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Exceptionally preserved hyolithids from the middle Cambrian of North China

Published online by Cambridge University Press:  30 June 2021

Haijing Sun Open the ORCID record for Haijing Sun [Opens in a new window] ,
Zhixin Sun  and
Fangchen Zhao Open the ORCID record for Fangchen Zhao [Opens in a new window]
Haijing Sun*
Affiliation:
State Key Laboratory of Isotope Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou510640, China CAS Centre for Excellence in Deep Earth Science, Guangzhou510640, China State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Centre for Excellence in Life and Palaeoenvironment, Chinese Academy of Sciences, Nanjing210008, China
Zhixin Sun
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Centre for Excellence in Life and Palaeoenvironment, Chinese Academy of Sciences, Nanjing210008, China University of Chinese Academy of Sciences, Beijing100049, China
Fangchen Zhao
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Centre for Excellence in Life and Palaeoenvironment, Chinese Academy of Sciences, Nanjing210008, China University of Chinese Academy of Sciences, Beijing100049, China
*
Author for correspondence: Haijing Sun, Email: [email protected]
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Abstract

Hyoliths are extinct enigmatic organisms of early lophotrochozoan affinity known globally from the Palaeozoic Era and were especially diverse and abundant in the Cambrian Period. However, the commonly incomplete preservation of hyolith exoskeletons and our limited knowledge of their soft anatomy makes their ecological and biological aspects unclear. Konservat-Lagerstätte are crucial windows to unlock the mysteries of hyoliths. Here we report a new occurrence of exceptionally preserved hyolithid hyoliths from the middle Cambrian Mantou Formation (Miaolingian, Wuliuan) in Shandong Province, North China. The preserved soft organs of the new species Novakotheca weifangensis sp. nov. include a U-shaped gut and possible pharynx, oesophagus, stomach and digestive gland, which provide significant new information for the reconstruction of the digestive system of hyolithids. Two taphonomic modes of hyoliths described herein are recognized: soft tissue preservation through pyritization and three-dimensional shell preservation through phosphatization. Morphological variations due to different preservational pathways in the same species are revealed, highlighting the taphonomic bias on taxonomy. The ecological association between hyoliths and small brachiopod epibionts is a direct example of species interactions, providing insights into the ecological structures and adaptability of early animals during Cambrian time.

Keywords

Hyolithasoft anatomytaphonomyepibiont associationBurgess Shale-type Lagerstätte
Type
Original Article
Information
Geological Magazine , Volume 158 , Issue 11 , November 2021 , pp. 1951 - 1959
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Allison, PA and Bottjer, DJ (2011) Taphonomy: Process and Bias Through Time (Second Edition). Dortrecht: Springer.CrossRefGoogle Scholar
Babcock, LE and Robison, RA (1988) Taxonomy and paleobiology of some Middle Cambrian Scenella (Cnidaria) and hyolithids (Mollusca) from western North America. The University of Kansas Paleontological Contributions 121, 1–22.Google Scholar
Butterfield, NJ (2001) Cambrian food webs. In Palaeobiology II (eds Briggs, DEG and Crowther, PR), pp. 40–3. Oxford: Blackwell Science.CrossRefGoogle Scholar
