Early Cambrian (Stage 4) brachiopods from the Shipai Formation in the Three Gorges area of South China

Abstract. Diverse and abundant fossil taxa have been described in the lower Cambrian Shipai Formation in the Three Gorges area of Hubei Province, South China, but the taxonomy and diversity of the co-occurring brachiopod fauna are still far from clear. Here we describe the brachiopod fauna recovered from the Shipai Formation in the Three Gorges area of South China, including representatives of the subphylum Linguliformea: linguloids (Lingulellotreta ergalievi, Eoobolus malongensis, and Neobolidae gen. indet. sp. indet.), and an acrotretoid (Linnarssonia sapushanensis); and representatives from the subphylum Rhynchonelliformea: the calcareous-shelled Kutorginates (Kutorgina sinensis, Kutorgina sp., and Nisusia liantuoensis). This brachiopod assemblage and the first occurrence of Linnarssonia sapushanensis shell beds permit correlation of the Shipai Formation in the Three Gorges area of Hubei Province with the Stage 4 Wulongqing Formation in the Wuding area of eastern Yunnan. This correlation is further strengthened by the first appearance datum (FAD) of the rhynchonelliform brachiopod Nisusia in the upper silty mudstone of both the Shipai and Wulongqing formations. The new well-preserved material, derived from siliciclastic rocks, also gives critical new insights into the fine shell structure of L. sapushanensis. Microstructural studies on micromorphic acrotretoids (like Linnarssonia) have previously been restricted to fossils that were acid-etched from limestones. This is the first study to carry out detailed comparative ultrastructural studies on acrotretoid shells preserved in siliciclastic rocks. This work reveals a hollow tube and solid column microstructure in the acrotretoid shells from the Shipai Formation, which is likely to be equivalent of traditional column and central canal observed in shells dissolved from limestones.

Here, we build on this earlier work by comprehensively documenting the abundant brachiopods from the silty mudstones, siltstones, and shales of the Shipai Formation in the Xiachazhuang, Wangjiaping, and Aijiahe sections, Three Gorges area, Hubei Province. The recovered brachiopod fauna comprises six families, including Acrotretidae, Lingulellotretidae, Eoobolidae, Neobolidae, Nisusiidae, and Kutorginidae. This brachiopod fauna displays close similarity to the Guanshan fauna previously described from the Wulongqing Formation (Stage 4), eastern Yunnan (Hu et al., 2013;Zhang et al., 2020a, b). Taxonomic resolution of the brachiopod fauna from the lower Cambrian Shipai Formation is an important contribution to understanding of the diversification of Cambrian brachiopods and their faunal successions in South China. It is also critical for regional biostratigraphy and correlation with other lower Cambrian terranes. Additionally, the abundant and often very well-preserved acrotretoids in the Shipai Formation display important shell structural details, providing the first opportunity to describe these structures from siliciclastics.

Geological setting
The Three Gorges area in Hubei Province of South China is located on the northern margin of the Yangtze Platform ( Fig. 1.1), where Neoproterozoic and lower Paleozoic successions are well developed and widely distributed around the southeastern limb of the Huangling Anticline ( Fig. 1.2). Many sections here have been suggested as standard stratigraphic sections in China (Chen et al., 2006;Wang et al., 2009), and the depositional succession along the Three Gorges area is regarded as an auxiliary stratotype section of the traditional lower Cambrian in South China (Wang et al., 1987;Zhang and Hua, 2005;Zhu et al., 2007;. The depositional succession through the Ediacaran-Cambrian Series 2 interval yields abundant shale-hosted fossils that have contributed significantly to the study of early animal evolution (Guo et al., 2014;Fu et al., 2019;Topper et al., 2019). The depositional sequence in the study area includes, in ascending order, the Ediacaran Dengying Formation, the lower Cambrian Yanjiahe Formation, Shuijingtuo Formation, Shipai Formation, Tianheban Formation, and Shilongdong Formation ( Fig. 1.3).
