A predatory bivalved euarthropod from the Cambrian (Stage 3) Xiaoshiba Lagerstätte, South China

Bivalved euarthropods represent a conspicuous component of exceptionally-preserved fossil biotas throughout the Lower Palaeozoic. However, most of these taxa are known from isolated valves, and thus there is a limited understanding of their morphological organization and palaeoecology in the context of early animal-dominated communities. The bivalved euarthropod Clypecaris serrata sp. nov., recovered from the Cambrian (Stage 3) Hongjingshao Formation in Kunming, southern China, is characterized by having a robust first pair of raptorial appendages that bear well-developed ventral-facing spines, paired dorsal spines on the trunk, and posteriorly oriented serrations on the anteroventral margins of both valves. The raptorial limbs of C. serrata were adapted for grasping prey employing a descending stroke for transporting it close the mouth, whereas the backwards-facing marginal serrations of the bivalved carapace may have helped to secure the food items during feeding. The new taxon offers novel insights on the morphology of the enigmatic genus Clypecaris, and indicates that the possession of paired dorsal spines is a diagnostic trait of the Family Clypecarididae within upper stem-group Euarthropoda. C. serrata evinces functional adaptations for an active predatory lifestyle within the context of Cambrian bivalved euarthropods, and contributes towards the better understanding of feeding diversity in early ecosystems.

Description. Complete individuals vary in sagittal length between 14-16 mm, and are consistently preserved flattened in oblique or dorsolateral view (Figs 1-3). The bivalved carapace covers ca. 50% of the trunk length (sag.), obscuring the morphology of the anterior body region (Figs 1A,H, 2A,C-E and 3B). The valves are approximately sub-oval in profile, and vary in size between 7-8 mm long (sag.) and 5-6 mm wide (transverse) between individuals (e.g. Figs 1A and 2E). The valves meet sagitally on the dorsal side of the trunk (Fig. 1A); the dorsal hinge represents approximately a third of the total carapace length (sag.), whereas the posterior rounded margin of the valves extend further posteriorly (Fig. 2E). The anteroventral margin of the valves is gently curved, and bears up to four short spines that confer a partially serrated appearance (Figs 1A,H, 2A,C-E and 3A). Each valve possesses a narrow elevated marginal rim (Figs 1A,H, 2C-E and 3A). The lateral eyes are bulbous and sit on flexible peduncles at the anterior end of the body ( Fig. 2A-C); the bivalved carapace covers the proximal portion of both eyestalks and anterior edge of the head (Fig. 4). The first pair of appendages is situated in close proximity to the eyes. Each of the first appendages consists of eight podomeres with a cylindrical profile (Figs 1D-F,H-J, 2A,B and 3A). The most proximal podomere observable is the broadest (trans.) and lacks any projections (Fig. 1D,E). The second to seventh podomeres carry well-developed ventral spines that become progressively reduced in length towards the distal end of the limbs. Most podomeres carry a single spine that originates from the antero-ventral edge, in close proximity to the anterior margin of the corresponding article ( Fig. 1D,E,I,J). The fifth podomere, however, differs in the possession of two spines instead of one. In all instances, the ventral spines are orientated at approximately 40-90 o relative to the main limb axis, facing towards the distal end of the limb in extended position (Fig. 4). The distal tip of the appendages -corresponding to the eighth podomere -is sub-conical and without spines. The articulated raptorial limbs evince considerable flexure in different specimens, indicating a broad range of motion (Figs 1A,D,E,H-J, 2A,B, 3AE and 4B). The proximal bases on the raptorial limbs are obscured by the bivalved carapace, and thus the precise organization at the anterior margin of the body is uncertain. The trunk has a sub-conical outline, and gently tapers towards the posterior end. The ring-like trunk tergites become more elongate (sag.) towards the posterior end (Figs 1A, 2A,C and 3B). Given that the carapace hinge is shorter than the length of the carapace, the trunk exposes a variable number of tergites ranging from some 13 (Fig. 2C) and up to more than 20 (Fig. 3B); approximately six or seven tergites are exposed dorsally on the anterior half of the trunk, each of these tergites bears a pair of delicate dorsal spines with a length of 1.5 mm (Figs 1A,B, 2C and 3B) that face postero-dorsally at an acute angle relative to the main body axis. Specimens preserved in oblique view demonstrate that each of the dorsal spines emerges from a rounded socket that is closely associated with the anterior edge of each of the trunk tergites (Fig. 3B,D). The anterior portion of the trunk is differentiated into a 'thoracic' region, in which each of the tergites bears a