Early Triassic Trace Fossils from the Three Gorges Area of South China: Implications for the Recovery of Benthic Ecosystems Following the Permian–Triassic Extinction

Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Early Triassic trace fossils from the Three Gorges area of South China: Implications for the recovery of benthic ecosystems following the Permian–Triassic extinction

Xiaoming Zhao a,b,JinnanTonga, Huazhou Yao b,ZhijunNiub,MaoLuoc, Yunfei Huang d, Haijun Song a,⁎ a State Key Laboratory of Biogeology and Environmental Geology, School of Earth Sciences, China University of Geosciences, Wuhan, Hubei 430074, China b Wuhan Institute of Geology and Mineral Resources, Wuhan, Hubei 430205, China c School of Earth and Environment, University of Western Australia, Perth 6009, Australia d School of Geosciences, Yangtze University, Wuhan, Hubei 430100, China article info abstract

Article history: The Lower Triassic Daye and Jialingjiang formations of the Three Gorges area (South China) record the recovery Received 21 December 2014 interval of benthic tracemaking invertebrates following the P–Tr mass extinction. A total of 17 ichnospecies in 14 Received in revised form 4 April 2015 ichnogenera are documented from Smithian and Spathian strata. Our trace fossil data, in combination with Accepted 6 April 2015 previously published studies, show that ichnodiversity in the Middle Yangtze region increased markedly in the Available online 17 April 2015 early Spathian. Trace fossils in the Smithian are dominated by simple, small, horizontal burrows, including Didymaulichnus and Planolites, whereas Spathian trace fossils are diverse and abundant with moderate–high bio- Keywords: Trace fossils turbation levels and complex burrow networks, such as Thalassinoides. Both burrow sizes and penetration depths Benthic ecosystem increased gradually from the early Spathian to the middle–late Spathian, implying a gradual recovery pattern for Biotic recovery benthic ecosystems. Early Triassic ichnofossils are characterised by aspects of opportunistic behaviour (e.g., low- Early Triassic to-moderate ichnodiversity, low-to-moderate bioturbation, small burrow widths, and shallow tiering), suggesting Three Gorges area stressed environmental conditions. The recovery tempo and pattern of ichnocoenoses in South China is likely structured by temporal and spatial changes of the refuge zone in the Early Triassic. © 2015 Elsevier B.V. All rights reserved.

1. Introduction et al., 2013). However, recent palaeontological data show that a fitful recovery of many marine organisms began in the Smithian and Spathian, The largest mass extinction in geological history happened near the including nektons, such as ammonoids and conodonts (Brayard et al., Permian–Triassic (P–Tr) boundary and killed over 90% of marine species 2009; Stanley, 2009), benthic foraminifers and calcareous algae (Song (Erwin, 1993; Song et al., 2013). Biotic recovery following this event has et al., 2011b), and even metazoan reefs (Brayard et al., 2011). As a result, attracted much attention in recent years and remains the topic of much the mechanisms that caused biotic recovery in the Early Triassic are still a debate. It has long been considered that the P–Tr mass extinction was subject of debate. followed by a period of delayed biotic recovery that lasted until the Trace fossils are good indicators of palaeoenvironmental conditions Middle Triassic (Stanley, 1990). The Early Triassic is an interval and the behaviours of benthic invertebrates. They have been used to characterised by continued low biodiversity (Erwin, 1993), blooms reveal the tempo and pattern of ecologic recovery following the P–Tr of opportunistic and disaster taxa (Bottjer et al., 2008), reduction in mass extinction (e.g., Twitchett and Wignall, 1996; Wignall et al., 1998; thesizeofbothmetazoans(Twitchett, 2007) and protozoans (Song Twitchett, 1999, 2006; Pruss and Bottjer, 2004; Twitchett and Barras, et al., 2011a), and the absence of metazoan reefs (Flügel, 2002)and 2004; Zonneveld, 2004; Beatty et al., 2005, 2008; Fraiser and Bottjer, of calcareous algae (Flügel, 1985). Carbon and sulphur isotopic data 2009; Zonneveld et al., 2010a, 2010b; Chen et al., 2011, 2012; Hofmann illustrate a series of large fluctuations throughout the Early Triassic et al., 2011; Baucon et al., 2014). These ichnofossil data, derived from (Payne et al., 2004; Tong et al., 2007; Song et al., 2014a), reflecting global localities, show that benthic invertebrate trace-makers at boreal stressed marine environments. Recent geochemical data show that palaeolatitudes, e.g., Spitsbergen (Wignall et al., 1998) and western the stressed environments of the Early Triassic are characterised by a Canada (Zonneveld, 2004; Beatty et al., 2005, 2008; Zonneveld et al., long-term hot climate (Sun et al., 2012; Romano et al., 2013)aswellas 2010a, 2010b), recovered before those at low and middle palaeolatitudes, severe oceanic anoxia (Wignall et al., 2010; Song et al., 2012; Grasby e.g., the western United States (Pruss and Bottjer, 2004; Twitchett and Barras, 2004; Fraiser and Bottjer, 2009), northern Italy (Twitchett and ⁎ Corresponding author. Wignall, 1996; Twitchett, 1999; Twitchett and Barras, 2004), the Lower E-mail address: [email protected] (H. Song). Yangtze region of South China (Chen et al., 2011), and Western

Australia (Chen et al., 2012). However, recent studies showed that a Lower Triassic successions widely crop out across the entire Yangtze diverse and complex ichnofauna began to occur in the late Griesbachian Platform (Tong and Yin, 2002). The studied area belonged to the middle in Italy (Hofmann et al., 2011). Thus, the environmental factors that part of the upper Yangtze platform located at the eastern Tethys during structure the temporal and spatial patterns of Early Triassic ichnofossil the Early Triassic (Feng et al., 1997). The P–Tr boundary and Lower assemblages are still unclear and additional quantitative analyses are Triassic rocks at the Three Gorges area are well exposed (Fig. 2A). required (Fraiser and Bottjer, 2009). Lower Triassic sequences deposited in the Three Gorges region of In this study, abundant and diverse trace fossils from the Lower Tri- South China constitute the Daye and Jialingjiang formations (Figs. 3, 4), assic successions in the Three Gorges area were described and analysed. which lie conformably above the Upper Permian Dalong Formation and Five proxies, including ichnodiversity, forms and complexity, bioturba- are in turn overlain by the Middle Triassic Badong Formation (Wang tion index, burrow sizes, and tiering levels, were used to evaluate the and Xia, 2004; Zhao et al., 2005, 2010, 2013). tempo and pattern of benthic ecosystem recovery in the aftermath of The Daye Formation in this area is subdivided into four members. the P–Tr mass extinction in the Middle Yangtze region of South China. Member I is composed of laminated black shale interbedded with grey Additionally, the latest geochemical data combined with a hypothesised muddy limestone and is dominated by horizontal lamination (Fig. 2A). recovery model (Song et al., 2014b) were used to explain the temporal It is approximately 51.3 m thick at the South Xiakou section and 46.6 m and spatial patterns of Early Triassic ichnofossil assemblages. thick at the North Xiakou section. This member yields an abundance of thin-shelled fossils, including the bivalves Claraia spp., Eumorphotis spp., 2. Studied sections and stratigraphic setting and Posidonia spp., as well as the ammonoids Ophiceras, Lytophiceras, Prionolobus,andGyronites (Li et al., 2009). Trace fossils are absent. Thus, The South and North Xiakou sections are situated 3 km west of the black shale- and muddy limestone-dominated sequences preserving Jianyangping, Xiakou Town, Xingshan County of Hubei Province and epifaunal bivalves and ammonoids indicate an offshore setting. approximately 80 km away from Yichang City (Fig. 1). These two sections Member II consists mainly of light-grey medium to thickly bedded are located along both banks of the Xiangxi River, a branch of the Yangtze micritic limestone and vermicular limestone. The Early Triassic vermic- River. The present study made use of a previously established site along ular limestone has been proposed to be produced by chemical or micro- the south bank (starting at 110°48′13″ E, 31°06′52″ N, referred to as bial coacervation, or the diagenetic differentiation under low-energy South Xiakou section) as well as a newly surveyed section on the north environmental conditions (see Zhao et al., 2008). It is approximately bank of the Xiangxi River (starting at 110°48′17″ E, 31°06′53″ N, referred 50.9 m thick at the South Xiakou section and 43.4 m thick at the North to as North Xiakou section). The trace fossil assemblages of both sites Xiakou section. This member yields the bivalve Posidonia spp. and the have been systematically studied in this study. ammonoid Flemingites (Li et al., 2009). Trace fossils are very rare. Only

