here. As such, the endoliths that we observed may be more convincingly assigned to E. lata, with most of the minor bulbous swellings interpreted as enhanced cellular preservation. Such slightly expanded bulbs observed in our samples may be due to differing quality of preservation rather than representing heterocysts or akinetes, which should be much fewer in number and more regularly distributed (Muro-Pastor et al. 2012).
ACCEPTED MANUSCRIPT Dextrorotatory threaded decoration of Endoconchia was first reported by Runnegar (1985b) and interpreted as the reflection of one kind of molluscan shell microstructure called crossed-lamellar aragonite. Although the original shells of Conotheca were not preserved, this may suggest that some features with Cambrian
PT
molluscan skeletons are shared.
RI
5.2 Terminal carbon spherule
SC
Pyrite crystals are the most common propelled grains in AITs that occurred with
NU
phosphatized fossils during late Neoproterozoic and Cambrian. Here we report several peculiar cases of carbon spherules at the distal ends of AI tunnels. A
MA
distinctive terminal grain found from thin section was analysed by Laser Raman spectroscopy, and the resulting spectra identifies the material as organic carbon by
PT E
D
showing a notable D-band (disordered organic matter) and G-band (graphitic organic matter) (She et al., 2016). A few spherules isolated from within a crushed fossil
CE
possess the same character in Raman spectra (Fig. 6A). Another two carbonaceous grains were observed during SEM examination and could be morphologically
AC
correlated with those spherules examined via Laser Raman analysis (Fig. 6B-C). Auxiliary EDS mapping also reveals the relative abundance of C and absence of Ca, P and Fe, thus excluding the possibility of apatite or pyrite and reinforcing a carbonaceous composition (Fig. 6D).
Carbonaceous matter might have been accumulated in the end of AIT tunnels when pyrite crystals swept up carbon pigment in the substrate. In this scenario, the
ACCEPTED MANUSCRIPT carbonaceous matter should be a thin film attached to the leading faces of the propelled grains (Tyler and Barghoorn, 1963). But in our materials, the carbonaceous grains exhibit intact spherical profiles without evidence of compression in their tunnel-facing backsides, which might be resulted by dissolved pyrite crystals.
PT
Meanwhile, the margins of AIT cross-sections are relatively rounded, and directly
RI
coincide with the outlines of the carbon spherules, rejecting that these tunnels were
SC
sculptured by angular pyrite crystals. These features indicate these carbonaceous grains may have themselves been responsible for AIT formation rather than passive
NU
accumulation or secondary filling (Fig. 4A, 6A). The presence of generally
MA
smooth-walled tunnels and carbonaceous terminal grains may also explain the observation of more diverse AIT morphologies, as well as expand the criteria for
PT E
(McLoughlin et al., 2007).
D
distinguishing AIT, in addition to the widely recognized polygonal cross-section
The carbonaceous terminal grains of AITs are exceedingly rare. Indeed, only one
CE
case has been reported from an agate amygdale in 2.7 Ga basalt of the Maddina
AC
Formation, Western Australia. The micro-tubes with organic particles in the agate amygdale are tiny (0.5 to 5 μ m in diameter) and present irregular polygonal cross-sections. It might suggest that the dissolution of matrix enhanced by organic compounds played a more important role in the formation of these filamentous structures (Lepot et al., 2009). The carbonaceous spherules in our materials are much bigger, and seem coincident with the rounded interior AIT cross-sections, suggesting an ample supply of organic materials in Cambrian phosphate deposition as compared
ACCEPTED MANUSCRIPT to Archean basalt. Although AITs have been regarded as signs of early life, recent studies have revealed that AITs may also be generated in environments lacking organic material (Wacey et al., 2016). The AITs with rounded cross-sections and carbonaceous terminal grains, however, may possibly be more direct and reliable
PT
indicators of early life.
RI
5.3 Mechanism of preservation
SC
The most remarkable issues here are the new-found co-occurrence of euendolith
NU
traces and AITs, in addition to their distinctions in preservation. Namely, the microborings of E. lata in our materials, as in many previous descriptions (Runnegar
MA
1985a; Li, 1997; Qian et al., 2007), are microbial traces left in calcareous shells, preserved and expressed as convex phosphate filling casts; while the AITs are
PT E
D
represented as tunnels engraved in fossil moulds, with later diagenetic calcite fillings. The endolith casts appear to have been interrupted by AITs (Fig. 3F), suggesting that
CE
when the AITs were generated, the lithification of phosphate was already in the late stage or had completed.
AC
In addition, thin sections provide us with more clues about the relationship between phosphatic parts and calcite cements, which may support our model for the preservational mechanism of the AITs and co-occurring E. lata.
Firstly, no matter how the AITs were made, they should have been originally continuous. However, all of the AITs found in the Kuanchuanpu material are interrupted or discontinuous, which indicates that the fossils likely underwent
ACCEPTED MANUSCRIPT secondary reworking. One sample (ELIXX16-31) shows a relatively complete AIT with a terminal crystal at the end (Fig. 7A). This example may imply that AITs traveled through the phosphatic fossils frequently, and should likely be observable in the pristine surrounding sediments. In thin sections, however, calcite cementation shows
PT
no evidence of AITs. No tubular structures have been observed within the surrounding
RI
host rock, and all of the AITs within our fossil materials are instead interrupted at the
SC
fossil/host rock interface (Fig. 7B–C).
NU
This observation is consistent with the hypothesis that the original fossil-hosting sediments were reworked and redeposited as phosphatic grains and bio-clasts after
MA
transportation as Zhu (1996), suggested to be the common mode of forming SSF assemblages. As observed in CL examination, the background luminescence of AIT
D
infillings and host-rock carbonate cements are identical, suggesting the AITs were
PT E
infilled during late-stage diagenetic carbonate with host-rock cementation (Fig. 7D). In
CE
summary, such a co-occurrence can be chronologically explained as below:
(1) The original main constituent of Conotheca tube wall is presumed to be
AC
calcitic or aragonitic (Qian and Bengtson, 1989). (2)E. lata constructed tunnels within those tube walls, even when the host organisms were alive (Golubic, 1975) (Fig. 8A-B). (3) During early diagenesis, due to a weakly acidic environment, the bodies of the microbial euendoliths had been destroyed and the Conotheca tube walls were at least partially dissolved in varying degrees (Li, 1997) (Fig. 8C). (4) The next stage of early diagenesis began with the initiation of phosphatic precipitation, wherein the space of dissolved tube walls or body cavities became filled by phosphate, resulting in
ACCEPTED MANUSCRIPT mouldic or steinkern preservation, and the hollowed tunnels of E. lata became casts (Fig. 8C-D). In some situations, the filamentous cast and substrate merged without a distinctive boundary, indicating that they were formed simultaneously in this stage (Fig. 2E). (5) With deeper burial into the substrate of partially solidified phosphatized
PT
sediments (Mcloughlin, 2007), thermal decomposition of the surrounding organic
RI
remains released gas such as CH4 and CO2 that propelled small grains to move
SC
through the substrates and formed the AIT tunnels. Since the phosphatic precipitation had ceased, those traces could remain without being altered by other diagenetic
NU
incident (Fig. 8E). (6) In next stage, the phosphatized sediments were destroyed by
MA
some mechanical forces. The fossils were scattered and became bioclasts. After transport and redeposition, calcareous cementation began and diagentic calcite filled
D
in the interstitial spaces between dissolved shells and tunnels made during the AIT
PT E
formation (Zhu, 1996; Stockfors and Peel, 2005) (Fig. 8F). After acid treatment in laboratory, all of the calcareous parts were dissolved and only the phosphatic parts of
CE
these micro-structures remained, namely the convex filaments as euendolith casts
AC
and concave tubes or grooves referred to as AITs.
5.4 Recognition of AITs and endolithic borings in micro-fossils
The AITs described here are consistent with those found in fossils from late Neoproterozoic Weng’an Biota (Xiao and Knoll, 1999; Liu, 2006) in both preservation and substrate. This type of AIT formation likely also extends to later period of the Cambrian, especially in comparable preservational windows (Hinz-Schallreuter et al., 1998; Stockfors and Peel, 2005b; Zhang and Pratt, 2008; Wacey et al., 2008b;
ACCEPTED MANUSCRIPT Olempska and Wacey., 2016). The continuous occurrence of these structures suggests that the major phosphate deposition during Late Neoproterozoic and Early Cambrian was also a favorable environment for AIT formation, and their association with other phosphatic fossils is likely to be expected.
PT
When presented alone, micro-tubes on fossils might be interpreted in multiple
RI
ways. If they occur with true endolithic traces, however, distinctions in preservation
SC
may provide additional qualifications to help reduce the ambiguity in identification.
NU
The preservational mechanism observed here clearly demonstrates their different origins, specifically the later diagenetic stage of AIT formation, which must be
MA
subsequent to the phosphorite precipitation.The diverse morphological features of the AITs are also distinct from the biogenic characteristics of the microborings found on
D
phosphatic and phosphatized substrates in the geologic record (Rolfe, 1962;
PT E
Bengtson, 1976; Soudry and Nathan, 2000; Königshof and Glaub, 2004), including uniform size, rounded cross-sections or terminations and specific distribution or
CE
orientation patterns. The phosphatic casts of E.lata could reflect the original shapes of
AC
their microborings, just like using polymerizing resins to replicate modern euendoliths (Radtke and Golubic, 2011), and thus great morphological discrepancies between these endolithic microborings and the AITs could be observed. The irregular distribution of longitudinal striations on the microtube walls is incompatible with the hypothesis of a multi-filamentous euendolith (Stockfors and Peel, 2005b).