pair of delicate -possibly biramouslimbs that become progressively smaller towards the posterior end. The endopods have a slender construction; individual podomeres are not clearly visible (Figs 2C-E and 3B). Exopods cannot be clearly observed, with the exception of a single limb that is shorter and evinces a paddle-shaped outline (Fig. 3C). The last three trunk tergites are limbless, and form a discrete abdominal area (Figs 1A, 2A,D,E and 3B). The body terminates in a subconical telson that is longer (sag.) and narrower (trans.) than any of the preceding ring-like tergites (Figs 1A, 2A,C-E, 3B and 4A). An elongate pair of tail flukes (also referred to as 'cerci' , 'furcae' , 'rami' , 'uropods' , or 'tail processes' by different authors [15][16][17][18][19][20][21][22][23][24] ) emerges at the posterior end of the trunk; each tail fluke narrows distally Scientific RepoRts | 6:27709 | DOI: 10.1038/srep27709 into an acute tip, giving it an acuminate outline, and is orientated at approximately 30 o relative to the main body axis (Figs 1G and 2C-F). The tail flukes articulate with the posterior base of the conical telson, are free throughout their length, do not overlap basally, and display a discrete longitudinal ridge that defines the outer margin (Fig. 2F). The inner margins of the tail flukes bear numerous elongate setae that face posteriorly (Figs 1G and 2F). There is some variation in the dimension of the tail flukes in different specimens, particularly regarding their proximal width (compare Figs 1G and 2F). Although these differences most likely reflect some intraspecific variation within the population, such as sexual dimorphism or ontogeny, it is not possible to further elaborate given the limited number of specimens with preserved tails. The digestive tract is the only part of the internal anatomy preserved in the available fossils (Figs 1A,H, 2C-E and 3B). The gut consists of a simple tube, approximately 400-700 μ m wide (trans.), preserved with a distinctively three-dimensional profile. The presence of sediment in the gut is suggestive of early diagenetic permineralization and subsequent replacement by clay minerals, as Abbreviations: pdn, podomere number in raptorial appendages; dts, dorsal trunk spine; gut, digestive tract; ha, hinge articulation; lv, left valve; mr, marginal rim; ms, marginal spine; ra, raptorial appendage; rv, right valve; set, setae; tf, tail fluke; Tn, observable trunk tergites. posited for Chengjiang fossils 34 . Although the carapace obscures the anterior organization of the gut tract, the latter structure extends posteriorly into the telson, indicating that the anus is located terminally between the tail flukes ( Fig. 1A,G,H).

Comparisons with other Cambrian bivalved euarthropods.
Clypecaris serrata evinces similarities with several bivalved stem-group euarthropods known from Cambrian deposits (Figs 4 and 5A). The best comparison can be made with the Chengjiang euarthropod C. pteroidea 29,31 (Figs 3E and 5B). C. serrata closely resembles C. pteroidea in the overall shape and extent of trunk coverage of the bivalved carapace, the presence of paired stalked eyes, a tapering subconical trunk composed of ca. 20 ring-like tergites, slender trunk endopods, a limbless abdominal region consisting of three tergites plus a conical telson, paired non-overlapping acuminate tail flukes with longitudinal ridges and posteriorly facing setae, and simple tubular gut. New observations of C. pteroidea indicate the presence of paired dorsal sockets (Fig. 3E) -identical in their shape and distribution to those observed in C. serrata (Fig. 3B,D)-that imply the possession of similar spines to those observed the new taxon (Fig. 5B). The fundamental difference between both Clypecaris species is the possession of partially serrated anteroventral carapace margins in C. serrata (Figs 1A,C,H, 2A,C-E and 3A), whereas the valve margins of C. pteroidea are completely smooth (Fig. 3E). Given the incomplete preservation of the type material 29,31 , it is uncertain whether the first appendage pair of C. pteroidea had a raptorial construction as observed in C. serrata (Fig. 5A,B). Regardless of this complication, the close morphological parallels observed between C. serrata and C. pteroidea support their close phylogenetic relationship as members of Family Clypecarididae 29 . Both Clypecaris species somewhat resemble the bizarre euarthropod Erjiecaris minusculo 20 in terms of general appearance and body tergite count, and particularly in the possession of acuminate tail flukes that do not overlap proximally (Fig. 5C). Other aspects of the body organization are strikingly different however, as Erjiecaris is distinguished by a uniquely partially fused bivalved carapace with a broad triangular outline, sessile dorsal eyes, and the absence of longitudinal ridges or setae on the tail flukes 20 . Thus, Erjiecaris may be a close relative of Clypecaris, but definitely not a member of Clypecarididae.
