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Feeding Strategy and Locomotion of Cambrian Hyolithides

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Feeding Strategy and Locomotion of Cambrian Hyolithides Available online at www.sciencedirect.com ScienceDirect Palaeoworld 27 (2018) 334–342 Feeding strategy and locomotion of Cambrian hyolithides a,∗ a b c,d b Hai-Jing Sun , Fang-Chen Zhao , Rong-Qin Wen , Han Zeng , Jin Peng a State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China b Resources and Environmental Engineering College, Guizhou University, Guiyang 550025, China c College of Earth Sciences, University of Chinese Academy of Sciences, No. 19 Yuquan Road, Beijing 100049, China d Department of Paleobiology, National Museum of Natural History, P.O. Box 37012, MRC-121, Washington, DC 20013-7012, USA Received 7 November 2017; received in revised form 8 March 2018; accepted 26 March 2018 Available online 3 April 2018 Abstract The Chengjiang (Cambrian Stage 3) and Balang (Cambrian Stage 4) Konservat-Lagerstätten of South China have produced abundant hyolithide hyoliths; however, little attention has been paid to their feeding strategy and the role it played in the ecosystem. Hyolithides preserved in coprolites from the Chengjiang Biota and associated with a Tuzoia carcass from the Balang Fauna reveal the fluid feces consuming and scavenging strategies of this group. Size distribution of hyolithides demonstrates that their dietary habit is ontogenetically dependent, with juveniles having ingested organic-rich material whereas adult food consumption was more likely by a variety of species-dependent methods The first discovery of hyolithides in association with locomotion traces and burrows indicates they were not only epibenthic vagrants, but also shallow horizontal burrowers. The new discoveries reported herein enhance our understanding of the feeding strategy and other behaviours of Cambrian hyolithides. © 2018 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. Keywords: Hyolithides; Feeding habit; Trace fossil; Cambrian; Chengjiang Biota; Balang Fauna 1. Introduction quently appear in the gut remains or coprolites of predators as an important food item (Chen et al., 1996; Chen and Li, 1997; Chen, Extensive study of exceptionally preserved Cambrian 2004; Vannier and Chen, 2005). Although both qualitative and Burgess Shale-type biotas offers deep insights into the trophic quantitative analyses have been applied to the Chengjiang Biota relationships of early life and permits further reconstruction to reconstruct the ecosystem and trophic links among animals of their ecosystems (Dunne et al., 2008; Vannier, 2012). The (Hu, 2005; Vannier and Chen, 2005; Zhao et al., 2010, 2012, Chengjiang Biota (Cambrian Stage 3) in Yunnan Province and 2014), little attention has been paid to the feeding behaviours the Balang Fauna (Cambrian Stage 4) in Guizhou Province, of the hyoliths (Chen, 2004; Vannier and Chen, 2005), and the South China, are two of the contributors to our understanding role that they played in the ecosystem has long been overlooked. of Cambrian animals and their interactions. Hyoliths are one of Similarly, with respect to the hyoliths in the Balang Fauna, only the most numerous and diverse biomineralising animals during limited work has focused on the dietary habit of the hyolithides the Cambrian, and ranged throughout the Paleozoic until their (Sun et al., 2016) and their biological associations with other Permian extinction. Hyolithides, as one of the main epifaunal animals (Sun et al., 2017). Definitive traces produced by these groups, are abundant in the Chengjiang and Balang lagerstätten animals have remained undocumented until now. (Peng et al., 2005; Zhao et al., 2010, 2012, 2014), and they fre- Our report focuses on three groups of specimens, two from the Chengjiang Biota containing hyolithides that we assign to ‘Ambrolinevitus’ ventricosus Qian and the other from the Balang ∗ Fauna that consists of indeterminate individuals. The former two Corresponding author at: State Key Laboratory of Palaeobiology and Stratig- are concentrated in fecal deposits, and one of them was described raphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, earlier by Chen (2004) and Vannier and Chen (2005). The latter China. from the Balang Fauna consists of individuals located on and E-mail address: [email protected] (H.J. Sun). https://doi.org/10.1016/j.palwor.2018.03.003 1871-174X/© 2018 Elsevier Ireland Ltd Elsevier B.V. and Nanjing Institute of Geology and Palaeontology, CAS. Published by Elsevier B.V. All rights reserved. H.J. Sun et al. / Palaeoworld 27 (2018) 334–342 335 around a Tuzoia sp. carcass. These specimens allow us to make 2010; Hu et al., 2013; Botting et al., 2015; Martí Mus, 