Viewing the AITs and endolithic traces through the lens of taphonomy, distinctions between these two types of structures is evident. In general, due to the process of
ACCEPTED MANUSCRIPT additional phosphate coating or infilling, micro-tubes occurring on secondarily phosphatized coatings, internal moulds or steinkerns are almost certainly AITs (our materials; Olempska and Wacey, 2016); whereas on shells and hard parts that are phosphorite replaced or original phosphate, more careful investigation is needed. If
PT
those tubules possess some of characteristics in which are accordance with the
RI
former, like grains at terminal ends, longitudinal striations, random orientations and
SC
distributions, or highly irregular morphology, the assignment to AITs is considerably more likely (Hinz-Schallreuter et al., 1998; Conway Morris et al., 1994; Stockfors and
NU
Peel, 2005b; Zhang and Pratt, 2008), while other structures lacking these features
MA
may represent true biogenic structures (Bengtson et al., 1992; Hua et al., 2003).
PT E
D
6 Conclusions
We report the first appearance of well-preserved ambient inclusion trails (AITs) in
CE
the Palaeozoic, together with a new and earliest occurrence of euendoliths Endoconchia lata from the SSF assemblage of the early Cambrian Kuanchuanpu
AC
Formation in South China. In addition, the organic carbonaceous spherules in AITs are first seen in the circumstance of phosphatic fossils from Late Neoproterozoic and Early Cambrian, expanding the geological record of such a terminal grain type to a larger setting and the criteria of AIT recognition. The study of euendolith preservation and their new-found co-occurrence with AITs enables direct comparison between these two microstructures, which in turn helps to reveal their differences in formation,
ACCEPTED MANUSCRIPT preservation, and morphology. We infer the preservational mechanism of these two structures to help explain their co-occurrence, suggesting a later diagenetic stage origin of the AITs present on the phosphatized Kuanchuanpu fossils. Demarcation between these two types of microstructures in the geologic record should be assisted
PT
not only by static morphological, but also by dynamic taphonomic considerations.
RI
Acknowledgments
SC
The authors thank H. Gong, Y. Pang, W. Yang, J. Sun, J. Luo (State Key Laboratory
NU
for Continental Dynamics, Northwest University, Xi’an, China) for their assistance both in the field and with lab work. We also thank colleagues Z. Zhang，L. Li，H. Yun for
MA
their constructive discussions, and T. Zhou (Xi’an Jiaotong University) for helping 3D visualization. The authors also thank three anonymous reviewers and editor T. Algeo
PT E
D
for their helpful comments and suggestions. This work was supported by the Natural Science Foundation of China (NSFC grant 41621003), the "973 project" of the of
Science
and
Technology
of
China
(grants
2013CB835002,
CE
Ministry
2013CB837100), and the State Key Laboratory of Palaeobiology and Stratigraphy (No.
AC
163107).
References
Brasier, M., McLoughlin, N., Green, O., Wacey, D., 2006. A fresh look at the fossil evidence for early Archaean cellular life. Philos. Trans. R. Soc. B 361, 887–902.
Bengtson, S., 1976. The structure of some Middle Cambrian conodonts and the early
ACCEPTED MANUSCRIPT evolution of conodont structure and function. Lethaia 9, 185–206.
Bengtson, S., Conway Morris, S., Cooper, B.J., Jell, P.A. & Runnegar, B.N., 1990. Early Cambrian fossils from South Australia. Australasian Association of
PT
Palaeontologists Memoir 9, 20–24, 232–256.
Bengtson, S., Yue, Z., 1992. Predatorial borings in late Precambrian mineralized
SC
RI
exoskeletons. Science 257, 367–369.
Campbell, S., 1982. Precambrian endoliths discovered. Nature 299, 429–431.
MA
boreholes. J. Paleontol 68, 1–23.
NU
Conway Morris, S., Bengston, S., 1994. Cambrian predators: possible evidence from
Chen, J., 2004. The Dawn of Animal World. Jiangsu Science and Technology Press,
PT E
D
Nanjing, p. 366. [in Chinese].
Dong, Y., M.., Ji, Q., Wang, S., 1984. The discovery of microscopic trace fossils in the
CE
Sinian Doushantuo Formation in southwestern China. Scientia Geologica Sinica 346–347 (in Chinese with English abstract).
AC
Furnes, H., Banerjee, N.R., Muehlenbachs, K., Staudigel, H. & de Wit, M.J. 2004. Early life recorded in Archean pillow lavas. Science 304, 578–581.
Golubic, S., 1969. Distribution, taxonomy and boring patterns of marine endolithic algae. Am. Zool 9, 747–751.
Golubic, S., Perkins, R.D., Lukas, K.J., 1975. Boring microorganisms and microborings incarbonate substrates. In: Frey, R.W. (Ed.), The Study of Trace
ACCEPTED MANUSCRIPT Fossils. Springer, Heidelberg, 229–259.
Golubic, S., Campbell, S.E., Drobne, K., Cameron, B., Balsman, W.L., Cimmerman, F., and Dubois, L., 1984. Microbial endolithss-a benthic overprint in the sedimentary record, and a palaeobathemetric cross–reference with formaninifera. J. Paleontol
PT
58, 351–361.
RI
Golubic, S., Seong-Joo, L., Browne, K.M., 2000. Cyanobacteria: architects of
NU
Springer-Verlag, Heidelberg, pp. 57–67.
SC
sedimentary structures. In: Riding, R.E., Awramik, S.M. (Eds.), Microbial Sediments.
MA
Grey, K., 1986. Problematic microstructures in the Proterozoic Discovery Chert, Bangemall Group, Western Australia. Ambient grains or microfossils? Geol. Surv.
D
Western Australia Prof. Papers for 1984, Perth, pp. 22–31.
PT E
Hinz-Schallreuter, I., 1998. Population structure, life strategies and systematic of phosphatocope ostracods from the Middle Cambrian of Bornholm. Mitt. Mus. Nat.kd.
CE
Berl. Geowiss. Reihe 1, 103–134.
AC
Hua, H., Pratt, B. R., Zhang, L., 2003. Borings in Cloudina Shells: Complex Predator-Prey Dynamics in the Terminal Neoproterozoic. PALAIOS 18, 454–459.
Knoll, A.H., Barghoorn, E.S., 1974. Ambient pyrite in Precambrian chert: new evidence and a theory. Proc. Natl. Acad. Sci. U. S. A. 71, 2329–2331.
Knoll, A. H., Golubic, S., Green, J., Swett, K., 1986. Organically preserved microbial endoliths from the late Proterozoic of East Greenland. Nature 321, 856–857.
ACCEPTED MANUSCRIPT Königshof, P., Glaub, I., 2004. Traces of microboring organisms in Palaeozoic conodont elements. Geobios 37, 416–424.
Lepot, K., Philippot, P., Benzerara, K., & WANG, G. Y., 2009. Garnet-filled trails associated with carbonaceous matter mimicking microbial filaments in Archean
PT
basalt. Geobiology, 7, 393–402.
RI
Li, G., 1997. Early Cambrian phosphate-replicated endolithic algae from Emei,
SC
Sichuan, SW China. Bulletin of National Museum of Natural Science [Taiwan] 10,
NU
193–216.
MA
Li, Z., 1984, The discovery and its significance of Early Cambrian small shelly fossils in Hexi Area, Xixiang, Shaanxi. Geology of Shaanxi 2, 73–78 (in Chinese with
D
English abstract)
PT E
Liu, P., Yin, C., 2006, Enigmatic microtunnels––The drag marks of Pyrites on the Phosphatized Spheroidal Fossils from Sinian Doushantuo Formation at Weng’an,
CE
Guizhou Province, Geological Review 52, 11–16 (in Chinese with English abstract).
AC
McLoughlin, N., Brasier, M.D., Wacey, D., Green, O.R., Perry, R.S., 2007. On biogenicity criteria for endolithic microborings on early Earth and beyond. Astrobiology 7, 10–26.
Muro-Pastor, A., Hess, W. R., 2012, Heterocyst differentiation: from single mutants to global approaches. Trends in Microbiology 20, 548–557.
Olempska, E., Wacey, D., 2016. Ambient inclusion trails in Palaeozoic crustaceans
ACCEPTED MANUSCRIPT (Phosphatocopina
and
Ostracoda).
Palaeogeography,
Palaeoclimatology,
Palaeoecology 441, 949–958.
Qian, Y., Bengtson, S., 1989. Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China. Fossils and Stret
PT
24, 1–156.
fossils
from
the
basal
of
China.
Acta
NU
Micropalaeontologica Sinica 24, 222–228.
Cambrian
SC
cyanobacterian
RI
Qian, Y., Li G., Jiang Z., Chen, M., Yang, A., 2007. Some phosphatized
MA
Radtke, G., & Golubic, S., 2011. Microbial euendolithic assemblages and microborings in intertidal and shallow marine habitats: insight in cyanobacterial
D
speciation. Lecture Notes in Earth Sciences 131, 233–263.