Butterfield, NJ (2003) Exceptional fossil preservation and the Cambrian Explosion. Integrative and Comparative Biology 43, 166–77.CrossRefGoogle ScholarPubMed
Chen, JY (2004) The Dawn of Animal World. Nanjing: Jiangsu Science and Technology Press (in Chinese).Google Scholar
Chen, X, Zhao, Y and Wang, P (2003) Preliminary research on hyolithids from the Kaili Biota, Guizhou. Acta Micropalaeontologica Sinica 20, 296–302 (in Chinese with English abstract).Google Scholar
Creveling, JR, Knoll, AH and Johnston, DT (2014) Taphonomy of Cambrian phosphatic small shelly fossils. Palaios 29, 295–308.CrossRefGoogle Scholar
Delaney, ML (1998) Phosphorus accumulation in marine sediments and the oceanic phosphorus cycle. Global Biogeochemical Cycles 12, 563–72.CrossRefGoogle Scholar
Devaere, L, Clausen, S, Alvaro, JJ, Peel, JS and Vachard, D (2014) Terreneuvian orthothecid (Hyolitha) digestive tracts from northern Montagne Noire, France; taphonomic, ontogenetic and phylogenetic implications. PLoS One 9, e88583. doi: 10.1371/journal.pone.0088583.CrossRefGoogle ScholarPubMed
Dornbos, SQ, Bottjer, DJ, Chen, JY, Gao, F, Oliveri, P and Li, CW (2006) Environmental controls on the taphonomy of phosphatized animals and animal embryos from the Neoproterozoic Doushantuo Formation, Southwest China. Palaios 21, 3–14.CrossRefGoogle Scholar
Farrell, ÚC (2014) Pyritization of soft tissues in the fossil record: an overview. The Paleontological Society Papers 20, 35–58.CrossRefGoogle Scholar
Farrell, ÚC, Briggs, DEG, Hammarlund, EU, Sperling, EA and Gaines, RR (2013) Paleoredox and pyritization of soft-bodied fossils in the Ordovician Frankfort Shale of New York. American Journal of Science 313, 452–89.CrossRefGoogle Scholar
Forchielli, A, Steiner, M, Kasbohm, J, Hu, S and Keupp, H (2014) Taphonomic traits of clay-hosted early Cambrian Burgess Shale-type fossil Lagerstätten in South China. Palaeogeography, Palaeoclimatology, Palaeoecology 398, 59–85.CrossRefGoogle Scholar
Gaines, RR, Briggs, DEG and Zhao, Y (2008) Cambrian Burgess Shale-type deposits share a common mode of fossilization. Geology 36, 755.CrossRefGoogle Scholar
Galle, A and Parsley, RL (2005) Epibiont relationships on hyolithids demonstrated by Ordovician trepostomes (Bryozoa) and Devonian tabulates (Anthozoa). Bulletin of Geosciences 80, 125–38.Google Scholar
Galle, A and Plusquellec, Y (2002) Systematics, morphology, and paleobiogeography of Lower Devonian tabulate coral epibionts: Hyostragulidae fam. nov. on hyolithids. Coral Research Bulletin 7, 53–64.Google Scholar
Houbrick, RS, Stürmer, W and Yochelson, EL (1988) Rare mollusca from the Lower Devonian Hunsrück Slate of southern Germany. Lethaia 21, 395–402.CrossRefGoogle Scholar
Hughes, NC (1995) Trilobite taphonomy and taxonomy: a problem and some implications. Palaios 10, 283–5.CrossRefGoogle Scholar
Kammerer, CF, Deutsch, M, Lungmus, JK and Angielczyk, KD (2020) Effects of taphonomic deformation on geometric morphometric analysis of fossils: a study using the dicynodont Diictodon feliceps (Therapsida, Anomodontia). PeerJ 8, e9925. doi: 10.7717/peerj.9925.CrossRefGoogle Scholar
Li, LY, Skovsted, CB, Yun, H, Betts, MJ and Zhang, XL (2020) New insight into the soft anatomy and shell microstructures of early Cambrian orthothecids (Hyolitha). Proceedings of the Royal Society B: Biological Sciences 287, 20201467. doi: 10.1098/rspb.2020.1467.CrossRefGoogle Scholar
Li, LY, Zhang, XL, Skovsted, CB, Yun, H, Pan, B and Li, GX (2019) Homologous shell microstructures in Cambrian hyoliths and molluscs. Palaeontology 62, 515–32.CrossRefGoogle Scholar
