Anisian (Middle Triassic) marine ichnocoenoses from ...

Global and Planetary Change 157 (2017) 194–213

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Anisian (Middle Triassic) marine ichnocoenoses from the eastern and western margins of the Kamdian Continent, Yunnan Province, SW China: Implications for the Triassic biotic recovery

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Xueqian Fenga, Zhong-Qiang Chena,⁎, Adam Woodsb, Yu Peia, Siqi Wua, Yuheng Fanga, Mao Luoc, Yaling Xua a b c

State Key laboratory of Biogeology and Environmental Geology and School of Earth Science, China University of Geosciences (Wuhan), Wuhan 430074, China Department of Geological Sciences, California State University Fullerton, Fullerton, CA 92834, USA School of Life and Environmental Sciences & Centre for Integrative Ecology, Deakin University, Melbourne, Burwood Campus, Victoria 3125, Australia

A R T I C L E I N F O

A B S T R A C T

Keywords: Ichnology Burrow complexity Burrow size Penetration depth Recovery Habitat selectivity

Two Anisian (Middle Triassic) marine ichnocoenoses are reported from the Boyun and Junmachang (JMC) sections located along the eastern and western margins of the Kamdian Continent, Yunnan Province, Southwest China, respectively. The Boyun ichnoassemblage is middle Anisian in age and is dominated by robust Rhizocorallium, while the JMC ichnoassemblage is of an early Anisian age and is characterized by the presence of Zoophycos. The ichnoassemblage horizons of the Boyun section represent an inner ramp environment, while the JMC section was likely situated in a mid-ramp setting near storm wave base as indicated by the presence of tempestites. The ichnofossil-bearing successions are usually highly bioturbated in both the Boyun (BI 3–5, BPBI 5) and JMC (BI 3–4, BPBI 3–4) sections. Three large, morphologically complicated ichnogenera: 1) Rhizocorallium; 2) Thalassinoides; and, 3) Zoophycos characterize the Anisian ichnocoenoses. Of these, Rhizocorallium has mean and maximum tube diameters up to 20.4 mm and 28 mm, respectively, while Thalassinoides mean and maximum tube diameters are 14.2 mm and 22 mm, respectively. Zoophycos is present in the early Anisian strata of the JMC section, and represents the oldest known occurrence of this ichnogenus following the latest Permian mass extinction. Similar to coeval ichnoassemblages elsewhere in the world, the Yunnan ichnocoenoses embrace a relatively low ichnodiversity, but their burrows usually penetrate deeply into the sediment, and include large and complex Rhizocorallium and Thalassinoides. All of these ichnologic features are indicative of recovery stage 4 after the latest Permian crisis. Anisian ichnoassemblages occur globally in six different habitat settings, and all show similar ecologic characteristics except for slightly different degrees of ichnotaxonomic richness, indicating that depositional environment is not a crucial factor shaping the recovery of the trace-makers, but may have an impact on their ichnodiversity. When compared with some important Early Triassic (mainly Spathian) ichnoassemblages worldwide, the Anisian ichnocoenoses examined for this study are slightly less diversified, and possess more or less the same maximum burrow sizes, but the penetration depth of burrows and the distribution of burrow sizes are much larger than those from the Early Triassic. It is worthy of note that the lower ichnodiversity of the Anisian ichnocoenoses may have resulted from intense bioturbation by deeper tiers, representing a taphonomic product that is totally unrelated to environmental stress. In addition, Anisian Rhizocorallium and Thalassinoides have much larger burrow sizes than the same ichnotaxa from the Lower Triassic, implying that ichnocoenoses may have recovered in Spathian, but did not stabilize until the Anisian.

1. Introduction Early Triassic ichnocoenoses are the crucial tool in revealing ecologic recovery processes prior to the final re-establishment of marine ecosystems in the Middle Triassic (Chen and Benton, 2012). However,

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very few studies have differentiated Early Triassic and Middle Triassic ichnoassemblages, although the latter are believed to represent full recovery since the final biotic recovery occurred during that time (Twitchett, 2006). When compared with widely reported Early Triassic

Corresponding author. E-mail address: [email protected] (Z.-Q. Chen).

http://dx.doi.org/10.1016/j.gloplacha.2017.09.004 Received 8 May 2017; Received in revised form 5 September 2017; Accepted 7 September 2017 Available online 11 September 2017 0921-8181/ © 2017 Elsevier B.V. All rights reserved.


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cf. pannonica Moj (Dong, 1997); Member II is composed of argillaceous limestone interbedded with bands of dolomite. Member III is made up of massive dolomite. Abundant ichnotaxa described below are present throughout Units 1–3 of Member II (Fig. 2A). Of these, the Member I bivalves are assignable to the Myophoria (Costatoria) goldfussi mansuyi Assemblage, characteristic of early Anisian faunas in South China (Zhang et al., 2008). Moreover, the Middle Triassic succession at Boyun is very similar to that exposed in the nearby Louping area, ~50 km west of Boyun (Fig. 1). In fact, Member I and the lower and middle parts of Member II of the Guanling Formation record similar successions over the entire interior region of the Yangtze Platform, South China along the Yunnan-Guizhou border areas (Zhang et al., 2008, 2014). In Luoping a similar bivalve fauna dominated by Myophoria (Costatoria) goldfussi mansuyi with common presence of Unionites spicatus Chen, Posidonia cf. pannonica Moj, and Natiria costata (Münster) has also been reported from the lower part of Member I of the Guanling Formation (Zhang et al., 2008). More importantly, the Nicoraella kockeli conodont zone has been found in the middle part of Member II of the Guanling Formation at the Dawazi and Shangshikan fossil excavation quarries of the Luoping Biota exposed in the Louping area (Zhang et al., 2008, 2014; Hu et al., 2011; Benton et al., 2013; Luo et al., 2014). The Nicoraella kockeli Zone includes elements such as Nicoraella germanicus, N. kockeli, and Cratognathodus sp. that are indicative of the Pelsonian age of the middle Anisian (Zhang et al., 2009). Given its higher stratigraphic position than the early Anisian bivalve assemblage, and location just beneath the Pelsonian conodont zone, the Rhizocoralliumdominated trace-fossil assemblage from the Member II of the Guanling Formation in the Boyun area is tentatively assigned to the Pelsonian (middle Anisian) in age.

ichnoassemblages, Middle Triassic ichnofaunas have been less documented worldwide, but include the Muschelkalk ichnofauna from the Germanic Basin (Knaust, 2007), Ladinian ichnofauna from Northwest Sardinia, Italy (Knaust and Costamagna, 2012), Ladinian ichnocoenoses from the Williston Lake area, British Columbia, Canada (Zonneveld et al., 2001), several Anisian ichnoassemblages from the Lower Muschelkalk of southern and southwest Poland (Jaglarz and Uchman, 2010; Kowal-Linka and Bodzioch, 2011; Chrzastek, 2013), a Pelsonian (middle Anisian) ichnoassemblage from northwestern margin of Gondwana, Levant Basin, south Israel (Korngreen and Bialik, 2015), and a Middle Triassic ichnoassemblage from Svalbard, western Spitsbergen (Mørk and Bromley, 2008). No Middle Triassic ichnocoenoses have been reported from marine settings in China, although coeval terrestrial ichnoassemblages from North China (Qi et al., 2007) and brackish facies ichnofaunas from the Huangmaqing Formation of the Lower Yangtze region of South China (Bi et al., 1996) are documented. The Boyuan and Junmachang (JMC) sections, situated along the eastern and western margins of the Kamdian Continent, Yunnan Province, Southwest China record abundant Middle Triassic ichnofossils. The ecologic characteristics of these two Middle Triassic tracefossil assemblages are documented and compared to coeval and some important Lower Triassic (mainly Spathian) ichnoassemblages from around the world in order to evaluate the recovery processes of marine ecosystems following the latest Permian crisis. 2. Geological and stratigraphic settings of the study sections Lower–Middle Triassic successions are well developed across the entire South China block (Benton et al., 2013), which was located near the tropics within the eastern part of the Paleo-Tethys Ocean during the Permian-Triassic transition (Ziegler et al., 1998). The South China block was occupied by a massive carbonate platform, termed the Yangtze Platform (Wang, 1985), and flanked by distal ramp to basinal settings to the north and the Nanpanjiang basin to the south (Feng et al., 1997); the massive Yangtze Platform is usually subdivided into lower, middle and upper portions. During the Middle Triassic, both the Lower and Middle Yangtze regions were uplifted due to the consolidation of both the south China and north China blocks (Wang, 1985; Feng et al., 1997), while the northern part of the Upper Yangtze region was uplifted and exposed, leading to the deposition of non-marine sediments (Feng et al., 1997); a shallow platform setting still existed in the southern part of this region, with the development of some restricted depressions in the interior of the platform (Enos et al., 2006; Benton et al., 2013). In addition, an uplifted landmass, namely the Kamdian Continent (also called oldland by local geologists), has been situated along the western part of the South China block since the late Neoproterozoic (Wang, 1985). This inherited continent was conspicuous among the surrounding shallow seas that are, now, located in the Yunnan Province today from the late Neoproterozoic to Triassic, and it was gradually peneplaned after the Jurassic due to uplift of surrounding areas (Wang, 1985). Large carbonate platforms were situated along the eastern and western margins of the Kamdian continent during the Early–Middle Triassic (Feng et al., 1997). As a result, marine Middle Triassic strata are particularly complete in the Yunnan areas (Fig. 1), and are assigned to the Guanling and Beiya formations at the Boyun and JMC sections, respectively.