Fig. 1. A, Palaeogeographic map of the Early Triassic with approximate locations of the Lower Triassic successions containing ichnofossil assemblages. B, Inset map of the People's Republic of China. C, Locality of the studied sections. Modiﬁed after Scotese (2001). 102 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 2. Field photos of the Lower Triassic South and North Xiakou sections. A, The Permian–Triassic boundary successions exposed at the South Xiakou section. B, The Lower Triassic successions exposed at the North Xiakou section. C, The topmost Daye Formation and the lowest Jialingjiang Formation at the South Xiakou section. D, Calcarenitic limestone in Member II of the Jialingjiang Formation. E, Small-scale cross beddings in Member II of the Daye Formation. F, Cross beddings in Member IV of the Daye Formation. small, horizontal burrows Planolites montanus were found at the base of (Fig. 2F) indicates a highly agitated marine-water environment. Trace Member II. The occurrence of Planolites has been documented as an fossils are abundant and diverse in micritic limestone and vermicular indicator of restricted oxygen conditions (Martin, 2004). Accordingly, limestone, including horizontal burrows, vertical burrows, branched the limestone-dominated sequence, together with the epifaunal burrows, and complex burrow networks. As a result, the succession Posidonia–Flemingites assemblage and horizontal bedding and small- with oolitic limestone and diverse trace fossils suggests a paralic setting. scale cross-bedding structures (Fig. 2E), suggests an offshore transitional The Jialingjiang Formation is subdivided into four members. Member I setting. is dominated by light-grey thin or medium-thick stratiﬁed muddy dolo- Member III is dominated by light-grey micritic limestone and ver- mite and minor thin- to medium micritic limestone (Fig. 2C). Evaporite micular limestone with minor components of yellow-grey calcareous solution breccias occur occasionally in some dolomite beds. The thickness mudstone (Fig. 2B). It is approximately 381.4 m thick at the South of this member is approximately 17.3 m. Trace fossils are absent. The Xiakou section and approximately 105 m thick at the North Xiakou dolomite-dominated succession possibly suggests a lagoon setting. section. Trace fossils are abundant and diverse, including horizontal Member II is composed of thin-medium micritic limestone, vermicular burrows, vertical burrows, branched burrows, and complex burrow limestone, and calcarenitic limestone (Fig. 2D). The thickness of this networks. The limestone-dominated succession combined with planar member is approximately 170.5 m. Erosional surfaces and ﬂat pebble con- lamination suggests an offshore setting. glomerates were found in some wackestone/packstone beds, indicating Member IV is characterised by thinly- to medium bedded micritic storm-wave dominated conditions. Trace fossils are abundant and diverse limestone, oolitic limestone, and vermicular limestone. The thickness in micritic limestone and vermicular limestone, including horizontal of Member IV is approximately 36.7 m at the North Xiakou section. burrows, vertical burrows, and complex burrow networks. The sharp The occurrence of oolitic limestone and cross-bedding structures occurrence of normally graded unit on the vermicular limestone suggests X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 103

Fig. 3. Stratigraphic distribution of trace fossils with bedding plane bioturbation index (BPBI, Miller and Smail, 1997) at the South Xiakou section. Conodont zones: 1, Clarkina yini and C. meishanensis Zones; 2, Hindeodus parvus Zone; 3, Isarcicella stachei and I. isarcica Zones; 4, Neoclarkina krystyni Zone; 5, Neoclarkina discreta Zone; 6, Sweetospathodus kummeli Zone; 7, Neospathodus dieneri Zone; 8, Novispathodus eowaageni Zone; 9, Novispathodus pingdingshanensis Zone. Bivalve assemblages: ①, Claraia stachei–Claraia griesbachi Assemblage; ②, Claraia concentrica–Claraia hubeiensis Assemblage; ③, Eumorphotis multiformis–E. inaequicostata Assemblage; ④, Posidonia circularis–P. cf. wengensis Assemblage. Ammonoid zones: I, Ophiceras– Lytophiceras Zone; II, Prinolobus–Gyronites Zone; III, Flemingites Zone.

bioturbation under fair-weather conditions. This evidence indicates that Member IV is approximately 70 m thick. This member is dominated Member II was formed between the fair-weather wave base and the by light-grey thickly bedded dolomite with evaporite solution breccia, storm wave base, i.e., in an offshore transitional zone. suggesting a lagoon setting. Member III is characterised by greyish-white micrite dolomite. The The Griesbachian is characterised by conodont Hindeodus parvus, thickness of this member is approximately 95 m. Some oolitic beds Isarcicella isarcica, Neoclarkina krystyni zones, ammonoid Ophiceras– were found in the dolostone, suggesting a lagoon-to-shoreface setting. Lytophiceras zone, and bivalve Claraia stachei–Claraia griesbachi 104 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 4. Stratigraphic distribution of trace fossils with bedding plane bioturbation index (BPBI, Miller and Smail, 1997) at the Lower Triassic North Xiakou section.

