Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T12:05:04.328Z Has data issue: false hasContentIssue false
  • English
  • Français

Appendages of an early Cambrian metadoxidid trilobite from Yunnan, SW China support mandibulate affinities of trilobites and artiopods

Part of: From Snowball Earth to the Cambrian Explosion: Evidence from China

Published online by Cambridge University Press:  05 April 2017

HAN ZENG Open the ORCID record for HAN ZENG [Opens in a new window] ,
FANGCHEN ZHAO Open the ORCID record for FANGCHEN ZHAO [Opens in a new window] ,
ZONGJUN YIN  and
MAOYAN ZHU
HAN ZENG
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China Department of Paleobiology, National Museum of Natural History, P.O. Box 37012, MRC-121, Washington, DC, 20013–7012, USA University of Chinese Academy of Sciences, No. 19 Yuquan Road, Beijing 100049, China
FANGCHEN ZHAO*
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China
ZONGJUN YIN
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China
MAOYAN ZHU
Affiliation:
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, No. 39 East Beijing Road, Nanjing 210008, China College of Earth Sciences, University of Chinese Academy of Sciences, No. 19 Yuquan Road, Beijing 100049, China
*
†Author for correspondence: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Appendage anatomy contributes crucial data for understanding the evolution and ecology of Euarthropoda. The Palaeozoic trilobites show a great diversity of exoskeletons in the fossil record. However, soft parts, especially appendages, have only been discovered from a few trilobite species. Here we report extraordinarily preserved appendages in the trilobite species Hongshiyanaspis yiliangensis Zhang & Lin in Zhang et al. 1980 (Redlichiida, Metadoxididae) from a single mudstone layer of the Xiazhuang fossil assemblage within the Hongjingshao Formation (Cambrian Series 2, Stage 3) near Kunming, Yunnan, SW China. The appendages exhibit the common architecture revealed by other trilobites and artiopods by consisting of a pair of uniramous antennae followed by a series of paired homonomous biramous limbs. The antennae in holaspid individuals comprise up to 27 spinous podomeres and their ontogeny occurs by lengthening of the podomeres. The post-antennal biramous limbs are similar to those in other polymerid trilobites and artiopods by having a single-segmented protopodite and an endopodite comprising seven segments, but possess a unique wide tripartite exopodite with long setae. Sophisticated appendage anatomy, including the body–limb junction, fine setae, putative muscle bundles and duct-type tissues, are also revealed. Appendages of trilobites, artiopods and other upper stem-group euarthropods are compared and summarized. The H. yiliangensis appendages highlight the high morphological disparity of exopodites and the conservativeness of endopodites in trilobites and artiopods. This morphological pattern, together with similar body patterning seen in crustaceans but not in chelicerates, supports the mandibulate affinities of trilobites and at least some artiopods.