The Ediacaran Dengying Formation carbonates are disconformably overlain by Terreneuvian (Fortunian-Stage 2) lower Cambrian deposits. The lowermost Cambrian unit is the Yanjiahe Formation, containing abundant small shelly fossils (SSF) that are assigned to three SSF assemblage zones (in ascending order): the Anabarites trisulcatus-Protohertzina anabarica assemblage zone, the Purella antiqua assemblage zone, and the Aldanella yanjiaheensis assemblage zone (Guo et al., 2008(Guo et al., , 2014Chang et al., 2017Chang et al., , 2018Steiner et al., 2020). The Shuijingtuo Formation (black shale and limestone) disconformably overlies the Yanjiahe Formation, and has yielded abundant and diverse shelly fossils, including brachiopods, in addition to the oldest eodiscoid trilobites in South China (Wang et al., 1987;Lin et al., 2004;Steiner et al., 2007;Dai and Zhang, 2011;Yang et al., 2015;Z.L. Zhang et al., 2020). Conformably overlying the Shuijingtuo Formation is the Shipai Formation, which is dominated by yellow siltstone and grayish-yellow silty mudstone, intercalated by limestones. It is richly fossiliferous, including diverse trilobites, brachiopods, hyolithids, and bradoriids (Wang et al., 1987). The upper boundary of the Shipai Formation is marked by the contact with the argillaceous striped and oolitic limestone of the Tianheban Formation, which is itself conformably overlain by the dolomitic Shilongdong Formation ( Fig. 1.3).

Materials and methods
Fossils were collected from the Shipai Formation in the Xiachazhuang, Aijiahe, and Wangjiaping sections, Three Gorges area, Hubei Province (Fig. 1). So far, >4500 individual valves have been collected from the Shipai Formation at Yichang by the work-team of the Early Life Institute (ELI), and all specimens are deposited in the Northwest University Early Life Institute, Xi'an, China. Fossils were examined under a Zeiss Smart Zoom 5 Stereo micrographic system and imaged with a Canon camera 5D Mark IV. Some specimens were analyzed with the Scanning Electron Microscope (SEM) at the State Key Laboratory of Continental Dynamics, Northwest University. When most acrotretoid specimens are cracked out, they are usually preserved as internal molds in the mudstone. In order to better display the structures, a number of latex casts were prepared with a PVB ethanol solution and latex. Some fossils and latex casts were photographed after coating with ammonium chloride (NH 4 Cl).
Building on the geometric morphometric work of Zhang et al (2020a), another 16 specimens from the Shipai Formation were selected for geometric morphometric analysis (Supplementary Data 1-3). Landmarks and semi-landmarks (Fig. 9) were digitized with the free software TpsDig2 v. 2.26 (Rohlf, 2015). The data matrix was then analyzed using TpsRelw v. 1.65 (Rohlf, 2015) to explore potential changes in morphospace and to visualize shell shape using thin plate splines. The interpretation of the Cambrian Stage 4 brachiopod faunal similarities was facilitated by multivariate cluster analysis (based on Raup-Crick similarity) (Supplementary Data 4), using the computer program PAST (version 3.06; Hammer et al., 2001).  Description.-Shell ventribiconvex, subcircular to transversely oval in outline (Fig. 2). Shell valves ornamented with concentric growth lines ( Fig. 2.1, 2.2).
Materials.-ELI QJP-SP-001-613, ELI AJH-SP-001-136. There are 749 slabs collected from the middle to upper part of the Shipai Formation in the Xiachazhuang and Aijiahe sections. However, the exact number of individual ventral and dorsal valves can only be approximated because many specimens overlap each other. As of now, 484 specimens have been examined and photographed.
Remarks.-In the Shipai Formation, acrotretoid brachiopod shells are preserved as patchy aggregations on the bedding plane, while acrotretoids from the Wulongqing Formation form thicker shell beds (∼11-13 pavements within 1 cm thick bed). Morphology of the specimens from the Shipai Formation is similar to L. sapushanensis Duan et al., 2021 from the lower Cambrian Wulongqing Formation (Stage 4). Both taxa have a similar shell outline, catacline to procline ventral pseudointerarea, a pronounced dorsal median buttress, and cardinal muscle scars, as well as similar dimensions and ratios of key characters of the ventral valves (L. sapushanensis from the Wulongqing Formation: L/W = 89%, L a /L = 34%, L c / L = 21%; Duan et al., 2021; data of the specimens from the Shipai Formation in Table 1, and location of measurements in Fig. 5).
