Shell Microstructures of the Helcionelloid Mollusc Anabarella Australis from the Lower Cambrian

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Shell Microstructures of the Helcionelloid Mollusc Anabarella Australis from the Lower Cambrian Shell microstructures of the helcionelloid mollusc Anabarella australis from the lower Cambrian (Series 2) Xinji Formation of North China Luoyang Lia, b, Xingliang Zhanga, *, Christian B. Skovsteda, b, *, Hao Yuna, Guoxiang Lic, Bing Panb, c a State Key Laboratory of the Continental Dynamics, Shaanxi Key Laboratory of Early Life and Environments, Department of Geology, Northwest University, Xi’an 710069, PR China; b Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden; c State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China. *Corresponding authors. Email: [email protected]; [email protected] Although various types of shell microstructures are uncovered from Cambrian molluscs, precise organization and mineralogical composition of Terreneuvian molluscs are rarely known. Anabarella was one of the first helcionellid molluscs to appear in the Terreneuvian, and ranged up to Cambrian Epoch 3 in age. Here, shell microstructures of Anabarella australis have been studied based on new collections from the lowermost Cambrian (Series 2) Xinji Formation of the North China Block. Results show that A. australis has a laminar inner shell layer that consists of crossed foliated lamellar microstructure (CFL). Nacreous, crossed-lamellar and foliated 1 aragonite microstructures previously documented in Terreneuvian A. plana are here revised as preservational artefacts of the CFL layers. This complex skeletal organization of Anabarella suggests that mechanisms of molluscan biomineralization evolved very rapidly. Morphologically, specimens from the Chaijiawa section show a distinct “pseudo-dimorphism” pattern as external coatings are obviously identical to Anabarella, while associated internal moulds are similar to the helcionelloid genus Planutenia. In contrast, internal moulds from the Shangzhangwan section show considerable morphological variation owing to preservational bias, which are more similar to specimens from South Australia, Northeast Greenland and Germany. These observations demonstrate that the wide morphological variants of internal moulds of Anabarella worldwide are in large part preservational artefacts, and are unlikely to represent the real intra- and interspecific variability of the animal. In these cases, Planutenia is confirmed to be a subjective synonym of Anabarella. Keywords: Cambrian; Helcionelloida; Shell Microstructure; Taxonomy Introduction One outstanding innovation in the evolutionary history of early life is the advent of biomineralized skeletons among metazoans during the Cambrian explosion, with many phylum-rank clades first acquiring the capacity to produce a variety of biominerals (e.g. carbonate, phosphate, and silica minerals) in an astounding range of 2 organizations and functions (Bengtson 2005; Zhuravlev & Wood 2008; Wood & Zhuravlev 2012). Molluscs were among the first metazoans to construct mineralized external shells under exquisite controls over biomineralization by underlying tissues (the mantle). They produce polymorphs of calcium carbonate (calcite and/or aragonite, vaterite) in highly organized macro-micro architectures within the shells (Checa 2000; Addadi et al. 2006). At present, 40 types of shell microstructures (prismatic, nacre, crossed lamellar, foliated, homogeneous, etc.) have been determined in mollusc shells in terms of hierarchical organization, biocompositional nature, crystallographic orientation, etc. (Carter et al. 1990; Sato & Sasaki 2015). As a successful animal group in Cambrian marine environments, molluscs constituted conspicuous elements among the Cambrian small shelly fossil assemblages (Bengtson et al. 1990; Gravestock et al. 2001). In recent years, intensive studies on their shell microstructures indicated that Cambrian molluscs evolved very rapidly in their shell organizations in addition to morphological diversity and disparity. Various types of microstructural fabrics have been recognized such as lamello-fibrillae (Feng & Sun 2003), foliated calcite (Vendrasco et al. 2010a, b), and foliated aragonite (Li et al. 2017). Notwithstanding, shell microstructures of Cambrian molluscs are rarely known, especially the Terreneuvian members that are evolutionarily closer to ancestral forms. The Fortunian maikhanellid shells, characterized by cap-shaped morphology with scale-like ornamentations, have been assigned to the Mollusca by many authors (e.g. Bengtson 1992; Ponder et al. 2007). Various types of fibrous microstructures, broadly assigned to lamello-fibrillae, were 3 previously described in some maikhanellid taxa, e.g. Maikhanella Zhegallo, 1982 and Canopoconus Jiang, 1982. Such fibrous