Li, GX, Zhu, MY, Steiner, M and Qian, Y (2004) Skeletal faunas from the Qiongzhusian of southern Shaanxi: biodiversity and lithofacies-biofacies links in the Lower Cambrian carbonate settings. Progress in Natural Science 14, 92–6.CrossRefGoogle Scholar
Liu, F, Skovsted, CB, Topper, TP and Zhang, ZF (2020a) Revision of Triplicatella (Orthothecida, Hyolitha) with preserved digestive tracts from the early Cambrian Chengjiang Lagerstätte, South China. Historical Biology, published online 21 April 2020. doi: 10.1080/08912963.2020.1747059.CrossRefGoogle Scholar
Liu, F, Skovsted, CB, Topper, TP and Zhang, ZF (2021) Soft part preservation in hyolithids from the lower Cambrian (Stage 4) Guanshan Biota of South China and its implications. Palaeogeography, Palaeoclimatology, Palaeoecology 562, 110079. doi: 10.1016/j.palaeo.2020.110079.CrossRefGoogle Scholar
Liu, F, Skovsted, CB, Topper, TP, Zhang, ZF and Shu, DG (2020b) Are hyoliths Palaeozoic lophophorates? National Science Review 7, 453–69.CrossRefGoogle ScholarPubMed
Lobo-da-Cunha, A (2019) Structure and function of the digestive system in molluscs. Cell and Tissue Research 377, 475–503.CrossRefGoogle ScholarPubMed
Malinky, JM (1990) Early and Middle Cambrian Hyolitha (Mollusca) from Northeastern China. Journal of Paleontology 64, 228–40.CrossRefGoogle Scholar
Malinky, JM (2003) Ordovician and Silurian hyoliths and gastropods reassigned from the Hyolitha from the Girvan district, Scotland. Journal of Paleontology 77, 625–45.2.0.CO;2>CrossRefGoogle Scholar
Malinky, JM (2006) Revision of Hyolitha from the Ordovician of Estonia. Paläontologische Zeitschrift 80, 88–106.CrossRefGoogle Scholar
Malinky, JM and Yochelson, EL (2007) On the systematic position of the Hyolitha (Kingdom Animalia). Memoirs of the Association of Australasian Palaeontologists 34, 521–36.Google Scholar
Mao, JR, Zhao, YL, Yu, P and Qian, Y (1992) Some middle Cambrian hyolithids from Taijiang, Guizhou. Acta Micropalaeontologica Sinica 9, 257–65.Google Scholar
Marek, L (1963) New knowledge on the morphology of Hyolithes . Sborník Geologických věd, řada Paleontologie 1, 53–73.Google Scholar
Marek, L and Galle, A (1976) The tabulate coral Hyostragulurn, an epizoan with bearing on hyolithid ecology and systematics. Lethaia 9, 51–64.CrossRefGoogle Scholar
Marek, L, Parsley, RL and Galle, A (1997) Functional morphology of hyolithids based on flume studies. Věstník Českého geologického ústavu 72, 351–8.Google Scholar
Martí Mus, M (2016) A hyolithid with preserved soft parts from the Ordovician Fezouata Konservat-Lagerstätte of Morocco. Palaeogeography, Palaeoclimatology, Palaeoecology 460, 122–9.CrossRefGoogle Scholar
Martí Mus, M and Bergström, J (2005) The morphology of hyolithids and its functional implications. Palaeontology 48, 1139–67.CrossRefGoogle Scholar
Martí Mus, M, Jeppsson, L and Malinky, JM (2014) A complete reconstruction of the hyolithid skeleton. Journal of Paleontology 88, 160–70.CrossRefGoogle Scholar
März, C, Poulton, SW, Beckmann, B, Küster, K, Wagner, T and Kasten, S (2008) Redox sensitivity of P cycling during marine black shale formation: dynamics of sulfidic and anoxic, non-sulfidic bottom waters. Geochimica et Cosmochimica Acta 72, 3703–17.CrossRefGoogle Scholar
Meshkova, NP and Sysoev, VA (1981) Nakhodka slepkov pishchevapitel’nogo apparata nizhnekembrieskikh khiolitov [The discovery of traces of the digestive system in Lower Cambrian hyoliths]. In Problematiki Fanerozoya, Vol. 481 (ed. Sokolov, BS), pp. 82–5. Moscow: Trudy Instituta Geologii i Geofiziki Sibirskoe Otdelenie, Akademiya Nauk SSSR. (in Russian).Google Scholar