Description.-Shell tear-shaped in outline (Fig. 6), ∼142% as long as wide with maximum width anterior to mid-length; ventral valve length 4.50 mm and width 3.37 mm on average; ventral pseudointerarea orthocline and triangular ( Fig. 6.4, 6.5), with well-developed flexure lines, occupying 75% of valve width and 37% of valve length; elongate oval pedicle foramen placed at posterior tip of pseudointerarea with average apical angle of 69°; foramen 0.22 mm wide on average, occupying 31% of the length and 9% of the width of the pseudointerareas; pedicle foramen usually preserved as a mud-infilled ridge or groove. Shell surface bears weakly developed concentric growth lines. Shell shows a strong elemental abundance of Ca and P, compared with the surrounding rock in the μ-XRF study ( Fig. 6.7, 6.8), suggesting that the original composition of the shell is calcium phosphate.
Materials.-Eleven specimens (including fragments) collected from middle-upper part of the Shipai Formation at the Xiachazhuang and Wangjiaping sections.
Remarks.-The first record of Lingulellotreta ergalievi Koneva in Gorjansky and Koneva, 1983 was from the lower Cambrian Shabakty Group (Ushbaspis limbata Zone) of the Malyi Karatau Range, south Kazakhstan (Gorjansky and Koneva, 1983). Holmer et al. (1997) restudied the material and made detailed morphological comparison to specimens described as "L." malongensis (Rong, 1974) by Jin et al. (1993) from the Chengjiang fauna in eastern Yunnan, and argued that "L." malongensis from the Chengjiang fauna should be referred to Lingulellotreta, and therefore that L. malongensis be regarded as a senior synonym of L. ergalievi. Zhang et al. (2020a) compared brachiopods from the Chengjiang and Guanshan faunas, and referred the species in the Chengjiang Lagerstätte to Lingulellotreta yuanshanensis Zhang et al., 2020a and the species from the Guanshan Biota to Eoobolus malongensis (Rong, 1974). Zhang et al. (2020a) demonstrated that L. yuanshanensis from South China (Chengjiang fauna) differs from the Kazakhstan Lingulellotreta ergalievi in several characters, including the ratio of valve length and width, the apical angle, and the longer ventral pseudointerarea (L p /L = 49% in L. yuanshanensis from Chengjiang fauna, South China; L p /L = 34% in L. ergalievi from South Kazakhstan) (see measurements in Zhang et al., 2020a).
However, specimens from the Shipai Formation described herein have striking similarities to L. ergalievi from the lower Cambrian Shabakty Group, Malyi Karatau Range of South Kazakhstan . These include an orthocline ventral valve pseudointerarea, as well as similar outlines and similarities in the ratios of the ventral valve (herein: L/W = 142%, L p /L = 37%; Holmer et al., 1997: L/W = 139%, L p /L = 34% of ventral valves). Thus, the formerly so-called L. malongensis from the Shipai Formation at the Wangjiaping section (Zhang et al., 2015) should be referred to L. ergalievi.
Eoobolus malongensis from the Shipai Formation can be distinguished from most of the species assigned to the genus in having a relatively narrow ventral pseudointerarea and a short pedicle groove with parallel lateral margins. It is also difficult to recognize any pustulose ornamentation on the postmetamorphic shell surface. However, comparison of shells from siliciclastic deposits to those acid-etched from carbonates is commonly a problem because taphonomic factors tend to alter morphological characters.
Dorsal median septum well developed, extending to mid-valve or two-thirds of valve length. Shell surface may have setae (marked by white arrow in SEM image, Fig. 11.3). Shell surface bears closely spaced concentric growth lines and dark speckled marks ( Fig. 11.4), which are likely to be diagenetic mineral deposits with high concentration of Fe ( Fig. 11.5); shell shows a strong elemental abundance of Ca, P, and S compared with the surrounding rock in the μ-XRF study ( Fig. 11 (Zhang et al., 2020b), but without data on the ventral valve and more abundant materials, the discrimination of the material remains uncertain. Hence the specimens are referred to Neobolidae gen. indet. sp. indet. awaiting new data.
Emended diagnosis.-Shell subequally biconvex, semicircular to transverse-oval in outline; hinge line slightly shorter than or equal to the maximum width. Cardinal extremities slightly obtuse to almost rectangular. Ventral valve moderately convex, ventral umbo strongly raised; ventral interarea high, catacline. Dorsal valve with anacline interarea. Radial ornament with 6-11 ribs per 5 mm, rib crests bearing hollow spines.