Clypecaris species also share a broad similarity with the waptiids, a loosely defined group of Cambrian bivalved euarthropods whose main defining feature is the possession of a paddle-like tail composed of a pair of partially overlapping dorsoventrally flattened flukes with rounded margins (Fig. 5D-H). Clypecaris species resemble waptiids in the presence of a bivalved carapace that covers the anterior body region, paired stalked eyes, delicate endopods, and a limb-less abdominal area (compare Fig. 5A,B with Fig. 5D-H). However, whereas  waptiids have a paddle-like tail formed by dorsoventrally flattened flukes that overlap each other at their proximal bases (Fig. 5D-H), the flukes of C. serrata and C. pteroidea are elongate, do not overlap proximally, and bear numerous posterior-facing straight setae (Figs 1G, 2F and 5A,B). Some waptiids, such as Waptia fieldensis 30,[35][36][37] , Chuandianella ovata 31,38 and Pauloterminus spinodorsalis 39 are also distinguished by the possession of multiarticulated tail flukes with three podomeres (Fig. 5F-H); intriguingly, the multiarticulated tail flukes are lacking in Synophalos xynos 32 and Plenocaris plena 40 , which may inform on the distinction between these taxa and 'legitimate' waptiids. Waptiids are further distinguished from Clypecaris species by a trunk composed of fewer tergites, and the presence of an antenniform first appendage pair, as observed in Plenocaris 40 (Fig. 5E), Waptia 35,36 (Fig. 5H), and potentially also in Pauloterminus 39 (Fig. 5G). Comparisons with other Cambrian bivalved taxa are less phylogenetically informative, and mostly reflect symplesiomorphies of stem-group Euarthropoda. Both Clypecaris species broadly resemble Canadaspis perfecta 16,30 , Perspicaris recondita 15 and Perspicaris dictynna 15 in the possession of a carapace, stalked eyes and ring-like trunk tergites. However, these taxa differ from Clypecaris in having a more robust overall construction, antenniform first appendages with small paired setae on each podomere, a longer dorsal hinge, more elongate (sag.) valves, small marginal spines on the abdominal tergites borders, and tail flukes with setae on both the inner and outer margins 15,16,41,42 . Other relevant bivalved taxa include Branchiocaris pretiosa 41,43 , Odaraia alata 17,41,44 , Pectocaris spatiosa 29 , Jugatacaris agilis 18 , Nereocaris exilis 19 , Nereocaris briggsi 21 , and Loricicaris spinocaudatus 21 . These comparatively larger bivalved euarthropods are mainly distinguished from Clypecaris in the broader coverage of the carapace, and a body composed of dozens of trunk tergites, among other discrepancies in terms of head organization (e.g. anterior sclerite 44 ) and posterior termination (e.g. morphology of tail flukes 21 ). Among these bivalved stem-group euarthropods, the presence of a hook-like anteroventral process in the valves of Nereocaris 19,21 evocates the serrated margin of C. serrata (Figs 1A,C,H, 2A,C-E and 3A); however, the lack of additional derived characters uniting these taxa suggests that the presence of valve hooks/serrations in these taxa is convergent.
