The middle Cambrian Linyi Lagerstätte from the North China Craton: a new window on Cambrian evolutionary fauna

Abstract The rapid appearance of major animal groups and complex marine communities during the Cambrian explosion is recorded in large part in Burgess Shale-type lagerstätten. However, the restricted temporal and spatial distribution of known lagerstätten continues to hinder the formation of a comprehensive perspective on Cambrian evolutionary faunas. Here we describe the Linyi Lagerstätte (ca. 504 mya), a new Cambrian Miaolingian lagerstätte from the Zhangxia Formation in Shandong Province, North China. The Linyi Lagerstätte contains a variety of well-preserved soft-bodied fossils, among which the non-trilobite arthropods, particularly the mollisoniids and radiodonts, are the most important groups. The new assemblage is remarkable for its excellent preservation of arthropod limbs, eyes and guts, as well as for its close similarity in taxonomic composition to Laurentian lagerstätten. The distinctive Linyi Lagerstätte holds great promise for providing additional insights into the morphological disparity, community structure and paleogeographic range of marine faunas during the middle Cambrian (Miaolingian).


INTRODUCTION
Current understanding of the origin and early diversification of metazoans and marine communities during the Cambrian explosion is based primarily on the exceptional fossil records of Burgess Shaletype (BST) lagerstätten. Many fossils from these sites contain relic soft parts, which are normally absent in the fossil record, and thus provide critical evidence bearing on the structure of Cambrian marine communities and the appearance of key evolutionary innovations [1][2][3]. Together, nearly 20 Cambrian lagerstätten preserve a detailed record of early animal evolution from Cambrian Epoch 2 to the Miaolingian [4,5], and new lagerstätten are still being discovered [6][7][8][9]. Nevertheless, most of the well-known Cambrian lagerstätten are restricted to a few terranes, with most of them (over a dozen) occurring in South China (Epoch 2) or Laurentia (Miaolingian) (Fig. 1). This striking geographical imbalance is particularly evident in the middle Cambrian, with the major Miaolingian lagerstätten, including the Burgess Shale in British Columbia (western Canada) and five lagerstätten in the Great Basin (western USA), being located predominantly in Laurentia [10][11][12][13]. The Miaolingian period witnessed the apogee of the Cambrian evolutionary fauna and was the key interval between the aftermath of the Cambrian explosion and the Great Ordovician Biodiversification Event [2,14,15]. However, the scarcity and limited spatial distribution of Miaolingian lagerstätten have hindered efforts to understand the evolutionary and ecological changes that occurred during this time. Hence the need for an intensified search for Miaolingian lagerstätten in other terranes such as North China, where recent discoveries of typical Miaolingian BST fossils [16][17][18] have made this area a particularly inviting prospect.
Here we report the discovery of a new Miaolingian lagerstätte in the lower part of the Panchegou C The Author(s) 2022. Published by Oxford University Press on behalf of China Science Publishing & Media Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.  Figure 1. Spatial and temporal distribution and taxonomic diversity of 16 major Cambrian lagerstätten, and the position of the Linyi Lagerstätte. Numbers in the stratigraphic distribution chart correspond to those plotted in the paleogeographic map. The diversity data for the key Cambrian lagerstätten dealt with in this study were obtained from Refs [7,8,12,13,49] and this study. Global paleogeography for the early and middle Cambrian are modified from Ref. [50] and Ref. [41]. Abbreviations: SC, South China; La, Laurentia; Si, Siberia; Au, Australia; NC, North China.
Member of the Zhangxia Formation (lower Drumian) in Shandong Province, North China (Figs 1 and 2). The Linyi Lagerstätte contains a diverse and well-preserved BST fossil assemblage, providing unique insights into the structure, taphonomy and paleobiogeographical relationships of Miaolingian marine communities outside of North America.

