Spatial variation in the diversity and composition of the Lower Cambrian (Series 2, Stage 3) Chengjiang Biota, Southwest China

Palaeogeography, Palaeoclimatology, Palaeoecology 346-347 (2012) 54–65

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Spatial variation in the diversity and composition of the Lower Cambrian (Series 2, Stage 3) Chengjiang Biota, Southwest China Fangchen Zhao a,⁎, Shixue Hu b, Jean-Bernard Caron c, Maoyan Zhu a, Zongjun Yin a, Miao Lu a a b c

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China Chengdu Institute of Geology and Mineral Resources, Chengdu Center of China Geological Survey, Chengdu 610081, China Department of Natural History-Palaeobiology, Royal Ontario Museum, 100 Queen's Park, Toronto, Ontario, Canada M5S 2C6

a r t i c l e

i n f o

Article history: Received 1 February 2012 Received in revised form 2 May 2012 Accepted 23 May 2012 Available online 30 May 2012 Keywords: Cambrian Chengjiang Biota Taphonomy Paleoecology Community Diversity Konservat Lagerstätten

a b s t r a c t Strata hosting the Lower Cambrian (Series 2, Stage 3) Chengjiang Biota (Maotianshan Shale Member, Yu'anshan Formation) occur throughout the eastern part of Yunnan Province, Southwest China. In this study, literature-based faunal inventories from 10 areas (representing 34 localities), together with 22,038 new specimens collected at three localities from three of the 10 areas, were analyzed quantitatively to assess large-scale spatial variation in taxonomic diversity and composition. Our analyses show substantial covariation between local paleoenvironmental settings and species diversity, and suggest the presence of three general taphofacies in the Maotianshan Shale Member, from west to east: low diversity (26 species) characterizes the Wuding area, where fossiliferous strata have undergone extensive bioturbation; high diversity (215 species) characterizes the Chengjiang–Haikou–Anning areas, where fossiliferous strata consist of stacked couplets of thin event and background mudstone layers; moderate diversity (55 species) characterizes the Malong area, where fossiliferous strata consist of indistinctly bedded shale showing fewer single-event layers but abundant background layers. In spite of variations in sampling effort between sites, spatial patterns in species diversity and community composition were controlled primarily by variation in depositional environments along a proximal offshore to lower shoreface gradient, which influenced both ecological and taphonomic factors. The offshore settings (Haikou–Chengjiang–Anning areas) show relatively high species diversity and exceptional preservation of soft-bodied fossils, reflecting rapid burial in distal tempestites. Relatively high degrees of bioturbation, time-averaging and hydrodynamic disturbance caused a substantial decrease in the quality of preservation and number of soft-bodied species in the Wuding and Malong areas. Arthropods are the most diverse group in most localities, followed by priapulids, poriferans, brachiopods, lobopods and hyoliths. This study shows that the Chengjiang Biota lends itself very well to high resolution characterization of spatial variation in taxonomic diversity, faunal composition and fossil preservation. Furthermore, the Chengjiang Biota may provide a unique opportunity to assess the roles of environmental factors, taphonomy and ecological controls on species diversity at local to regional spatial scales. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Cambrian Konservat Lagerstätten such as the Chengjiang Biota and the Burgess Shale preserve far more biological and ecological information than do ordinary fossil deposits containing biomineralized organisms only (e.g., Hou et al., 1999; Conway Morris, 2000; Butterfield, 2003; Chen, 2004; Hou et al., 2004; Briggs and Fortey, 2005). Yet in spite of the critical importance of Konservat Lagerstätten for understanding the origin and development of modern-style ecosystems following the “Cambrian explosion” (e.g., Vannier and Chen, 2000; Chen et al., 2007; Hu et al., 2007; Caron and Jackson, 2008; Dunne et al., 2008), the degree

⁎ Corresponding author. E-mail address: [email protected] (F. Zhao). 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2012.05.021

to which species diversity and composition vary between localities, and the environmental, taphonomic, ecological and evolutionary factors controlling this variation, are still poorly understood. Very few studies have tackled these issues, and most quantitative analyses have been limited to single fossil localities (Conway Morris, 1986; Caron and Jackson, 2006, 2008; Dornbos and Chen, 2008; Zhao et al., 2009). The Chengjiang Biota in Yunnan Province, China holds great potential for detecting and analyzing metacommunity patterns, as abundant and diverse coeval fossil assemblages are known from many localities distributed over a large geographic area (Fig. 1) (e.g., Zhang et al., 2001; Chen, 2004; Hou et al., 2004; Zhu et al., 2006; Shu, 2008; Zhao et al., 2010). The known occurrence of Chengjiang fossils initially was restricted to Chengjiang County, particularly near Maotianshan, where fossils of soft-bodied organisms were first discovered (e.g., Zhang and Hou, 1985; Chen et al., 1996). Subsequently, systematic geological investigations in east-central Yunnan resulted in the discovery of important new localities, especially those

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Fig. 1. Distribution of early Cambrian outcrops in Eastern Yunnan, showing main fossiliferous areas and localities (with GPS coordinates) yielding the Chengjiang Biota. Areas and localities in bold were analyzed in this study. Abbreviations: B = background mudstone; E = event mudstone. Modified from Hu (2005) and Zhao et al. (2010).