assemblage (Wang and Xia, 2004; Li et al., 2009; Zhao et al., 2013). The Posidonia circularis–P. cf. wengensis bivalve assemblage (Li et al., 2009; Dienerian contains the Sweetospathodus kummeli and Neospathodus Zhao et al., 2013). A carbon isotopic curve has been produced for the dieneri conodonts-zones, Prionolobus–Gyronites ammonoid zone, and South Xiakou section (Tong et al., 2007), which has been considered a the Claraia concentrica–Claraia hubeiensis and Eumorphotis multiformis– good proxy for the Early Triassic stratigraphic correlation because Early Eumorphotis inaequicostata bivalve assemblages (Li et al., 2009; Zhao Triassic carbon isotope profiles derived from various depositional settings et al., 2013). The Smithian is defined by the Novispathodus eowaageni in South China yield comparable excursion patterns (e.g., Payne et al., conodont zone, Flemingites–Euflemingites ammonoid zone, and the 2004; Tong et al., 2007). X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 105

3. Materials and methods planes, such as the ichnofabric index (ii, Droser and Bottjer, 1986)and bedding plane bioturbation index (BPBI). Here, BPBI was measured fol- In this study, trace fossils in the Lower Triassic succession at Xiakou lowing the method of Miller and Smail (1997): BPBI1 = no bioturbation, have been investigated bed-by-bed. A total of 17 ichnospecies in 14 BPBI2 = 0–10% disruption, BPBI3 = 10–40% disruption, BPBI4 = 40–60% ichnogenera were identified based on field observations and descrip- disruption, and BPBI5 = 60–100% disruption. Furthermore, the forms and tions of specimens collected from the Daye and Jialingjiang formations complexity of trace fossils as well as the sizes of burrows have proven to (Figs. 5–8). In addition, taxonomic revision of the Lower Triassic trace be good indicators of palaeoenvironmental conditions, especially for the fossils previously reported from the Middle Yangtze region (Yang oxygen content of sediments (e.g., Twitchett, 1999; Pruss and Bottjer, et al., 1992; Ma et al., 2008) was undertaken based upon the original 2004) and were consequently used in this study. Burrow diameters descriptions and illustrations (Table 1). were measured on bedding planes and in vertical exposures. A total of Several semi-quantitative methods have been proposed to document 43 bedding planes were measured to determine the size distribution variations in the extent of bioturbation on vertical profile and bedding of trace fossils, including one bedding plane in Member II of the Daye

Fig. 5. Lower Triassic trace fossils at the South and North Xiakou sections (coin diameter is 2 cm). A, B, Arenicolites isp. on the upper bedding plane of the middle part of Member III of the Daye Formation, North Xiakou section (A) and the middle part of Member II of the Jialingjiang Formation, South Xiakou section (B), upper surface. C, Chondrites ﬁliformis from the middle part of Member III of the Daye Formation, North Xiakou section, upper surface. D, E, Circulichnis montanus from the middle part of Member III of the Daye Formation, South Xiakou section (D) and the base of Member II of the Jialingjiang Formation, South Xiakou section (E), upper surface. F, Cochlichnus kochi on the upper bedding plane of the upper part of Member III of the Daye Formation, South Xiakou section, upper surface. 106 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 6. Lower Triassic trace fossils at the South and North Xiakou sections (coin diameter is 2 cm). A–C, Didymaulichnus lyelli on the upper bedding plane of the upper part of Member III of the Daye Formation, North Xiakou section (A), the lower part of Member III of the Daye Formation, South Xiakou section (B), and the lower part of Member II of the Jialingjiang Formation, South Xiakou section (C), upper surface. D, Diplocraterion parallelum from the upper part of Member III of the Daye Formation, South Xiakou section, upper surface. E, Diplocraterion isp. from the middle part of Member II of the Jialingjiang Formation, South Xiakou section, cross section. Arrow 1: spreite laminae, arrow 2: limb. F, Gordia molassica on the upper bedding plane of the upper part of Member III of the Daye Formation, North Xiakou section, upper surface.

Formation; 24 and 3 bedding planes in Members III and IV of the Daye (Figs. 3, 4). Arenicolites isp. is preserved as vertical to slightly oblique Formation, respectively; and 15 bedding planes in Member II of the U-tubes without spreite. The penetration depth of burrows is difﬁ- Jialingjiang Formation. Tiering levels, describing the distribution of cult to measure. On bedding planes, this trace fossil occurs as pairs benthic organisms within space (Ausich and Bottjer, 1982; Bottjer and of holes (Fig. 5A, B). The burrow diameters of tubes range from 1 to Ausich, 1986), were also assessed in this study. 8 mm and the spacing of limbs from 3 to 10 mm (Fig. 9A, B). These traces are found associated with P. montanus and Palaeophycus 4. Characteristics of Early Triassic trace fossils at the studied sections tubularis. Arenicolites is generally classiﬁed as a dwelling trace, which could be made by various types of animals, e.g., polychaete 4.1. Arenicolites isp. worms (Swinbanks, 1981) and amphipod crustaceans (Bromley, 1996). The several types of Arenicolites preserved in the Lower Jurassic The trace fossil Arenicolites, a common ichnotaxon in the Lower Neill Klinter Formation suggest that these burrows could have acted Triassic of Three Gorges region, occurs in Members III and IV of the both as permanent domiciles and as temporary shelters (Dam, Daye Formation and the base of Member II of the Jialingjiang Formation 1990). X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 107

Fig. 7. Lower Triassic trace fossils at the South and North Xiakou sections (coin diameter is 2 cm). A, B, Mammillichnis? isp. from the upper part of Member III of the Daye Formation, South Xiakou section, subface. C, Oldhamia radiata from the lower part of Member III of the Daye Formation, North Xiakou section, upper surface. D, Oldhamia isp. from the lower part of Member III of the Daye Formation, North Xiakou section, upper surface. E, Palaeophycus heberti on the upper bedding plane of the middle part of Member III of the Daye Formation, North Xiakou section, upper surface. F, G, Palaeophycus tubularis on the upper bedding plane of the lower part of Member II of the Jialingjiang Formation, South Xiakou section (F) and the middle part of Member III of the Daye Formation, North Xiakou section (G), upper surface.