PT E
Rolfe, W.D.I., 1962. The cuticle of some Middle Silurian ceratiocaridid Crustacea from Scotland. Palaeontology 5, 30–51.
CE
Runnegar, B., 1985a. Early Cambrian endolithic algae. Alcheringa 9, 179–182.
AC
Runnegar, B., 1985b. Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringa: An Australasian Journal of Palaeontology 9, 245–257.
She, Z. B., Zhang, Y. T., Liu, W., Song, J., Zhang, Y., Li, C., Strother P., Papineau, D., 2016. New observations of Ambient Inclusion Trails (AITs) and pyrite framboids in the
Ediacaran
Doushantuo
Formation,
South
Palaeoclimatology, Palaeoecology 461, 374-388.
China. Palaeogeography,
ACCEPTED MANUSCRIPT Soudry, D., Nathan, Y., 2000. Microbial infestation: a pathway of fluorine enrichment in bone apatite fragments (Negev phosphorites, Israel). Sedimentary Geology 132, 171–176.
Steiner, M., Li, G., Qian, Y., Zhu, M., 2004. Lower Cambrian small shelly fossils of
PT
northern Sichuan and southern Shaanxi (China), and their biostratigraphic
RI
importance. Geobios 37, 259–275
SC
Steiner, M., Li, G., Qian, Y., Zhu, M., and Erdtmann, B.-D. 2007. Neoproterozoic to
NU
early Cambrian small shelly fossil assemblages and a revised biostratigraphic correlation of the Yangtze Platform (China). Palaeogeography, Palaeoclimatology,
MA
Palaeoecology 254: 67–99.
D
Steiner, M., Qian, Y., Li, G., Hagadorn, J. W., and Zhu, M. 2014. The developmental
PT E
cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeography, Palaeoclimatology, Palaeoecology 398:
CE
97–124.
AC
Stockfors, M., Peel, J.S., 2005a. Endolithic Cyanobacteria from the Middle Cambrian of North Greenland. GFF 127, 179–185.
Stockfors, M., Peel, J.S., 2005b. Euendoliths and cryptoendoliths within late Middle Cambrian brachiopod shells from North Greenland. GFF 127, 187–194.
Sawaki, Y., Nishizawa, M., Suo, T., Komiya, T., Hirata, T., & Takahata, N., et al., 2008. Internal structures and u–pb ages of zircons from a tuff layer in the meishucunian formation, yunnan province, south china. Gondwana Research 14, 148–158.
ACCEPTED MANUSCRIPT Tyler, S.A., Barghoorn, E.S., 1963. Ambient pyrite grains in Precambrian cherts. American Journal of Science 261, 424–432.
Wacey, D., McLoughlin, N., Green, O.R., Parnell, J., Stoakes, C.A., Brasier, M.D., 2006. The ~ 3.4 billion-year-old Strelley Pool Sandstone: a new window into early
PT
life on Earth. Int. J. Astrobiol 5, 333–342.
RI
Wacey, D., Kilburn, M.R., McLoughlin, N., Parnell, J., Stoakes, C.A., Grovenor,
SC
C.R.M., Brasier, M.D., 2008a. Use of NanoSIMS in the search for early life on Earth:
NU
ambient inclusion trails in a c. 3400 Ma sandstone. J. Geol. Soc. Lond. 165, 43–53.
MA
Wacey, D., Kilburn, M., Stoakes, C., Aggleton, H., Brasier, M., 2008b. Ambient Inclusion Trails: their recognition, age range and applicability to early life on Earth.
D
In: Dilek, Y., et al. (Eds.), Links Between Geological Processes, Microbial Activities
PT E
& Evolution of Live. Springer Science + Business Media B.V, pp. 113–134.
Wacey, D., Saunders, M., Kong, C., & Kilburn, M. R., 2016. A new occurrence of
CE
ambient inclusion trails from the ~1900-million-year-old Gunflint Formation, Ontario:
AC
nanocharacterization and testing of potential formation mechanisms. Geobiology 14(5).
Xiao, S., Knoll, A.H., 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32, 219–240.
Zhang X., Pratt, B. R., 2008. Microborings in Early Cambrian phosphatic and phosphatized fossils. Palaeogeography, Palaeoclimatology, Palaeoecology 267: 185–195
ACCEPTED MANUSCRIPT Zhang, Y., Golubic, S., 1987. Endolithic microfossils (cyanophyta) from early Proterozoic stromatolites, Hebei, China. Acta Micropaleontologica Sinica 4, 1–12 (in Chinese with English abstract).
Zhu, M., Jiang, Z., He, T., 1996. A preliminary study on the preservation, shell
PT
composition and m icrostructures of Cambrian small shelly fossils. Acta
SC
RI
Micropalaeomologica Sinica 13, 241–254 (in Chinese with English abstract).
NU
Fig. 1. Geological map and stratigraphic column of the fossil locality. (A). Geological
MA
map indicating the Cambrian strata and location of the fossil locality at the Zhangjiagou section in Xixiang County, Shaanxi Province. (B). Stratigraphic column
D
showing the occurrence of small shelly fossils. Numbers 1–4 represent the four
PT E
lithostratigraphic units in Kuanchuanpu Formation.
CE
Fig. 2. SEM images of euendolithic cyanobacteria Endoconchia lata on the
AC
Conotheca from the Kuanchuanpu Formation in Xixiang, China. (A). Tubular Conotheca with a cone-in-cone pattern, note phosphatic casts of Endoconchia lata borings on the innermost tube surface (ELIXX7-35). (B). Enlargement of A, within the white circle it is a spheroidal end and arrows show the string of swellings along filaments. (C–D). The most common occurrences of E. lata are surfaces of skeletal fossils moulds and the infills between original shells. White box in (D) show the cross-sections of endoliths casts (ELIXX3-120 and ELIXX16-88). (E). Some of the
ACCEPTED MANUSCRIPT filaments gradually melting into moulds (ELIXX66-63). (F). E. lata with dextrorotatory threaded decoration (ELIXX5-164).
PT
Fig. 3. Overviews of Ambient Inclusion Trails (AITs) in Conotheca. (A–B). Basic morphology of AITs as micro-tunnels and grooves, most of them are characterized by
RI
striated wall sculptures of minor ridges (ELIXX5-125 & ELIXX5-177). (C). A maze-like
SC
assemblage of AITs on a SSF internal mould (ELIXX5-173). (D). High density of AIT
NU
assemblages, forming a coarse surface (ELIXX6-52). (E). Co-occurrence of E. lata and AITs. Arrows show the position of the casts of E.lata, and within the circle it is the
MA
AITs. (ELIXX10-100). (F). Co-occurrence of E. lata and AITs, casts of E. lata being destroyed by AITs (ELIXX29-46). The 2 pictures are the same sample in different
PT E
D
orientations.
CE
Fig. 4. Detailed morphological features of AITs. (A). Rounded cross-sections and a
AC
spherical terminal grain in the other AIT (ELIXX52-290). (B). Variations of AIT sizes, within the circle is the minimum one among our materials (ELIXX15-129). (C). Grand AIT grooves (maximum one among current samples) with typical longitudinal wall striations, noting that the distribution of ridges is irregular (ELIXX32-15). (D). AIT tunnels with relatively smooth wall (ELIXX29-18). (E–F). Complex conjunctions of multiple AITs (ELIXX15-134; ELIXX19-53).
ACCEPTED MANUSCRIPT Fig. 5. Distribution of AITs inside an un-identified fossil. (A). SEM image of one specimen with conspicuous AITs (ELIXX29-22). (B). 3D visualization of (A). Green parts represent hollowed AIT tunnels and the fossil entity has been converted into translucent mask for better illustration. (C). A tomographic image of (B), showing
PT
cross-sections of AITs. (D). 3D visualization of AITs of (A), sample has been rotated to
SC
RI
present a better view of both small and large AITs.
NU
Fig. 6. Spherical AIT terminal grains and their chemical composition. (A). Raman spectra of spherical terminal grains. Top-Left: CL image of one thin section, showing
MA
an AIT with a granular particle in the distal end (white box) and the cross marks the position where the Raman analysis was positioned; Top-Middle: SEM image of stray
PT E
D
spherules from a crushed fossil (Scale bar=50μm). (B). SEM image of one spherical terminal grain (enlarged from Fig. 4A). The rounded cross-section fits the spherules
CE
outline (ELIXX52-290). (C). SEM image of another spherical terminal grain. The striated wall sculptures of AIT match the profile of the grain (white arrows)
AC
(ELIXX71-44). (D). EDS mapping of (B), indicating the concentration of C and lack of Ca, P and Fe.
Fig. 7. The relationship between AITs, host fossils and carbonate substrates. (A). A continual trail on an embryo-like fossil, indicating the paths of AITs penetrated between fossil and surrounding substrates frequently (ELIXX16-31). (B–C). Crossed
ACCEPTED MANUSCRIPT polarizing microscope photographs of thin sections with AITs. The black parts are fossils constituted by collophane, the bright parts are calcite cements. It is notable that those AITs show no extension in to the calcareous substrates. (D). CL image of the area in (C), showing the background color of AITs infilling and the calcite cements are
RI
PT
identical.