near Haikou (Luo et al., 1997), which have yielded the oldest vertebrates (Shu et al., 1999, 2003). Another highly productive locality, found in Shankou village in Anning (Chen, 2004), features abundant priapulid worms (Dornbos and Chen, 2008). Moving northwestward from Anning, highly fossiliferous layers discovered near Wuding (Fig. 1) contain abundant shelly and lightly sclerotized fossils but only rare soft-bodied specimens (Zhang et al., 2001; Chen et al., 2002; Hu, 2005). Minor outcrops of the Cambrian sequence occur near Kunming and the east shore of Dianchi Lake (Fig. 1), but these areas are poorly known and relatively few fossils have been reported in the literature (Luo et al., 1999; Zhang et al., 2001; Chen et al., 2002; Steiner et al., 2005). Moving northeastward from Yiliang, shelly fossils are abundant, but soft-bodied and lightlysclerotized organisms are relatively sparse in most areas except around Malong (Kuangshan section, Hu, 2005). The aim of the present investigation is to analyze spatial variation in species diversity and biotic composition of the Chengjiang Biota within all areas where it is known to occur. We also evaluated the potential factors giving rise to this variation, and investigated their effects upon the original biological and ecological signals.

2. Geological setting, age and sedimentology The Lower Cambrian Chengjiang Biota (~520 Ma) occurs within the Maotianshan Shale Member of the Yu'anshan Formation in Eastern Yunnan, in a biozone characterized by the trilobite genera Eoredlichia and Wutingaspis (Zhu et al., 2001b; Hu, 2005; Figs. 1 and 2A). The depositional environment of the Yu'anshan Formation has variously been interpreted as a normal shallow marine shelf (Luo et al., 1982), a partially restricted marine embayment (Erdtmann and Steiner, 2001), a delta front (Jin et al., 1991), or a foreshore and nearshore shelf (Pu et al., 1992). Importantly, storm-generated tempestites, first recognized by Sun et al. (1987) and Sun and Chen (1988) are conspicuous stratigraphic features throughout much of the Yu'anshan Formation. These previous studies were based on limited observations and did not specifically investigate the depositional environment of the soft-bodiedfossil-bearing mudstones. Zhu et al. (2001b) argued that such mudstones represent distal tempestites deposited in a proximal offshore to lower shoreface setting that was frequently influenced by stormderived freshwater input. More recent detailed sedimentological and

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Fig. 2. Stratigraphical correlations of the Maotianshan Shale Member sample sections, showing (A) the generalized stratigraphy of the Lower Cambrian in Eastern Yunnan and the detailed stratigraphy of the Maotianshan Shale Member in (B) the Sapushan section, Wuding area, (C) the Mafang section, Haikou area and (D) the Kuangshan section, Malong area.

taphonomic analyses (Hu, 2005) supported this interpretation and further suggested that deposition occurred along a shallow, gently sloping muddy shelf. 3. Materials and methods We tabulated, based on exhaustive literature search, all 229 Chengjiang Biota animal species described since 1985 (Appendix 1). Four species published in late 2011 were also tabulated (including Galeaplumosus abilus Hou et al., 2011, the first putative hemichordate recorded in the biota) but were not analyzed in this study. The most up to date taxonomic status for each species was used (i.e., all synonymous species were counted only once). For each species, we recorded their presence or absence in the Maotianshan Shale Member in ten areas (representing 34 localities) in Eastern Yunnan (Fig. 1; Appendix 1). Four areas (Hua'ning, Dongchuan, Huize and Xundian), representing seven localities, are known to yield soft-bodied fossils but were not included in this study because of insufficient knowledge about the localities and limited fossil inventories. The 10 areas

studied herein are defined based on earlier studies. Collections were made in various localities within particular areas, and each of these localities was empirically determined by earlier workers to yield similar fossil assemblages. However, the precise locality and stratigraphic information for each specimen was not recorded for the most part. Thus, it was not possible to study the biotic content per locality. Each of the 10 areas surveyed represents mixed fossil assemblages that can be considered averages of species composition present within particular areas and time-averaged assemblages of unknown duration. Semi-quantitative estimates of species abundance in each area are also provided—when available—based on previous publications (see Appendix 1). Because of the lack of precise locality and stratigraphic information in past studies, we conducted additional fieldwork in the areas of Wuding (Sapushan section), Haikou (Mafang section) and Malong (Kuangshan section) (Fig. 1), using standard sampling procedures in each locality. The strata sampled occur in the middle to upper parts of the Maotianshan Shale Member (Fig. 2) and are assumed to be closely similar in age. A total of 11,236 fossil-bearing slabs were collected (fossils occurring on both part and counterpart were counted only once), with 90% of the fossils