Description.-Shell biconvex, sub-circular to transverse, sub-rectangular in outline, length about three-quarters of width. Hinge line equal to or slightly shorter than maximum shell width (∼95% of the maximum width). Cardinal extremities form right angles. Shell surface bears numerous fine radial ribs that bifurcate in the adult phase to ∼6-11 costae per 5 mm along the anterior margin.
Ventral valve semicircular or transversely sub-rectangular in outline, ∼67% as long as wide; ventral valve moderately convex with the maximum height at the apex; apex pointed and raised, perforated by a round suproapical foramen (∼0.54 mm in diameter) (Fig. 12.4, 12.5, marked by arrows). Ventral interarea high, with a triangular pseudodelthyrium occupying about one-third of interarea width (Fig. 12.4). Shell bears prominent radial lines and vague concentric lines; rib crests bearing hollow spines.
Dorsal valve subquadrate, ∼78% as long as wide, with a small swelling at the umbo (Fig. 12.7-12.9); apex recurved In addition, >10 specimens were also collected from the Shipai Formation from the Xiachazhuang section, but it is difficult to distinguish ventral or dorsal valves because all are incomplete shells.
Remarks.-Nisusia liantuoensis was first recorded from the Shipai Formation of Liantuo, Yichang City, South China (Zeng, 1987). Spinose ornament is unclear in Zeng (1987), hence Holmer et al. (2019) suggested this species designation may be questionable. Specimens from the Shipai Formation at Xiachazhuang section bear a strong resemblance to N. liantuoensis from Liantuo (shell subequally biconvex, semicircular in outline; ventral umbo strongly raised; ventral interarea high; the maximum height of the ventral valve at apex), and the new material from Xiachazhuang section also preserves the characteristic hollow spines of Nisusia.
Specimens from the Shipai Formation in the Xiachazhuang section are also similar to Nisusia grandis Roberts and Jell, 1990, from the Coonigan Formation (Wuliuan Stage) of western New South Wales; both have well-defined concentric lamellae and ventral valve interareas. But the new material differs from Nisusia grandis in having a rectimarginate anterior commissure and in lacking a ventral sulcus.
As discussed by Holmer et al. (2017Holmer et al. ( , 2018, Nisusia has two pedicle openings, an apical foramen and a posterior median opening (between the delthyrium and notothyrium). Nisusia liantuoensis from the Shipai Formation shows a well-developed apical opening (Fig. 12.4, 12.5, marked by arrows) and bears a posterior median opening (Fig. 12.4, marked by double arrows). The new material is also similar to Nisusia sulcata Rowell and Caruso, 1985, from the Marjum Formation (Drumian) of western Utah, USA (Holmer et al., 2018, fig. 1B, E). However, N. liantuoensis differs in having the maximum height of the ventral valve at the apex rather than at the central part of the valve. Remarks.-Kutorgina holds special significance as it is one of the oldest brachiopods with a carbonate shell and primitive Kutorgina had a cosmopolitan distribution during the early to middle Cambrian (Malakhovskaya, 2013), and has been recovered from China (Lu, 1979;Zhang et al., 2007b;Liu et al., 2015), Canada (Voronova et al., 1987), America (Nevada) (Walcott, 1905), Greenland (Skovsted and Holmer, 2005), Siberia (Gorjansky and Popov, 1985), Kazakhstan (Koneva, 1979), Kyrgyzstan (Popov and Tikhonov, 1990), and southeast Australia (Roberts and Jell, 1990). The wide geographic distribution of Kutorgina in the late early Cambrian may indicate that the larvae of Kutorgina were planktotrophic . Species of Kutorgina have few distinctive characters, and morphological features vary throughout ontogeny. The kutorginides may be easily recognized by the wide posterior margin, coarse external concentric ornamentation of sharp rugae and ridges, and growth lines following the valve outline (Malakhovskaya, 2013). Specimens from the Shipai Formation in the Three Gorges area with coarse, wide-spaced concentric growth lines clearly belong in Kutorgina.
Emended diagnosis.-Shell sub-trapezoid, with rounded anterior and lateral margins; shell width is somewhat shorter than shell length, hinge line about three-fifths of the shell width. Ventral valve moderately convex, interarea apsacline; umbo slightly raised over the posterior margin; sulcus narrow, shallow, and starts from the postmedian part of the valve. The ornamentation consists of concentric growth lamellae (∼18-20 lamellae over the entire shell).