The raptorial first appendage pair arguably represents one of the most distinctive characters of C. serrata (Figs 1D-F,H-J, 2A,B and 3A). Raptorial limbs are rare among bivalved stem-group euarthropods, as the first pair of limbs is generally expressed as a pair of uniramous sensorial antennae with several podomeres 8,21,35,36 (Fig. 5). Occacaris oviformis and Forfexicaris valida both from the Chengjiang biota, are among the few Cambrian bivalved taxa with raptorial anterior appendages 29,31 . However, the limbs of Occacaris and Forfexicaris differ from C. serrata in that only two or four podomeres bear spines, and these are orientated towards the dorsal side instead of ventrally. These characteristics reflect a different functional morphology, even if the basic premise of grasping food items is similar (Fig. 4B). Although Branchiocaris has been described as a possessing a set of raptorial appendages 8,21,41,45 , these limbs lack spines, do not flex ventrally, and originate from a different segment altogether (i.e. second appendage pair). The only bivalved stem-group euarthropods that consistently display a raptorial first appendage are Isoxys [22][23][24] and Surusicaris 46 . In these cases, however, the spine-bearing raptorial limbs are rotated such that they bend following an ascending motion. Thus, the broad functional similarities between the raptorial limbs of C. serrata relative to those of Isoxys and Surusicaris are best regarded as cases of convergent evolution. Raptorial limbs with multiple podomeres bearing ventral-facing spines are also observed in more distant total-group euarthropods, such as the radiodontans. The raptorial limbs of C. serrata resemble the radiodontan frontal appendages in terms of their overall construction and functional morphology. In particular, the presence of ventral facing spines with an anterior orientation in C. serrata is reminiscent of the spine construction in the radiodontans Hurdia, Laggania and Amplectobelua 47 . The frontal appendages of radiodontants differ greatly in terms of their podomere count and patterns of spine organization 46,47 , as well as their segmental origin from the protocerebral segment 1 , and thus their similarities with C. serrata are best regarded as a result of their common function.

Discussion
Phylogenetic affinities. The presence of widespread body sclerotization, complete appendage arthropodization, and stalked lateral eyes followed posteriorly by the raptorial first appendage pair indicate that Clypecaris serrata can be reliably interpreted as a member of scion Deuteropoda (i.e. upper stem-group Euarthropoda + crown-group Euarthropoda; see ref. 1). Assigning the new taxon to a particular lineage, however, is more problematic. The appearance of C. serrata -and more broadly that of Cambrian bivalved forms (Fig. 5)superficially resembles several carapace-bearing pancrustaceans, for example branchiopods and malacostracans. Indeed, early studies discussed Cambrian bivalved euarthropods in this general context 15,16,29,43,48 , and recent accounts have even argued that some of these taxa -such as waptiids -may be nested within the mandibulate crown-group 35,36 . The bivalved carapace of C. serrata obscures critical features of the anterior organizationparticularly the structure of the post-oral appendages -and the lack of detailed post-cephalic appendicular data encumbers specific comparisons with members of crown-group Euarthropoda. In the absence of fine morphological detail, the similarities with bivalved Cambrian stem-group euarthropods represent the most reliable indicators for the affinities of C. serrata, and suggest that the new taxon is most likely a member of upper stem-group Euarthropoda (see topologies in refs. 1,12,21,45) (Fig. 6). Rather problematically, the phylogenetic position of C. serrata cannot be established more accurately, as C. pteroidea and waptiids have been consistently omitted from recent phylogenetic studies of Palaeozoic euarthropods 3,5,19,21 . Within upper stem-group Euarthropoda, bivalved forms with elongate bodies composed of numerous (commonly more than 30) short ring-like tergites (e.g. Branchiocaris 43 , Odaraia 17 , Pectocaris 29 , Nereocaris 21 , Jugatacaris 18 ) have been consistently resolved as basal members of this lineage. If the presence of an elongate body with short tergites reflects a symplesiomorphic state among bivalved euarthropods as suggested by recent topologies 19,21 , the body organization of Clypecarididae would support a position closer to the euarthropod crown-group (Fig. 6). Following this logic, waptiids could potentially occupy an even more crownwards position relative to Clypecarididae given their apparently lower tergite count 32,35,36,39,40 ; however, the precise relationships between the waptiids (Fig. 5D-H) and clypecaridids, including C. serrata, remain an open question pending a comprehensive revision of the phylogenetic of these extinct organisms.