SC
Fig. 8. Mechanism of AIT and euendoliths preservation. (A–D). Forming of euendolith
NU
casts. (E). AITs formed later than phosphate infilling of euendolithic microborings. (F). Cementation after the redepositing of AIT-hosted fossils and AITs were infilled with
MA
calcareous matters. (“V shapes”cross-sections of shells; “Round shape”： embryo-like organism; Background colour: light blue- water; dark blue-phosphate; gray-carbonate
AC
CE
PT E
D
cement).
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Highlights
Earliest record of well-preserved AITs and co-occoured euendolith Endoconchia
lata in Palaeozoic. Discrepancies between AITs and endolith traces in formation, preservation and
PT
RI
morphology are revealed.
Rare type of AIT propelled grains as organic carbon spherules are reported.
AITs formed during the late phase or after the phosphorite lithification.
Our data suggest most microtubular structures on secondarily phosphatized
NU
SC
AC
CE
PT E
D
MA
fossils should be AITs.
Xiao-guang Yang, Jian Han, Xing Wang, James D. Schiffbauer, Kentaro Uesugi, Osamu Sasaki, Tsuyoshi Komiya PII: DOI: Reference:
S0031-0182(16)30465-5 doi: 10.1016/j.palaeo.2017.03.028 PALAEO 8251
To appear in:
Palaeogeography, Palaeoclimatology, Palaeoecology
Received date: Revised date: Accepted date:
13 September 2016 28 March 2017 30 March 2017
Please cite this article as: Xiao-guang Yang, Jian Han, Xing Wang, James D. Schiffbauer, Kentaro Uesugi, Osamu Sasaki, Tsuyoshi Komiya , Euendoliths versus ambient inclusion trails from Early Cambrian Kuanchuanpu Formation, South China. The address for the corresponding author was captured as affiliation for all authors. Please check if appropriate. Palaeo(2017), doi: 10.1016/j.palaeo.2017.03.028
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Euendoliths versus Ambient Inclusion Trails from Early Cambrian Kuanchuanpu Formation, South China
PT
Xiao-guang Yanga, Jian Hana*, Xing Wanga, James D. Schiffbauerb, Kentaro Uesugic,
RI
Osamu Sasakid, Tsuyoshi Komiyae a
SC
State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University, 229 Taibai Road, Xi'an 710069, P.R. China ([email protected])
b
MA
Columbia 65211, Missouri, USA
NU
Department of Geological Sciences, University of Missouri, 101 Geology Building,
c
PT E
Sayo-gun, Hyogo, Japan
D
Japan Synchrotron Radiation Research Institute (JASRI), 1-1-1 Kouto, Sayo-cho,
d
Tohoku University Museum, Tohoku University, 6-3 Aoba, Aramaki, Aoba-ku, Sendai,
e
CE
Japan
Department of Earth Science and Astronomy, Graduate School of Arts and Sciences,
AC
The University of Tokyo, Tokyo 153-8902, Japan
* To whom correspondence should be addressed. E-mail: [email protected]
Abstract: Abundant microstructures have been discovered in small skeletal fossils (SSFs) and embryo-like fossils collected from the Lower Cambrian Kuanchuanpu Formation (ca. 535 Ma) in Xixiang County, Shaanxi Province, China. These involve
ACCEPTED MANUSCRIPT two co-occurring structures: (1) long, unbranched cylindrical filaments, which are comparable to phosphatic casts of microborings constructed by euendolithic cyanobacteria (Endoconchia lata) in morphology and preservation pathway; and (2) meandering micro-tubes or grooves on fossil moulds (and steinkerns) of a wide range
PT
of sizes and morphological diversities, perceived as ambient inclusion trails (AITs).
RI
Herein, we also report a new occurrence of organic carbon spherules as
SC
AIT-propelled material, which is rare in comparable fossils. From direct comparison of endolithic traces and AITs, we propose a mechanism to account for their notably
NU
different preservation, and further attempt to offer an explanation for their
MA
co-occurrence. Their differential preservation suggests a chronological, taphonomic sequence of their formation. We interpret that E. lata microborings formed prior to
D
phosphate sedimentation, whereas AITs are likely generated in a later phase of (or
PT E
after) phosphorite precipitation but before calcareous re-cementation. Dissecting the sequence of formation of these structures, in conjunction with detailed morphological
CE
observations, assists in distinguishing true biologically produced endoliths from
AC
otherwise abiogenically produced microstructures.
Keywords: cyanobacteria; Endoconchia lata; microborings; small skeletal fossils; phosphatized fossils
1. Introduction
Microtubular structures recorded in rocks have been reported broadly through
ACCEPTED MANUSCRIPT geologic time, from the Archean through the Palaeozoic, and in various matrices, such as chert, sandstone, or phosphorite. (Tyler and Barghoorn, 1963; Knoll and Barghoorn, 1974; Grey, 1986; Xiao and Knoll, 1999; Brasier et al., 2006; Wacey et al., 2006, 2008a, b; McLoughlin et al., 2007). Such structures are often termed “ambient
PT
inclusion trails” (AITs), and a recent summary of AIT studies suggests that AITs are
RI
predominantly generated by migration of mineral crystals, often pyrite, through a
SC
lithified fine-grained substrate (Wacey et al., 2008b). So far, most AITs are known from thin sections of Archean and Proterozoic rocks, although AITs have additionally been
NU
identified from Palaeozoic fossils (Olempska and Wacey, 2016). While analogous
MA
Palaeozoic tubular structures are more often surmised as traces of boring animals or endolithic micro-organisms (Hinz-Schallreuter et al., 1998; Stockfors and Peel, 2005b;
D
Conway Morris et al., 1994; Zhang and Pratt, 2008). Mircoborings made by endoliths
PT E
(Knoll et al., 1986; Campbell, 1982; Golubic, 1969; Zhang and Golubic, 1987; Golubic et al., 1984, 2000; Furnes et al., 2004; Stockfors and Peel, 2005a) or possibly by
CE
predatory animals (Bengtson et al., 1992; Hua et al., 2003) are widespread through at
AC
least the Phanaerozoic record, yet the recognition of AIT is still somehow equivocal, especially with regarding to the bioturbation in Palaeozoic.
Herein, we describe a co-occurrence of AITs and euendolithic traces from phosphatized microfossils of the Lower Cambrian Kuanchuanpu Formation in Xixiang County, Shaanxi Province, China, and report a new occurrence of organic carbon spherules as AIT-propelled material (or terminal grains).
Previous studies on either AITs or euendoliths tend to treat these structures
ACCEPTED MANUSCRIPT separately. Their co-occurrence in phosphatized microfossils from the Kuanchuanpu Formation, however, permits direct comparison from a single unit. Recognition of chronological ordering of these structures during the taphonomic sequence of the fossils thus enables us to conceptualize a preservational model to explain their
PT
co-occurrence and help us to recognize the diagenetic stage of AIT formation in this
NU
SC
morphology between AITs and euendolith traces.
RI
case. As we describe here, there are distinctions in the formation, preservation, and
MA
2. Geological Setting
All specimens described herein were collected from the Lower Cambrian
D
Kuanchuanpu Formation in Xixiang County, Shaanxi Province. This fossil locality
PT E
belongs to the northern margin of the Yangtze Block and was first reported by Li (1984) as the Zhangjiagou Section, named after the nearby village about 55 km to the
CE
southwest of the administrative center of Xixiang (Fig. 1A).
AC
The Kuanchuanpu Formation is well exposed at this section, with a total thickness of ca. 21 m. It disconformably underlies the black shale of the Lower Cambrian Guojiaba Formation, and conformably overlies the Neoproterozoic Upper Dolomite Member of the Dengying Formation. From lower to upper, the Kuanchuanpu Formation can be subdivided into 4 units as follows: (1) grey blocks of microsparitic limestone (0.8 m); (2) grey and white blocks of phosphorus limestone (2.2 m); (3) thick-bedded dark grey microsparitic limestone (17.4 m); (4) thin-bedded light grey
ACCEPTED MANUSCRIPT silty-fine dolomitic limestone (0.6 m) (Fig. 1B).
In contrast to the sparsely fossiliferous units 1 and 4, units 2 and 3 contain a high abundance of various small shelly fossils (SSFs), including Protohertzina anabarica, Canopoconus calvatus, Conotheca subcurvata, Olivooides multisulcatus, and
PT
Olivooides mirabilis. Preliminary taxon counts show that Conotheca is the dominant
et
al.
2012),
with
SSF
taxa
comparable
to
the
Anabarites
SC
(Peng
RI
genus. The fossiliferous horizon belongs to the Fortunian Stage, Terreneuvian Series
NU
trisulcatus-Protohertzina anabarica assemblage zone (Steiner et al. 2007). The assemblage can be correlated with that in the Meishucun section, Yunnan Province,
MA
South China, which, from U–Pb dating, has been assigned an age of ca. 536.5±2.5 Ma (Sawaki et al. 2008). From additional comparisons of SSF assemblages and other
D
radiometric dating results, Steiner et al. (2014) estimated the age of comparable fossil
CE
PT E
horizons to be approximately 535 Ma.