2.2. JMC section The JMC section (GPS: N26°01.752′, E100°06.635′) is located near the Junmachang Pasture of Eryuan County, western Yunnan Province (Fig. 1). The study area is located in the passive western margin of the Yangtze Block and western margins of the Kamdian Continent, where a terrestrial-shallow marine carbonate platform developed. The Lower–Middle Triassic succession in JMC consists of the Qingtianbao and Beiya formations in ascending order (Feng et al., 1997; Dong et al., 2013). The former is dominated by siliciclastic deposits and yields abundant bivalves: Claraia wangi, Eumorphotis multiformis, and Eumorphotis inaequicostata of Early Triassic age (Chen, 1983). The Middle Triassic succession is assigned to the Beiya Formation, which is broken up into three members. Member I is dominated by argillaceous limestone and intraclastic limestone interbedded with banded dolomitic limestone and bioclastic limestone, and yields abundant bivalves. Member II is made up of massive dolomite; Member III is made up of laminated micritic limestone (Dong et al., 2013). Of these, Member I is subdivided into Units 1–3 in the studied section and yields abundant trace fossils (Fig. 2B). The Member I bivalves include Myophoria (Costatoria) goldfussi mansuyi, and Asoella illyrica (Chen, 1983), which are also assignable to the early Anisian bivalve assemblage that occurs in Member I of the Guanling Formation in South China (Chen, 1983; Zhang et al., 2008). Accordingly, the Member I ichnotaxa of the Beiya Formation are early Anisian in age. 3. Paleoenvironmental analysis

2.1. Boyun section 3.1. Boyun section The Boyun section (GPS: N24°43.126′, E103°57.788′) is located at Boyun Village within the town of Caiyun, Shizong County, eastern Yunnan Province (Fig. 1). Here the Middle Triassic succession is comprised of the Guanling Formation (Feng et al., 1997; Enos et al., 2006), which is divided into three members. Member I consists of calcareous silty mudstone and mudstone, yielding abundant bivalves: Myophoria (Costatoria) goldfussi mansuyi Hsü, Unionites spicatus Chen, and Posidonia

Member II of the Guanling Formation at the Boyun section comprises three distinct units (Fig. 2). Of these, Unit 1 is characterized by thin-bedded lamellar limestone in the lower part and alternating argillaceous limestone, bioclastic limestone and micritic limestone in the middle and upper part. The thin-bedded argillaceous limestone yields abundant trace fossils, which are dominated by robust Rhizocorallium. 195


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Fig. 1. A, Locations of the Boyun and Junmachang (JMC) sections, Yunan Province, South China. B, Middle Triassic paleogeographic map of the South China block (base map follows Feng et al., 1997), showing the position of the two sections.

thinly-laminated argillaceous limestone. Robust Rhizocorallium, and abundant body fossils, including crinoids, ammonoids, gastropods, and broken bivalve shells (Fig. 3A–B, E–F), indicate a very shallow,

The thin-bedded lamellar limestone of the lower part of Unit 1 thins upwards, while the micritic limestone of the middle and upper parts thickens up-section. As a result, the entire sequence is dominated by 196


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Fig. 2. Columnar sections of the Anisian successions exposed at Boyun and JMC, showing stratigraphic distributions of trace fossils. Bioturbation indices (BI) (Taylor and Goldring, 1993) are assessed as BI 0 to 6, indicating bioturbation from lowest to highest intensities, respectively. Bedding plane bioturbation indices (BPBI) are evaluated based on the degree of bedding plane coverage by burrows (Miller and Smail, 1997), which range from 1 to 5, indicating coverage from least to most, respectively. Conodont zone of the Boyun updated by Zhang et al. (2009), bivalve assemblages zone of the JMC by Chen (1983).

ammonoids and the thin-bedded argillaceous limestone yields abundant Thalassinoides and Rhizocorallium, indicative of an oxygenated setting during the Pelsonian. Thus, both lithofacies and paleoecology suggest that Unit 2 represents an open, shallow platform environment. The lower part of Unit 3 is composed of intraclastic limestone and massive dolomite; light grey, thin-bedded argillaceous limestone and bioclastic limestone make up the middle part of the unit, and stromatolites comprise the upper part of Unit 3. The lower, intraclastic limestone was likely deposited under high energy conditions. No body fossils or trace fossils are found in the massive dolomite suggesting a stressed environment. The thin-bedded argillaceous limestone and bioclastic limestone contain Thalassinoides and Rhizocorallium as well as horizontal burrows. Abundant crinoid fossils occur in the thin-bedded argillaceous limestone (Fig. 3G). All burrows sizes are smaller than those found in the argillaceous limestones of Unit 1 and Unit 2, and indicate a low energy, semiclosed setting with suboxic bottom water. The stromatolites in the upper part of Unit 3 are similar to those that

oxygenated inner ramp setting. The lower part of Unit 2 is composed of dolomite and thick-bedded limestone (Fig. 3C–D). Stromatolites occur in the middle part of Unit 2, while medium- to thick-bedded argillaceous limestone, dolomite and a thin-bedded bioclastic limestone make up the upper part of Unit 2. The basal dolomite and thick bedded limestone yield rare body fossils; trace fossils are also rarely found, but are typically small, simple, horizontal Planolites. The stromatolite horizon typically exhibits stratified columnar structures that contrast with the surrounding rocks. Stromatolite columns are up to 20 cm high and can be traced laterally for about 15 m (Fig. 3H). The stromatolitic laminae are crinkled and laterally linked in cross section; initial laterally-linked hemispheroids at the base pass into discrete, vertically-stacked hemispheroids upwards to produce columnar forms. Discrete, vertically stacked hemispheroids are composed of closely linked hemispheroidal laminae that are 4–6 mm thick; stromatolite columns are usually 3–5 cm in diameter and grow to a maximum height of 10 cm. The thick-bedded micritic limestone yields 197


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Fig. 3. Field photos of the Anisian successions (Units 1, 2 and 3 of Member II of the Guanling Formation) from the Boyun section. A–B, Thin-bedded argillaceous limestone slabs from Unit 1 contain abundant Rhizocorallium. C, Field photo showing medium- to thick-bedded micritic limestone from Unit 2. D, Field photo showing dolomite in Unit 3. E–F, Abundant ammonoids (arrows in F), gastropods (arrow in E) and broken bivalve shells from the thin-bedded, laminated muddy limestone in Unit 1; the coin is about 2 cm in diameter. G, Crinoids body fossils in the lower part in Unit 3. H, Stromatolites from the upper part of Unit 1.