microstructures have also been widely reported in Terreneuvian helcionelloid molluscs, e.g. Latouchella Cobbold, 1921 and Archaeospira Yu, 1979 (Feng et al. 2002; Feng & Sun 2003). The helcionelloid mollusc Anabarella Vostokova, 1962 has been known to range stratigraphically from Cambrian Terreneuvian to Series 3. Its shell is highly compressed laterally, with apex tightly coiled, almost connecting to the apertural margin (Gubanov et al. 1999; Gravestock et al. 2001; Gubanov & Peel 2003; Gubanov et al. 2004; Parkhaev 2004a, b). Although shell microstructures of Terreneuvian molluscs are mainly preserved as fibrous forms (Feng & Sun 2003; Vendrasco et al. 2015; Li et al. 2017), to our knowledge, Anabarella and its relative Watsonella Grabau, 1900 are the only known two taxa recording blade or lath-like crystallites of aragonite with a stepwise growth pattern among Cambrian Terreneuvian molluscs (Runnegar 1985; Kouchinsky 1999). Those observations imply that shell microstructures of Anabarella, Watsonella, and probably other Terreneuvian molluscan taxa might have developed different types of crystal forms (rod, lath, blade, tablet, etc.), and evolutionarily advanced organizations in addition to fibers of lamello-fibrillae. The new materials of Anabarella australis Runnegar in Bengtson et al., 1990 from the lowermost Cambrian Xinji Formation (upper Stage 3 or lower Stage 4) of North China allow us to recognize the complex hierarchical shell microstructure of this characteristic helcionelloid species. More interestingly, owing to preservational bias, 4 internal mould specimens of Anabarella are quite different from its external coatings, but greatly resemble the helcionelloid genus Planutenia Elicki, 1994, and hence enable a taxonomic revision. Geological setting, material and methods The Xinji Formation, deposited along the south margin of North China Block during the global transgression event in Cambrian Series 2, is particularly well-exposed in Longxian County, Shaanxi Province (Fig. 1A). In the Chaijiawa section, the Xinji Formation rests disconformably on the Ediacaran Dongpo Shale, and is conformably overlain by massive dolostones of the Zhushadong Formation. This rock unit, approximately 34m thick, is deposited in a shoal or back-shoal environment, and can be subdivided into three parts: the basal sandstones with phosphatic intraclasts (0.65m thick), the mid bioclastic limestones (4.8m thick), and the upper calcareous sandstones (27.7m thick) (Li et al. 2016; Yun et al. 2016; Fig. 1B). Rock samples were treated with buffered 5% acetic acid to retrieve acid-resistant microfossils. Selected specimens were mounted, sputter-coated with gold and examined with a Scanning Electron Microscope FEI Quanta 400 FEG in Northwest University. Microfossils described below are all reposited at the Department of Geology, Northwest University, Xian, China. A total of 160 internal moulds from Chaijiawa section were imaged in lateral view with their apex posterior oriented to the left, while oppositionally positioned 5 steinkerns were mirror imaged (Fig. 4A). Two landmarks and 48 sliding semi-landmarks were digitized by LYL with the software TpsDig.232. The two landmarks respectively corresponded to the sharp curvatures in the umbilicus and ad-apertural dorsum of the shell, while semi-landmarks were digitized in a clockwise direction (Fig. 4B). The software TpsUtil.64 was applied to transfer curves to landmarks and create the sliders file defining the semi-landmarks. The superimposition method applied here is the Generalized Procrustes Analysis (GPA), computed by the software TpsRelw32. It calculates the consensus configuration or mean shape, which serves as the reference for the superimposition of all specimens. Semi-landmarks are slid by minimizing Procrustes distances between individual specimens and the average configuration. Relative warp analysis (RWA) was carried out to obtain a lower-dimensional ordination of individuals in the morphospace. The thin-plate splines (TPS) were used to depict the morphological variation corresponding to the extremes of PC1 and PC2 as TPS-grids. Systematic palaeontology Phylum Mollusca Cuvier, 1797 Class Helcionelloida Peel, 1991 Order Helcionellida Geyer, 1994 Family Helcionellidae Wenz, 1938 Genus Anabarella Vostokova, 1962 6 1994 Planutenia Elicki: 82, figs 5/2, 13. 1996 Planutenia (Elicki); Elicki: 166, pl. 5, figs 1–9. 2003 Planutenia (Elicki); Elicki: 386, fig. 16. 2007 Planutenia (Elicki); Skovsted & Peel: 735, figs 4G, H. 2010 Planutenia (Elicki); Skovsted & Peel: 756, fig. 2.7. Diagnosis. From Gubanov et al. (2004). Small, bilaterally symmetrical univalve mollusc with advolute or slightly involute, rapidly expanding, laterally compressed shell, and coiled through about one whorl. Shell smooth or slightly
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