AC
3. Materials and Methods
The majority of our collected samples came from the top of Kuanchuanpu Formation unit 2. Fossil material was extracted from rock samples using acid maceration with an 8% acetic acid solution. The residuals were examined using standard binocular microscopy. After optical inspection, selected specimens were coated with gold and examined using a FEI Quanta 400F scanning electron microscope (SEM), equipped with an Oxford Instruments energy dispersive X-ray
ACCEPTED MANUSCRIPT spectrometer (EDS). Related thin sections were additionally examined using crossed polarizing microscopy and cathodoluminescence microscopy (CL). Spot analysis by laser micro-Raman spectroscopy was additionally utilized for clarification of the chemical composition of some enigmatic, spherical AIT terminal grains. We
PT
deliberately crushed one phosphatic fossil to retrieve such terminal grains distributed
RI
on different sides of the host specimen. These grains, together with another terminal
SC
particle found from thin section, were spotted with a 50× objective and a 20 μm diameter pinhole in a Renishaw inVia confocal Raman microscope equipped with a
NU
514.5nm laser. After Raman analysis, the spherical grains were subsequently coated
MA
with gold and imaged via SEM. Select specimens were additionally investigated with a ScanXmate-D160TSS105/11000 X-ray microcomputed tomographic microscope
D
(µCT) in Tohoku University, Japan (110 KeV, 0.812 μm3/pixel), as well as synchrotron
PT E
radiation X-ray tomographic microscopy (SRXTM) of SPring-8 in Hyogo, Japan (20 KeV, 0.37 μm3/pixel). All µCT and SRXTM data were processed with VG Studio 2.2
CE
Max software for tomographic analysis and 3D visualization. All analyzed specimens
AC
are housed in the Early Life Institute, Northwest University, Xi'an, Shaanxi, China.
4. Description
4.1 Euendoliths
The euendoliths observed here are preserved as phosphatic casts on the surface of steinkerns or moulds of tube-like SSFs, such as Conotheca. Conotheca is a
ACCEPTED MANUSCRIPT millimeter-sized, cone-shaped, tubular SSF that occurs widely in deposits of Siberia, China, India, and France, and ranges from the Lower to Middle Tommotian Stage of the Cambrian Period. The tube of Conotheca is straight to curved, with a closed and somewhat blunt base, and a straight aperture. It is circular in transverse section and
PT
shows no indication of internal septa (Steiner et al., 2004). Most Conotheca samples
RI
examined here exhibit a multi-layered cone-in-cone construction, although the
SC
skeletal carbonate is not preserved (Fig. 2C–D). In these samples, the euendolith casts are always oriented parallel or sub-parallel to each layer and they never cross
NU
different layers.
MA
The euendolith casts appear as long, non-branched, cylindrical filaments (Fig. 2A–C), with a mean diameter of 6.9 μm (range = 5.5 to 7.5 μm), and an observed
D
length of up to approximately 300 μm. A clear moniliform shape can be observed in
PT E
some of our specimens, consisting of isodiametric spheroidal expansions, with consistent diameters of about 9 μm.
Some parts of the filaments bear a distinctive
CE
oblique decoration (Fig. 2F), appearing as tiny threads on the surface of the
AC
phosphatic infill. These threads, or micro-filaments, are typically separate, with some interlacing and appearing to form pseudo-branches. The joints of these pseudo-branches show that the filaments are actually in different planes, indicating overlap of independent microfilaments (Fig. 2B).
4.2 Ambient Inclusion Trails
The AITs are present as meandering micro-grooves or tubes with longitudinal wall
ACCEPTED MANUSCRIPT striations on various types of phosphatized fossils, including the internal moulds or steinkerns of SSFs, unknown fragments, and rounded fossils (Fig. 3, 6). The Kuanchuanpu Formation in the sampled region is famous for rounded embryo fossils, such as Olivooides; the rounded fossils examined here, although similar in size, lack
PT
both characteristic surface ornaments and internal structures, and thus we
RI
conservatively refer to them as embryo-like fossils. The AITs occur singly, or
SC
sometimes form various assemblages. The AITs predominantly appear gently curved, while some have sharp changes in direction (Fig. 3B, 4C–D). These features are
NU
highly comparable to those AITs described by Knoll and Barghoorn (1974), Xiao and
MA
Knoll (1999), Wacey et al. (2008b), and Olempska and Wacey (2016). The distribution of AITs is random, they can be found almost everywhere within the fossils, regardless
D
of taxonomy or different biological tissues.
PT E
Detailed observations of the copious AIT-hosting specimens reveal that the morphology of AITs in microscale is extremely irregular in several respects: (1) The
CE
size of AITs from our materials ranges from a minimum of 2.5 µm (Fig. 4B) to 75 µm
AC
(Fig. 4C), while those with a diameter of 10–20 µm being the most common. Starting or ending points are difficult to determine in the current specimens, and so an approximation of length would be tenuous. (2) The shapes of the AIT cross-sections were usually thought to be polygonal or rectangular, but some distinctively rounded ones can be found, along with some that host spherical, organic carbon terminal grains (Fig. 6). The margins of the AITs match closely with the edge of grains (Fig. 4A, 6B–C). Lateral study prove that the spherical terminal grains are primarily composed
ACCEPTED MANUSCRIPT of organic carbon (Fig. 6). (3) Most of the AITs are characterized by longitudinal fluting. This surface decoration is formed by non-intersecting, concave-sided ridges running parallel to each other. These features are also variable, with some arranged neatly with a relatively uniform size (Fig. 3A, 4B), and others showing varied widths and
PT
intervals within a single trail, especially in the larger ones (Fig. 4C, 7). In yet other
RI
specimens, these wall striations are faint, giving the appearance of smooth inner walls
SC
and perhaps suggesting that they may have been altered to varying degrees (Fig. 4D, F). Additional perforations were observed along the sidewall in many instances (Fig.
NU
4D).
MA
The assemblages of AITs also show irregular patterns, mainly divided into two types: (1) dense concentrations of single tubes, intercrossing and cutting through
PT E
surface (Fig. 3D).
D
each other (Fig. 3C,4E); and (2) numerous congested micro-tubes, forming a ragged
CE
From µCT and SRXTM techniques, we generated a three-dimensional reconstruction of one specimen with well-developed AITs (ELIXX29-22). The irregular
AC
cross-sections (Fig. 5C) and the randomly oriented AITs with dramatic change in size (Fig. 5D) are well displayed by the tomographic image and 3D visualized model.
5. Discussion
5.1 Euendolithic identity
The genus Endoconchia was established by Runnegar (in Bengtson et al., 1990)
ACCEPTED MANUSCRIPT with two species described: E. lata and E. angusta. E.lata is characterized by a constant diameter of 10 μm while E.angusta is much thinner (about 3 μm) with some distinct bulbous chambers in the ends and some points along the filaments, which could expand to 5 μm and were similar with the structures of heterocysts. The
PT
morphology of those micro-filaments described here corresponds well with the genus
RI
Endoconchia, and their consistent parallel arrangement along the original shell
SC
material also suggests an euendolithic identity (Fig. 10 in Bengtson et al., 1990, pp
NU
22–24).
The filaments in our materials, however, present a slightly smaller diameter than
MA
E. lata (Runnegar, 1985a, b; in Bengtson et al., 1990) and show more continuous and well-developed spheroidal swellings (Fig. 1B). Such a smaller diameter could also be
D
seen from E. lata in Maidiping Formation of Sichuan, China, which is about 2.5–5 μm
PT E
(Qian et al., 2007). Spheroidal expansions are more common in the other species E. angusta, but the diameter of these bulbs or bead structures as described in E.
CE
angusta can reach twice the size of ordinary filaments (Runnegar 1985a; Bengtson et
AC
al., 1990; Li, 1997). This much variability is not observed in E.lata, and is not observed here. As such, the endoliths that we observed may be more convincingly assigned to E. lata, with most of the minor bulbous swellings interpreted as enhanced cellular preservation. Such slightly expanded bulbs observed in our samples may be due to differing quality of preservation rather than representing heterocysts or akinetes, which should be much fewer in number and more regularly distributed (Muro-Pastor et al. 2012).
ACCEPTED MANUSCRIPT Dextrorotatory threaded decoration of Endoconchia was first reported by Runnegar (1985b) and interpreted as the reflection of one kind of molluscan shell microstructure called crossed-lamellar aragonite. Although the original shells of Conotheca were not preserved, this may suggest that some features with Cambrian
PT
molluscan skeletons are shared.
RI
5.2 Terminal carbon spherule
SC
Pyrite crystals are the most common propelled grains in AITs that occurred with
NU
phosphatized fossils during late Neoproterozoic and Cambrian. Here we report several peculiar cases of carbon spherules at the distal ends of AI tunnels. A
MA
distinctive terminal grain found from thin section was analysed by Laser Raman spectroscopy, and the resulting spectra identifies the material as organic carbon by
PT E
D
showing a notable D-band (disordered organic matter) and G-band (graphitic organic matter) (She et al., 2016). A few spherules isolated from within a crushed fossil
CE
possess the same character in Raman spectra (Fig. 6A). Another two carbonaceous grains were observed during SEM examination and could be morphologically
AC
correlated with those spherules examined via Laser Raman analysis (Fig. 6B-C). Auxiliary EDS mapping also reveals the relative abundance of C and absence of Ca, P and Fe, thus excluding the possibility of apatite or pyrite and reinforcing a carbonaceous composition (Fig. 6D).