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consisting of both part and counterpart. The tops and bottoms of slabs and the orientations of individual fossils were recorded in the field in some cases, as well as the degree of association/disassociation of the fossils and other relevant taphonomic, biotic and sedimentological information (e.g., presence of fossils occurring in clusters). Fossils were counted per taxon (to the lowest taxonomic rank possible) in each section, and preservational characteristics were tabulated for taphonomic analysis (see Appendix 2). In order to compare fossil preservation patterns between areas, we created two datasets. In dataset A, three complementary parameters related to the degree of disarticulation/disassociation were erected based on the percentage and number of species represented by: 1) articulated/associated specimens only; 2) disarticulated/ disassociated specimens only; and 3) mixed articulated/associated and disarticulated/disassociated specimens. In dataset B, specimens with soft-tissue preservation were divided into two categories (types 1 and 2): type 1 consists of specimens showing the highest degree of preservation (i.e., least amount of decay), often preserving noncuticularized tissues such as internal organs (e.g., gut) and fine anatomical structures (e.g., eyes, antennae, gill-blades of arthropods); type 2 consists of specimens preserving only the most resilient tissues, typically heavily cuticularized parts (e.g., arthropod carapaces), and with fine details like arthropod limbs not preserved. A third category consists of specimens preserving only biomineralized parts. A specimen possessing biomineralized parts could preserve soft-tissues and therefore could also be coded type 1 or 2 for the degree of soft-tissue preservation. In each section, fossils came from various mudstone layers, and therefore our collections represent induced time averaged assemblages of unknown duration. In the Mafang section, fossils from event mudstones were counted separately from those in background mudstones, while in the Kuangshan and Sapushan sections this distinction could not be made, and all fossils collected were counted as a whole. Our abundance data matrix contains 22,038 specimens collectively assigned to 98 species (Appendix 2), and includes 9937 specimens preserved in event mudstones and 1735 specimens preserved in background mudstones from the Mafang section in Haikou (also see Zhao et al., 2009), 7075 specimens from the Kuangshan section in Malong, and 3291 specimens from the Sapushan section in Wuding. Unidentifiable specimens and undescribed species were not included in our data matrix. All specimens used in this study are housed in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGPAS). All species (except problematic and indeterminate taxa) were assigned to their respective phyla or to the lowest taxonomic groups possible based on previous publications. Selected rock samples were cut normal to bedding and then dry polished using fine sandpaper. Millimeter-scale resolution logs were produced based on high definition digital images (1200 dpi) for detailed sedimentological analyses. Several quantitative analytical techniques (principal component analysis (PCA), cluster analysis, rarefaction curves) were employed to investigate species richness and composition within different areas. Because most of our data came from the literature and were not associated with abundance information we use the presence/absence of species as the basis for most of our analyses. The Mafang section was separated into different taphofacies (background and event mudstones; see Zhao et al., 2009) to investigate how taphonomic factors potentially affected species composition within a given area. These data were tabulated and analyzed separately from the other localities present in the Haikou area, including previous investigations conducted at Mafang (i.e., species counts from the Mafang locality based from the literature were kept separate from species counts based from our new excavations). In the three sections that we sampled, access to abundance data allowed us to test the effect of abundance on species diversity. However, to limit the effect of variations in sampling intensity, we used rarefaction curves to compare species richness in the three sections studied and comparisons were made at the level of the least sampled assemblages (Sapushan section and background beds of the Mafang section).

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4. Regional diversity Until mid 2011, 229 animal species representing at least 17 phyla or main taxonomic groups (including stem groups) and over 23 ecological groups have been reported from the Maotianshan Shale Member (Appendix 1, Tables 1–3). Areas characterized by large number of species are Haikou (161), Chengjiang (138) and Anning (80), followed by Malong (55), Jinning (34), Wuding (26), Kunming (25), Chenggong (17), Yiliang (16) and Qujing (15; Table 1). Arthropods are by far the dominant group, ranking first in all areas (Fig. 3) and accounting for an average of 55.5% of species per area (Table 2). Priapulids rank second, followed by poriferans, brachiopods, lobopods and hyoliths. Phyla with large number of species tend to be present in most areas (Table 1), while phyla with few species generally are absent in most areas (e.g., chordates average just 0.7% of total diversity, with most species occurring only in the Haikou area). Many species occur in just one or a few areas or are rare enough to have been missed in some areas. The total number of unique species (i.e., endemic to a single area) is 105, representing 45.9% of the total number of species identified (Fig. 4). Most of these species (93) occur in the Haikou, Anning and Chengjiang areas, and are not known elsewhere. Only 12 species are unique to other areas (Fig. 4). By contrast, only four species, Isoxys auritus, Mafangscolex sinensis, Kunmingella douvillei and Naraoia longicaudata, are present in all areas (Table 3); among these, only Kunmingella possesses biomineralized parts (a weakly mineralized carapace). The number of common species (which are here defined as those present in five or more areas) is just 29, or 12.7% of the total number of species (Fig. 4, Table 3). Common species tend to be abundant in areas with a small total number of species; for example, in Yiliang and Chenggong common species tend to be represented predominantly by species that are common throughout the region (81% and 82%, respectively). Twelve or 41% of common species have biomineralized parts. However, the proportion of common species having biomineralized parts in areas with low species number (all areas with less than 34 species) varies from 27% (Qujing) to 50% (Wuding) and is not significantly different—perhaps with the exception of Wuding—from other areas with a larger number of species present (where biomineralized species range from 40% to 43%). By comparison, biomineralized species only represent 21% of all known species across all areas suggesting that common species with biomineralized parts

Table 1 Number of species per phylum (including unknown species) ranked in abundance per areas compared to data collected in one locality from both event (E) and background beds (B) (Mafang section, Haikou area, see Appendix 1). For abbreviations, see Fig. 1. Phylum