Functional morphology and palaeoecology. Clypecaris serrata features a distinctive combination of morphological adaptations that point towards an active predatory lifestyle (Fig. 4) the most striking of which is the structure of the first appendage pair. The presence of ventral-facing spines on most of the podomeres (Fig. 1A,D-F,I-J), coupled with the robust construction of these limbs relative to the trunk endopods (Figs 2D and 3B), indicate that they were adapted for a grasping function. The first appendages in C. serrata occupy the typical position of the deutocerebral limb pair in upper stem-group euarthropods 1,8,42 , and thus imply that these appendages had a pre-oral site of attachment to the body. The raptorial limbs would have operated by Scientific RepoRts | 6:27709 | DOI: 10.1038/srep27709 performing a downward stroke that brought the ventral-facing spines together, grasping the prey and bringing it to close proximity of the mouth (Fig. 4B). The construction of the raptorial limbs in C. serrata suggests that they worked in a similar way to the arthropodized frontal appendages of radiodontans (e.g. Anomalocaris, Laggania, Hurdia), as the latter also bear ventral facing spines that are used for grasping prey and bringing it close to the mouth opening 47,[49][50][51] . The anteroventral position of the valve serrations in C. serrata also suggests their potential involvement in feeding. The acute end of the serrations faces posteriorly, and thus follows the orientation of the ventral spines in the raptorial appendages. We hypothesize that the serrations may have worked in tandem with the spine-bearing limbs to secure the prey close to the mouth during capture and feeding (Fig. 4B), which would imply that C. serrata sought after highly mobile prey that required to be forcibly immobilized prior to consumption. An alternative interpretation of the valve serrations of C. serrata as having a defensive function seems less likely, as the acute projections are rather short and would not effectively protect the body unless the animal was specifically attacked from the underside. Collectively, the available evidence suggests a specialized suite of adaptations for feeding, and tentatively offer novel insights into the otherwise limited understanding of Cambrian bivalved euarthropod palaeoecology. The interpretation of C. serrata as an active predator is consistent with its overall body construction, including mobile stalked eyes, delicate endopods and well-developed tail flukes with setae, which suggests that it had a primarily nektobenthic habitus. Finally, the presence of long paired dorsal spines on C. serrata, and strongly suggested in C. pteroidea based on the presence of paired dorsal sockets (Fig. 3E), is unique among Cambrian bivalved euarthropods (Fig. 5), and most likely served as a defensive mechanism against larger predators.

Ecological implications. Investigations on the palaeobiology of the Xiaoshiba Konservat-Lagerstätten
have yielded soft-bodied organisms with diverse palaeoecologies, including the sessile tube-dwelling worm Selkirkia sinica 52 , epibenthic mollusc-like animal Wiwaxia foliosa 25 , suspension feeding lobopodian Collinsium ciliosum 26 , and deposit feeding euarthropods (e.g. fuxianhuiids and trilobites) 8,27 . The recognition of an active nektobenthic predatory mode life for Clypecaris serrata reveals a previously unnoticed ecological niche for the Xiaoshiba biota, and thus contributes towards a more complete understanding of the multi-tiered community structure preserved in this important early Cambrian deposit. In a broader context, C. serrata reflects a greater diversity of feeding strategies explored by Cambrian bivalved euarthropods than previously considered. With the exception of Isoxys 23,24 and Surusicaris 46 , most Cambrian bivalved forms have been tentatively regarded as either deposit or filter feeders 18,19,21,29 , or are too poorly known to gain significant insights about their autoecology. The predatory mode of life in C. serrata adds up to recent findings indicating that some Cambrian euarthropods explored niches that deviated from the palaeoecology of their close relatives, as also exemplified by the discovery of suspension/filter feeding-radiodontans 53,54 .

Materials and Methods
Eleven specimens assigned to Clypecaris serrata sp. nov. were collected from the lowermost part of Hongjinshao Formation (Cambrian Stage 3) in eastern Kunming, China, where many exquisitely preserved fossils known as the Xiaoshiba Lagerstätten have been reported. According to the co-occurring trilobites, the fossil assemblage is within the uppermost part of the Qiongzhusian Stage 25 , existing approximately 515 million years ago. All specimens dealt with in this study are housed in the Key Laboratory for Palaeobiology, Yunnan University (YKLP).
Specimens were photographed by using a Leica M205C photomicroscope. All images were processed in Adobe Photoshop CS 4. Some of these digital photographs are accompanied by interpretative drawings to assist the interpretation of key features.