Description.-Shell biconvex, rounded to sub-pentagonal. Shell surface ornamented with coarse, widely spaced concentric growth lamellae that are best developed on the postmedian part of the valve, no visible prominent micro-ornamentation. The distance between growth lamellae is 0.64 mm on average. Ventral valve rounded to sub-pentagonal in outline ( Fig. 13.1-13.5), with rounded anterior and lateral margins. The ratio of shell length to width ranges from 0.84-1.10 (average 0.92). Dorsal valve moderately convex to semicircular in outline ( Fig. 13.6-13.8), ∼73% as long as wide. Umbo small and slightly raised over the posterior margin ( Fig. 13.8). SEM shows external shell with pyrite crystals (Fig, 13.9, 13.10). No information on the internal morphology is preserved.
Materials.-Thirty-four specimens comprising 14 ventral valves, six dorsal valves, and fragments, all from the upper part of the Shipai Formation at Xiachazhuang section.  Lu (1979) shows that the ventral valve is moderately convex, ∼13 mm wide, with an apsacline interarea. New material from the Shipai Formation is similar to K. sinensis Rong in Lu, 1979 from the Xinji Formation (Lu, 1979). Both have a moderately convex ventral valve, similar shell size (shell width of Shipai Formation specimens ranges from 6-14 mm), as well as concentric growth lamellae (ranging from 18-20 lamellae). However, K. sinensis from the Xinji Formation is represented by a single ventral valve with  (Zhang et al., 2007b), which is also recovered as "crack-outs" from siliciclastic deposits. Both have strong concentric growth lamellae, as well as other closely comparable morphology, such as shell size (K. chengjiangensis: L = 9.70 mm, W = 11.12 mm on average, data from Zhang et al., 2007b; K. sinensis: L = 9.40 mm, W = 11.02 mm on average), and the distance between growth lines (K. chengjiangensis: 0.6-0.8 mm; K. sinensis: ∼0.64 mm on average). However, K. sinensis from the Shipai Formation has a more convex and acuminate ventral valve as compared with K. chengjiangensis.
In addition, Kutorgina chengjiangensis from the Chengjiang Lagerstätte features a stout and annulated pedicle previously described as protruding from between the delthyrium and notothyrium (Zhang et al., 2007b). However, recent reexamination shows that the pedicle emerges from the apical foramen (Holmer et al., 2018). Unfortunately, K. sinensis from the Shipai Formation are preserved as exterior molds without soft tissues, which precludes detailed study of the pedicle morphology. Additionally, study of the apical foramen is problematic due to poor preservation of the ventral apex.
Kutorgina sp. Figure 14 Description.-Shell planoconvex or slightly biconvex, up to 14 mm wide; surface ornamented by concentric growth lines. No median sulcus or fold developed in the shell valve. Ventral valve transversely oval or semicircular with rounded anterior and lateral margins. Posterior of ventral valve not well preserved. Dorsal valve almost flat and slightly convex, ∼75% as long as wide; posterior margin almost straight, and slightly shorter than the maximum shell width (located in the middle of the shell). No information on the internal morphology is preserved.
Remarks.-Kutorgina sp. has a similar shell size as K. sinensis, but it can be distinguished from K. sinensis by the ornamentation and shell shape. Kutorgina sinensis is ornamented with concentric growth lamellae (∼5-7 lamellae per 5 mm), while Kutorgina sp. has 10-15 concentric growth lines per 5 mm. Kutorgina sp. is similar to K. reticulata Poulsen, 1932 (Skovsted andHolmer, 2005) in having transversely oval or semicircular outline, almost flat dorsal valve with a straight posterior margin, and shell surface with concentric growth lines. But it differs in lacking developed dorsal median fold and ventral median sulcus. Further detailed comparison is difficult due to insufficient material available for the study.

Brachiopod assemblages from the Shipai Formation
Xiachazhuang section.-Brachiopod assemblages from the Xiachazhuang section are much more abundant and diverse compared to those from the Aijiahe and Wangjiaping sections. Six hundred thirteen slabs with >4000 Linnarssonia sapushanensis valves have been recovered from the Shipai Formation in the Three Gorges area. Most fossils were collected from the silty mudstone and siltstone in the middle to upper part of the Shipai Formation, ∼120 m above the base. Here, Linnarssonia sapushanensis are commonly aggregated as shell concentrations on the same bedding plane (Fig. 15.1-15.4).