Areas

Sample locality

WD AN HK Arthropoda 19 Priapulida 1 Porifera Brachiopoda 2 Lobopodia 1 Hyolitha 2 Vetulicolia Cnidaria Ctenophora Chordata Chancelloriids 1 Sipuncula Echinodermata Annelida Phoronida Mollusca Chaetognatha Unknown Total number of 26 species

30 14 9 6 4 2 2 2 2 1 1 2 1

JN

NK CG CJ

58 20 18 16 6 3 18 8 2 2 12 1 6 4 1 5 1 6 4 7 1

11 2 1 1

YL

64 9 26 5 7 4 4 3 3 2 1

ML QJ

9 24 2 4 11 4 5 1 2 4 2 1

MF(E) MF(B)

10 36 2 7 2 8 6 1 7 3 4 4

18 2 8 2 2 1 1

1

1 1 1

1 3 80

1 1 17 1 161 34 25

1 2 17

8 2 138 16 55

4 15 81

34

58

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Table 2 Proportion of species per phylum (including unknown species) across all areas compared to data collected in one locality from both event (E) and background beds (B) (Mafang section, Haikou area, see Table 1 and Appendix 1). For abbreviations, see Fig. 1. Rank

Phylum

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Arthropoda Priapulida Porifera Brachiopoda Lobopodia Hyolitha Vetulicolia Cnidaria Ctenophora Chordata Chancelloriids Sipuncula Echinodermata Annelida Phoronida Mollusca Chaetognatha Unknown

Areas

Sample locality

Mean

Range

MF(E)

MF(B)

55.5% 11.2% 8.0% 7.8% 4.1% 4.0% 1.6% 1.0% 0.7% 0.7% 0.6% 0.3% 0.2% 0.1% 0.1% 0.2% 0.1% 3.8%

36.0%–73.1% 3.8%–17.6% 0–20.0% 0–25.0% 0–7.5% 0–11.8% 0–4.0% 0–3.7% 0–2.5% 0–4.3% 0–3.8% 0–2.5% 0–1.3% 0–0.7% 0–0.7% 0–1.3% 0–0.6% 0–11.8%

44.4% 8.6% 9.9% 7.4% 8.6% 3.7% 4.9% 4.9% 0 0 1.2% 0 0 0 0 1.2% 0 4.9%

52.9% 5.9% 23.5% 5.9% 0 5.9% 2.9% 2.9% 0 0 0 0 0 0 0 0 0 0

PCA scores for areas with relatively high number of species tend to lie in the right-hand portion of the diagram probably owing to the presence of a large number of species which are unique to these areas or are rare enough so that they were not sampled in other areas (Figs. 4 and 5A–C). Areas having low number of species (Fig. 5C) tend to group together to the center left of the PCA along the first axis (Fig. 5A). A position close to the center suggests that most of the species present in areas with low number of species tend to be present in most other studied areas, including those with larger number of species (Fig. 5D). These species tend to have wide geographic distributions confirming our previous empirical observations based on the smaller subset of common species (Table 3). Cluster analysis also indicates that the degree of similarity decreases with increasing number of species (Fig. 5E). As with the PCA, this is probably due to the large number of unique species present in areas with high number of species (Fig. 5D).

5. Taphonomic analysis 5.1. Preservation of Chengjiang fossils—overall regional patterns

might be more common and abundant (see Appendix 2) for taphonomic reasons (i.e., potentially as part of time averaged assemblages), and/or simply represent species adapted to a wider range of environmental conditions (eurytopic species).

As noted by Hu (2005), the Maotianshan mudstones can be grouped into three general taphofacies. Moving from west to east, the Wuding area is characterized by low diversity (26 species have been documented, mostly brachiopods, hyoliths and arthropods), intense bioturbation (Fig. 6A, F) and an abundance of biomineralized fossils (Fig. 7A, D, G, J, M). Around Dianchi Lake (including Chengjiang, Chenggong, Kunming City, Haikou, Anning and Jinning;

Table 3 Distribution of common species across all areas studied. Common species are defined as those that are present in five or more areas. Abbreviations: Arth = Arthropoda; Pria = Priapulida; Brach = Brachiopoda; Hyol = Hyolitha; Lobo = Lobopodia; Un = Unknown; Pori = Porifera; VC = very common; C = common; R = rare; VR = very rare; Documented occurrences without information on abundance are marked by (X); C1 = life habit; C2 = species with biomineralized parts; C3 = fossil concentration (e.g., showing evidence of large number of individuals on the same slabs), PE = Pelagic, NK = Nektobenthic, EV = epifaunal vagrant, ES = epifaunal sessile, IV = infaunal vagrant; for area abbreviations, see Fig. 1. Species name (phylum)