4.2. Chondrites filiformis Heer, 1877 animals that probably lived in oxygen-poor conditions (Bromley and Ekdale, 1984; Kotake, 1991). Chondrites isacommonichnotaxoninthePhanerozoicandisknown from a wide variety of marine sedimentary rocks, including mudstone, 4.3. Circulichnus montanus (Vyalov, 1971) sandstone, and limestone (Simpson, 1956; Bromley and Ekdale, 1984). Here, C. filiformis was found in wackestone in Member III of the Daye This ichnogenus of circular to ovate traces from the Triassic of Russia Formation (Figs. 3, 4). C. filiformis, a highly branched burrow system, is was originally termed Circulichnis by Vyalov (Vyalov, 1971), but the cor- preserved parallel or slightly oblique to the bedding plane (Fig. 5C). rect orthography is actually Circulichnus, as discussed by Keighley and The branching angles range between 30° and 60°. The tunnel diameter Pickerill (Keighley and Pickerill, 1997). C. montanus occurs in the middle of C. filiformis ranges from 1 to 3 mm, and the vertical depth is less than part of Member III of the Daye Formation and at the base of Member II of 4 mm. The tunnels are filled with clay material that is darker than the the Jialingjiang Formation (Figs. 3, 4). This trace fossil is a circular to host rock. These traces are found to be associated with Didymaulichnus slightly ellipsoidal trace. The burrow diameter ranges from 3 to 5 mm. lyelli, Paleodictyon isp., and P. montanus. Chondrites is generally interpreted Circle or ellipse diameter ranges from 15 to 27 mm. These traces are pre- as a fodinichnion probably produced by endobenthic deposit-feeding served on the bedding plane in positive relief (Fig. 5D, E). Circulichnus is 108 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 8. Lower Triassic trace fossils at the South and North Xiakou sections (coin diameter is 2 cm). A, Paleodictyon isp. from the middle part of Member III of the Daye Formation, South Xiakou section, upper surface. B, C, Planolites montanus from the middle part of Member II of the Jialingjiang Formation, South Xiakou section and the middle part of Member III of the Daye Formation, upper surface. D, E, Thalassinoides isp. on the upper bedding plane of the upper part of Member II of the Jialingjiang Formation, South Xiakou section, upper surface. F, Planolites montanus and Skolithos isp. from the middle part of Member II of the Jialingjiang Formation, South Xiakou section, cross section. G, Skolithos isp. from the upper part of Member II of the Jialingjiang Formation, South Xiakou section, cross section.

widely distributed in various types of marine sedimentary rocks and is a Cochlichnus is known from a wide variety of marine environments, monospeciﬁc facies-crossing ichnotaxon that has been recorded not and it is also common in non-marine deposits (e.g., Maples and only in marine deposits but also in nonmarine facies (Fillion and Archer, 1989; Goldring et al., 2005). This ichnogenus has been regarded Pickerill, 1984; Keighley and Pickerill, 1997). The origin of Circulichnus either as a grazing trace, a locomotion trace, or a feeding structure (Chen remains obscure. et al., 2012), and its proposed trace-makers include worms or worm- like animals, nematodes, and dipterous insect larvae (Metz, 1998). 4.4. Cochlichnus kochi (Ludwig, 1869) 4.5. Didymaulichnus lyelli (Rouault, 1850) The ichnospecies was originally put in Belorhaphe by Ludwig (Ludwig, 1869), but was referred to as C. kochi by Calver (Calver, This ichnospecies was originally described as Fraena lyelli by Rouault 1968). C. kochi occurs in the top limestone of Member III of the Daye For- (1850), but was referred to as D. lyelli by Young (1972). D. lyelli is a com- mation (Fig. 3). This trace fossil is a sinusoidal, tunnel-like trace with mon ichnotaxon in the Lower Triassic of the Three Gorges region and has uniform diameter (Fig. 5F). The tunnel diameters range from 0.5 to been found in Member III of the Daye Formation and Member II of the 2 mm. The sinusoidal wavelength ranges from 5 to 30 mm. These traces Jialingjiang Formation (Figs. 3, 4). This trace fossil occurs as a curved, were found to be associated with Planolites montanus, and both have bilobate structure with marginal smooth lobes and a central furrow been found occupying the same bedding surface of wackestone. (Fig. 6A–C). The bilobate width ranges from 2 to 12 mm, and the furrow X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 109

Table 1 Lower Triassic ichnotaxa from the studied sections and other areas of the Middle Yangtze region.

Formation Locality Ichnotaxa Revision References

Member II of the Daye Formation Xingshan, Hubei Planolites montanus This study Member III of the Daye Formation Xingshan, Hubei Arenicolites isp. This study Member III of the Daye Formation Xingshan, Hubei Chondrites ﬁliformis This study Member III of the Daye Formation Xingshan, Hubei Circulichnis montanus This study Member III of the Daye Formation Xingshan, Hubei Cochlichnus kochi This study Member III of the Daye Formation Xingshan, Hubei Didymaulichnus lyelli This study Member III of the Daye Formation Xingshan, Hubei Diplocraterion parallelum This study Member III of the Daye Formation Xingshan, Hubei Gordia molassica This study Member III of the Daye Formation Xingshan, Hubei Mammillichnis? isp. This study Member III of the Daye Formation Xingshan, Hubei Oldhamia radiate This study Member III of the Daye Formation Xingshan, Hubei Oldhamia isp. This study Member III of the Daye Formation Xingshan, Hubei Planolites montanus This study Member III of the Daye Formation Xingshan, Hubei Palaeophycus tubularis This study Member III of the Daye Formation Xingshan, Hubei Palaeophycus heberti This study Member III of the Daye Formation Xingshan, Hubei Paleodictyon isp. This study Member III of the Daye Formation Guangji, Hubei Megagrapton isp. Yang et al. (1992, p. 4, pl. 1, Fig. 5) Member III of the Daye Formation Guangji, Hubei Phycodes isp. Yang et al. (1992, p. 4, pl. 1, Fig. 3) Member III of the Daye Formation Guangji, Hubei Teichichnus isp. Planolites montanus Yang et al. (1992, p. 4, pl. 1, Fig. 2) Member III of the Daye Formation Guangji, Hubei Thalassinoides isp. Yang et al. (1992, p. 4, pl. 1, Fig. 4) Member IV of the Daye Formation Xingshan, Hubei Arenicolites isp. This study Member IV of the Daye Formation Xingshan, Hubei Diplocraterion parallelum This study Member IV of the Daye Formation Xingshan, Hubei Planolites montanus This study Member IV of the Daye Formation Xingshan, Hubei Palaeophycus tubularis This study Member II of the Jialingjiang Formation Xingshan, Hubei Arenicolites isp. This study Member II of the Jialingjiang Formation Xingshan, Hubei Circulichnis montanus This study Member II of the Jialingjiang Formation Xingshan, Hubei Didymaulichnus lyelli This study Member II of the Jialingjiang Formation Xingshan, Hubei Diplocraterion isp. This study Member II of the Jialingjiang Formation Xingshan, Hubei Palaeophycus tubularis This study Member II of the Jialingjiang Formation Xingshan, Hubei Planolites montanus This study Member II of the Jialingjiang Formation Xingshan, Hubei Skolithos isp. This study Member II of the Jialingjiang Formation Xingshan, Hubei Thalassinoides isp. This study Member II of the Jialingjiang Formation Huangshi, Hubei Helminthopsis abeli Ma et al. (2008, Fig. 3K) Member II of the Jialingjiang Formation Huangshi, Hubei Palaeophycus tubularis Ma et al. (2008, Fig. 3D) Member II of the Jialingjiang Formation Huangshi, Hubei Palaeophycus cf. heberti Ma et al. (2008, Fig. 3E) Member II of the Jialingjiang Formation Huangshi, Hubei Phycodes palmatus Ma et al. (2008, Fig. 3A, B) Member II of the Jialingjiang Formation Huangshi, Hubei Planolites beverleyensis Ma et al. (2008, Fig. 3F, M) Member II of the Jialingjiang Formation Huangshi, Hubei Planolites isp. Planolites montanus Ma et al. (2008, Fig. 3G, I, L) Member II of the Jialingjiang Formation Huangshi, Hubei Rhizocorallium cf. jenense Ma et al. (2008, Fig. 3C) Member II of the Jialingjiang Formation Huangshi, Hubei Scalarituba cf. missouriensis Ma et al. (2008, Fig. 3H, N) Member II of the Jialingjiang Formation Guangji, Hubei Chondrites isp. Palaeophycus tubularis Yang et al. (1992, p. 5, pl. 1, Fig. 6) Member II of the Jialingjiang Formation Guangji, Hubei Palaeophycus isp. Yang et al. (1992, p. 5) Member II of the Jialingjiang Formation Guangji, Hubei Protopaleodictyon isp. Paleodictyon isp. Yang et al. (1992, p. 4–5) Member III of the Jialingjiang Formation Guangji, Hubei Asteriacites isp. Yang et al. (1992, p. 7, pl. 1, Fig. 7) Member III of the Jialingjiang Formation Guangji, Hubei Helminthopsis isp. Yang et al. (1992, p. 6, pl. 1, Fig. 8) Member III of the Jialingjiang Formation Guangji, Hubei Phycodes isp. Yang et al. (1992, p. 6, pl. 1, Fig. 3) Member III of the Jialingjiang Formation Guangji, Hubei Hormosiroidea isp. Yang et al. (1992, p. 8, pl. 1, Fig. 9) Member III of the Jialingjiang Formation Guangji, Hubei Planolites isp. Yang et al. (1992, p. 6, pl. 1, Fig. 1) Member III of the Jialingjiang Formation Guangji, Hubei Rhizocorallium isp. Diplocraterion isp. Yang et al. (1992, p. 7, pl. 1, Fig. 10)