RESULTS
The Linyi Lagerstätte is exposed in the Sikou section (35 • 08 04.1 N, 118 • 04 15.9 E) on the western side of Liuzhuang village, a northwestern suburb of Linyi City ( Fig. 2A and B). BST fossils were collected from alternating event and background beds in a 5-meter-thick interval of black and greenish shale (Fig. 2C-E) situated 10.5-15.2 m above the base of the Panchegou Member of the Zhangxia Formation. This horizon has yielded over 35 fossil taxa, including four trilobites, one agnostoid, at least nine soft-bodied arthropods, two lophophorates, at least seven sponges, one chancelloriid, one priapulid, seven problematica, four macroalgae and four trace fossils ( Supplementary Fig. 5). Arthropods are the most diverse metazoan group, comprising 12 species and two indeterminate taxa. The Linyi Lagerstätte ranges from the upper part of the Megagraulas coreanicus trilobite Zone to the lower part of the Crepicephalina convexa trilobite Zone [19], an interval corresponding to the early Drumian [19,20]. It is slightly younger than the Burgess Shale and is equivalent in age to the Wheeler Formation Lagerstätte (Fig. 1). The Panchegou Member was deposited in a platform margin to outer shelf setting and contains scattered carbonate platform deposits [21]. The presence in the Linyi Lagerstätte of taxa occupying diverse ecological niches points to the existence of a complex food web (Supplementary Figs 5B and 7). As in the Chengjiang biota [22], the fossil community of the Linyi biota was dominated by epifaunal organisms (trilobites, chelicerate arthropods, lophophorates and sponges), though nektonic arthropods (radiodonts and bivalved arthropods) also seem to have played important roles. Predators account for ∼25% of the species, a proportion similar to that of the Burgess Shale [23] but slightly less than that of the Chengjiang biota.

Arthropods
Trilobites, the most common arthropods, are represented by four species in four genera (Fig. 3F, Supplementary Figs 1 and 2F). Hundreds of complete trilobites have been collected, and some of them show exceptional preservation of portions of the digestive system ( Fig. 3F and Supplementary  Fig. 1B) [24]. The less abundant agnostoids are represented exclusively by Ammagnostus laiwuwnsis (Supplementary Fig. 2E).
The chelicerates are represented by two mollisoniid genera, Thelxiope and Mollisonia. Thelxiope is a poorly known arthropod characterized by welldeveloped spines on the dorsal exoskeleton. Previously, this rare genus comprised four species collectively represented by fewer than 10 specimens from Laurentia and West Gondwana [25]. The most distinctive species, T. spinosa, is represented by a single specimen from the Wheeler Formation of Utah [25,26]. The single known specimen of T. spinosa from Sikou ( Fig. 3A and B) represents the first occurrence of this species outside of Laurentia, and it preserves obvious soft tissue. T. tangi sp. nov. from the Linyi Lagerstätte preserves cephalic gnathobases with teeth that are differentiated antero-posteriorly ( Fig. 3C-E and Supplementary Fig. 4, also see Supplementary Data). The discovery of Thelxiope in the Linyi Lagerstätte expands the known diversity, disparity and palaeogeographical distribution of this rare arthropod. The complete specimen of Mollisonia from Sikou can be assigned to the type species M. symmetrica (Fig. 3G), and it represents the first discovery of this genus in North China. Isolated gnathobases of chelicerate-like taxa have also been found in Linyi (Supplementary Fig. 2C and D). These specimens display homogeneous teeth on the masticatory margin, an arrangement that is different from that of Habelia and Sidneyia from the Burgess Shale and from that of Wisangocaris from the Emu Bay Shale.
Radiodonts are also common. The hurdiid Cordaticaris striatus, the most common non-trilobite arthropod in the Linyi Lagerstätte, exhibits a heartshaped central element and frontal appendages equipped with at least seven extremely long bladelike endites (Fig. 4A-E). This species is thought to be intermediate in feeding mode between pure sediment sifters and suspension feeders [18]. Two frontal appendages of an amplectobeluid (Fig. 4F and Supplementary Fig. 2I) have not yet been assigned to a genus. These two fossils increase the known disparity and geographic range of the amplectobeluids, and make North China the third region outside of South China and Laurentia where this group has been found [26]. Also present are the cosmopolitan bivalved arthropods Isoxys and Tuzoia. The commonest of these is I. shandongensis, which was the first species to be described from the Linyi Lagerstätte [27]; one specimen of this arthropod preserves appendages and a pair of eyes ( Fig. 3H and I). Tuzoia is represented by an incomplete specimen of T. cf. manchuriensis (Supplementary Fig. 3I). Finally, a single specimen of an incomplete trunk bearing reniform digestive glands with ramified diverticula (Supplementary Fig. 2A and B), together with another, incomplete arthropod with at least 10 segments, suggest the presence of additional new arthropod taxa in the Linyi Lagerstätte ( Supplementary Fig. 3C).