Isoxys auritus (Arth) Mafangscolex sinensis (Pria) Kunmingella douvillei (Arth) Naraoia longicaudata (Arth) Branchiocaris? Yunnanensis (Arth) Leanchoilia illecebrosa (Arth) Diandongia pista (Brach) Kunyangella cheni (Arth) Eoredlichia intermedia (Arth) Heliomedusa orienta (Brach) Waptia ovata (Arth) Naraoia spinosa (Arth) Ambrolinevitus ventricosus (Hyol) Cricocosmia jinningensis (Pria) Microdictyon sinicum (Lobo) Maotianshania cylindrica (Pria) Kuanyangia pustulosa (Arth) Yunnanocephalus yunnanensis (Arth) Stellostomites eumorphus (Un) Paraleptomitella dictyodroma (Pori) Glossolites magnus (Hyol) Isoxys paradoxus (Arth) Canadaspis laevigata (Arth) Tabelliscolex hexagonus (Pria) Lingulellotreta malongensis (Brach) Amplectobelua symbrachiata (Arth) Retifacies abnormalis (Arth) Isoxys curvirostratus (Arth) Leptomitus teretiusculus (Pori) Number of common species (N) Total number of species (T) N/T

Areas

Fre.

WD

AN

HK

JN

NK

CG

CJ

YL

ML

QJ

C R C VR

C C VC VC C C VC X C C VC C X C R C R C R C C R X VR C C R R X 29 80 36%

VC VC VC VC C VC C R C C VC C C VC R

C X VC X X X X X X X X

C C C VC X X R X X X

C X C C X X X

VC C VC VC C VC R C C C VC VC VC VR R VC R C VC C R R R VR VC C R R C 29 138 21%

C X C C X X X X X X X

C C VC VC R R R

C R VC VC R R

VC C C R VC C R C R

VR

14 26 54%

X X

X C X

X X X X

X R C C C C R C VR C C R R C 28 161 17%

R X X

X X X

X R X VR

X R 20 34 59%

17 25 68%

X 14 17 82%

X

X

13 16 81%

X R VC C VC R R R

C R R R VR VR X R R R R 25 55 45%

C

R R

X

11 15 73%

Ecological and biological characters C1

10 10 10 10 9 9 9 8 8 8 8 7 7 7 6 6 6 6 6 5 5 5 5 5 5 5 5 5 5

PE IV EV EV NK EV ES EV EV ES NK EV ES IV EV IV EV EV PE ES ES PE EV IV ES NK EV PE ES

C2

*

* * *

*

C3 * * * * * * * * * * * * *

* * * * *

* *

* * * *

*

* *

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processes (Zhao et al., 2009). Event mudstone beds contain the highest number of species (215 have been documented, including many of the rarer animal groups such as chordates and ctenophores; Appendix 1), and also show excellent soft-tissue preservation (Fig. 7C, F, I, L, O), mainly in the Chengjiang, Haikou and Anning areas. In the eastern part of Eastern Yunnan, the taphofacies of the Malong area is characterized by moderate number of species (55 have been documented), and the quality of soft-bodied fossil preservation is poorer than in the Chengjiang, Haikou and Anning areas (Fig. 7B, E, H, K, N). Fossiliferous strata in the Malong area are composed of indistinctly bedded shales showing mixing of background and event mudstones possibly due to some level of bioturbation, but more likely due to hydrodynamic reworking or transport (Fig. 6B, G). The latter interpretation is based on the presence of uniformly distributed organic detritus, the presence of micro-grading structures as well as preferred orientations of some fossils within the mudstones. Event-background beds might be too thin to be detected in some cases. However, the Malong area is close to an abundant source of sediment (the “Niushouhsan underwater swell”) suggesting that this last hypothesis is perhaps less likely. 5.2. Quantitative analysis of fossil preservation and species composition

Fig. 3. Comparisons of species abundance of major taxonomic groups among the study areas, based on data in Table 1 and Appendix 1. Abbreviations: WD = Wuding County, AN = Anning, HK = Haikou, MF (E) = the Mafang section (event mudstones), MF (B) = the Mafang section (background mudstones), JN = Jinning County, NK = Near Kunming, CG = Chenggong County, CJ = Chengjiang County, YL = Yiliang County, ML = Malong County, QJ = Qujing.

Fig. 1), Maotianshan mudstones consist of stacked couplets of thin, single-event and background mudstone layers (Zhu et al., 2001b; Hu, 2005; Zhao and Zhu, 2007; Zhao et al., 2009; Fig. 6C–E, H–J). Fossils in background mudstones consist predominantly of indeterminate organic elements and fecal or algal strings, with few and poorly preserved soft-bodied animals, indicating that fossils have undergone significant pre- or syn-burial decay and represent limited timeaveraged assemblages. In contrast, fossils in event mudstones contain greater number of species, specimens and well-preserved soft-bodied animals (Fig. 7C, F, I, L, O), which were smothered by storm-generated mud clouds more or less within the same environment (i.e., the fossil assemblages are autochthonous or para-autochthonous). Fossil assemblages in background and event mudstones in the same section represent a single local community subjected to different taphonomic

Fig. 4. Variation in species diversity and ratios as a function of cumulative number of sites occupied, showing that sites yielding species restricted to a particular site have the highest total number of species (105), including 57 from the Haikou area, six from the Anning area, 30 from the Chengjiang area and 12 from other areas.

