The First Report of the Acrotretoid Brachiopod Hadrotreta from the Tsinghsutung Formation Cambrian (Series 2, Stage 4), Guizhou, South China

Simple Summary A number of well-preserved fossils of Hadrotreta were found in the Tsinghsutung Formation of Cambrian Series 2, Stage 4 in Jianhe, Guizhou, south China by etching rocks with 2–3% acetic acid. This is the first report of Hadrotreta in south China. According to the global palaeogeographical distribution of Hadrotreta shows an expanding trend from the Cambrian Age 4 to the Miaolingian Epoch, and this genus was mainly found at low latitudes. In the Cambrian Epoch 2, Age 4, Hadrotreta only appeared in south China and the Laurentia palaeocontinent, and was mostly associated with deep-water continental shelf environments. Later, Hadrotreta expanded its distribution to become virtually cosmopolitan during the Miaolingian Epoch and is mostly preserved in shallow-water platform environments. Abstract Hadrotreta is a worldwide acrotretoid brachiopod reported from the Cambrian Series 2 to Miaolingian. Here, a number of well-preserved fossils of Hadrotreta, identified as Hadrotreta cf. H. timchristiorum, were found in the Protoryctocephalus arcticus Zone of the Tsinghsutung Formation of Cambrian Series 2, Stage 4 in Jianhe, Guizhou, south China. This is the first report of Hadrotreta in China, which enriches its global palaeogeographical distribution. Hadrotreta is very similar to acrotretoids such as Kostjubella, Vandalotreta, Linnarssonia, and Eohadrotreta. It differs from them with its well-developed ventral boss-like apical process, apical pits, and dorsal median sulcus. In view of the palaeogeography of Hadrotreta, this genus was mainly distributed in low-latitude regions. Hadrotreta was only found in south China and Laurentia during the Cambrian Age 4, then expanded its distribution to other regions such as Siberia, Baltica, the Kazakh Terranes, the Far East, and Gondwana Pange during the Miaolingian Epoch. Hadrotreta seems to have shifted from deeper water to shallow-water environments during the period from the Cambrian Series 2 to the Miaolingian.

Recently, a number of well-preserved specimens of Hadrotreta fossils, identified as Hadrotreta cf.H. timchristiorum, were collected from the middle and upper Tsinghsutung Formation of Cambrian Series 2, Stage 4 in Jianhe, Guizhou, south China.This paper is the first report of Hadrotreta from China.Its detailed morphology and internal structures show that Hadrotreta is very similar to other genera such as Eohadrotreta, Vandalotreta, Kostjubella, and Linnarssonia.This paper expands the global palaeogeographical distribution and summarizes the spatiotemporal distribution of Cambrian Hadrotreta.

Geological Setting
The study area was located in Jianhe County, 240 km to the southeast of Guiyang City, and belonged to the transition slope area between the Yangtze platform and Jiangnan basin [30].The Cambrian strata in the Jianhe area are widely distributed, including the Niutitang, Jiumengchong, Bianmachong, Balang, Tsinghsutung, Kaili, Jialao, and Loushanguan formations in ascending order [31,32].
The studied section is located in Songshan, Balang Village, Jianhe County, and is adjacent to the Wuliu-Zengjiayan section, the Global Stratotype Section of the Cambrian Miaolingian [31,32].The Tsinghsutung Formation of the Songshan section is in conforming contact with the overlying Kaili Formation and underlying Balang Formation, and the sedimentary age is assigned to the Cambrian Epoch 2, Age 4, with a lithological composition of limestone, dolomite, and mudstone.The Tsinghsutung Formation has a thickness of about 272.2 m.It is divided into a lower portion composed of greyish-grey, mediumthick limestone, an upper part comprising a medium-thick layer, a thin layer of limestone and a thick silty muddy layer, and a top layer of grey-black dolomite (Figure 1) [31][32][33].Zhang et al. considered the Tsinghsutung Formation of the Songshan section in Jianhe to have been deposited in a low-energy, deep-water shelf-shelf margin environment [34].In terms of biostratigraphy based on trilobites, the Tsinghsutung Formation in the Songshan section of Jianhe is divided into an Arthricocephalus chauveaui zone in the lower part and a Protoryctocephalus arcticus zone in the middle-to-top part.Here, we report the collection of Hadrotreta cf.H. timchristiorum in the Protoryctocephalus arcticus zone.