make up the middle part of Unit 2; the stromatolites can be traced laterally for about 20 m.

up of argillaceous limestone and thin bedded mudstone (Fig. 4A); bioclastic limestone and nodular limestone make up the middle part of Unit 1, and thin- to medium-bedded, laminated argillaceous limestone and mudstone comprise the upper part of the unit. Crinoids, brachiopods, and bivalves occur in the lower to middle part of Unit 1 (Fig. 4H), and Rhizocorallium occur in the argillaceous limestone of the lower part. Crinoids, brachiopods and bivalves, together with Thalassinoides and

3.2. Junmachang (JMC) section Member I of the Beiya Formation at the JMC section is comprised of 3 units based on lithology (Fig. 2). The lower portion of Unit 1 is made 198


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Fig. 4. Field photos of the Anisian successions (Units 1, 2 and 3 of Member I of the Beiya Formation) from the JMC section. A, Argillaceous limestone and thin-bedded mudstone from the Unit 1. B, Argillaceous limestone from the Unit 2. C, Intraclastic limestone with graded carbonates intraclasts in the upper part, and hummocky cross-stratification in the lower part (white line) of Unit 2. D, Intraclastic limestone with broken burrow intraclasts in Unit 3. E, Intraclastic limestone with graded carbonates intraclasts and cross bedding in Unit 3. F, Fossils molds of brachiopods (white arrows) from the argillaceous limestone of Unit 2. G, Graded bedding (a), horizontal bedding (b) and low-angled cross bedding (c) were recognized from the intraclastic limestone in Unit 3. H, Brachiopods and crinoids fossils from the argillaceous limestone of Unit 1.

(Fig. 4C). The intraclasts at the base of Unit 2 are mainly composed of argillaceous limestone beds and burrow fragments. Graded bedding and low-angle cross bedding are recognized from the intraclastic limestone, indicating tempestites or storm deposits (Dong et al., 2013). The argillaceous limestone yields ammonoids and brachiopods (Fig. 4F) along with Thalassinoides.

horizontal Planolites, are recognized from the upper part of Unit 1. Overall, the lithofacies and fossil assemblages indicate a very shallow inner ramp setting with oxygenated bottom water. The lower part of Unit 2 is characterized by intraclastic limestone, argillaceous limestone (Fig. 4B), and nodular limestone, while the upper part is made up of intraclastic limestone and banded limestone 199


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Fig. 5. Ichnotaxa from the Member II of the Guanling Formation from the Boyun section. A, Arenicolites isp. (Ar), Thalassinoides callianassa (Th) and Rhizocorallium commune var. auriforme (Rh) from Unit 1. B–C, Thalassinoides callianassa from middle part of Unit 3. D, Arenicolites isp. (Ar) from a bedding plane, lower part of Unit 1. E–F, Spongeliomorpha isp. from the upper part of Unit 1; note the abundant scratches on the tube (white arrows).

that indicate a mid-ramp setting near or above storm wave base but below fair-weather wave base in an area that had strong storm activity, and the upper part of each cycle is indicative of a mid-ramp with less storm activity than the middle part. The lithofacies and fossil assemblages of each small-scale cycle of Unit 3 indicate a deepening-upwards depositional setting.

Unit 3 is characterized by alternating beds of bioclastic limestone, intraclastic limestone and banded limestone to thick-bedded limestone (Fig. 4D–E). Three small-scale depositional cycles are recognized from Unit 3, and are characterized by an increase in thickness of the upper limestone and a decrease in thickness of the lower intraclastic limestone upwards though the unit. In each small-scale cycle, the basal bioclastic limestone yields bivalve shells or crinoids, together with Thalassinoides and U-shaped Rhizocorallium. Complex Zoophycos are also documented from the lower bioclastic limestone that occurs within the first smallscale cycle at the base of Unit 3. In the middle part of Unit 3, the intraclastic limestone and banded limestone contain graded bedding, horizontal bedding and hummocky cross-stratification (Dong et al., 2013). The intraclasts are mainly composed of argillaceous limestone and burrow fragments that are believed to represent the reworking and transport of burrows by storm actions (Fig. 4G), and therefore indicate a mid-ramp setting near or above storm wave base but below fairweather wave base. Overall, Unit 3 records three settings in each smallscale cycle: the basal bioclastic limestone was deposited in a relatively low-energy subtidal environment, the middle part contains tempestites

4. Methodology Trace fossil taxonomic identification was based on field observations and descriptions of specimens collected from outcrop. Several proxies were analyzed to determine ecologic recovery in the aftermath of the latest Permian mass extinction as indicated by trace fossils, including burrow size variation, ichnodiversity, behavioral complexity, and tiering. Measurements of burrow diameters were undertaken on bedding planes and in vertical exposures. Most burrow diameters were measured at the part of the burrow that was most representative of the average width. Sediment penetration depths of trace fossils were also measured on vertical exposures, and tiering levels were assessed based 200


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5.4. Rhizocorallium Zenker, 1836

on these measurements (Bottjer and Ausich, 1986). Ichnofabric indices (ii, Droser and Bottjer, 1986), bioturbation indices (BI, Taylor and Goldring, 1993) and bedding plane bioturbation indices (BPBI, Miller and Smail, 1997) are powerful tools that provide a semi-quantitative way to measure the extent of bioturbation recorded in sedimentary beds. The methods of measuring bioturbation indices in vertical outcrop (Taylor and Goldring, 1993), and on bedding planes (Miller and Smail, 1997) were applied here to measure the degree of bioturbation throughout the Anisian succession. Bioturbation indices are used to indicate bioturbation from lowest (BI = 0) to highest (BI = 6) levels. BPBI were employed to determine the approximate percentage of bedding planes covered by burrows (Miller and Smail, 1997).

Rhizocorallium is a complex U-shaped burrow that has been interpreted as an indication of recovery of trace-fossil assemblages after major mass extinctions. Knaust (2013) proposed a new classification scheme of Rhizocorallium, which proposed three valid ichnospecies or varieties: Rhizocorallium jenense, R. commune var. auriforme and R. commune var. irregular. All three ichnospecies or varieties are documented herein. 5.4.1. Rhizocorallium jenense Zenker, 1836 Abundant U-shaped burrows were observed in the Boyun section. The burrows are very small, 10–40 mm in width, unbranching, and have abundant scratches in both marginal limbs and protrusive spreiten. Burrows tend to have a steep inclination ranging from 30° to 80°. These burrows are preserved in micrite or marlstone. The spreiten are pronounced in most specimens, but occasionally unclear in some individuals due to poor preservation or a steep inclination (Fig. 6A). R. jenense has been regarded as the dwelling trace (domichnion) of a suspension feeder such as crustaceans (Knaust, 2013; Buatois et al., 2017).

5. Systematic ichnology The Boyun trace-fossil assemblage is found within several thinbedded argillaceous limestones within a small hill neighboring Boyun Village, Caiyun Town, where the ichnofossil-rich limestone blocks are well exposed near the road. The JMC ichnoassemblage is mainly found in thin-bedded limestones and argillaceous limestones with graded bedding and hummocky cross-stratification, which are interbedded with banded limestone and intraclastic limestone. Seven ichnogenera (containing eight ichnospecies) are described and illustrated herein.

5.4.2. R. commune var. auriforme Hall, 1843 Most burrows are small and unbranching, and they are preserved in negative epirelief, but occasionally a combination of negative and positive epirelief occurs where parts of the burrow are filled with sediment. Burrows are orientated horizontally to slightly inclined from the bedding plane at an angle of < 10°. Most burrows are 3–8 cm long and 3–5 cm wide. Limb tubes are 0.5–2.0 cm (average value ~1.0 cm) in diameter. Some specimens only possess partial spreiten, which are protrusive. Scratches are occasionally observed on the marginal tubes (Figs. 5A, 6B–D, 9B, D–F).