The number and proportion of species (Fig. 8A) represented by articulated/associated specimens are much greater (84%) at Mafang (event mudstones) than in the other two areas combined (Malong and Wuding), including the background mudstones at Mafang. Interestingly, the Malong (Kuangshan section) fossil assemblage appears nearly identical in terms of its ratio of articulated/associated species to the fossil assemblage from background mudstones in the Mafang section. This pattern suggests similar taphonomic bias but affecting a slightly different assemblage of organisms owing to only moderate shared species and βdiversity levels between the two localities (Fig. 11). In terms of quality of preservation (Fig. 8B), the best preserved specimens (type 1) are observed at Mafang, in event mudstones. Such observations, combined with a high ratio of articulated/associated soft-bodied species belonging to a range of taxa in this section, indicate rapid burial and limited decay of a smothered community. Taphonomic experiments have shown that in the absence of decay, many soft-bodied fossils could still remain well preserved after significant transport (Allison, 1986). While some level of transport of some specimens, especially of nektobenthic and pelagic species is more likely (but see Zhang et al., 2006 and Zhang and Hou, 2007 for evidence of minor transport of benthic organisms), we believe that most animals, in particular those comprising the benthos, are probably autochthonous or para-autochthonous. This conclusion is based on the discovery of animals in conspecific and polytaxic clusters (Hu, 2005; Han et al., 2006), on the fact that there is no indication of preferred orientation or sorting of specimens, and on the presence of failed escaped traces suggesting that certain animals reacted to burial (Hu, 2005; Zhao et al., 2009). In contrast, in Malong (Kuangshan section) the relatively low ratio of articulated/associated soft-bodied species, and the low quality of preservation, corroborate independent sedimentological evidence of storm-related transport. Some specimens were presumably killed during storm events, while others were already dead and in various states of decomposition. In the Wuding area (Sapushan section), the high ratio of disarticulated/disassociated species and the lack of species with wellpreserved soft-tissues more likely reflect an increase in bioturbation, suggesting oxic bottom conditions at the time of burial. Both the number of estimated species and the rarefaction curves clearly show large differences in species richness and evenness between the three regional taphofacies when similar number of specimens are compared (Fig. 9). All curves are slowly rising, suggesting that one should expect to find additional species with more sampling, but that overall the four areas are well sampled. The rarefaction curve for the Sapushan section (Wuding area) is based on the smallest number of species and is more nearly horizontal, suggesting lower evenness (i.e., the number of specimens per species fluctuates

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Fig. 5. A, scatterplots of principal component analysis (PCA) axes 1 and 2 for ten fossil areas plus fossil assemblages from both event and background mudstones of the Mafang section, Haikou, based on the species presence/absence data. Percentage of total variance accounted for by axis 1 = 42.2% and by axis 2 = 15.2%. B, same scatterplots of PCA as in A, but with axis 1 and axis 3, which accounts for 10.6% of the variation observed. C, number of species per fossil area along axis 1 of the PCA, showing gradual increase in number of species along the axis. D, percentage of common species per fossil locality along axis 1 of the PCA, showing similar species compositions among areas with low species richness. Common species are defined as species present in five or more areas (see Table 3). E, cluster analysis of sample areas, based on the single linkage algorithm computed by the Euclidean distance index to create the distance matrix; the number indicates similarity levels. PCA and cluster analyses were performed with the PAST software package of Hammer et al. (2001). Abbreviations: WD = Wuding County, AN = Anning County, JN = Jinning County, HK = Haikou County, MF (E) = the Mafang section (event mudstones), MF (B) = the Mafang section (background mudstones), NK = Near Kunming, CG = Chenggong County, CJ = Chengjiang County; YL = Yiliang, ML = Malong County; QJ = Qujing.

widely). Species richness and evenness are highest in the Mafang section (event mudstones) in the Haikou area. The Mafang section (background mudstones) in the Haikou area and the Kuangshan section in the Malong area lie between the previous two sections in terms of species richness and evenness, and are most similar to each other. Based on the quality of fossil preservation and species diversity levels (abundance and richness), we here expand the definition of the three main taphofacies previously recognized in the Maotianshan Shale Member: Taphofacies I (best preservation), with common type 1 soft-bodied fossils preserved in distinct event mudstone layers, is best developed in the Chengjiang–Haikou–Anning areas; Taphofacies II (good preservation), with rare type 1 soft-bodied fossils preserved in mixed background and event mudstones, characterizes the Malong– Qujing areas; and Taphofacies III (poor preservation), with rare type 2 soft-bodied fossils and abundant biomineralized specimens preserved in extensively bioturbated shales, characterizes the Wuding area. Fig. 10 shows the distribution of species within each of the three taphofacies. Some 215 species occur in the Anning, Haikou and Chengjiang areas (Taphofacies I). A majority of these species (69.3%) are unique to these areas, while the remaining species are also known in the other two taphofacies (II only = 19.1%, III only = 6.5% and II + III = 5.1%). There are only four species (1.8%) present in Malong and Wuding which are not known in the Taphofacies I areas; the majority of species in Taphofacies II and III also occur in Taphofacies I. However, relatively few species are shared between Taphofacies II and III (20% of species in Taphofacies II are also present in Taphofacies III, and 44% of species in Taphofacies III are also present in Taphofacies II), indicating that the species compositions of the Malong and Wuding areas are noticeably different from each other.