2016; new interpretations concerning the feeding strategies and other Zhu et al., 2016), and rarely preserved in three dimensions behaviours of hyolithides, and provide additional details regard- (Sun et al., 2016). Because of inadequate preservation of the ing the flow of energy within the ecosystem from the perspective hyolithide gut, the feeding habit of these organisms remained of hyolithide hyoliths. In addition, we provide the first report of largely speculative, and no detailed comparison of feeding traces of hyolithide locomotion and horizontal burrowing. habit between hyolithides and orthothecids was possible. The hyolithides, with their slow and limited locomotion, were ear- 2. Material and methods lier interpreted as generalized omnivores, including deposit or detritus feeders (Runnegar et al., 1975; Marek and Yochelson, The hyoliths from the Chengjiang Biota are preserved in 1976; Dzik, 1980), filter feeders (Runnegar et al., 1975), and yellowish-green claystones from the Maotianshan Member of possible grazers (Marek and Yochelson, 1976). Subsequently, the Yu’anshan Formation in Shankou Village of Anning County serial discoveries of epibionts (bryozoans and tubular corals) and Ma’anshan Village of Chengjiang County, Yunnan Province, that lived only on the conchs of hyolithides (Marek and Galle, China. Trilobites associated with these individuals are indica- 1976; Malinky, 1990, 2006; Galle and Plusquellec, 2002; Galle tive of the Eoredlichia-Wutingaspis Zone (Steiner et al., 2001), and Parsley, 2005) indicated that the hyolithides were rheophylic which correlates with unnamed Cambrian Series 2 Stage 3 organisms and low level filter feeders (Marek et al., 1997). How- (Zhao et al., 2012). A specimen from the Balang Fauna is ever, the hyolithide Haplophrentis reesei Babcock and Robison, preserved in greenish-grey mudstone of the Balang Formation 1988 from the middle Cambrian Spence Shale with its incom- in the Wenglingtang section in Kaili City, Guizhou Province, plete gut (central string) filled with sediments was regarded China, which lies within the Arthricocephalus chauveaui Zone. as a deposit feeder (Babcock and Robison, 1988). An excep- This zone correlates with unnamed Cambrian Series 2 Stage 4 tionally preserved simple U-shaped and sediment-free gut of (Yan et al., 2014). For detailed geographical, stratigraphical, and a hyolithide was illustrated by Butterfield (2001, 2003) from depositional information on these sections see Zhu et al. (2001), the middle Cambrian Mount Cap Formation and interpreted Peng et al. (2005), Zhao et al. (2012) and Sun et al. (2017). Spec- by him as evidence for a suspension-feeding habit (Butterfield, imens discussed in this report are housed in the Nanjing Institute 2001). In contrast, a hyolithide reported from the early Cambrian of Geology and Palaeontology, Chinese Academy of Sciences Chengjiang Biota with a complex folded and sediment-filled ali- (specimens with prefixes SK and NIGPAS); and the palaeonto- mentary tract was interpreted as herbivore or sediment feeder logical collection of Guizhou University (specimen with prefix (Chen, 2004). Recently, two hyolithides from the base of the KW). Cambrian Emigrant Formation, USA and the Balang Formation, Our material was examined and imaged by the standard light China were reported as having a three dimensionally preserved microscopy, SU3500 Scanning Electron Microscope (SEM) gut consisting of a spiral intestine wound about a nearly straight with Electron Dispersive X-ray (EDX), digital macrophotogra- rectum (Sun et al., 2016). These specimens support the deposit or phy [Nikon D300S with an AF-S Micro Nikkor 105 mm f/2.8G detritus-feeding habit of hyolithides as suggested earlier (Marek lens], and a Carl Zeiss SteREO Discovery V12 microscope and Yochelson, 1976; Babcock and Robison, 1988; Chen, 2004). linked to an AxioCam HR3 digital microscope CCD camera. A subsequently discovered hyolithide that has an exception- Photographs were stacked and rendered using Adobe Photoshop ally preserved gut possessing an oesophagus, a central tube, CS6 and CorelDraw X4 softwares. and lateral winding fecal string was described from the Ordovi- cian Fezouata Konservat-Lagerstätte of Morocco by Martí Mus 3. Previous work on feeding habit of hyolithide hyoliths (2016). The illustrated tentacled mouth of that specimen was reconstructed as a generalized organ to adapt to suspension- The group Hyolitha is usually divided into two subgroups: detritus-deposit feeding spectrum (Martí Mus, 2016). The more orthothecides and hyolithides. The skeleton of the former con- recently described tentacled Haplophrentis with a U-shaped gut sists of a conical shell and a planar-retractable operculum, from the
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