These shell beds range from loosely to densely packed (∼18 valves per 1 cm 2 ) ( Fig. 15.1) with moderate degrees of fragmentation. In the L. sapushanensis shell beds in the Xiachazhuang section, the size frequency distribution of 103 shells shows that individuals with shell widths between 1.23- 2.10 mm are the most frequent (up to 86%) (Fig. 16). The orientation angle of the shells of L. sapushanensis was also statistically analyzed and plotted in a rose diagram, showing that they have random orientations (Fig. 16). Many shells retain well-preserved microstructures. Linguloid brachiopods are quite common in the Shipai Formation, and two species have been recognized: Lingulellotreta ergalievi and Eoobolus malongensis. The majority of the linguloid specimens were collected from the siltstone in the middle-upper part of the Shipai Formation, ∼150 m above the base of the Shipai Formation (Fig. 1.3). Eoobolus malongensis, which is the most common species in this unit, is preserved as individuals or shell concentrations (Figs. 7, 8). All specimens of E. malongensis are flattened and compressed, but retain    (Zhang et al., 2020a). In the Shipai Formation, Lingulellotreta ergalievi is relatively rare, has a longer ventral pseudointerarea than Eoobolus malongensis, and has an elongate, oval-shaped pedicle foramen. In this unit, Eoobolus and Lingulellotreta are usually <5 mm wide and long. However, the Eoobolus-yielding level in the Shipai Formation also includes larger macro-morphic brachiopods, generally ∼10 mm wide (8.9 mm in length and 9.7 mm in width) (Fig. 11).The shell surface of the macro-morphic brachiopods bears closely spaced concentric growth lines, and a prominent dorsal median septum is present (Fig. 11.2). The specimens (Fig. 11) are most similar to brachiopods belonging to Neobolidae, but the limited material precludes more robust taxonomic discrimination.
In the top silty shale of the Shipai Formation, ∼200 m above the base of the Shipai Formation ( Fig. 1.3), the fauna is dominated by calcareous-shelled kutorginates (Nisusia liantuoensis, Kutorgina sinensis, and Kutorgina sp.). All specimens of Kutorgina have a distinctive shell ornamentation, and are sub-pentagonal or semicircular with strongly spaced concentric growth lines on the surface of the shell. Nisusia has prominent radial lines and has strikingly similar morphology to those from the Wulongqing Formation (Guanshan fauna), eastern Yunnan (Hu et al., 2013;Li et al., 2017). In South China, the first appearance datum (FAD) of the rhynchonelliform Nisusia is in the upper silty shale of the Shipai and Wulongqing formations.
Aijiahe and Wangjiaping sections.-The Wangjiaping section is the type section of the Shipai fauna (Zhang and Hua, 2005) and is exposed around the northern bank of the Yangtze River near Wangjiaping Village, ∼40 km west of Yichang City (Fig. 1.2). Presently, the Shipai Formation at the Wangjiaping section is poorly exposed and mostly covered, making new collections difficult. Linguloid brachiopods such as Palaeobolus, Eoobolus, and Lingulellotreta have been reported from the argillaceous siltstone and silty mudstone in the middle part of the Shipai Formation in the Wangjiaping and Aijiahe sections (Zhang et al., 2015). The brachiopod assemblage in the Aijiahe section consists mainly of acrotretoid brachiopods, which is similar to that from the Xiachazhuang section. Acrotretoids collected from the silty mudstone in the middle-upper part of the Shipai Formation in the Aijiahe section are usually preserved as individuals or shell concentrations (brachiopod-trilobite) (Fig. 17). Four specimens of Eoobolus malongensis have been recovered from the brick-red silty mudstone in the top of the Shipai Formation in the Aijiahe section. All the individuals of E. malongensis were preserved as flattened internal molds with similar color to the surrounding muddy matrix.