Hadrotreta Material and Specimen Visualization
The specimens from the limestones of the Tsinghsutung Formation in the Songshan section were etched in a solution of 2-3% acetic acid, as proposed by Jeppsson et al. [35].The samples obtained by sifting, washing, and drying were then selected under a stereomicroscope to obtain the fossil material.Scanning electron microscope (SEM) images of coated fossils were taken with EVO18 and SU3500 with 15-20 kV and 70-80 Pa at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences.For some specimens, SEM imaging was carried out at 20 kV with a COXEM-30 from Guizhou University.

Hadrotreta Material and Specimen Visualization
The specimens from the limestones of the Tsinghsutung Formation in the Songshan section were etched in a solution of 2-3% acetic acid, as proposed by Jeppsson et al. [35].The samples obtained by sifting, washing, and drying were then selected under a stereomicroscope to obtain the fossil material.Scanning electron microscope (SEM) images of coated fossils were taken with EVO18 and SU3500 with 15-20 kV and 70-80 Pa at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences.For some specimens, SEM imaging was carried out at 20 kV with a COXEM-30 from Guizhou University.
Diagnosis.Shell transversely oval or subcircular, ventribiconvex, shell ornamented by fine growth lines.Ventral valve low subconical; pseudointerarea flat to gently concave, catacline to gently procline, divided medially by shallow intertrough; external pedicle foramen small, subelliptical, immediately posterior of apex; apical process boss-like and entirely anterior of apex of valve, limited laterally by vascula lateralia; and apical pits welldeveloped, immediately lateral of pedicle tube.Dorsal valve gently convex, anteriorly with broad, shallow median sulcus; dorsal pseudointerarea orthocline to gently anacline, divided by median groove into two propareas; and cardinal muscle scars relatively long.For detail, see Rowell [40] (p.12).
Discussion.Hadrotreta was first established by Rowell [40].The type species is Acrotreta primaea, which was reported in the lower to middle Cambrian Pioche Shale of Nevada, USA, by Walcott [41], who placed in the genus Acrotreta base on the character of pseudointerarea, which was similar to Acrotreta attenuata [41,42].Hadrotreta was then established by Rowell [40], who revised the classification based on the presence of a short pseudointerarea, a lower median ridge rather than a leaf-like septum, a short-small pedicle foramen, and the shape and location of the apical process.
The morphological characteristics of Hadrotreta are roughly similar to Kostjubella, Vandalotreta, Linnarssonia, and Eohadrotreta, although with important differences (Table 1).For example, Hadrotreta and Kostjubella have a well-developed shallow median sulcus and median ridge of the dorsal valve, the difference being that the latter ventral valve pseudointerarea are catacline to slightly apsacline with a deeper intertrough, and the maximum height anterior to the umbo and apical process is confined to a boss-like raised area surrounding the internal foramen (Table 1) [9,43,44].When comparing Hadrotreta with Vandalotreta [45], the ventral valve boss-shaped apical process of the latter does not fill the apex, and the dorsal median sulcus and median ridge are vestigial or weakly developed (Table 1) [46].The genus Linnarssonia [47] differs from Hadrotreta in that the ventral valve apical pits are not developed, the pedicle foramen is not enclosed in a larval shell, the ventral pseudointerarea are catacline to procline, the dorsal pseudointerarea is weakly developed, the cardinal muscle scars are arranged more closely, the dorsal median ridge is high and short, and the dorsal median buttress is well developed (Table 1) [7].The difference between Eohadrotreta [8] and Hadrotreta is that the ventral valve of the former lacks a well-developed apical process and apical pits, and the dorsal median sulcate is absent (Table 1).Streng, [49] Holmer & Popov, [3] and Duan et al., [7] Li and Holmer, [8] At present, the genus Hadrotreta contains the following species: H. primaea [18,20,28,[40][41][42]50], H. taconica [25], H. timchristiorum [23], H. djagoran [51], H. fragilis [19], H. extentusa [17,21], H. pallialis [16], ?H. primaea [52], Hadrotreta sp.[22,24,25], Hadrotreta rara?[27], and Hadrotreta? sp.[29].H. taconica differs from the type species by the ventral apical pits anterior to the pedicle foramen and the lack of a boss-like termination to the dorsal median ridge.It differs from H. trimchristiorum by a larger dorsal pseudointerarea and a deeper ventral intertrough.H. timchristiorum is more similar to H. primaea; both have a well-developed, boss-like apical process.H. timchristiorum differs from the type species mainly in having a narrow and shallow ventral intertrough, as well as a shorter and less-developed dorsal pseudointerarea, and a smaller and shorter dorsal cardinal muscle field.H. djagoran was revised to Vandalotreta djagoran by Holmer et al. [46].
Biology 2023, 12, x 6 of 14 pedicle foramen is situated in the posterior part of the apical process and apical pits are situated lateral to and slightly anterior of the pedicle tube (Figure 3h-j); cardinal muscles are situated lateral to the vascula lateralia, at the lateral margins of the ventral pseudointerarea, with a well-preserved honeycomb-like cell structure (Figure 3j,l,n).The ventral visceral region and the lateral cateria are well-preserved, and the lateral cateria are relatively short.Five fines lateral cateria extend from the apical process to the anterior, which is situated between the normal lateral cateria (Figure 3g).The dorsal valve is subcircular, and the ratio of the length to width is approximately 0.9433 (Table 2), with a slightly convex apex.The dorsal shell is ornamented with fine, concentric ridges, separated by a broad, shallow anterior sulcus (Figure 4a-c), and the shell appears with a lamellar structure.The dorsal pseudointerarea is narrowly triangular, orthocline to anacline with a column-structured median groove (Figure 4l), the ratio (Figure 4d,g,j,m), and the ratio of the median septum length to the dorsal valve is about 0.6862 (Table 2).The submedian septum is situated in the lateral median septum.The dorsal cardinal muscle is a long ellipse, situated between the lateral of the median septum and extending to the edge of the dorsal valve from the pseudointerarea (Figure 4e,f,h,i), with a well-preserved honeycomb-like cell structure (Figure 4k), the same as in the cardinal muscles in the ventral valve (Figure 3n).The ratio of the pseudointerarea length to the dorsal valve length is about 0.2211 (Table 2).Material.Ten dorsal valves and twelve ventral valves from acid-resistant residues of limestone samples from the Tsinghsutung Formation, Songshan section in the Guizhou Province, China.