widthfrom1to4mm(Fig. 9D, E). Didymaulichnus has been interpreted Diplocraterion with two approximate parallel limbs is observed in as a trail left by gastropods (Glaessner, 1969), trilobites (Crimes and Fig. 6E. Spreite laminae in the cross section view are clear. The limbs Herdman, 1970), or polycladid ﬂatworms (Zonneveld et al., 2010a). from 4 to 5 mm in diameter and from 17 to 24 mm apart. This trace fossil occurs associated with P. tubularis and P. montanus. 4.6. Diplocraterion parallelum Torell, 1870 4.8. Gordia molassica (Heer, 1865) D. parallelum was found in Members III and IV of the Daye Formation (Fig. 3). D. parallelum consists of vertical U-shaped burrows with parallel G. molassica occurs on the bedding plane in Member III of the Daye tubes and a unidirectional spreite. This trace fossil is seen in two dimen- Formation (Figs. 3, 4). This trace fossil consists of overlapping loops sions on upper bedding planes as dumbbell shapes including two circles and meandering trails (Fig. 6F). The width ranges from 2 to 10 mm as horizontal sections (Fig. 6D). The limbs range from 5 to 6 mm in diam- (Fig. 9C) and remains consistent in each trail. Loop distances are less eter and from 8 to 10 mm apart. These traces were found to be associated than 40 mm in diameter. This ichnogenus has been regarded either as with Arenicolites isp. and P. montanus. Diplocraterion is generally regarded a feeding burrow or trail produced by polychaetes (Książkiewicz et al., as a dwelling burrow of suspension feeders or benthic predators such as 1977), or a locomotion trace produced by worms or gastropods (Yang, polychaete annelid, enteropneusts, echiurans, and sipunculans (Fürsich, 1984; Aceñolaza and Buatois, 1993; McCann, 1993). 1974; Ekdale and Lewis, 1991; Zonneveld et al., 2010a). 4.9. Mammillichnis? isp. 4.7. Diplocraterion isp. Mammillichnis? isp. occurs in the middle part of Member III of the Diplocraterion isp. occurs in the upper part wackestone of Member II Daye Formation (Fig. 3). These traces are preserved as hemispherical of the Jialingjiang Formation (Fig. 3). A more complete vertical section of mounds (Fig. 7A, B). The mounds consist of a 1–3 mm high hemicircular 110 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 9. Size of trace fossils in the Daye and Jialingjiang formations. A, Arenicolites isp. from Member III of the Daye Formation. B, Arenicolites isp. from Member II of the Jialingjiang Formation. C, Gordia molassica from Member III of the Daye Formation. D, Didymaulichnus lyelli from Member III of the Daye Formation. E, Didymaulichnus lyelli from Member II of the Jialingjiang Formation. F, Paleodictyon isp. from Member II of the Daye Formation. G, Thalassinoides isp. from Member II of the Jialingjiang Formation. apex. The diameter of mounds ranges from 2 to 4 mm. The classic approximately 0.5 mm and remains consistent in each ray. The diameter Mammillichnis consists of a subhemispherical tubercle being surrounded of the whole radiating structure is approximately 30 mm. This trace fossil by a tyre-like ring (see Chamberlain, 1971, pl. 30, Figs. 6, 7). However, is associated with D. lyelli and G. molassica. these traits are not clear in our samples. Mammillichnis? isp. was found to be associated with P. montanus. Chamberlain (1971) suggested three 4.12. Palaeophycus heberti (de Saporta, 1872) possible explanations for the origin of Mammillichnis including resting or hiding trace of an animal, body fossils of juveniles or eggs deposited P. heberti occurs in the middle part of Member III of the Daye Forma- in the sediment, or excurrent end of tubular burrow where animal tion (Fig. 4). This trace fossil is preserved as slightly curved, smooth worked sediment for food or packed it with faecal pellets. burrows parallel to bedding (Fig. 7E). The filling is structureless and similar to host rock. The cross-section is circular or oval and the diame- 4.10. Oldhamia radiata Forbes, 1849 ter ranges from 1 to 2 mm. These traces are associated with P. montanus and both have been found occupying the same bedding surface of Only one O. radiata sample was collected from the lower part of wackestone. Palaeophycus is generally interpreted as repichnia or Member III of the Daye Formation (Fig. 4). This trace fossil is preserved domichnia probably produced by carnivorous or omnivorous inverte- on the upper surface of wackestone as radiating daisy-shaped rays brates (Pemberton and Frey, 1982; Keighley and Pickerill, 1995) and (Fig. 7C). In total of 13 separate rays were identified on the bedding arthropods (Zonneveld et al., 2010a). plane. Rays vary in length from b4 mm to 10 mm long. The width is approximately 0.5 mm and remains consistent in each ray. This trace fossil is associated with P. tubularis and both have been found occupying 4.13. Palaeophycus tubularis Hall, 1847 the same bedding surface of wackestone. Oldhamia is generally interpreted as a fodinichnion probably produced by worm-like organ- The trace fossil P. tubularis, a common ichnotaxon in the Lower isms (MacNaughton, 2007). Triassic of the Three Gorges region, occurs in Members III and IV of the Daye Formation and the lower part of Member II of the Jialingjiang 4.11. Oldhamia isp. Formation (Figs. 3, 4). P. tubularis, as a straight or slightly curved, unbranched burrow system with circular or oval cross-section, is pre- Oldhamia isp. occurs in the lower part of Member III of the Daye For- served parallel or slightly oblique to the bedding plane (Fig. 7F, G). mation (Fig. 4). This trace fossil consists of irregular radiating burrows The burrows range from 1 to 12 mm in width and from 6 to 80 mm in parallel to bedding (Fig. 7D). Individual rays are irregularly curved to length (Fig. 10). The filling is structureless and similar to host rock. nearly straight and vary in length b3 mm to 10 mm long. The width is These traces were found to be associated with D. lyelli and P. montanus. X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 111