5.1. Arenicolites Salter, 1857 5.1.1. Arenicolites isp. Arenicolites is a common ichnotaxon in the Lower Triassic successions of the Yangtze region. Here, Arenicolites occurs in Member II of the Guanling Formation, Boyun section. Arenicolites is preserved as vertical U-shaped burrows without spreiten. The most common features of Arenicolites are paired shafts on bedding planes (Fig. 5A, D). Most burrows at the Boyun section have diameters of 8–10 mm. The distance between the limbs is consistent among several pairs of shafts, and is ~ 30 mm. Fillings of most burrows consists of relatively coarse bioclastic limestone that is easily distinguishable from surrounding argillaceous limestone. Poor preservation prevents ichnospecific determination. This ichnogenus has been interpreted as a dwelling trace (domichnia), which could be produced by various kinds of organisms such as polychaete worms, amphipod crustaceans, and insects (Bromley, 1996; Rindsberg and Kopaska-Merkel, 2005).

5.4.3. R. commune var. irregulare Mayer, 1954 R. commune var. irregulare is the most abundant form of Rhizocorallium in the two sections. The burrows are mostly preserved in positive epirelief, but occasionally a combination of negative and positive epirelief occurs where parts of the burrow are filled with sediment. Burrows are horizontally orientated, but are occasionally inclined to the sediments. Most burrows are 10–80 cm long and 3–12 cm wide, with maximum length and width up to 120 cm and > 15 cm, respectively. The limb tubes are 0.5–3.6 cm in diameter, with an average value ~2.0 cm in diameter. The spreiten are always well preserved; most specimens possess complete protrusive spreiten (Figs. 7, 8, 9A, C, G–H, 10A, F). R. commune var. irregulare was interpreted as the feeding trace (fodinichnion) of a deposit feeder (Knaust, 2013).

5.2. Palaeophycus Hall, 1847 5.2.1. Palaeophycus isp. Palaeophycus commonly intersect with each other and pass over one another. They are subparallel to the bedding plane, however, some Palaeophycus have been strongly weathered so that they appear to be oblique to bedding planes. Burrows are mostly smooth, and are typically 3–8 mm in diameter (Fig. 6F, H). Palaeophycus could be interpreted as domichnia produced by small predaceous or suspensionfeeding animals such as annelids, crustaceans, or other arthropods (Pemberton and Frey, 1984; Chen et al., 2012).

5.5. Spongeliomorpha de Saporta, 1887 5.5.1. Spongeliomorpha isp. Horizontal, robust, unlined network burrow system ornamented with scratch traces with various orientations. Spongeliomorpha is preserved as convex hyporeliefs on the upper surface of the limestone units of the Boyun section (Fig. 5E–F). Branching is common, and typically displays a Y-shaped morphology. Width of the burrows average 20 mm; burrows commonly broaden at the Y-shaped junctions. Scratches are seen in burrow casts as external ridges of different size and shape; several scratch segments are spotted, and lead to blind tunnels that increase in diameter toward their terminations (Fig. 5E). Spongeliomorpha, Thalassinoides, and Ophiomorpha are interpreted as decapod crustacean burrows, which occur as intergradational forms (Fursich, 1973; Bromley and Frey, 1974), ranging from unlined scratch-marked Spongeliomorpha excavated in firmgrounds to lightly lined, smoothwalled Thalassinoides indicative of uncompacted but stable sediments, to Ophiomorpha excavated in shifting, unconsolidated sand. Abundant large Thalassinoides burrows are documented from both study sections,

5.3. Planolites Nicholson, 1873 5.3.1. Planolites beverleyensis Billings, 1862 This ichnogenus includes unlined, rarely branched, straight to tortuous, smooth, horizontal to slightly inclined burrows that are circular to elliptical in cross-section. Burrows are usually filled with sediment distinguishable from the host rock. They are typically 3–10 mm in diameter (Figs. 6E, G, 10C), frequently intersect each other, and are densely packed. Planolites is thought to represent reworking of the sediment by the deposit-feeding activities of polychaetes or worm-like creatures (Crimes et al., 1977; Bromley, 1996; Chen et al., 2011). 201


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Fig. 6. Ichnotaxa from the Member II of the Guanling Formation from the Boyun section. A, Rhizocorallium jenense from upper part of Unit 1, the dotted white box shows the intersecting surface of a R. jenense specimen with a steep inclination of 80° of the bedding plane. B–D, R. commune var. auriforme; note the recrystallization of faecal pellets in the maginal tubes and spreiten (white arrows and dotted block) from upper part of Unit 1. E and G, Planolites beverleyensis from Unit 2. F, Palaeophycus isp. from Unit 2. H, Palaeophycus isp. from Unit 3.

5.6. Thalassinoides Ehrenberg, 1944

in similar limestone units that have approximately the same burrow sizes as Spongeliomorpha, however, the blind tunnel scratches in the Spongeliomorpha burrows clearly allow us to differentiate them from Thalassinoides.

5.6.1. Thalassinoides callianassa, Ehrenberg, 1944 This trace fossil occurs as branching burrows that form networks with characteristic Y-shaped junctions (Figs. 5A–C, 10B, D, E). Most 202


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Fig. 7. Robust R. commune var. irregulare from the thin bedded limestone of Unit 1 of the Member II of the Guanling Formation, Boyun section. A and C–F are photographs from the same bedding plane, while B is from second bedding plane.

fish, and decapod crustaceans (Hakes, 1977; Myrow, 1995; Ekdale and Bromley, 2003; de Carvalho et al., 2007; Rodriguez-Tovar and Uchman, 2006; Knaust and Costamagna, 2012).

burrows are 8–14 mm in diameter; some can reach a diameter of 22 mm in the JMC section (Fig. 10B, E). These features match well with Thalassinoides callianassa, as illustrated by Häntzschel (1975). Burrow networks are represented by smooth, rounded burrows that commonly broaden at the Y-shaped junctions and thin distally. The formation of Thalassinoides traces has been attributed to the behavior of many organisms, including cerianthid sea anemones, enteropneustacron worms, 203


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Fig. 8. Close-up showing robust R. commune var. irregulare from the thin-bedded limestone of Unit 1 of Member II of the Guanling Formation, Boyun section; these examples (A–H) occur on the same bedding planes as the ichnofossils in Fig. 7.

section on the basis of its peculiar morphology, the difference in component materials and in the colour contrast between the spreiten and the surrounding sediments. There are two basic forms: helical and planar (Häntzschel, 1975; Miller, 1991; Knaust, 2004; Buatois et al., 2017). The spreiten are fairly easy observed with a width of 2–5 mm. We observed several examples of the planar type of Zoophycos in the bioclastic limestone of Member I of the Beiya Formation, JMC section (Fig. 10G–H). The central axis is preserved as a shaft in one specimen (Fig. 10H). Both the spreiten and the central vertical shaft may

5.7. Zoophycos Massalongo, 1855 5.7.1. Zoophycos isp. Zoophycos occurs as simple to complex, protrusive forms, and has helicoidal circular spreiten that are different from those of Rhizocorallium; marginal limbs are poorly preserved. Normally, Zoophycos is represented by helicoidal spiralled or irregular spreiten, surrounding a central axis often marked by a vertical shaft. This ichnogenus can be easily recognized both on bedding surfaces and in cross204


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Fig. 9. Ichnotaxa from Member II of the Guanling Formation at the Boyun section. A and C, R. commune var. irregulare from Unit 3. B, Rhizocorallium jenense from Unit 3 showing recrystallization of faecal pellets in the maginal tubes (white dotted block). D–F, Moderate and small size R. commune var. auriforme from Unit 2, scratches are common on maginal tubes (white dotted block) in E. G–H, Robust R. commune var. irregulare from the argillaceous limestone of Unit 1.

most likely produced by worm-like animals (Knaust, 2004). Bottjer et al. (1988) analyzed bathymetric trends in the history of Zoophycos and pointed out that Zoophycos occurs in both deep-sea and shallowwater Paleozoic strata, whereas Zoophycos is mostly reported from deep-water sediments in post-Paleozoic strata (Zhang et al., 2015).

penetrate to a depth > 2 cm into the sediment. These burrows are assigned to an uncertain ichnospecies of Zoophycos due to poor preservation of the marginal limbs. The earliest known Triassic Zoophycos has been described from Middle Triassic (Upper Muschelkalk) carbonates of the German Basin, which occurs in a very simple planar form with lobate spreiten, and was 205


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Fig. 10. Ichnotaxa from Member I of the Beiya Formation, JMC section. A, F, R. commune var. irregulare from Unit 3. B, Thalassinoides callianassa from the limestone of Unit 3. C, Planolites beverleyensis from Unit 2. D–E, Thalassinoides callianassa from the argillaceous limestone of Unit 2. G–H, Planar Zoophycos isp. from the lower part of Unit 3, a central axis preserved as a shaft can be observed in H (white arrow).