Description.Shell transversely oval or subcircular, ventribiconvex (Figure 2); shell ornamented by concentric growth lines.The ventral valve is conical, the ratio of the ventral valve length to width is approximately 0.8945 (Table 2), and the concentric sculpture on the shell surface is strongly developed, gradually becoming sparse from the posterior to the anterior (Figure 3a-f).The apex of the ventral shell is slightly convex to subconical, and the vertex is in the middle to the anterior of the shell (Figure 3a,b,d,f).The posterior edge of the ventral shell is short and rounded, the beak slightly protrudes forward, and the larval shell is covered by hemispherical pits (Figure 3c,f,m).The pedicle tube with a narrow and shallow intertrough touches the larval shell posterior (Figure 3e,g,j).A high, broadly boss-like apical process is well preserved in the ventral interior, with a lamellar structure and column structure in the transverse section (Figure 3i,k,l,o).The rounded pedicle foramen is situated in the posterior part of the apical process and apical pits are situated lateral to and slightly anterior of the pedicle tube (Figure 3h-j); cardinal muscles are situated lateral to the vascula lateralia, at the lateral margins of the ventral pseudointerarea, with a well-preserved honeycomb-like cell structure (Figure 3j,l,n).The ventral visceral region and the lateral cateria are well-preserved, and the lateral cateria are relatively short.Five fines lateral cateria extend from the apical process to the anterior, which is situated between the normal lateral cateria (Figure 3g).Abbreviations: D-dorsal valve; V-ventral valve; N-number of specimens; X-mean; S-standard deviation; min-minimum observed size; and max-maximum observed size.In other abbreviations, all measurements are in millimetres.L-length of the valve; Lp-length of pseudointerarea, Ls-length of the median septum; Lc-length of cardinal muscle scar; Lf-length of foramen; W-width of the valve; Wp-width of pseudointerarea; Wc-width of cardinal muscle scar; Wg-width of median groove; and Wf-width of the foramen.
The dorsal valve is subcircular, and the ratio of the length to width is approximately 0.9433 (Table 2), with a slightly convex apex.The dorsal shell is ornamented with fine, concentric ridges, separated by a broad, shallow anterior sulcus (Figure 4a-c), and the shell appears with a lamellar structure.The dorsal pseudointerarea is narrowly triangular, orthocline to anacline with a column-structured median groove (Figure 4l), the ratio of the pseudointerarea width to shell width is nearly 0.3761, and the ratio of the median groove width to the pseudointerarea is about 0.4226 (Table 2).A triangular median buttress is beneath the median groove, connected with the spindle-like median septum (Figure 4d,g,j,m), and the ratio of the median septum length to the dorsal valve is about 0.6862 (Table 2).The submedian septum is situated in the lateral median septum.The dorsal cardinal muscle is a long ellipse, situated between the lateral of the median septum and extending to the edge of the dorsal valve from the pseudointerarea (Figure 4e,f,h,i), with a well-preserved honeycomb-like cell structure (Figure 4k), the same as in the cardinal muscles in the ventral valve (Figure 3n).The ratio of the pseudointerarea length to the dorsal valve length is about 0.2211 (Table 2).
Comparison.The majority of acrotretoid brachiopods from the Tsinghsutung Formation belong to Hadrotreta, and have been identified as such based on the oval pedicle foramen on the outside of the larval shell, the boss-like apical process of the ventral valve, the presence of deep apical pits lateral to the internal pedicle tube, and the low, forked dorsal median ridge.Hadrotreta cf.H. timchristiorum differs from the type species, H. primaea, from the Pioche Shale of the Great Basin, by a weakly developed median ridge system in the dorsal valve and apical pits laterally located in the internal foramen.Hadrotreta cf.H. timchristiorum is distinguished from H. taconica in Canada by a larger dorsal pseudointerarea, larger dorsal muscle scars, a less protruding apical process, and a more well-defined ventral intertrough.The material in the Tsinghsutung Formation is similar to that of H. timchristiorum in the Parahio Formation, but differs in having a relatively well-developed ventral apical process and vascula lateralia (Figure 3g,l), with well-developed dorsal cardinal muscle fields (Figure 4f,i,k,o).
The evidence from south China (this study) and Canada indicates that Hadrotreta seems to have lived in deep-water outer shelf environments during the Cambrian Age 4 (Table 3) [13,25].Materials from Canada also show that Hadrotreta was also found in shallowwater environments of the inner shelf (Table 3) [25].However, during the Miaolingian, Hadrotreta lived in shallow-water environments (Table 3) [18,20,23,28], which shows a wide ecological range for Hadrotreta.The global palaeogeographical distribution of Hadrotreta shows an expanding trend from the Cambrian Age 4 to the Miaolingian Epoch.Moreover, during the Cambrian Age 4, Hadrotreta seems to have lived in deeper-water environments.In contrast, it was in relatively shallow-water environments in the Miaolingian Epoch (Table 3).The evidence from south China (this study) and Canada indicates that Hadrotreta seems to have lived in deep-water outer shelf environments during the Cambrian Age 4 (Table 3) [13,25].Materials from Canada also show that Hadrotreta was also found in shallow-water environments of the inner shelf (Table 3) [25].However, during the Miaolingian, Hadrotreta lived in shallow-water environments (Table 3) [18,20,23,28], which shows a wide ecological range for Hadrotreta.The global palaeogeographical distribution of Hadrotreta shows an expanding trend from the Cambrian Age 4 to the Miaolingian Epoch.Moreover, during the Cambrian Age 4, Hadrotreta seems to have lived in deeper-water environments.In contrast, it was in relatively shallow-water environments in the Miaolingian Epoch (Table 3).