Fig. 10. Size of trace fossil Palaeophycus tubularis in the Daye and Jialingjiang formations. A, Lower Member III of the Daye Formation. B, Middle Member III of the Daye Formation. C, Member IV of the Daye Formation. D, Lower Member II of the Jialingjiang Formation. E, Middle Member II of the Jialingjiang Formation. F, Upper Member II of the Jialingjiang Formation. G, Burrow size of Palaeophycus tubularis variations through the Early Triassic. Note the line with quadrates shows the maximum diameter values and the line with diamonds shows the mean diameter values.

4.14. Paleodictyon isp. Planolites is generally interpreted as a backfilled structure probably produced by deposit-feeding activities of worm-like organisms (Pemberton Two specimens of Paleodictyon isp. were found in the middle Member and Frey, 1982). III of the Daye Formation (Figs. 3, 4). The bigger one occupies an area of approximately 6 × 8 cm2, but the specimen is certainly larger than that 4.16. Skolithos isp. (Fig. 8A). On the same bedding plane, C. filiformis and P. montanus are present. The present specimens are not well preserved, but this Skolithos isp. occurs in the middle part of Member II of the preservational state is sufficient to reconstruct the original shape. Jialingjiang Formation (Fig. 3). These traces are preserved as simple Paleodictyon isp. is preserved as honeycomblike network of five- to six- straight, unlined tubes in the cross section (Fig. 8F, G). The tubes have sided meshes. The mesh diameter ranges from 8 to 12 mm. The string cylindrical to sub-cylindrical cross sections, 3–4 mm in diameter, and width varies between 3 and 8 mm (Fig. 9F). Analysis of modern are not branched. The penetration depth is approximately 45 mm. The Paleodictyon suggests two alternative interpretations: (1) a burrow filling is structureless and similar to host rock. Skolithos isp. was consistent with interpretation of the ancient form as a trace fossil, (2) a found associated with P. montanus. Skolithos is generally regarded compressed form of a hexactinellid sponge (Rona et al., 2009). Therefore, as domichnia probably produced by many creatures such as insects, further work is needed to uncover the nature of Paleodictyon. arachnids, and arthropods (Ratcliffe and Fagerstrom, 1980; Netto et al., 2007). Skolithos is a common and easily recognised ichnotaxon in the Precambrian and Phanerozoic and is known from various deposi- 4.15. Planolites montanus Richter, 1937 tional environments from the deep-sea to non-marine (Droser, 1991). Skolithos has been found in the Griesbachian and Dienerian of Canada P. montanus, one of the most common ichnotaxon in the Lower (Zonneveld et al., 2010a), but the tube diameter and penetration Triassic of Three Gorges region, occurs in Members II, III, and IV of the depth of those traces is apparently smaller than our specimen. Daye Formation and Member II of the Jialingjiang Formation (Figs. 3, 4). These traces are preserved as straight or gently curved, unbranched 4.17. Thalassinoides isp. burrows parallel or slightly oblique to the bedding plane (Fig. 8B, C). Burrow diameter ranges from less than 1 mm to 12 mm (Fig. 11). Their Thalassinoides isp. occurs as positive reliefs on the upper surface of length range from 5 mm to over 150 mm but is typically 20–50 mm. vermicular limestone bed from the top of Member III of the Jialingjiang The burrows are filled with clayed material that is darker than the host Formation (Fig. 3). The trace fossil Thalassinoides isp. consists of both rock. P. montanus is the dominant ichnospecies in the Lower Triassic Y-shaped and irregular branching burrows (Fig. 8D, E). Burrow diameter assemblage and has been found to be associated with Arenicolites isp., rangesfromlessthan3mmto11mm.Thefilling is structureless and sim- C. filiformis, C. kochi, D. parallelum, Diplocraterion isp., Mammillichnis? ilar to host rock. These traces were found associated with P. tubularis and isp., P. heberti, P. tubularis, Paleodictyon isp., and Thalassinoides isp. P. montanus. Thalassinoides is a common ichnotaxon of the Phanerozoic 112 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