6. Ichnofabrics and trace fossils: proxies of ecologic recovery after the latest Permian mass extinction

Anisian successions at the two study localities (Fig. 2); results indicate that bioturbation indices are rather high (ii 3–5) in most bioturbated beds from the examined strata. The bedding planes from the Pelsonian successions of the Boyun section contain robust Rhizocorallium and Thalassinoides with coverage > 80% (BPBI 5). In contrast, most bioturbated bedding planes in the early Anisian successions of the JMC

6.1. Extent of bioturbation Bioturbation indices (BI) were assessed from lower to middle 206


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section contain Palaeophycus, small Rhizocorallium, and other associated forms, with coverage of up to 60% for an overall BPBI of 4; only a few bioturbated beds reach coverage of up to 80% with a BPBI of 5.

indicating a high level of tiering (Fig. 14).

6.2. Ichnodiversity, burrow sizes, trace-fossil form and complexity, and infaunal tiering

7.1. Comparisons with coeval ichnoassemblages elsewhere in the world

7. Comparisons and implications for biotic recovery

Although Middle Triassic successions are well-exposed in many places in South China (Benton et al., 2013), Anisian-aged ichnofossilrich successions are only exposed in the Tianshengqiao section of the Upper Yangtze region (Luo et al., 2016). The Tianshengqiao section is situated near the village of Tianshengqiao, ~20 km west of the county town of Shizong County, and ~ 30 km northwest of the Boyun section examined for this study. The Middle Triassic strata are similar to those exposed in Boyun (Luo et al., 2016); the coeval ichnoassemblage from the Tianshengqiao section records rather high ichnofabric indices (ii 3–5), an average depth of 10 cm penetrated into the sediment, a rather low ichnodiversity with only four ichnogenera (Palaeophycus, Planolites, Thalassinoides, and Rhizocorallium) and high trace fossil complexity with the appearance of key ichnotaxa such as Rhizocorallium and Thalassinoides in a subtidal depositional setting (Luo et al., 2016). Outside of South China, Anisian-aged ichnoassemblages have also been reported from the Lower Muschelkalk of southern and southwest Poland (Jaglarz and Uchman, 2010; Kowal-Linka and Bodzioch, 2011; Chrzastek, 2013), and Svalbard (Mørk and Bromley, 2008), as well as from the Levant Basin of southern Israel (Korngreen and Bialik, 2015), and the Germanic Basin (Knaust, 1998, 2007, 2013). Rhizocorallium with retrusive limbs with which the bottom layers contain abundant Planolites and Thalassinoides, were collected from the Lower Muschelkalk (Early Anisian) of the Gogolin Formation from small active quarries located in the vicinity of Zyglin (northern edge of Upper Silesia, South Poland) (Kowal-Linka and Bodzioch, 2011). Seven early Anisian ichnotaxa are recognized from a hypersaline depositional environment in the Tatra Mountains, Western Carpathians, South Poland (Jaglarz and Uchman, 2010). Rhizocorallium is 65–120 mm long and at least 30–55 mm wide; the marginal tunnels are 6–15 mm in diameter (Jaglarz and Uchman, 2010), Y- or T-shaped Thalassinoides burrows are 5–15 mm wide (Jaglarz and Uchman, 2010). Sixteen ichnospecies representing 11 ichnogenera have been documented from the Lower Muschelkalk (an Anisian age), of Raciborowice Górne (North Sudetic Synclinorium, SW Poland), along with an unidentified trace fossil and coprolites (Chrzastek, 2013). The Lower Muschelkalk succession was deposited on a shallow carbonate ramp affected by frequent storms (Chrzastek, 2013). Only Rhizocorallium and Thalassinoides have burrow sizes larger than 20 mm in diameter, furthermore, some Thalassinoides burrows can reach up to 30 mm in diameter; the remaining traces have burrow diameters smaller than 10 mm (Chrzastek, 2013). An abundant and diverse ichnofauna in the Middle Triassic of the Germanic Muschelkalk Basin provides insights into the ichnologic record at the beginning of the Mesozoic. It shows that about forty ichnospecies are present, belonging to about two dozen ichnogenera (Knaust, 2004, 2007, 2010, 2013). Twenty-three ichnospecies in 12 ichnogenera were collected from the Lower-Middle Muschelkalk (Anisian). The depositional environment of the Lower Muschelkalk was an epicontinental sea that was characterized by restricted conditions with oxygen depletion, starved sedimentation (omission), and re-sedimentation. Accordingly, deep tiering and complex ichnofabrics are not well developed and are concentrated along discrete horizons in the Germanic Basin (Knaust, 2007). The ichnofauna of the early Middle Triassic sequence in Svalbard is dominated by Thalassinoides, which is usually 1–5 cm in diameter, 5–20 cm in length, and mostly separated as individual nodules forming horizons of burrow galleries (Mørk and Bromley, 2008). Rhizocorallium and Taenidium are rare, but preferably occur in shallower tiers than Thalassinoides (Mørk and Bromley, 2008). All three ichnogenera may be found to be compacted on each other on bedding surfaces (Mørk and