Conclusions
Well-preserved Hadrotreta fossils from the Tsinghsutung Formation of the Cambrian Series 2, Stage 4 at the Songshan section, Jianhe, Guizhou, China, identified as Hadrotreta cf.H. timchristiorum, are the first of this genus to be reported in China, increasing its known distribution.Hadrotreta is similar to Kostjubella, Vandalotreta, Linnarssonia, and Eohadrotreta, but the former has a well-developed ventral boss-like apical process, apical pit, shallow intertrough, and dorsal median sulcus, which separate it from the other genera.
According to its palaeogeographical distribution, Hadrotreta is mainly found at low latitudes.In the Cambrian Epoch 2, Age 4, Hadrotreta only appeared in south China and the Laurentia palaeocontinent, and was mostly associated with deep-water continental shelf environments.Later, Hadrotreta expanded its distribution to become virtually cosmopolitan during the Miaolingian Epoch and is mostly preserved in shallow-water platform environments.

Figure 1 .
Figure 1.Stratigraphic columns of the Tsinghsutung Formation at the Songshan section in Jianhe County, Guizhou Province, south China, showing the stratigraphic horizon of acrotretoid Hadrotreta cf.H. timchristiorum.

Table 2 .
Main dimensions and ratios of the dorsal and ventral valve structure (size unit: mm).

Table 2 .
Main dimensions and ratios of the dorsal and ventral valve structure (size unit: mm).

Table 3 .
The classification, diversity, age, and sedimentary environment of Hadrotreta Rowell, 1966 (this table only compares the published confirmed species, however, undetermined species, similar species, and doubted species are not discussed).