Carbonaceous matter might have been accumulated in the end of AIT tunnels when pyrite crystals swept up carbon pigment in the substrate. In this scenario, the
ACCEPTED MANUSCRIPT carbonaceous matter should be a thin film attached to the leading faces of the propelled grains (Tyler and Barghoorn, 1963). But in our materials, the carbonaceous grains exhibit intact spherical profiles without evidence of compression in their tunnel-facing backsides, which might be resulted by dissolved pyrite crystals.
PT
Meanwhile, the margins of AIT cross-sections are relatively rounded, and directly
RI
coincide with the outlines of the carbon spherules, rejecting that these tunnels were
SC
sculptured by angular pyrite crystals. These features indicate these carbonaceous grains may have themselves been responsible for AIT formation rather than passive
NU
accumulation or secondary filling (Fig. 4A, 6A). The presence of generally
MA
smooth-walled tunnels and carbonaceous terminal grains may also explain the observation of more diverse AIT morphologies, as well as expand the criteria for
PT E
(McLoughlin et al., 2007).
D
distinguishing AIT, in addition to the widely recognized polygonal cross-section
The carbonaceous terminal grains of AITs are exceedingly rare. Indeed, only one
CE
case has been reported from an agate amygdale in 2.7 Ga basalt of the Maddina
AC
Formation, Western Australia. The micro-tubes with organic particles in the agate amygdale are tiny (0.5 to 5 μ m in diameter) and present irregular polygonal cross-sections. It might suggest that the dissolution of matrix enhanced by organic compounds played a more important role in the formation of these filamentous structures (Lepot et al., 2009). The carbonaceous spherules in our materials are much bigger, and seem coincident with the rounded interior AIT cross-sections, suggesting an ample supply of organic materials in Cambrian phosphate deposition as compared
ACCEPTED MANUSCRIPT to Archean basalt. Although AITs have been regarded as signs of early life, recent studies have revealed that AITs may also be generated in environments lacking organic material (Wacey et al., 2016). The AITs with rounded cross-sections and carbonaceous terminal grains, however, may possibly be more direct and reliable
PT
indicators of early life.
RI
5.3 Mechanism of preservation
SC
The most remarkable issues here are the new-found co-occurrence of euendolith
NU
traces and AITs, in addition to their distinctions in preservation. Namely, the microborings of E. lata in our materials, as in many previous descriptions (Runnegar
MA
1985a; Li, 1997; Qian et al., 2007), are microbial traces left in calcareous shells, preserved and expressed as convex phosphate filling casts; while the AITs are
PT E
D
represented as tunnels engraved in fossil moulds, with later diagenetic calcite fillings. The endolith casts appear to have been interrupted by AITs (Fig. 3F), suggesting that
CE
when the AITs were generated, the lithification of phosphate was already in the late stage or had completed.
AC
In addition, thin sections provide us with more clues about the relationship between phosphatic parts and calcite cements, which may support our model for the preservational mechanism of the AITs and co-occurring E. lata.
Firstly, no matter how the AITs were made, they should have been originally continuous. However, all of the AITs found in the Kuanchuanpu material are interrupted or discontinuous, which indicates that the fossils likely underwent
ACCEPTED MANUSCRIPT secondary reworking. One sample (ELIXX16-31) shows a relatively complete AIT with a terminal crystal at the end (Fig. 7A). This example may imply that AITs traveled through the phosphatic fossils frequently, and should likely be observable in the pristine surrounding sediments. In thin sections, however, calcite cementation shows
PT
no evidence of AITs. No tubular structures have been observed within the surrounding
RI
host rock, and all of the AITs within our fossil materials are instead interrupted at the
SC
fossil/host rock interface (Fig. 7B–C).
NU
This observation is consistent with the hypothesis that the original fossil-hosting sediments were reworked and redeposited as phosphatic grains and bio-clasts after
MA
transportation as Zhu (1996), suggested to be the common mode of forming SSF assemblages. As observed in CL examination, the background luminescence of AIT
D
infillings and host-rock carbonate cements are identical, suggesting the AITs were
PT E
infilled during late-stage diagenetic carbonate with host-rock cementation (Fig. 7D). In
CE
summary, such a co-occurrence can be chronologically explained as below:
(1) The original main constituent of Conotheca tube wall is presumed to be
AC
calcitic or aragonitic (Qian and Bengtson, 1989). (2)E. lata constructed tunnels within those tube walls, even when the host organisms were alive (Golubic, 1975) (Fig. 8A-B). (3) During early diagenesis, due to a weakly acidic environment, the bodies of the microbial euendoliths had been destroyed and the Conotheca tube walls were at least partially dissolved in varying degrees (Li, 1997) (Fig. 8C). (4) The next stage of early diagenesis began with the initiation of phosphatic precipitation, wherein the space of dissolved tube walls or body cavities became filled by phosphate, resulting in
ACCEPTED MANUSCRIPT mouldic or steinkern preservation, and the hollowed tunnels of E. lata became casts (Fig. 8C-D). In some situations, the filamentous cast and substrate merged without a distinctive boundary, indicating that they were formed simultaneously in this stage (Fig. 2E). (5) With deeper burial into the substrate of partially solidified phosphatized
PT
sediments (Mcloughlin, 2007), thermal decomposition of the surrounding organic
RI
remains released gas such as CH4 and CO2 that propelled small grains to move
SC
through the substrates and formed the AIT tunnels. Since the phosphatic precipitation had ceased, those traces could remain without being altered by other diagenetic
NU
incident (Fig. 8E). (6) In next stage, the phosphatized sediments were destroyed by
MA
some mechanical forces. The fossils were scattered and became bioclasts. After transport and redeposition, calcareous cementation began and diagentic calcite filled
D
in the interstitial spaces between dissolved shells and tunnels made during the AIT
PT E
formation (Zhu, 1996; Stockfors and Peel, 2005) (Fig. 8F). After acid treatment in laboratory, all of the calcareous parts were dissolved and only the phosphatic parts of
CE
these micro-structures remained, namely the convex filaments as euendolith casts
AC
and concave tubes or grooves referred to as AITs.
5.4 Recognition of AITs and endolithic borings in micro-fossils
The AITs described here are consistent with those found in fossils from late Neoproterozoic Weng’an Biota (Xiao and Knoll, 1999; Liu, 2006) in both preservation and substrate. This type of AIT formation likely also extends to later period of the Cambrian, especially in comparable preservational windows (Hinz-Schallreuter et al., 1998; Stockfors and Peel, 2005b; Zhang and Pratt, 2008; Wacey et al., 2008b;
ACCEPTED MANUSCRIPT Olempska and Wacey., 2016). The continuous occurrence of these structures suggests that the major phosphate deposition during Late Neoproterozoic and Early Cambrian was also a favorable environment for AIT formation, and their association with other phosphatic fossils is likely to be expected.
PT
When presented alone, micro-tubes on fossils might be interpreted in multiple
RI
ways. If they occur with true endolithic traces, however, distinctions in preservation
SC
may provide additional qualifications to help reduce the ambiguity in identification.
NU
The preservational mechanism observed here clearly demonstrates their different origins, specifically the later diagenetic stage of AIT formation, which must be
MA
subsequent to the phosphorite precipitation.The diverse morphological features of the AITs are also distinct from the biogenic characteristics of the microborings found on
D
phosphatic and phosphatized substrates in the geologic record (Rolfe, 1962;
PT E
Bengtson, 1976; Soudry and Nathan, 2000; Königshof and Glaub, 2004), including uniform size, rounded cross-sections or terminations and specific distribution or
CE
orientation patterns. The phosphatic casts of E.lata could reflect the original shapes of
AC
their microborings, just like using polymerizing resins to replicate modern euendoliths (Radtke and Golubic, 2011), and thus great morphological discrepancies between these endolithic microborings and the AITs could be observed. The irregular distribution of longitudinal striations on the microtube walls is incompatible with the hypothesis of a multi-filamentous euendolith (Stockfors and Peel, 2005b).
Viewing the AITs and endolithic traces through the lens of taphonomy, distinctions between these two types of structures is evident. In general, due to the process of
ACCEPTED MANUSCRIPT additional phosphate coating or infilling, micro-tubes occurring on secondarily phosphatized coatings, internal moulds or steinkerns are almost certainly AITs (our materials; Olempska and Wacey, 2016); whereas on shells and hard parts that are phosphorite replaced or original phosphate, more careful investigation is needed. If
PT
those tubules possess some of characteristics in which are accordance with the
RI
former, like grains at terminal ends, longitudinal striations, random orientations and
SC
distributions, or highly irregular morphology, the assignment to AITs is considerably more likely (Hinz-Schallreuter et al., 1998; Conway Morris et al., 1994; Stockfors and
NU
Peel, 2005b; Zhang and Pratt, 2008), while other structures lacking these features
MA
may represent true biogenic structures (Bengtson et al., 1992; Hua et al., 2003).