The Pelsonian ichnoassemblage in Boyun includes 8 ichnospecies and 6 ichnogenera (Figs. 5–9): Arenicolites isp., Palaeophycus isp., Planolites beverleyensis, Thalassinoides callianassa, Spongelimorpha isp., Rhizocorallium jenense, R. commune var. auriforme, and R. commune var. irregulare, among which the robust, U-shaped Rhizocorallium are the most abundant. The early Anisian ichnoassemblage at JMC contains 6 ichnospecies and 5 ichnogenera (Figs. 2, 10): Palaeophycus isp., Planolites beverleyensis, Thalassinoides callianassa, R. commune var. auriforme, R. commune var. irregulare, and Zoophycos. In addition, abundant broken burrows are also found as intraclasts. Rhizocorallium, Planolites, Palaeophycus, and Thalassinoides burrows are very common on the upper surfaces of blocks. Recrystallization of faecal pellets is common in the maginal tubes and spreiten of Rhizocorallium (Figs. 6B–D, 9B). The marginal tubes of Rhizocorallium contain sparse and crossing scratches (Fig. 8G). Burrow sizes of Arenicolites, Palaeophycus, Planolites, Thalassinoides, and Rhizocorallium were determined from bedding planes from both the Boyun and JMC sections (Fig. 11). Mean and maximum diameters of Arenicolites burrows are 9.5 mm and 13 mm, respectively (n = 28, Fig. 11A). Palaeophycus has mean and maximum burrow diameters of 5.3 mm and 8 mm, respectively (n = 38, Fig. 11D). The same measures of Planolites are 6.2 mm and 10 mm, respectively (n = 112, Fig. 11C), and that of Thalassinoides are 14.2 mm and 22 mm, respectively (n = 102, Fig. 11B). Rhizocorallium (n = 248) have mean and maximum tube diameters up to 20.4 mm and 28 mm, respectively (Fig. 11E). Rhizocorallium is a U-shaped burrow, thus the measurements of the width of the burrows are also useful for assessment of the burrow size. Rhizocorallium (n = 248) have mean and maximum burrow width up to 72 mm and 110 mm, respectively (Fig. 11F). A total of 546 burrows from the Boyun and JMC ichnoassemblages were measured, and their maximum and mean diameters are 28 mm and 15 mm, respectively (Fig. 14C). The seven ichnogenera from the Boyun and JMC ichnoassemblages represent a wide variety of morphologic forms. They include simple, horizontal burrows (Planolites), vertical burrows (Arenicolites), oblique/ or horizontal, branching burrows (Palaeophycus), and complex burrow networks (Spongeliomorpha, Thalassinoides, Rhizocorallium, and Zoophycos). These traces can also be categorized into fodinichnia, domichnia, pascichnia, and repichnia ethologic types. As a result, tracefossil behavioral diversity was considerably high. The Boyun ichnoassemblage is dominated by Rhizocorallium which is a considerably complex burrow form, and is collected from almost every bioturbated bedding plane with coverage > 80% in the Pelsonian successions of the Boyun section. The JMC ichnofauna has less bioturbation coverage than at Boyun; most bioturbated beds contain less Rhizocorallium and other traces than at Boyun, and the burrow sizes of most burrows are also smaller than those at Boyun. Infaunal tiering is indicated by the depth that the burrows penetrated into beds. The shallow tier comprises structures produced in the upper 6 cm of the substrate, the mid-tier represents those produced between 6 and 12 cm depth in the substrate, and the deep tier is made up of those emplaced below12 cm. The 6-cm boundary reflects the approximate depth above which organisms are challenged by disturbances rather than by maintaining contact with the sediment-water interface and below which these difficulties are reduced in severity (Bottjer and Ausich, 1986; Bush et al., 2007; Mángano and Buatois, 2014). The Anisian vertical burrows (i.e., Arenicolites) and complex burrow networks (i.e., Rhizocorallium, and Thalassinoides) extended to mean and maximum depths of 7 cm and 12 cm into the sediment, 207


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Fig. 11. Measurements of burrow diameters of Arenicolites, Thalassinoides, Planolites, Palaeophycus, and Rhizocorallium (measurements both of the U-shaped burrow widths and marginal tubes). N = number of burrows; MD = mean diameter; MW = mean burrow width (Rhizocorallium).

elsewhere in the world, we conclude that: (1) most localities record relatively low or moderate ichnodiversity (< 10 ichnotaxa), which may be lower than many records from the Spathian (latest Early Triassic), but exhibit a rather high abundance, except for ichnoassemblages from the Germanic Basin (Fig. 12); (2) the reoccurrence of Zoophycos after the latest Permian mass extinction in the early Anisian succession of the JMC section, South China is older than that documented from late Muschelkalk (late Anisian-Ladinian) of the Germanic Basin; (3) the most common Anisian ichnotaxa found in the Boyun section from South China are Rhizocorallium and Thalassinoides, where more than a thousand robust specimens were collected, while the northern Upper Silesia locality of South Poland is only dominated by Rhizocorallium. The

Bromley, 2008). Seven Pelsonian (middle Anisian) ichnotaxa are recognized from a mixed carbonate/siliciclastic environment of the Ra'af Formation from the northwestern margin of Gondwana, Levant Basin, south Israel (Korngreen and Bialik, 2015). Large Rhizocorallium occurs with Planolites and are associated with relatively high ichnofabric indices of 4–5 (Droser and Bottjer, 1986). The occurrence of Rhizocorallium increases toward the top of the section, with an average diameter exceeding 25 mm (Korngreen and Bialik, 2015). The diversity of trace fossils is augmented by the appearance of Taenidium and Thalassinoides traces (Korngreen and Bialik, 2015). To sum up, when compared with coeval ichnoassemblages from 208


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Fig. 12. Global distributions and ichnodiversities of the Anisian ichnoassemblages in time and space (base maps follow Scotese, 2014), the red color bar represents ichnogenera, the blue one is ichnospecies. 1, Boyun (BY), Yunnan, South China (this study); 2, JMC, Yunnan, South China (this study); 3, Tianshengqiao (TSQ), Yunnan, South China (Luo et al., 2016); 4, Upper Silesia, South Poland (USP) (Kowal-Linka and Bodzioch, 2011); 5, Tatra Mountains, Southern Poland (TM) (Jaglarz and Uchman, 2010); 6, Raciborowice Górne, SW Poland (RG) (Chrzastek, 2013); 7, Western Spitsbergen, Svalbard, Norway (WS) (Mørk and Bromley, 2008); 8, Gondwana margins, south Israel, Levant Basin (SI) (Korngreen and Bialik, 2015); 9, Germanic Basin (GB) (Knaust, 2007, 2013). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 13. Distrubitions of each ecological proxy and ichnofabrics of the Anisian ichnoassemblages worldwide which are in different depositional settings (six types in total), the number of the global localities is the same with those in Fig. 12. Burrow diameter refers to the diameters of the Rhizocorallium and Thalassinoides burrows; tiering level is followed by the criteria proposed by Bottjer and Ausich (1986) and revised by Mángano and Buatois (2014); grades of bioturbation are indicated by ichnofabric indices (ii), bioturbation indices (BI), and bedding plane bioturbation indices (BPBI); key ichnogenera refers to Rhizocorallium, Thalassinoides, Spongeliomorpha, and Zoophycos; ichnodiversity is represented by the richness of ichnospecies in global localities.

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Germanic Basin records higher ichnodiversity than most other areas; (4) ichnofabric indices (ii), bioturbation indices (BI), and bedding plane bioturbation indices (BPBI) for Middle Triassic localities are as follows: Boyun, BI 3–5, BPBI 5; JMC, BI 3–4, BPBI 3–4; Tianshengqiao, ii 3–5; SW Poland, ii = 1–5, bi = 1–4; and, south Israel (northwest margin of Gondwana), ii 3–4 in the lower part; ii = 4–5 in the upper part; (5) burrow sizes of key ichnotaxa (mainly Rhizocorallium and Thalassinoides) were measured for the following localities: Boyun and JMC, where Rhizocorallium have mean and maximum tube diameters up to 20.4 mm and 28 mm and Thalassinoides are 14.2 mm and 22 mm, respectively (for measurements of other ichnotaxa, see Fig. 11); Tatra Mountains, Southern Poland, where the marginal tubes of Rhizocorallium are 6–15 mm in diameter, while Thalassinoides burrows are 5–15 mm wide; Raciborowice Górne, SW Poland, where Rhizocorallium and Thalassinoides have burrow sizes larger than 20 mm in diameter, and some Thalassinoides burrows can reach up to 30 mm in diameter; Svalbard, where Thalassinoides is usually 1–5 cm in diameter; and, south Israel (northwest margin of Gondwana), where the average diameter of Rhizocorallium can exceed 25 mm. Infaunal tiering, indicated by the depth of penetration of burrows into beds, was assessed quantitatively at the Tianshengqiao section where the average burrow penetration depth is 100 mm, and the Boyun section, where the average penetration depth is 120 mm; (6) the depositional environments of the Anisian ichnoassemblage-bearing successions vary among the study areas: the Boyun section was deposited in an inner ramp setting, the JMC section in a mid-ramp environment near storm wave base (as suggested by the presence of tempestites), and the Tianshengqiao section in a subtidal setting, the northern Upper Silesia, South Poland was deposited as the result of distal tempestite sedimentation; the Middle Triassic succession of the Tatra Mountains, South Poland represents a hypersaline ramp environment; the Raciborowice Górne, SW Poland was deposited in a shallow carbonate ramp affected by frequent storms; the early Middle Triassic sequence in Svalbard represents a low-energy shelf (outer ramp) setting; the southern Israel (northwestern margin of Gondwana) was a mixed carbonate/siliciclastic environment comprised of proximal marginal marine basins; the depositional environment of the Lower Muschelkalk in the Germanic Basin was an epicontinental sea (inner ramp) deposited under restricted conditions and depleted bottom water oxygen (Fig. 13).