Regional correlations of the Shipai Formation.-Absolute age of the Shipai Formation is poorly resolved. However, two trilobite biozones have been recognized in the Shipai Formation: the Redlichia meitanensis Zone in the lower parts of the succession and the Palaeolenus lantenosis Zone in the upper parts (Zhang et al., 1980;Wang et al., 1987;Zhang and Hua, 2005; X.L. . This indicates an age of Cambrian Stage 4, similar to the Wulongqing Formation in eastern Yunnan (Wang et al., 1987;Zhang et al., 2015). Brachiopods-particularly linguliform brachiopods (linguloids and acrotretoids)-from the Shipai Formation also corroborate a Cambrian Stage 4 age for the Shipai Formation (Z.F. . Brachiopods from Cambrian Stage 4 are presently known from all main continents, including South Australia, Antarctic, Greenland, Kazakhstan, Siberia, and China (Pelman, 1977;Holmer et al., 2001;Ushatinskaya and Malakhovskaya, 2001;Skovsted and Holmer, 2005;Betts et al., 2016Betts et al., , 2017Betts et al., , 2019Chen et al., 2019;Pan et al., 2019;Ushatinskaya and Korovnikov, 2019;Claybourn et al., 2020;Zhang et al., 2020a, b). Cluster analysis of Cambrian, Stage 4 linguliforms shows that the faunas from South China (Shipai Formation, Guanshan biota) and Kazakhstan cluster together (Fig. 19). This is defined by the occurrence of Eoobolus, Palaeobolus, Lingulellotreta, and Linnarssonia. Clustering of east Antarctica, South Australia, and North China is consistent with the biostratigraphic correlation of Claybourn et al. (2020) based on brachiopods.
The brachiopod fauna from the Shipai Formation is dominated by the acrotretoid Linnarssonia sapushanensis, which are commonly aggregated as patchy concentrations of shell valves on the same bedding plane (Fig. 15.1-15.4), notably in the Xiachazhuang section. In contrast, the acrotretoids from the Wulongqing Formation form thicker shell beds (∼11-13 pavements within a 1 cm thick bed) (Fig. 15.5-15.7). Differential accumulation styles of acrotretoid valves highlight differences between sedimentary paleoenvironments and energy regimes of the Shipai and Wulongqng formations. In the Wulongqing Formation of eastern Yunnan, where acrotretoid brachiopod shells form dense stacks, the shells were probably affected by high energy currents, and were briefly suspended before their final deposition on the sea floor. In contrast, acrotretoidshell beds from the Shipai Formation in the Hubei Province are characterized by lower density shell concentrations, probably the result of deposition in a deeper environment where current energy was minimal.
Similarities between Linnarssonia shell beds in the middle Shipai Formation in the Three Gorges area and the lower to middle Wulongqing Formation in Wuding area, eastern Yunnan suggest that these two successions may be roughly correlated. This is further corroborated by the first appearance datum (FAD) of the rhynchonelliform calcareous-shelled brachiopod Nisusia in the silty mudstone of both the Shipai and Wulongqing formations. Shell structures of acrotretoid brachiopods from fine siliciclastics.-Organophosphatic brachiopod shells usually consist of an organic periostracum, a mineralized laminar primary layer, and a secondary columnar layer (Holmer, 1989;Williams and Holmer, 1992;Williams et al., 1997;Holmer et al., 2008;Streng et al., 2008). The thin organic periostracum is usually exfoliated during taphonomic processes. The primary layer is generally very thin, usually not much more than 1 μm thick, and is easily lost during transportation and burial, resulting in the exposure of the secondary layer (Williams and Holmer, 1992;Williams et al., 1997). The secondary layer is mainly composed of an alternating arrangement of lamina and columns. The columnar shell structure is characteristic of acrotretid brachiopods (Holmer, 1989;Williams and Holmer, 1992), but has been demonstrated to occur in several lingulid brachiopods, including Lingulellotretidae, Dysoristidae, and Kyrshabaktellidae (Cusack et al., 1999;Skovsted and Holmer, 2006). Similar shell structures are also present in Canalilatus , the stem lineage of brachiopods Mickwitzia (Skovsted and Holmer, 2003;Holmer et al., 2008), Micrina (Williams and Holmer, 2002), and the tommotiid Tannuolina .
Journal of Paleontology 95(3):497-526 Ushatinskaya et al., 1988;Holmer, 1989;Williams and Holmer, 1992;Holmer et al., 2008;, no details of acrotretoid shell structures preserved in siliciclastic rocks have ever been described. Most acrotretoids in muddy deposits are preserved as internal molds (e.g., Duan et al., 2021), which precludes investigation of shell structural details (Mergl and Kordule, 2008;Mergl, 2019). However, specimens of the acrotretoid Linnarssonia from the silty mudstone of the Shipai Formation have well-preserved shell ultrastructures, allowing detailed study of the acrotretoid shell ultrastructure from siliciclastic deposits for the first time.