PT E
D
6 Conclusions
We report the first appearance of well-preserved ambient inclusion trails (AITs) in
CE
the Palaeozoic, together with a new and earliest occurrence of euendoliths Endoconchia lata from the SSF assemblage of the early Cambrian Kuanchuanpu
AC
Formation in South China. In addition, the organic carbonaceous spherules in AITs are first seen in the circumstance of phosphatic fossils from Late Neoproterozoic and Early Cambrian, expanding the geological record of such a terminal grain type to a larger setting and the criteria of AIT recognition. The study of euendolith preservation and their new-found co-occurrence with AITs enables direct comparison between these two microstructures, which in turn helps to reveal their differences in formation,
ACCEPTED MANUSCRIPT preservation, and morphology. We infer the preservational mechanism of these two structures to help explain their co-occurrence, suggesting a later diagenetic stage origin of the AITs present on the phosphatized Kuanchuanpu fossils. Demarcation between these two types of microstructures in the geologic record should be assisted
PT
not only by static morphological, but also by dynamic taphonomic considerations.
RI
Acknowledgments
SC
The authors thank H. Gong, Y. Pang, W. Yang, J. Sun, J. Luo (State Key Laboratory
NU
for Continental Dynamics, Northwest University, Xi’an, China) for their assistance both in the field and with lab work. We also thank colleagues Z. Zhang，L. Li，H. Yun for
MA
their constructive discussions, and T. Zhou (Xi’an Jiaotong University) for helping 3D visualization. The authors also thank three anonymous reviewers and editor T. Algeo
PT E
D
for their helpful comments and suggestions. This work was supported by the Natural Science Foundation of China (NSFC grant 41621003), the "973 project" of the of
Science
and
Technology
of
China
(grants
2013CB835002,
CE
Ministry
2013CB837100), and the State Key Laboratory of Palaeobiology and Stratigraphy (No.
AC
163107).
References
Brasier, M., McLoughlin, N., Green, O., Wacey, D., 2006. A fresh look at the fossil evidence for early Archaean cellular life. Philos. Trans. R. Soc. B 361, 887–902.
Bengtson, S., 1976. The structure of some Middle Cambrian conodonts and the early
ACCEPTED MANUSCRIPT evolution of conodont structure and function. Lethaia 9, 185–206.
Bengtson, S., Conway Morris, S., Cooper, B.J., Jell, P.A. & Runnegar, B.N., 1990. Early Cambrian fossils from South Australia. Australasian Association of
PT
Palaeontologists Memoir 9, 20–24, 232–256.
Bengtson, S., Yue, Z., 1992. Predatorial borings in late Precambrian mineralized
SC
RI
exoskeletons. Science 257, 367–369.
Campbell, S., 1982. Precambrian endoliths discovered. Nature 299, 429–431.
MA
boreholes. J. Paleontol 68, 1–23.
NU
Conway Morris, S., Bengston, S., 1994. Cambrian predators: possible evidence from
Chen, J., 2004. The Dawn of Animal World. Jiangsu Science and Technology Press,
PT E
D
Nanjing, p. 366. [in Chinese].
Dong, Y., M.., Ji, Q., Wang, S., 1984. The discovery of microscopic trace fossils in the
CE
Sinian Doushantuo Formation in southwestern China. Scientia Geologica Sinica 346–347 (in Chinese with English abstract).
AC
Furnes, H., Banerjee, N.R., Muehlenbachs, K., Staudigel, H. & de Wit, M.J. 2004. Early life recorded in Archean pillow lavas. Science 304, 578–581.
Golubic, S., 1969. Distribution, taxonomy and boring patterns of marine endolithic algae. Am. Zool 9, 747–751.
Golubic, S., Perkins, R.D., Lukas, K.J., 1975. Boring microorganisms and microborings incarbonate substrates. In: Frey, R.W. (Ed.), The Study of Trace
ACCEPTED MANUSCRIPT Fossils. Springer, Heidelberg, 229–259.
Golubic, S., Campbell, S.E., Drobne, K., Cameron, B., Balsman, W.L., Cimmerman, F., and Dubois, L., 1984. Microbial endolithss-a benthic overprint in the sedimentary record, and a palaeobathemetric cross–reference with formaninifera. J. Paleontol
PT
58, 351–361.
RI
Golubic, S., Seong-Joo, L., Browne, K.M., 2000. Cyanobacteria: architects of
NU
Springer-Verlag, Heidelberg, pp. 57–67.
SC
sedimentary structures. In: Riding, R.E., Awramik, S.M. (Eds.), Microbial Sediments.
MA
Grey, K., 1986. Problematic microstructures in the Proterozoic Discovery Chert, Bangemall Group, Western Australia. Ambient grains or microfossils? Geol. Surv.
D
Western Australia Prof. Papers for 1984, Perth, pp. 22–31.
PT E
Hinz-Schallreuter, I., 1998. Population structure, life strategies and systematic of phosphatocope ostracods from the Middle Cambrian of Bornholm. Mitt. Mus. Nat.kd.
CE
Berl. Geowiss. Reihe 1, 103–134.
AC
Hua, H., Pratt, B. R., Zhang, L., 2003. Borings in Cloudina Shells: Complex Predator-Prey Dynamics in the Terminal Neoproterozoic. PALAIOS 18, 454–459.
Knoll, A.H., Barghoorn, E.S., 1974. Ambient pyrite in Precambrian chert: new evidence and a theory. Proc. Natl. Acad. Sci. U. S. A. 71, 2329–2331.
Knoll, A. H., Golubic, S., Green, J., Swett, K., 1986. Organically preserved microbial endoliths from the late Proterozoic of East Greenland. Nature 321, 856–857.
ACCEPTED MANUSCRIPT Königshof, P., Glaub, I., 2004. Traces of microboring organisms in Palaeozoic conodont elements. Geobios 37, 416–424.
Lepot, K., Philippot, P., Benzerara, K., & WANG, G. Y., 2009. Garnet-filled trails associated with carbonaceous matter mimicking microbial filaments in Archean
PT
basalt. Geobiology, 7, 393–402.
RI
Li, G., 1997. Early Cambrian phosphate-replicated endolithic algae from Emei,
SC
Sichuan, SW China. Bulletin of National Museum of Natural Science [Taiwan] 10,
NU
193–216.
MA
Li, Z., 1984, The discovery and its significance of Early Cambrian small shelly fossils in Hexi Area, Xixiang, Shaanxi. Geology of Shaanxi 2, 73–78 (in Chinese with
D
English abstract)
PT E
Liu, P., Yin, C., 2006, Enigmatic microtunnels––The drag marks of Pyrites on the Phosphatized Spheroidal Fossils from Sinian Doushantuo Formation at Weng’an,
CE
Guizhou Province, Geological Review 52, 11–16 (in Chinese with English abstract).
AC
McLoughlin, N., Brasier, M.D., Wacey, D., Green, O.R., Perry, R.S., 2007. On biogenicity criteria for endolithic microborings on early Earth and beyond. Astrobiology 7, 10–26.
Muro-Pastor, A., Hess, W. R., 2012, Heterocyst differentiation: from single mutants to global approaches. Trends in Microbiology 20, 548–557.
Olempska, E., Wacey, D., 2016. Ambient inclusion trails in Palaeozoic crustaceans
ACCEPTED MANUSCRIPT (Phosphatocopina
and
Ostracoda).
Palaeogeography,
Palaeoclimatology,
Palaeoecology 441, 949–958.
Qian, Y., Bengtson, S., 1989. Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China. Fossils and Stret
PT
24, 1–156.
fossils
from
the
basal
of
China.
Acta
NU
Micropalaeontologica Sinica 24, 222–228.
Cambrian
SC
cyanobacterian
RI
Qian, Y., Li G., Jiang Z., Chen, M., Yang, A., 2007. Some phosphatized
MA
Radtke, G., & Golubic, S., 2011. Microbial euendolithic assemblages and microborings in intertidal and shallow marine habitats: insight in cyanobacterial
D
speciation. Lecture Notes in Earth Sciences 131, 233–263.
PT E
Rolfe, W.D.I., 1962. The cuticle of some Middle Silurian ceratiocaridid Crustacea from Scotland. Palaeontology 5, 30–51.
CE
Runnegar, B., 1985a. Early Cambrian endolithic algae. Alcheringa 9, 179–182.
AC
Runnegar, B., 1985b. Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringa: An Australasian Journal of Palaeontology 9, 245–257.
She, Z. B., Zhang, Y. T., Liu, W., Song, J., Zhang, Y., Li, C., Strother P., Papineau, D., 2016. New observations of Ambient Inclusion Trails (AITs) and pyrite framboids in the
Ediacaran
Doushantuo
Formation,
South
Palaeoclimatology, Palaeoecology 461, 374-388.
China. Palaeogeography,
ACCEPTED MANUSCRIPT Soudry, D., Nathan, Y., 2000. Microbial infestation: a pathway of fluorine enrichment in bone apatite fragments (Negev phosphorites, Israel). Sedimentary Geology 132, 171–176.