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7.2. Implications for biotic recovery after the latest Permian mass extinction 7.2.1. Comparisons with some important Early Triassic ichnoassemblages Lower Triassic ichnoassemblages have been reported from many places worldwide. Fifteen ichnogenera were documented from Lower Triassic successions exposed in the Lower Yangtze region, South China (Chen et al., 2011, 2015). A Smithian ichnoassemblage from Lichuan, Hubei Province, South China is made up of 13 ichnogenera in a 20 mthick thin-bedded argillaceous limestone (Feng et al., 2017a). The Lower Triassic succession at the Daxiakou section in the Middle Yangtze region yields 14 ichnogenera (Zhao et al., 2015); sixteen ichnogenera are documented from the Gaimao section exposed in the Upper Yangtze region, South China (Shi et al., 2015). Some important Lower Triassic ichnoassemblages have also been documented from outside of South China, including the western United States (Pruss and Bottjer, 2004; Fraiser and Bottjer, 2009; Mata and Bottjer, 2011); British Columbia, Canada (Beatty et al., 2008; Zonneveld et al., 2010); northern Hungary (Foster et al., 2015); northern Italy (Twitchett and Wignall, 1996; Twitchett, 1999; Hofmann et al., 2011, 2015); and western Australia (Chen et al., 2012). When compared with the Anisian ichnoassemblages examined for this study, most Lower Triassic ichnoassemblages possess a relatively higher ichnodiversity, slightly smaller maximum burrow diameters, and shallower penetration depths (Fig. 14). However, the distribution of burrow sizes is much greater in the Anisian sections examined for the current study than those from Lower Triassic localities (Fig. 14).

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Fig. 14. A, Percentage of the number of key ichnogenera burrows (Rhizocorallium and Thalassinoides) in total burrows from several Early Triassic (Smithian and Spathian) localities and the two studied Anisian-aged Boyun (BY) and Junmachang (JMC) sections. The Early Triassic ichnoassemblages data are from South China:Yashan (YS), Lichuan (LC), and Daxiakou (DXK) (Chen et al., 2011; Zhao et al., 2015; Feng et al., 2017a) and elsewhere in the world: western US (WU), northern Hungary (NH), Western Australia (WA), and northern Italy (NI) (Pruss and Bottjer, 2004; Fraiser and Bottjer, 2009; Mata and Bottjer, 2011; Foster et al., 2015; Twitchett, 1999; Hofmann et al., 2011, 2015; Chen et al., 2012). B, Tiering levels indicated by mean and maximum penetration depths from the Early Triassic (Smithian and Spathian) localities worldwide and the studied Anisian sections. C, Mean and maximum diameters of all the burrows from the Early Triassic (mainly Spathian) localities worldwide and the studied Anisian sections (blue blocks); Mean diameters of the Rhizocorallium (line with green dots) and Thalassinoides (line with red dots) burrows from the Early Triassic (mainly Spathian) localities worldwide and the studied Anisian sections. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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When coeval Anisian ichnoassemblages are compared from around the world, similar characteristics emerge: 1) ichnoassemblages are dominated by more complex forms such as Rhizocorallium and Thalassinoides; 2) relatively low ichnodiversity; 3) significantly increased burrow sizes (burrow sizes of the Rhizocorallium and Thalassinoides are up to 25 mm or even larger); and, 4) depth of penetration is deeper, even though Anisian trace fossils were deposited in different settings (Fig. 13). After a detailed analysis of ichnologic data from South China and comparison to the coeval and neighboring Luoping biota, which represent a stable, typically Mesozoic marine ecosystem (Hu et al., 2011; Chen and Benton, 2012), as well as comparisons with coeval ichnoassemblages from around the world, the middle Anisian Rhizocorallium not only has the highest richness and deepest penetration depth, but also exhibits the greatest morphologic complexity and largest burrow sizes, with some forms having tube diameters > 20 mm. Middle Anisian Rhizocorallium therefore is thought to be an indication of the final stage (Stage 4) of ecologic recovery following the latest Permian crisis (Twitchett, 2006; Pietsch and Bottjer, 2014). It seems contradictory to some extents that ichnodiversity is expected to return to pre-extinction levels during the final recovery stage (Stage 4) (Twitchett et al., 2004), however, global ichnologic data from the Anisian shows a relatively low ichnodiversity, which is even lower than that found during the Spathian (Early Triassic) from many places from around the world, not to mention lower than before the mass extinction, except for the Germanic Basin (Fig. 12). This dichotomy may be explained by the incomplete preservation of ichnotaxa or may have resulted from intense bioturbation by deeper tiers, representing a taphonomic product that is fully unrelated to extreme environment (Buatois and Mángano, 2013).

Interestingly, the mean burrow sizes of Thalassinoides and Rhizocorallium went through a significant increase from the Early Triassic to the Anisian; this increase is especially notable for Rhizocorallium (Fig. 14). Furthermore, pre-Spathian Early Triassic Rhizocorallium possesses a relatively smaller size, occupies shallower tiers, consists of fewer ichnospecies, and has limited ecologic/environmental and geographic distributions (Feng et al., 2017b). Pre-Spathian Rhizocorallium occurrences, therefore, indicate that a higher level of ecologic recovery had not occurred. The Spathian Rhizocorallium is made up of more ichnospecies and has a greater morphologic diversity as well as a broader environmental and geographic range; most ichnotaxa are relatively small (mostly < 20 mm in tube diameter) and less complex (Feng et al., 2017b), and thus indicate Stages 2–3 of ecologic recovery (Twitchett, 2006). 7.2.2. The first reoccurrence of Zoophycos in the early Anisian in South China Zoophycos is one of the most distinctive ichnogenera, with its earliest Mesozoic occurrence reported from the late Middle Triassic strata of the Germanic Basin (Knaust, 2004). Thus, there is a large gap across the Permian–Triassic transition where Zoophycos has not been previously found. The occurrence of Zoophycos in the early Anisian (early Middle Triassic) therefore provides information that allows for better understanding of the recovery of the Zoophycos trace maker in the aftermath of the Permian–Triassic mass extinction. The early Anisian-aged Zoophycos collected from the JMC section is similar to that from the upper Muschelkalk of the Germanic Basin dated to late Anisian–Ladinian: both have a very simple, planar form with lobate spreiten; the JMC specimens are preserved even more poorly than the Germanic Basin examples. The successions in the Germanic Basin are interpreted to have been deposited in a nearshore marine environment with proximal storm deposits, including tempestites (Knaust, 2004). Similarly, the Zoophycos-bearing bedding planes of the JMC section were also deposited in a ramp setting, near storm wave base, with tempestites indicating strong storm activity. These two earliest reoccurrences of Zoophycos following the latest Permian mass extinction show a preference for depositional settings with strong storm activity, indicating that the reappearance of Zoophycos in shallow marine environments was controlled by environmental setting to some extents. In addition, during the upper Muschelkalk (late Anisian-Ladinian), Zoophycos in Germanic Basin has been interpreted to have been produced by a trace maker that survived the latest Permian mass extinction, was re-established in nearshore settings, and progressively colonized deeper marine settings during the Mesozoic (Knaust, 2004). Considering the similar ichnologic features and depositional settings of Zoophycos found in South China and the Germanic Basin, it is reasonable to speculate that the producer of Zoophycos may have survived the latest Permian mass extinction, and was primarily re-established earlier in South China. However, because of the poorly-preserved specimens and restricted depositional settings, this hypothesis is up for debate. Undoubtedly, the first reappearance of Zoophycos in the early Anisian of South China has significance in terms of ichnodiversity and the complexity of infauna in the earliest Mesozoic.