Other groups
Animals other than arthropods are also abundant in the Linyi Lagerstätte, with sponges being the sec-ond most diverse group. Some of the sponges are here provisionally assigned to the genera Diagoniella, Halichondrites, Hydnodictya and ?Palaeosaccus, one new protospongiid genus, one indeterminate reticulosan and one possible aspicular sponge ( Fig. 5I and Supplementary Fig. 3H). Diagoniella is present in many other Miaolingian lagerstätten, but the two indeterminate protospongiid sponges may represent new taxa.
Chancelloriids are (Fig. 5H) represented by major sclerites resembling those of Allonnia, but there are also sclerites possibly bearing four main rays like those in Archiasterella. Therefore, we provisionally identify the chancelloriids as ?Allonnia.
Possible Selkirkia tubes are not rare, but only a few specimens preserve relic soft parts ( Fig. 5F and G). The large tubes have nearly parallel sides and are somewhat similar to S. spencei from the Spence Shale. Also, the anterior coiled gut in some specimens is similar to that of Paraselkirkia from the Chengjiang biota. Still, until a definitive proboscis is found the identity of these tubes will remain uncertain.
Brachiopods and hyoliths make up 67% of the total number of collected specimens, with brachiopods alone making up 50% of the total (Supplementary   5A). However, the diversity of these two taxa is very low, with just one species in each group having been identified thus far (Supplementary Fig. 3E). Some specimens of the hyolith Novakotheca weifangensis preserve relic soft tissue including the helens and digestive tract (Fig. 5A and Supplementary  Figs 2G and 3J).
Problematica are represented by medusiform (Supplementary Fig. 3F) and vermiform animals. Some of the vermiform fossils bear seriated transverse rings and an obvious digestive system (Fig. 5C and Supplementary Figs 2H and 3A), while others display a well-defined long pedicle and discoidal holdfast ( Fig. 5D and E). Some display a posterior structure (Supplementary Fig. 3B) reminiscent of that of archaic hemichordates such as Gyaltsenglossus and Spartobranchus from the Burgess Shale. A single specimen (Fig. 5B) bearing several rows of long bris-tles can be interpreted as an unknown polychaete. Exactly how many species all of the foregoing incomplete specimens represent is unknown at present.
Algae and trace fossils are abundant and occur in most beds ( Supplementary Fig. 2K) [28]. Some hyolith-bearing coprolites (Supplementary Fig. 3G) are strikingly similar to elliptical aggregates described from the Chengjiang biota; these structures may have been produced by epibenthic predators [29].

Taphonomy
Like other typical BST lagerstätten [30,31], fossiliferous strata in the Linyi Lagerstätte consist of stacked couplets of thin event and background mudstone beds (Fig. 2E). The 1-mm-thick background beds yield abundant but poorly preserved shelly fossils, mostly trilobites, brachiopods and hyolithids. In contrast, the 1-to 10-mm-thick event beds contain exquisitely preserved soft-bodied organisms.
The Linyi fossils are preserved as dark-colored carbonaceous films (Supplementary Fig. 6), a major taphonomic pathway shared with other BST deposits worldwide [32]. In addition to enrichment in carbon, elemental mapping has also revealed the presence of iron in a reddish-colored worm specimen ( Supplementary Fig. 6C). Micrographs showed that the iron was derived from the oxidation of pyrite. The preservational fidelity of typical BST fossils is high and includes the eye in Isoxys (Fig. 3H), limbs and digestive system in Thelxiope and the 'great appendage' arthropod ( Fig. 3A-E, and Supplementary Fig. 2A-D), and the gut in Changqingia (Fig. 3F), Maotunia (Supplementary Fig. 1B and figures in [29]), Novakotheca ( Fig. 5A and Supplementary Figs 2G and 3J), Thelxiope spinosa (Fig. 3A) and Selkirkia (Fig. 5F). In short, the well-preserved fossils of the Linyi Lagerstätte promise to yield new anatomical data relating to the early evolution of animals.