To further explore differences between the three taphofacies (including between localities within particular taphofacies), we employed a β diversity index, the Sørensen index (=2C / A + B, where A and B are the number of species in localities A and B, respectively, and C is the number of species shared by the two localities), which ranges from a value of 0 (no species overlap) to a value of 1 (complete species overlap; Wilson and Shmida, 1984; Koleff et al., 2003). Observed values of this index confirm that the Chengjiang, Haikou and Anning areas have higher number of shared species than the Malong and Wuding areas (Fig. 11), and that the Chengjiang, Haikou and Anning areas also show strong taxonomic overlap, with 59 species occurring in all three areas (Fig. 12). 6. Discussion Regional differences between fossil associations of the Chengjiang Biota are the results of a combination of environmental, taphonomic and ecological factors. Previous work on the Cambrian paleogeography of Eastern Yunnan revealed the presence of a west–east-oriented onshore–offshore gradient, based both on sedimentological evidence and the distribution of fossils (Zhu et al., 2001a; Chen et al., 2002; Hu, 2005). The precise location of the paleoshoreline is unknown, but its position must be far to the west of the Wuding area, which has been featured in many previous paleoenvironmental reconstructions (Hu, 2005). Related to this problem is the controversy surrounding the putative “Niushoushan Old Land” in the nearby Niushoushan region (now located east of Chengjiang). Although an “old land” origin was suggested by some authors (Luo et al., 1982; Chen et al., 2002), Zhu et al. (2001a) preferred to interpret this feature as an “underwater swell”. Our results, namely the absence of a paleoshoreline and the

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Fig. 6. Polished slabs and schematic diagrams of typical sedimentary facies. A, the Sapushan section, Wuding, showing intense bioturbation. B, the Kuangshan section, Malong, showing reworking and redeposition by hydrodynamic agents. C–E, sections showing background and single-event couplets: C, from the Shankou section (Anning); D, from the Xiaolantian section (Chengjiang); E, from the Mafang section (Haikou). F–J, schematic diagrams of textural/sedimentological characteristics for A–E; scale bar = 0.5 cm (overall color differences between polished slabs due to weathering).

presence of mudstone deposition in this area during the time of Maotianshan Shale deposition, corroborate this hypothesis. However, the Niushoushan swell probably only played a local role in controlling the distribution of facies, especially in the Yiliang–Malong–Qujing areas. An onshore–offshore trend is also recorded in the distribution of taphofacies. The proportion of single-event and background mudstones is a reliable indicator of paleobathymetry and distance from the paleoshoreline. In western areas such as Wuding, this is poorly discernible owing to pervasive bioturbation. Stacked couplets of thin, single-event and background mudstones are well developed in distal areas, including Haikou, Chengjiang and Kunming—the Jinning, Chenggong and Kunming localities are similar sedimentologically to the Chengjiang–Haikou–Anning areas, although the latter area shows a lower number of species. Our preferred explanation for this difference is that strata in the Chengjiang–Haikou–Anning areas are scantly exposed and have received relatively low sampling intensity and detailed study. Fossils in the background mudstones have undergone significant pre- or syn-burial decay and represent a death assemblage. In contrast, fossils from event mudstone layers, including soft-bodied organisms, were buried rapidly and thus show substantially less taphonomic bias (Zhao et al., 2009). The lack of obvious disturbance of sedimentary structure indicates that reworking or transport must have been minimal. Low bioturbation, low hydrodynamic disturbance and rapid burial by distal storm-generated mud flows were probably the most important factors promoting preservation of whole soft-bodied animals. Moving farther eastward, the proportion of single-event mudstones decreases. In the Malong–Qujing areas there is no evidence of stacked couplets of single-event and background mudstone layers,

indicating that reworking or transport must have mixed these layers. The gradual eastward deepening trend is also reflected in the eastward thinning and loss of silty tempestites (Fig. 13). While taphonomic factors significantly reduced number of species (including shared species) in the Malong and Wuding areas (representing Taphofacies II or III, respectively), most of the species present in these areas are known in the Chengjiang, Haikou and Anning areas (Taphofacies I). These shared species tend to be common to all areas and might be well adapted to variations in environmental conditions (eurytopic species). The many unique species discovered in the Haikou and Chengjiang areas, in particular, might be in large part due to increase in collecting activities in these areas—previous collectors preferentially excavated fossils in areas showing the best preservation of soft-bodied organisms. By contrast, most of the taphofacies II and III localities have been significantly less investigated. Despite taphonomic and collecting biases, the high proportion of species common to all taphofacies suggests that a similar community-type lived in most of the areas investigated and was subject to local environmental variations with settled differences in composition. 7. Conclusions Distinct spatial variation in the diversity of the Chengjiang Biota was confirmed over a large area in Eastern Yunnan, both in terms of local diversity and faunal composition. Regional variation was controlled mostly by changes in paleoenvironmental settings (nearshore to offshore gradients), taphonomic biases and ecological factors. The offshore settings (Haikou–Chengjiang–Anning areas) show high diversity and exceptional preservation of soft-bodied fossils due to rapid burial by distal storm

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Fig. 10. Species overlap (shared species) among the three general taphofacies in the Chengjiang, Haikou, Anning (Taphofacies I), Malong (Taphofacies II) and Wuding (Taphofacies III) areas. Number of species based on all taxa (see Appendix 1).