Moysiuk, J, Smith, MR and Caron, J-B (2017) Hyoliths are Palaeozoic lophophorates. Nature 541, 394–7.CrossRefGoogle ScholarPubMed
Pan, B, Skovsted, CB, Sun, HJ and Li, GX (2019) Biostratigraphical and palaeogeographical implications of Early Cambrian hyoliths from the North China Platform. Alcheringa 43, 351–80.CrossRefGoogle Scholar
Peng, SC, Yang, XF, Liu, Y, Zhu, XJ, Sun, HJ, Zamora, S, Mao, YY and Zhang, YC (2020) Fulu biota, a new exceptionally-preserved Cambrian fossil assemblage from the Longha Formation in southeastern Yunnan. Palaeoworld 29, 453–61.CrossRefGoogle Scholar
Porter, SM (2004) Closing the phosphatization window: testing for the influence of taphonomic megabias on the pattern of small shelly fossil decline. Palaios 19, 178–83.2.0.CO;2>CrossRefGoogle Scholar
Reid, RGB (1965) The structure and function of the stomach in bivalve molluscs. Journal of Zoology 147, 156–84.Google Scholar
Runnegar, B, Pojeta, J, Morris, NJ, Taylor, JD, Taylor, ME and McClung, G (1975) Biology of the Hyolitha. Lethaia 8, 181–91.CrossRefGoogle Scholar
Schiffbauer, JD, Xiao, SH, Cai, YP, Wallace, AF, Hua, H, Hunter, J, Xu, HF, Peng, YB and Kaufman, AJ (2014) A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression. Nature Communication 5, 5754. doi: 10.1038/ncomms6754.CrossRefGoogle ScholarPubMed
Skovsted, CB, Balthasar, U, Vinther, J, Sperling, EA and Álvaro, J (2021) Small shelly fossils and carbon isotopes from the early Cambrian (Stages 3–4) Mural Formation of western Laurentia. Papers in Palaeontology 7, 951–83.CrossRefGoogle Scholar
Steiner, M, Li, GX, Qian, Y, Zhu, MY and Erdtmann, BD (2003) Lower Cambrian small shelly faunas from Zhejiang (China) and their biostratigraphical implications. Progress in Natural Science 13, 852–60.CrossRefGoogle Scholar
Sun, HJ, Babcock, LE, Peng, J and Kastigar, JM (2017) Systematics and palaeobiology of some Cambrian hyoliths from Guizhou, China, and Nevada, USA. Alcheringa 41, 79–100.CrossRefGoogle Scholar
Sun, HJ, Babcock, LE, Peng, J and Zhao, YL (2016) Three-dimensionally preserved digestive systems of two Cambrian hyolithides (Hyolitha). Bulletin of Geosciences 91, 51–6.CrossRefGoogle Scholar
Sun, HJ, Smith, MR, Zeng, H, Zhao, FC, Li, GX and Zhu, MY (2018a) Hyoliths with pedicles illuminate the origin of the brachiopod body plan. Proceedings of the Royal Society B: Biological Sciences 285, 20181780. doi: 10.1098/rspb.2018.1780.CrossRefGoogle ScholarPubMed
Sun, HJ, Zhao, FC, Steiner, M, Li, GX, Na, L, Pan, B, Yin, ZJ, Zeng, H, Van Iten, H and Zhu, MY (2020) Skeletal faunas of the lower Cambrian Yu’anshan Formation, eastern Yunnan, China: Metazoan diversity and community structure during the Cambrian Age 3. Palaeogeography, Palaeoclimatology, Palaeoecology 542, 109580. doi: 10.1016/j.palaeo.2019.109580.CrossRefGoogle Scholar
Sun, HJ, Zhao, FC, Wen, RQ, Zeng, H and Peng, J (2018b) Feeding strategy and locomotion of Cambrian hyolithides. Palaeoworld 27, 334–42.CrossRefGoogle Scholar
Sun, ZX, Wang, PL and Yuan, JL (2015) The first complete Tuzoia manchuriensis from the Cambrian Series 3 of Weifang, Shandong Province. Acta Palaeontologica Sinica 54, 113–19 (in Chinese with English abstract).Google Scholar
Sun, ZX, Zeng, H and Zhao, FC (2020a) Occurrence of the hurdiid radiodont Cambroraster in the middle Cambrian (Wuliuan) Mantou Formation of North China. Journal of Paleontology 94, 881–6.CrossRefGoogle Scholar
Sun, ZX, Zeng, H and Zhao, FC (2020b) First occurrence of the Cambrian arthropod Sidneyia Walcott, 1911 outside of Laurentia. Geological Magazine 157, 405–10.CrossRefGoogle Scholar