DISCUSSION
Current understanding of metazoan diversity and evolutionary faunas following the Cambrian explosion is based primarily on localities in South China and Laurentia, especially the Chengjiang and Burgess Shale lagerstätten. To be sure, Cambrian soft-bodied fossils have been found in other places [33,34], but only the Emu Bay Shale (Stage 4) in East Gondwana and the Sinsk Formation in Siberia (Stage 4) exhibit a preservational fidelity and taxonomic diversity [35,36] comparable to those of the lagerstätten of South China and Laurentia (Fig. 1). This uneven spatial distribution is especially apparent in the middle Cambrian: BST fossils are available for most of the Miaolingian period, but with the exception of the Kaili biota in South China (earliest Wiliuan) [37], Miaolingian lagerstätten are known exclusively from the Spence Shale Member, Burgess Shale, and Wheeler, Marjum and Weeks formations in North America [10][11][12][13]26] (Fig. 1).
The limited known spatial distribution of Cambrian lagerstätten thus underscores the importance of the newly discovered Miaolingian Linyi Lagerstätte, which provides unique insights into the evolution and biogeography of Cambrian marine life. Several congeneric and even conspecific fossils are shared between the Linyi Lagerstätte and contemporaneous lagerstätte in Laurentia. Some of these taxa have been interpreted as cosmopolitan [38] or persistent taxa [39], while others, especially Thelxiope and Mollisonia, are rare even at their type localities [25]. The occurrence of T. spinosa and M. symmetrica in the Linyi Lagerstätte, and of Sidneyia and Cambroraster in the Upper Shale Member of the Mantou Formation [16,17], suggest a close relationship between the Miaolingian deposits of North China and those of Laurentia. This hypothesis is further supported by the results of cluster analysis, which show the Linyi Lagerstätte nested within the Laurentia group, next to the Burgess Shale (Fig. 6B). However, given the obvious differences between the Cambrian shelly faunas of North China and Laurentia [40], it remains unclear whether this pattern has any paleogeographic significance. Indeed, it is possible that middle Cambrian soft-bodied taxa exhibited no distinct biogeographic divisions, but further evaluation of this hypothesis will require additional data from other geographic units. Importantly, non-metric multidimensional scaling (nMDS) and network analyses of the major Cambrian lagerstätten suggest that the Linyi Lagerstätte may have provided a biogeographic link between East Gondwana and Laurentia ( Fig. 6A and C), a hypothesis that is further bolstered by recent paleomagnetic data [41]. However, it is unclear whether the Linyi Lagerstätte was situated adjacent to Laurentia or represents an independent transitional region between Laurentia and Gondwana.
The BST succession in North China consists of the Lower Shale Member BST assemblage (upper Cambrian Stage 4 to lower Wuliuan) [42][43][44] and the Upper Shale Member BST assemblage (uppermost Wuliuan) in the Mantou Formation [16,17,[45][46][47][48], and the Linyi Lagerstätte in the Panchegou Member (lower and middle Drumian) (Fig. 2B). Thus, North China is now an important region for investigating the early evolution of middle Cambrian animals, and its Miaolingian deposits have great potential for yielding additional exceptional biotas. Since the discovery of the Chengjiang biota in 1984, South China has gradually become the principal area for the study of early Cambrian lagerstätte. The discovery of the Linyi Lagerstätte may also open a new chapter in the study of middle Cambrian BST deposits in North China.   [21]. It crops out only in eastern Shandong Province (though probably in southeastern Liaoning Province as well) and is thought to have been deposited in a platform margin to outer shelf environment with scattered carbonate platform deposits [21]. At least five trilobite zones have been recognized in the Panchegou Member, from the lowermost Megagraulas coreanicus Zone to the uppermost Liopeishania lubrica Zone, which together correspond to most of the Drumian [21] (Fig. 2B). Fossils (n = 3023) were collected or counted in the Sikou section in localized excavations of four beds averaging 30 cm in thickness and 3 m 2 in area. All specimens are housed in the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGP).

Methods
Photographs were taken under crossed-polarized light using a Nikon D810 camera fitted with a Nikon AF-S Nikkor 105 mm lens. Back scattered electron (BSE) image capture and energy dispersive spectrometer (EDS) analysis were performed using a TESCAN MAIA 3 GMU field-emission scanning electron microscope. Images were processed using Adobe Photoshop to adjust tone, contrast and brightness. Sedimentological observations were performed on polished slabs.