Steiner, M., Li, G., Qian, Y., Zhu, M., 2004. Lower Cambrian small shelly fossils of
PT
northern Sichuan and southern Shaanxi (China), and their biostratigraphic
RI
importance. Geobios 37, 259–275
SC
Steiner, M., Li, G., Qian, Y., Zhu, M., and Erdtmann, B.-D. 2007. Neoproterozoic to
NU
early Cambrian small shelly fossil assemblages and a revised biostratigraphic correlation of the Yangtze Platform (China). Palaeogeography, Palaeoclimatology,
MA
Palaeoecology 254: 67–99.
D
Steiner, M., Qian, Y., Li, G., Hagadorn, J. W., and Zhu, M. 2014. The developmental
PT E
cycles of early Cambrian Olivooidae fam. nov. (?Cycloneuralia) from the Yangtze Platform (China). Palaeogeography, Palaeoclimatology, Palaeoecology 398:
CE
97–124.
AC
Stockfors, M., Peel, J.S., 2005a. Endolithic Cyanobacteria from the Middle Cambrian of North Greenland. GFF 127, 179–185.
Stockfors, M., Peel, J.S., 2005b. Euendoliths and cryptoendoliths within late Middle Cambrian brachiopod shells from North Greenland. GFF 127, 187–194.
Sawaki, Y., Nishizawa, M., Suo, T., Komiya, T., Hirata, T., & Takahata, N., et al., 2008. Internal structures and u–pb ages of zircons from a tuff layer in the meishucunian formation, yunnan province, south china. Gondwana Research 14, 148–158.
ACCEPTED MANUSCRIPT Tyler, S.A., Barghoorn, E.S., 1963. Ambient pyrite grains in Precambrian cherts. American Journal of Science 261, 424–432.
Wacey, D., McLoughlin, N., Green, O.R., Parnell, J., Stoakes, C.A., Brasier, M.D., 2006. The ~ 3.4 billion-year-old Strelley Pool Sandstone: a new window into early
PT
life on Earth. Int. J. Astrobiol 5, 333–342.
RI
Wacey, D., Kilburn, M.R., McLoughlin, N., Parnell, J., Stoakes, C.A., Grovenor,
SC
C.R.M., Brasier, M.D., 2008a. Use of NanoSIMS in the search for early life on Earth:
NU
ambient inclusion trails in a c. 3400 Ma sandstone. J. Geol. Soc. Lond. 165, 43–53.
MA
Wacey, D., Kilburn, M., Stoakes, C., Aggleton, H., Brasier, M., 2008b. Ambient Inclusion Trails: their recognition, age range and applicability to early life on Earth.
D
In: Dilek, Y., et al. (Eds.), Links Between Geological Processes, Microbial Activities
PT E
& Evolution of Live. Springer Science + Business Media B.V, pp. 113–134.
Wacey, D., Saunders, M., Kong, C., & Kilburn, M. R., 2016. A new occurrence of
CE
ambient inclusion trails from the ~1900-million-year-old Gunflint Formation, Ontario:
AC
nanocharacterization and testing of potential formation mechanisms. Geobiology 14(5).
Xiao, S., Knoll, A.H., 1999. Fossil preservation in the Neoproterozoic Doushantuo phosphorite Lagerstätte, South China. Lethaia 32, 219–240.
Zhang X., Pratt, B. R., 2008. Microborings in Early Cambrian phosphatic and phosphatized fossils. Palaeogeography, Palaeoclimatology, Palaeoecology 267: 185–195
ACCEPTED MANUSCRIPT Zhang, Y., Golubic, S., 1987. Endolithic microfossils (cyanophyta) from early Proterozoic stromatolites, Hebei, China. Acta Micropaleontologica Sinica 4, 1–12 (in Chinese with English abstract).
Zhu, M., Jiang, Z., He, T., 1996. A preliminary study on the preservation, shell
PT
composition and m icrostructures of Cambrian small shelly fossils. Acta
SC
RI
Micropalaeomologica Sinica 13, 241–254 (in Chinese with English abstract).
NU
Fig. 1. Geological map and stratigraphic column of the fossil locality. (A). Geological
MA
map indicating the Cambrian strata and location of the fossil locality at the Zhangjiagou section in Xixiang County, Shaanxi Province. (B). Stratigraphic column
D
showing the occurrence of small shelly fossils. Numbers 1–4 represent the four
PT E
lithostratigraphic units in Kuanchuanpu Formation.
CE
Fig. 2. SEM images of euendolithic cyanobacteria Endoconchia lata on the
AC
Conotheca from the Kuanchuanpu Formation in Xixiang, China. (A). Tubular Conotheca with a cone-in-cone pattern, note phosphatic casts of Endoconchia lata borings on the innermost tube surface (ELIXX7-35). (B). Enlargement of A, within the white circle it is a spheroidal end and arrows show the string of swellings along filaments. (C–D). The most common occurrences of E. lata are surfaces of skeletal fossils moulds and the infills between original shells. White box in (D) show the cross-sections of endoliths casts (ELIXX3-120 and ELIXX16-88). (E). Some of the
ACCEPTED MANUSCRIPT filaments gradually melting into moulds (ELIXX66-63). (F). E. lata with dextrorotatory threaded decoration (ELIXX5-164).
PT
Fig. 3. Overviews of Ambient Inclusion Trails (AITs) in Conotheca. (A–B). Basic morphology of AITs as micro-tunnels and grooves, most of them are characterized by
RI
striated wall sculptures of minor ridges (ELIXX5-125 & ELIXX5-177). (C). A maze-like
SC
assemblage of AITs on a SSF internal mould (ELIXX5-173). (D). High density of AIT
NU
assemblages, forming a coarse surface (ELIXX6-52). (E). Co-occurrence of E. lata and AITs. Arrows show the position of the casts of E.lata, and within the circle it is the
MA
AITs. (ELIXX10-100). (F). Co-occurrence of E. lata and AITs, casts of E. lata being destroyed by AITs (ELIXX29-46). The 2 pictures are the same sample in different
PT E
D
orientations.
CE
Fig. 4. Detailed morphological features of AITs. (A). Rounded cross-sections and a
AC
spherical terminal grain in the other AIT (ELIXX52-290). (B). Variations of AIT sizes, within the circle is the minimum one among our materials (ELIXX15-129). (C). Grand AIT grooves (maximum one among current samples) with typical longitudinal wall striations, noting that the distribution of ridges is irregular (ELIXX32-15). (D). AIT tunnels with relatively smooth wall (ELIXX29-18). (E–F). Complex conjunctions of multiple AITs (ELIXX15-134; ELIXX19-53).
ACCEPTED MANUSCRIPT Fig. 5. Distribution of AITs inside an un-identified fossil. (A). SEM image of one specimen with conspicuous AITs (ELIXX29-22). (B). 3D visualization of (A). Green parts represent hollowed AIT tunnels and the fossil entity has been converted into translucent mask for better illustration. (C). A tomographic image of (B), showing
PT
cross-sections of AITs. (D). 3D visualization of AITs of (A), sample has been rotated to
SC
RI
present a better view of both small and large AITs.
NU
Fig. 6. Spherical AIT terminal grains and their chemical composition. (A). Raman spectra of spherical terminal grains. Top-Left: CL image of one thin section, showing
MA
an AIT with a granular particle in the distal end (white box) and the cross marks the position where the Raman analysis was positioned; Top-Middle: SEM image of stray
PT E
D
spherules from a crushed fossil (Scale bar=50μm). (B). SEM image of one spherical terminal grain (enlarged from Fig. 4A). The rounded cross-section fits the spherules
CE
outline (ELIXX52-290). (C). SEM image of another spherical terminal grain. The striated wall sculptures of AIT match the profile of the grain (white arrows)
AC
(ELIXX71-44). (D). EDS mapping of (B), indicating the concentration of C and lack of Ca, P and Fe.
Fig. 7. The relationship between AITs, host fossils and carbonate substrates. (A). A continual trail on an embryo-like fossil, indicating the paths of AITs penetrated between fossil and surrounding substrates frequently (ELIXX16-31). (B–C). Crossed
ACCEPTED MANUSCRIPT polarizing microscope photographs of thin sections with AITs. The black parts are fossils constituted by collophane, the bright parts are calcite cements. It is notable that those AITs show no extension in to the calcareous substrates. (D). CL image of the area in (C), showing the background color of AITs infilling and the calcite cements are
RI
PT
identical.
SC
Fig. 8. Mechanism of AIT and euendoliths preservation. (A–D). Forming of euendolith
NU
casts. (E). AITs formed later than phosphate infilling of euendolithic microborings. (F). Cementation after the redepositing of AIT-hosted fossils and AITs were infilled with
MA
calcareous matters. (“V shapes”cross-sections of shells; “Round shape”： embryo-like organism; Background colour: light blue- water; dark blue-phosphate; gray-carbonate
AC
CE
PT E
D
cement).
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
AC
CE
PT E
D
MA
NU
SC
RI
PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Highlights
Earliest record of well-preserved AITs and co-occoured euendolith Endoconchia
lata in Palaeozoic. Discrepancies between AITs and endolith traces in formation, preservation and
PT
RI
morphology are revealed.
Rare type of AIT propelled grains as organic carbon spherules are reported.
AITs formed during the late phase or after the phosphorite lithification.
Our data suggest most microtubular structures on secondarily phosphatized
NU
SC
AC
CE
PT E
D
MA
fossils should be AITs.