The primary layer forming the ornamentation of the external shell surface (e.g., concentric fila) is preserved in some specimens of L. sapushanensis from the Shipai Formation ( Fig. 2.1). The secondary layer is also well developed, and has a columnar structure that is mainly composed of hollow tubes (diameter = 2.5 μm on average, range 1.6-3.8 μm), with solid columns (∼1 μm in diameter) that are composed of stacks of pinacoidal plates (Fig. 20.4,20.5). The hollow tubes in L. sapushanensis are comparable morphologically with those previously documented in other acrotretoid brachiopods, such as Anglulotreta (1.5-5 μm diameter) (Table 4) (Holmer, 1989;Williams and Holmer, 1992;Streng, 1999;Streng and Holmer, 2006;Streng et al., 2008;. The solid columns in the tubes (Fig. 20.5) and the solid columns that connected the laminae (Fig. 21.5) are comparable with those columnar central canals (∼1 μm in diameter) (Fig. 21.9). Latex casts of these hollow tubes and thin solid columns in L. sapushanensis ( Fig. 21.6, 21.7) also provide detailed molds for comparison with acid-etched material ( Fig. 21.8, 21.9).
It is generally accepted that the empty intralaminar spaces in acrotretoid shells originally contained an organic matrix, and that the slots between successive laminae and columnar canals were originally occupied by sheets and strands, respectively composed of proteins or chitin (Poulsen, 1971;Ushatinskaya et al., 1988;Holmer, 1989;Williams and Holmer, 1992). In L. sapushanensis from the Shipai Formation, the intralaminar spaces are commonly empty, thus exposing the hollow tubes in relief ( Fig. 20.4), but occasionally the spaces are filled with mineralized materials (Fig. 21.4). The interlaminar surfaces of lamellae are ornamented with circular pits (Fig. 20.7, 20.9) and hollow tube openings (Fig. 20.8), usually ∼500 nm and 2.5 μm, respectively. The hollow tubes may have contained unmineralized organic fibers that were lost post-mortem. Thus, the hollow tube and solid column of the acrotretoid column structure from the Shipai Formation could be the equivalent of the traditional column and central canal structure observed in shells dissolved from limestone (Fig. 22).

Conclusion
This is the first comprehensive description of the brachiopod faunas and their systematic diversity from the Shipai Formation (Stage 4) in the Three Gorges area of South China. This assemblage includes the representatives of the subphylum Linguliformea: linguloids (Lingulellotreta ergalievi, Eoobolus malongensis, and Neobolidae gen. indet. sp. indet.), an acrotretoid (Linnarssonia sapushanensis), and calcareous-shelled rhynchonelliforms (Kutorgina sinensis, Kutorgina sp., and Nisusia liantuoensis). Cluster analysis of linguliform, Cambrian Stage 4 brachiopods shows that the faunas of South China (Shipai Formation and the Wulongqing Formation) group closely with those from Kazakhstan.
The brachiopod fauna from the Shipai and Wulongqing formations both include the rhynchonelliform Nisusia, and preserve shell concentrations of the acrotretoid L. sapushanensis. In the Shipai Formation, L. sapushanensis are preserved in patchy aggregations on the same bedding plane, whereas in the Wulongqing Formation they form thick shell beds. This suggests that the Wulongqing Formation represents a slightly higher energy paleoenvironment than the quieter Shipai Formation.
In siliciclastics, brachiopods are commonly preserved as casts and molds and retention of shell material is generally rare. Brachiopods from the Shipai Formation however, retain shell material, the remarkable preservation of which is possibly due to deposition in a low energy paleoenvironment. Linnarssonia sapushanensis from the Shipai Formation has a hollow tube and solid column microstructure, which is likely to be the equivalent of traditional column and central canal-type microstructure often observed in acid-etched acrotretids. Knowledge of shell microstructures in Cambrian acrotretoids is primarily derived from specimens acid etched from limestones. This study provides the first detailed description of acrotretoid shell structures from Cambrian siliciclastics, providing an important comparison with acid-etched material.