Fig. 8. Comparisons of fossil preservation between Mafang (event mudstones, Taphofacies I and background mudstones), Malong (Kuangshan section, Taphofacies II) and Wuding (Sapushan section, Taphofacies III). A, Number and ratio of species consisting of associated specimens, disassociated specimens, and both associated and disassociated specimens per sampling section. B, Number and ratios of species consisting of soft-bodied type 1, softbodied type 2 and biomineralized specimens per areas (for detailed explanations see text, for data see Appendix 2). Abbreviations: B = background mudstone; E = event mudstone.

Fig. 9. Rarefaction curves of the Mafang (event mudstones, Taphofacies I and background mudstones), Malong (Kuangshan section, Taphofacies II) and Wuding (Sapushan section, Taphofacies III). Rarefaction curves were calculated using ECOSIM (Gotelli and Entsminger, 2001). Expected number of species were rarefied to the lowest number of specimens among the three sections studied (1735 specimens within background mudstones from the Mafang section in the Haikou area and 3291 specimens from the Sapushan section in the Wuding area) (for data see Appendix 2).

deposits. High levels of bioturbation and hydrodynamic disturbance resulted in low species richness in the Wuding and Malong areas. In spite of taphonomic and collecting biases, differences in fossil composition between the different areas are discernible, reflecting changes in species composition along an environmental gradient and representing a transition from nearshore to offshore facies trending in a present-day east–west direction. This study shows that some fossil Lagerstätten such

as the Chengjiang Biota are well preserved enough to enable high resolution analyses of spatial variation in diversity, faunal composition and taphonomy. Furthermore, it provides a unique chance to assess the relative importance of taphonomic versus ecologic controls on species diversity at a regional spatial scale for the first time. Supplementary data to this article can be found online at http:// dx.doi.org/10.1016/j.palaeo.2012.05.021.

Fig. 7. Representative fossils from the lower Cambrian Yu'anshan Formation, Maotianshan Member, showing the preservational characteristics of the three general taphofacies (I to III) present in Eastern Yunnan. A, D, G, J, M, fragmented specimens from the Sapushan section (Wuding area). B, E, H, K, N, articulated/associated specimens from the Kuangshan section (Malong area). C, F, I, L, O, details of the hard parts and soft tissues of articulated/associated specimens preserved in event mudstones from the Chengjiang and Haikou areas. A–C, Microdictyon sinicum Chen et al. (1989) (a lobopod): A, single disarticulated plate; B, cluster of plates preserved more or less in anatomical position but without evidence of associated soft tissues of the body; C, complete specimen showing plates. D–F, Mafangscolex sinensis Hou and Sun, 1988 (a priapulid): D, fragmented specimen showing poorly defined outlines; E, specimen with proboscis missing and blurred outline; F, specimen showing evidence of internal organs and preservation of the proboscis. G, isolated glabela of the trilobite Wutingaspis tingi Kobayashi, 1944 in Chen et al. (2002). H, the trilobite Malungia laevigata Lu, 1941 with disarticulated librigenae. I, specimen of the trilobite Eoredlichia intermedia Lu, 1941 showing preservation of antennae (Mafang section, Haikou area). J, Diandongia pista Rong, 1974 a common brachiopod showing typical crushing of the thick, originally phosphatic, shell. K, the brachiopod Kutorgina chengjiangensis Zhang et al., 2007 preserved typically without pedicle. L, the brachiopod Longtancunella chengjiangensis Hou et al. (1999) (represented by a stout pedicle marked by arrow); specimen attached to the ventral valve of the brachiopod D. pista Rong, 1974 (Mafang section, Haikou County). M, isolated sclerite of Allonina phrixothrix Bengtson and Hou, 2001 (a chancelloriid). N–O, Naraoia spinosa Zhang and Hou, 1985; N, specimen showing blurred body outline and remnants of cephalic diverticulae and midgut; O, specimen showing clear body outline and three-dimensional preservation of the mud-filled cephalic diverticulae and midgut (Mafang section, Haikou County). All scale bars are 5 mm, except in A and M (both 2 mm).

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Acknowledgments This research was supported by the Chinese Academy of Sciences (KZCX2-EW-115), the National Natural Science Foundation of China (Grant Nos. 40930211, 40725005, 41002002, J093006) and a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant 341944 (to J.-B.C). We thank Heyo Van Iten, David Rudkin and Joan Burke for editorial corrections, Lorna J. O'Brien for reading an earlier version of this manuscript and local farmer Yang Zhi for help with field work. The manuscript benefited from critical comments by Dr. Robert R. Gaines and one anonymous reviewer. References

Fig. 11. Number of shared species and β diversity values (Sørensen index) among the Anning (AN), Chengjiang (CJ), Haikou (HK), Malong (ML) and Wuding (WD) areas. Localities with similar Sørensen index values are grouped together, and mean values also are shown. Triangle = number of shared species; diamond = Sørensen index. The Sørensen index is a simple measure of beta diversity, ranging from a value of 0 (no species overlap) to a value of 1 (complete species overlap). Sørensen indices were calculated based on all taxa (Appendix 1) using EstimateS 7.5 (Colwell, 2004).

Fig. 12. Species overlap (shared species) among the Chengjiang, Haikou and Anning areas, for the same taphofacies (Taphofacies 1).

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