8. Conclusions Complex burrow forms (Spongeliomorpha, Thalassinoides, Rhizocorallium in Boyun, and Thalassinoides, Rhizocorallium, Zoophycos in JMC) are key parts of two Anisian (Middle Triassic) marine ichnocoenoses reported from the Boyun and JMC sections found along the eastern and western margins of the Kamdian Continent, Yunnan Province, South China. The Boyun ichnoassemblage contains six ichnogenera and is dominated by robust Rhizocorallium, while the JMC ichnoassemblage comprises five ichnogenera and is characterized by the presence of Zoophycos. The Boyun succession represents an inner ramp environment, and the JMC section was likely situated in a midramp setting near storm wave base as suggested by the presence of tempestites, which imply strong storm activity. The ichnofossil-bearing successions are usually highly bioturbated in both the Boyun (BI 3–5, BPBI 5) and JMC (BI 3–4, BPBI 3–4) sections. Three large, morphologically complex burrow forms, including Rhizocorallium, Thalassinoides, and Zoophycos characterize the Anisian ichnocoenoses. Of these, Rhizocorallium has mean and maximum tube diameters up to 20.4 mm and 28 mm, respectively, and Thalassinoides has mean and maximum tube diameters up to 14.2 mm and 22 mm, respectively. Zoophycos burrows are present in the early Anisian strata of the JMC section, and thus occurred earlier than the same ichnogenus, which is found in the upper Muschelkalk of the Germanic Basin, representing the oldest known occurrence of Zoophycos following the latest Permian mass extinction. Similar to coeval ichnoassemblages from elsewhere in the world, the Yunnan ichnocoenoses embrace a relatively low ichnodiversity and a great penetration depth into the sediment. All ecologic features suggest the Anisian ichnocoenoses represent recovery stage 4 after the latest Permian crisis. The global Anisian ichnoassemblages occur in six types of habitat settings, and they all show similar ecologic characteristics except for slightly different levels of ichnotaxonomic richness, indicating that depositional environment is not a crucial factor shaping the recovery of the trace-makers, but may have an impact on their ichnodiversity. When compared with some important Early

7.2.3. Ichnologic evidence indicating biotic recovery after the latest Permian mass extinction Anisian-aged trace fossils are very abundant in South China, especially in the Boyun section. The ichnodiversity is relatively low, even lower than that found in many Spathian-aged successions. If other ecologic proxies are taken into account, it is notable that burrow sizes, especially for the more complex forms like Rhizocorallium and Thalassinoides, are up to 20–30 mm in diameter, which are much larger than those from Lower Triassic successions worldwide. The complex burrows of the Anisian ichnoassemblages can penetrate to a depth of up to 12 cm into the sediment, implying that their tiering levels are deeper than those from Lower Triassic successions worldwide (Figs. 13, 14). 211


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Triassic (mainly Spathian) ichnoassemblages worldwide, the studied Anisian ichnocoenoses are slightly less diversified, and possess more or less the same maximum burrow size, but the penetration depth of burrows and total distribution of burrow sizes are much greater than those in the Early Triassic. The Anisian ichnocoenoses possess the lower ichnodiversity probably due to intense bioturbation by deeper tiers rather than environmental stress. In addition, Rhizocorallium and Thalassinoides also have larger burrow sizes than the same ichnotaxa from the Early Triassic, implying that ichnocoenoses may have recovered during Spathian, but did not stabilize until the Anisian. Acknowledgements We thank both Richard Hofmann and Luis Buatois for their critical comments and constructive suggestions, which have improved greatly the quality of the paper. This study was supported by the 111 Program of China, Ministry of Education of China (B08030), two NSFC research grants (41772007, 41572091), one research grant from the State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences (GPMR201302), and a scholarship from China University of Geosciences (Wuhan) sponsoring the first author to visit California State University Fullerton. It is a contribution to IGCP 630: Permian-Triassic extreme climate and environment and biotic responses. References Beatty, T.W., Zonneveld, J.-P., Henderson, C.M., 2008. Anomalously diverse Early Triassic ichnofossil assemblages in northwest Pangea: a case for a shallow-marine habitable zone. Geology 36, 771–774. Benton, M.J., Zhang, Q.Y., Hu, S.X., Chen, Z.Q., Wen, W., Liu, J., Huang, J.Y., Zhou, C.Y., Xie, T., Tong, J.N., Choo, B., 2013. Exceptional vertebrate biotas from the Triassic of China, and the expansion of marine ecosystems after the Permo–Triassic mass extinction. Earth-Sci. Rev. 123, 199–243. Billings, E., 1862. New species of fossils from different parts of the Lower, Middle and Upper Silurian rocks of Canada. In: Palaeozoic Fossils volume I (1861-1865). Geol. Surv. Can. Dawson Brothers, Montreal, pp. 96–168. Bi, D.C., Qian, M.P., Guo, P.X., 1996. Trace fossils and palaeoenvironment of Huangmaqing Formation (Middle Triassic) in lower Yangtze region. Ac. Palaeontol. Sin. 35, 455–469 (in Chinese). Bottjer, D.J., Ausich, W.I., 1986. Phanerozoic development of tiering in soft substrata suspension-feeding communities. Paleobiology 12, 400–420. Bottjer, D.J., Droser, M.L., Jablonski, D., 1988. Paleoenvironmental trends in the history of trace fossils. Nature 333, 252–255. Bromley, R.G., 1996. Trace Fossils: Biology, Taphonomy and Applications, 2nd edition. Chapman & Hall, London (361 pp.). Bromley, R.G., Frey, R.W., 1974. Redescription of the trace fossil Gyrolithes and taxonomic evaluation of Thalassinoides, Ophiomorpha and Spongeliomorpha. Geol. Soc. Denmark, Bull. 23, 311–335. Buatois, L.A., Mángano, G.M., 2013. Ichnodiversity and ichnodisparity: significance and caveats. Lethaia 46, 281–292. Buatois, L.A., Wisshak, M., Wilson, M.A., Mángano, G.M., 2017. Categories of architectural designs in trace fossils: a measure of ichnodisparity. Earth-Sci. Rev. 164, 102–181. Bush, A.M., Bambach, R.K., Daley, G.M., 2007. Changes in theoretical ecospace utilization in marine fossil assemblages between the mid-Paleozoic and late Cenozoic. Paleobiology 33, 76–97. de Carvalho, C.N., Viegas, P.A., Cachao, M., 2007. Thalassinoides and its producer: populations of Mecochirus buried within their burrow systems, Boca do Chapim Formation (Lower Cretaceous), Portugal. PALAIOS 22, 104–109. Chen, D.C., 1983. The Lower and Middle Triassic of western Yunan. Yunan Geol. 2, 219–226 (in Chinese with English abstract). Chen, Z.Q., Benton, M.J., 2012. The timing and pattern of biotic recovery following the end-Permian mass extinction. Nat. Geosci. 5, 375–383. Chen, Z.Q., Tong, J.N., Fraiser, M.L., 2011. Trace fossil evidence for restoration of marine ecosystems following the end-Permian mass extinction in the Lower Yangtze region, South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 299, 449–474. Chen, Z.Q., Fraiser, M.L., Bolton, C., 2012. Early Triassic trace fossils from Gondwana interior sea: implication for ecosystem recovery following the end-Permian mass extinction in south high-latitude region. Gondwana Res. 22, 238–255. Chen, Z.Q., Yang, H., Luo, M., Benton, M.J., Kaiho, K., Zhao, L.S., Huang, Y.G., Zhang, K.X., Fang, Y.H., Jiang, H.S., Qiu, H., Li, Y., Tu, C.Y., Shi, L., Zhang, L., Feng, X.Q., Chen, L., 2015. Complete biotic and sedimentary records of the Permian–Triassic transition from Meishan section, South China: ecologically assessing mass extinction and its aftermath. Earth Sci. Rev. 149, 67–107. Chrzastek, A., 2013. Trace fossils from the Lower Muschelkalk of Raciborowice Górne (North Sudetic Synclinorium, SW Poland) and their palaeoenvironmental

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