Fig. 11. Size range of trace fossil Planolites montanus in the Daye and Jialingjiang formations. A, Member II of the Daye Formation. B, Lower Member III of the Daye Formation. C, Middle Member III of the Daye Formation. D, Upper Member III of the Daye Formation. E, Member IV of the Daye Formation. F, Lower Member II of the Jialingjiang Formation. G, Middle Member II of the Jialingjiang Formation. H, Upper Member II of the Jialingjiang Formation. I, Burrow size of Planolites montanus variations through the Early Triassic. Note the line with quadrates shows the maximum diameter values and the line with diamonds shows the mean diameter values. and is known from a wide variety of marine sedimentary rocks. This region, including the Guangji and Huangshi areas (Table 1; Yang et al., ichnogenus is generally regarded as the work of deposit feeders or as 1992; Ma et al., 2008). domichnia produced by many creatures such as sea anemones, crusta- No trace fossil was uncovered in the dolomite of Member I of ceans, or enteropneust acron worms (Bromley and Frey, 1974; Bromley the Jialingjiang Formation at the studied section. The Member II and Ekdale, 1984; Bromley, 1996; Zonneveld et al., 2010a). ichnocoenosis is diverse, including eight ichnospecies in eight ichnogenera, viz. Arenicolites isp., C. montanus, D. lyelli, Diplocraterion 5. Trace fossils as indicators of benthic biotic recovery after the P–Tr isp., P. tubularis, P. montanus, Skolithos isp., and Thalassinoides isp. More- extinction over, P. tubularis and P. montanus have been reported from Member II of the Jialingjiang Formation elsewhere in the Middle Yangtze region 5.1. Trace fossil diversity (Table 1; Yang et al., 1992; Ma et al., 2008). In addition, Yang et al. (1992); Ma et al. (2008) reported Helminthopsis abeli, Paleodictyon Only one ichnospecies, P. montanus, was uncovered from Member II of isp., P. cf. heberti, Palaeophycus isp., Phycodes palmatus, Planolites theDayeFormationintheThreeGorges area. At present, no trace fossil beverleyensis, Rhizocorallium cf. jenense,andScalarituba cf. missouriensis has been found in this member in any other area of the Middle Yangtze in Member II from Guangji and Huangshi areas. region, including the Guangji and Huangshi areas (Table 1; Yang et al., Trace fossil assemblages of the Middle Yangtze region show an 1992; Ma et al., 2008). The two ichnospecies, D. lyelli and P. montanus, increase in trace fossil diversity from the absence of trace fossils in are present in the lower part of Member III of the Daye Formation Member I of the Daye Formation, to a comparatively low diversity (Figs. 3, 4). with two ichnospecies in Member II and the lower part of Member III Trace fossils in the middle and upper parts of Member III of the Daye of the Daye Formation, and ﬁnally to a considerably high diversity in Formation are diverse and abundant at the studied sections, including the upper Daye Formation and the Jialingjiang Formation. 14 ichnospecies in 12 ichnogenera, viz. Arenicolites isp., C. ﬁliformis, C. montanus, C. kochi, D. lyelli, D. parallelum, G. molassica, Mammillichnis? 5.2. Bedding plane bioturbation index isp., O. radiata, Oldhamia isp., Paleodictyon isp., P. heberti, P. tubularis,and P. montanus. Among these ichnospecies, P. montanus has also been No bioturbation is present in Member I of the Daye Formation at found in the Guangji area (Yang et al., 1992). Yang et al. (1992) also both the North and South Xiakou sections (Figs. 3, 4), thus indicating a found Megagrapton isp., Phycodes isp., and Thalassinoides isp. from BPBI of 1. No bioturbation is present in Member II of the Daye Formation Member III of the Daye Formation in the Guangji area. at North Xiakou section (Fig. 4). However, at the South Xiakou section, The Member IV ichnocoenosis consists of four ichnospecies in for the one bedding plane containing P. montanus in Member II of the four ichnogenera at the studied section, including Arenicolites isp., Daye Formation, the coverage is approximately 5% indicating a BPBI of D. parallelum, P. tubularis, and P. montanus. At present, no trace fossil 2. In Member III of the Daye Formation, approximately 30% of the stratum has been found in this member in any other area of the Middle Yangtze is comparatively well bioturbated, with a BPBI of 2–4(Figs. 3, 4). About X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 113 half of the strata of Member IV of the Daye Formation was covered by trace fossils, including Arenicolites isp., D. parallelum, P. tubularis, and P. montanus. Coverage of the bedding plane by signs of bioturbation ranges from 5% to 15%, indicating a BPBI of 2–3(Fig. 3). No bioturbation is present in Member I of the Jialingjiang Formation, thus indicating a BPBI of 1. Approximately 35% of the strata are bioturbated in Member II of the Jialingjiang Formation (Fig. 3). Several bedding planes containing C. montanus and P. tubularis have coverage of over 50%, suggesting a BPBI of 4–5 for these beds. No bioturbation was found from Member III of the Jialingjiang Formation in the Three Gorges area. However, one bedding plane containing Asteriacites isp. has coverage approximately 50%, indicating a BPBI of 4 for Member III of the Jialingjiang Formation in Guangji area (Yang et al., 1992, pl. 1, Fig. 8).

5.3. Trace fossil form and complexity

The trace fossil assemblage preserved in the Lower Triassic Daye and Jialingjiang formations shows a wide variety in trace fossil forms and complexity. Only one simple, horizontal ichnospecies, P. montanus,is present in Member II of the Daye Formation (Fig. 12A). The trace fossil assemblage in the lower part of Member III of the Daye Formation is dominated by simple, horizontal burrows, such as D. lyelli and P. montanus. Trace fossil behavioural diversity is comparatively high in the middle and upper parts of Member III of the Daye Formation, including simple, horizontal burrows, subhorizontal branched burrows, simple vertical burrows, subvertical branched burrows, and complex burrow networks (Fig. 12B). The trace fossil assemblage of Member IV of the Daye Formation is dominated by simple horizontal burrows and vertical burrows (Fig. 12C). The trace fossil assemblage in Member II of the Jialingjiang Formation is dominated by simple horizontal burrows, vertical burrows, and complex burrow networks (Fig. 12D). The trace fossil assemblages of the Middle Yangtze region show an increase in trace fossil complexity, from simple, horizontal Didymaulichnus and Planolites burrows of Member II and the lower part of Member III of theDayeFormationtocomplexburrownetworksintheupperDayeFor- mation and the Jialingjiang Formation. Furthermore, the presence of Thalassinoides, which is typically indicative of normal marine environments, represents an increase in behavioural complexity that typically indicates advanced recovery after the P-Tr crisis (Twitchett and Wignall, 1996; Pruss and Bottjer, 2004; Twitchett and Barras, 2004; Twitchett, 2006; Chen et al., 2011; Hofmann et al., 2011).

5.4. Trace fossil size

Burrow diameters were measured to determine the size distribution of each of Arenicolites isp., G. molassica, D. lyelli, P. tubularis, Paleodictyon isp., P. montanus, and Thalassinoides isp. (Figs. 9–11). Among these ichnospecies, both P. tubularis and P. montanus occur in multiple horizons (Figs. 10, 11), allowing comparisons of the burrow size of the same ichnotaxon throughout the Early Triassic. The smallest P. tubularis occurs in the lower Member III of the Daye fi Fig. 12. Ichnofaunas from the Lower Triassic of South China. A, Member II of the Daye Formation; the mean burrow diameter for 246 specimens in ve horizons Formation; B, Member III of the Daye Formation; C, Member IV of the Daye Formation; is 0.9 mm, and the maximum burrow diameter is 2.0 mm. Burrow sizes of D, Member II of the Jialingjiang Formation. themiddleMemberIIIoftheDayeFormationaresmall,withmeanand maximum burrow diameters of 1.8 mm and 2.6 mm, respectively (N = 28). A significant increase in burrow size of P. tubularis happened and Member II of the Jialingjiang Formation; the mean and maximum in Member IV of the Daye Formation; the mean and maximum burrow burrow diameters increase from 2.7 mm and 5.5 mm in Member IV of diameters reach 3.9 mm and 13.0 mm, respectively (N = 52). The burrow the Daye Formation to 4.1 mm and 12.0 mm in the middle Member II sizes of P. tubularis in the Jialingjiang Formation are similar to those found of the Jialingjiang Formation (Fig. 11). inMemberIVoftheDayeFormation(Fig. 10). The mean burrow diameters for all trace fossils measured in the The smallest P. montanus occurs in Member II of the Daye Formation; Three Gorges area show a persistent growth trend from Member II of the mean and maximum burrow diameters are 0.9 mm and 1.1 mm, the Daye Formation to the upper Member II of the Jialingjiang Forma- respectively (N = 10). The burrow sizes of Member III of the Daye For- tion (Fig. 13). The maximum burrow diameters show a similar trend, mation become larger, with mean burrow diameters of 1.1 mm, 1.2 mm, but reach a maximum in the middle and upper Member III of the Daye and 1.9 mm in the lower, middle, and upper parts, respectively (Fig. 11). Formation. The increase of trace fossil size is reflected in both the This size increase persists throughout Member IV of the Daye Formation growth of small ichnotaxa, e.g., Arenicolites isp., D. lyelli, P. tubularis, 114 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

was followed by a dramatic reduction in tiering levels (Twitchett, 1999; Ausich and Bottjer, 2001). Twitchett (1999, 2006) identiﬁed four distinct stages in tiering levels during the recovery interval from the P–Tr mass extinction: during stage 1, epifaunal and infaunal tiering was reduced to a bare minimum; during stage 2, infaunal tiering began to recover; during stage 3, epifaunal tiering began to recover; and during stage 4, pre- extinction tiering levels were once again present. In the Three Gorges area, the penetration depths from Member I to the lower part of Member III of the Daye Formation are very shallow, and the deepest tier is less than 3 mm, indicating stage 1 of ecological recovery. The middle and upper parts of Members III and IV of the Daye Formation have moderate penetration depths and thus belong to stage 2 of ecological recovery. The deepest tier in Member II of the Jialingjiang Formation is up to 74 mm, which is almost the level of Late Permian trace fossils found in Shangsi section in South China (Wignall et al., 1995), indicating stage 4 of recovery.