Sysoev, VA (1957) K morfologii, sistematike i sistematicheskomu polozheniu khiolitiov [On the morphology, systematics and systematic position of the Hyolithoidea]. Doklady Akademii Nauk SSSR 116, 304–7 (in Russian).Google Scholar
Sysoev, VA (1958) Nadotryad Hyolithoidea [Superorder Hyolithoidea]. In Osnovy paleontologii. Molluski-golovongie II (eds Orlov, Yu A, Luppov, NP and Drushchits, VV), pp. 184–90. Moscow: Akademii Nauk SSSR, 2 (in Russian).Google Scholar
Szczepanik, P and Sawłowicz, Z (2005) Pyritization of microfossils: crinoid remains from the middle Jurassic of Ogrodzieniec (Kraków-Czestochowa upland, Poland). Studia Geologica Polonica 124, 37–52.Google Scholar
Taylor, PD (2016) Competition between encrusters on marine hard substrates and its fossil record. Palaeontology 59, 481–97.CrossRefGoogle Scholar
Thoral, M (1935) Contribution à l’étude paléontologique de l’Ordovicien Inférieur de la Montagne Noire et revision sommaire de la faune cambrienne de la Montagne Noire. Montpellier: Imprimerie de la Charité.Google Scholar
Topper, TP, Holmer, LE and Caron, JB (2014) Brachiopods hitching a ride: an early case of commensalism in the middle Cambrian Burgess Shale. Scientific Reports 4, 6704. doi: 10.1038/srep06704.CrossRefGoogle ScholarPubMed
Topper, TP, Strotz, LC, Holmer, LE and Caron, J-B (2015) Survival on a soft seafloor: life strategies of brachiopods from the Cambrian Burgess Shale. Earth-Science Reviews 151, 266–87.CrossRefGoogle Scholar
Williams, A, James, MA, Emig, CC, Mackay, S and Rhodes, MC (1997) Anatomy. In Treatise on Invertebrate Paleontology Part H Brachiopoda Revised (ed. Kaesler, RL), pp. 7–188. Boulder, Colorado and Lawrence, Kansas: The Geological Society of America and The University of Kansas.Google Scholar
Yang, B, Steiner, M and Keupp, H (2015) Early Cambrian palaeobiogeography of the Zhenba–Fangxian Block (South China): independent terrane or part of the Yangtze Platform? Gondwana Research 28, 1543–65.CrossRefGoogle Scholar
Yang, B, Zhang, L, Danelian, T, Feng, QL and Steiner, M (2014) Chert-hosted small shelly fossils: expanded tool of biostratigraphy in the Early Cambrian. GFF 136, 303–8.CrossRefGoogle Scholar
Zhang, ZF, Strotz, LC, Topper, TP, Chen, FY, Chen, YL, Liang, Y, Zhang, ZL, Skovsted, CB and Brock, GA (2020) An encrusting kleptoparasite-host interaction from the early Cambrian. Nature Communication 11, 2625. doi: 10.1038/s41467-020-16332-3.CrossRefGoogle ScholarPubMed
Zhao, FC, Hu, SX, Caron, J-B, Zhu, MY, Yin, ZJ and Lu, M (2012) Spatial variation in the diversity and composition of the Lower Cambrian (Series 2, Stage 3) Chengjiang biota, Southwest China. Palaeogeography, Palaeoclimatology, Palaeoecology 346, 54–65.CrossRefGoogle Scholar
Zhu, MY, Babcock, LE and Steiner, M (2005) Fossilization modes in the Chengjiang Lagerstätte (Cambrian of China): testing the roles of organic preservation and diagenetic alteration in exceptional preservation. Palaeogeography, Palaeoclimatology, Palaeoecology 220, 31–46.CrossRefGoogle Scholar
Zhu, XJ, Peng, SC, Zamora, S, Lefebvre, B and Chen, GY (2016) Furongian (upper Cambrian) Guole Konservat-Lagerstätte from South China. Acta Geologica Sinica – English Edition 90, 30–7.Google Scholar
Zicha, O, Bruthansová, J and Kraft, P (2020) Epibionts on shells in the Šárka Formation: a sparsely occupied niche in the lower to middle Darriwilian (Oretanian, Ordovician) in the Prague Basin (Czech Republic). Palaeogeography, Palaeoclimatology, Palaeoecology 550, 109401. doi: 10.1016/j.palaeo.2019.109401.CrossRefGoogle Scholar