5.6. Benthic recovery from an ichnological perspective

Previous studies have shown that trace fossils underwent a dramatic reduction in diversity, complexity, size, and tiering level during the P–Tr mass extinction, followed by a slow recovery in the Early Triassic (Twitchett and Wignall, 1996; Twitchett, 1999; Pruss and Bottjer, 2004; Twitchett and Barras, 2004; Fraiser and Bottjer, 2009; Chen et al., 2011). Relative to populations in normal environmental settings, biotic assemblages that occurred in the immediate aftermath of the P–Tr mass extinction are characterised by low taxonomic diversity (Song et al., 2011b), high abundance (Rodland and Bottjer, 2001; Song et al., in review), and reduced body size of both metazoans (Twitchett, Fig. 13. A, Burrow size variations of trace fossils in the Daye and Jialingjiang formations. 2007) and protozoans (Song et al., 2011a). Environmental stresses B, Tiering levels indicated by the maximum penetration depths in the Daye and Jialingjiang following the P–Tr extinction result in similar characteristics in fossil formations. D2, Member II of the Daye Formation; D3, Member III of the Daye Formation; D4, assemblages that occur during extinction and survival intervals. In the Member IV of the Daye Formation; J2, Member II of the Jialingjiang Formation. studied areas, trace fossils were very rare in the Griesbachian–Smithian intervals. No trace fossil was found in the Griesbachian and Dienerian and P. montanus (Figs. 9–11), and the reappearance of some large strata in the studied areas. Only two ichnogenera were uncovered ichnotaxa, e.g., Thalassinoides isp. (Fig. 9G). The burrow diameters of from the Smithian strata. Trace fossil data from the Middle Yangtze Thalassinoides isp. rang from less than 4 mm to over 11 mm, and the region show that recovery of trace makers did not begin until the mean burrow diameter is 7.1 mm (N = 31), which is almost twice of Spathian. Spathian trace fossils in the Three Gorges, Huangshi, and that found in the Nanlinghu Formation of the Lower Yangtze region Guangji areas are very diverse and abundant, comprising up to 21 (Chen et al., 2011), but slightly greater than that found in the Virgin ichnogenera (Table 1). Almost all of these ichnofossil-based proxies, in- Limestone Member of the western United States (Pruss and Bottjer, cluding BPBI, complexity, burrow size, and tiering level, were at low 2004). levels in the Smithian. In contrast, these proxies in the Spathian were clearly at high levels and gradually increased from the early Spathian 5.5. Infaunal tiering to the middle–late Spathian. The recovery pattern of benthic ecosystems, as indicated by trace Tiering, the vertical stratification of marine benthic fauna above and fossils in the Middle Yangtze region, is similar to that found in Lower below the substrate level, is a useful measure of ecological recovery Yangtze region (Chen et al., 2011). Trace fossil assemblages from Italy (Ausich and Bottjer, 1982; Twitchett, 1999). Accordingly, tiering of and the western United States also show a similar pattern, with the Early Triassic trace fossil assemblages has previously been described in recovery of complex forms such as Rhizocorallium and Thalassinoides de- the Lower Yangtze region of South China (Chen et al., 2011), the western layed until the Spathian (Twitchett and Wignall, 1996; Twitchett, 1999; United States (Pruss and Bottjer, 2004; Fraiser and Bottjer, 2009), western Pruss and Bottjer, 2004; Twitchett and Barras, 2004). Recently, Fraiser Canada (Zonneveld et al., 2010a), and Western Australia (Chen et al., and Bottjer (2009) reported a relatively diverse trace fossil assem- 2012). In this study, infaunal tiering levels were assessed based on the blage from the Sinbad Limestone Member of the western United measurements of penetration depth of trace fossils from vertical expo- States. This ichnofossil assemblage is characterised by low-to- sures. Trace fossils in Member II andlowerMemberIIIoftheDayeForma- moderate ichnodiversity, low-to-moderate bioturbation, small burrow tion usually have simple, horizontal burrows (P. montanus), and infaunal widths, shallow tiering and non-specialised behaviour. Fraiser and tiering is generally very shallow and primarily in the 0 to −3mmtier.In Bottjer (2009) proposed that the Smithian trace fossil fauna reflects a the middle and upper parts of Member III of the Daye Formation, vertical phenomenon of opportunistic behaviour of benthic trace-maker popu- burrows of Arenicolites isp. extend to a depth of 9–14 mm into the sedi- lations rather than full recovery after the P–Tr mass extinction. ment, indicating a higher level of tiering. In Member IV of the Daye Early Triassic trace fossil assemblages from South China are also Formation and Member II of the Jialingjiang Formation, vertical burrows characterised by low-to-moderate ichnodiversity and bioturbation, of Skolithos isp. penetrate to a depth of up to 42–74 mm (Figs. 8F, G, 12). small burrows, and shallow tiering, suggesting the opportunistic behav- Tiering levels above and below the substrate have not remained con- iour in benthic trace-makers. Compared to the extremely diverse trace stant throughout the Phanerozoic, but have fluctuated between +100 cm fossil assemblages of the Middle Triassic (Zonneveld, 2001), the diversity and −100 cm (Ausich and Bottjer, 1982; Bottjer and Ausich, 1986). of Spathian trace fossils in South China is moderate. Opportunistic behav- Recently, it has been demonstrated that the P–Tr mass extinction event iour is also present in Lower Triassic protozoan foraminifers. Song et al. X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116 115

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Trace fossils and pseudofossils from the This study was supported by the 973 Program (2011CB808800), Wealden strata (non-marine Lower Cretaceous) of southern England. Cretac. Res. 26, 665–685. the National Natural Science Foundation of China (nos. 41240016, Grasby, S., Beauchamp, B., Embry, A., Sanei, H., 2013. Recurrent Early Triassic ocean anoxia. 41272372, 41172312, 41302010), and the 111 Project (B08030). It Geology 41, 175–178. 116 X. Zhao et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 429 (2015) 100–116

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