Keywords

arthropodstrilobitesappendagesMandibulataCambriansoft-part preservation
Type
Original Articles
Information
Geological Magazine , Volume 154 , Issue 6: THEMATIC ISSUE: From Snowball Earth to the Cambrian Explosion: Evidence from China , November 2017 , pp. 1306 - 1328
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aria, C. & Caron, J.-B. 2015. Cephalic and limb anatomy of a new isoxyid from the Burgess Shale and the role of “stem bivalved arthropods” in the disparity of the frontalmost appendage. PLoS ONE 10, e0124979.CrossRefGoogle ScholarPubMed
Aria, C., Caron, J.-B. & Gaines, R. 2015. A large new leanchoiliid from the Burgess Shale and the influence of inapplicable states on stem arthropod phylogeny. Palaeontology 58, 629–60.CrossRefGoogle Scholar
Bartels, C., Briggs, D. E. G. & Brassel, G. 1998. The Fossils of the Hunsrück Slate: Marine Life in the Devonian. Cambridge: Cambridge University Press, 324 pp.Google Scholar
Beecher, C. E. 1895. Structure and appendages of Trinucleus . American Journal of Science 3, 307–11.CrossRefGoogle Scholar
Bergström, J. 1972. Appendage morphology of the trilobite Cryptolithus and its implications. Lethaia 5, 85–94.CrossRefGoogle Scholar
Bergström, J. & Brassel, G. 1984. Legs in the trilobite Rhenops from the Lower Devonian Hunsrück Slate. Lethaia 17, 67–72.CrossRefGoogle Scholar
Billings, E. 1870. Notes on some specimens of Lower Silurian trilobites. Quarterly Journal of the Geological Society 26, 479–86.CrossRefGoogle Scholar
Boxshall, G. A. 2004. The evolution of arthropod limbs. Biological Reviews 79, 253–300.CrossRefGoogle ScholarPubMed
Boxshall, G. A. 2013. Arthropod limbs and their development. In Arthropod Biology and Evolution: Molecules, Development, Morphology (eds Minelli, A., Boxshall, G. A. & Fusco, G.), pp. 241–67. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Briggs, D. E. G., Lieberman, B. S., Hendricks, J. R., Halgedahl, S. L. & Jarrard, R. D. 2008. Middle Cambrian arthropods from Utah. Journal of Paleontology 82, 238–54.CrossRefGoogle Scholar
Briggs, D. E. G., Siveter, D. J., Siveter, D. J., Sutton, M. D., Garwood, R. J. & Legg, D. A. 2012. Silurian horseshoe crab illuminates the evolution of arthropod limbs. Proceedings of the National Academy of Sciences 109, 15702–5.CrossRefGoogle ScholarPubMed
Bruton, D. L. & Haas, W. 1999. The anatomy and functional morphology of Phacops (Trilobita) from the Hunsrück Slate (Devonian). Palaeontographica Abteilung A 253, 29–75.CrossRefGoogle Scholar
Budd, G. E. & Telford, M. J. 2009. The origin and evolution of arthropods. Nature 457, 812–17.CrossRefGoogle ScholarPubMed
Chen, J. Y., Edgecombe, G. D. & Ramsköld, L. 1997. Morphological and ecological disparity in naraoiids (Arthropoda) from the Early Cambrian Chengjiang fauna, China. Records of the South Australian Museum 49, 1–24.CrossRefGoogle Scholar
Chen, J. Y., Waloszek, D. & Maas, A. 2004. A new ‘great appendage’ arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero ventral appendages. Lethaia 37, 3–20.CrossRefGoogle Scholar
Chen, J. Y. & Zhou, G. Q. 1997. Biology of the Chengjiang fauna. Bulletin of the National Museum of Natural Science 10, 11–105.Google Scholar
Cisne, J. L. 1975. Anatomy of Triarthrus and the relationships of the Trilobita. Fossils and Strata 4, 45–63.CrossRefGoogle Scholar
Cisne, J. L. 1981. Triarthrus eatoni (Trilobita), anatomy of its exoskeletal, skeletomuscular, and digestive systems. Palaeontographia Americana 9, 99–142.Google Scholar
Davidson, E. H. & Erwin, D. H. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800.CrossRefGoogle ScholarPubMed
Dunbar, C. O. 1925. Antennae in Olenellus getzi n. sp. American Journal of Science 5, 303–8.CrossRefGoogle Scholar
Edgecombe, G. D. & Legg, D. A. 2014. Origins and early evolution of arthropods. Palaeontology 57, 457–68.CrossRefGoogle Scholar
Edgecombe, G. D. & Ramsköld, L. 1999. Relationships of Cambrian Arachnata and the systematic position of Trilobita. Journal of Paleontology 73, 263–87.CrossRefGoogle Scholar
Farrell, Ú. C., Martin, M. J., Hagadorn, J. W., Whiteley, T. & Briggs, D. E. G. 2009. Beyond Beecher's Trilobite Bed: widespread pyritization of soft tissues in the Late Ordovician Taconic foreland basin. Geology 37, 907–10.CrossRefGoogle Scholar
Fortey, R. A. 2001. Trilobite systematics: the last 75 years. Journal of Paleontology 75, 1141–51.2.0.CO;2>CrossRefGoogle Scholar
Geyer, G. & Peel, J. S. 2017. Middle Cambrian trilobites from the Ekspedition Bræ Formation of North Greenland, with a reappraisal of the genus Elrathina . Journal of Paleontology 91, 265–93.CrossRefGoogle Scholar
Harrington, H. J., Henningsmoen, G., Howell, B. F., Jaanusson, V., Lochman-Balk, C., Moore, R. C., Poulsen, C., Rasetti, F., Richter, E., Richter, R., Schmidt, H., Sdzuy, K., Struve, W., Størmer, L., Stubblefield, C. J., Tripp, R., Weller, J. M. & Whittington, H. B. 1959. Part O; Arthropoda 1. Boulder, Colorado: Geological Society of America; and Lawrence, Kansas: University of Kansas Press, 560 pp.Google Scholar
Haug, J. T., Maas, A., Haug, C. & Waloszek, D. 2013. Evolution of crustacean appendages. In The Natural History of the Crustacea, Volume 1: Functional Morphology and Diversity (eds Watling, L. & Thiel, M.), pp. 34–73. New York: Oxford University Press.CrossRefGoogle Scholar
Hollingsworth, J. S. 2008. The first trilobites in Laurentia and elsewhere. In Advances in Trilobite Research (eds Rábano, I., Gozalo, R. & García-Bellido, D.), pp. 171–75. Madrid: Instituto Geológico y Minero de España.Google Scholar
Hou, X. G. & Bergström, J. 1997. Arthropods of the lower Cambrian Chengjiang fauna, southwest China. Fossils and Strata 45, 1–116.Google Scholar
Hou, X. G., Clarkson, E. N. K., Yang, J., Zhang, X. G., Wu, G. Q. & Yuan, Z. B. 2008. Appendages of early Cambrian Eoredlichia (Trilobita) from the Chengjiang biota, Yunnan, China. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 99, 213–23.CrossRefGoogle Scholar
Hou, J. B., Hughes, N. C., Yang, J., Lan, T., Zhang, X. G. & Dominguez, C. 2017. Ontogeny of the articulated yiliangellinine trilobite Zhangshania typica from the lower Cambrian (Series 2, Stage 3) of southern China. Journal of Paleontology 91, 86–99.CrossRefGoogle Scholar
Hu, S. X., Zhu, M. Y., Luo, H. L., Steiner, M., Zhao, F. C., Li, G. X., Liu, Q. & Zhang, Z. F. 2013. The Guanshan Biota. Kunming: Yunnan Science and Technology Press, 204 pp.Google Scholar
Hu, S. X., Zhu, M. Y., Steiner, M., Luo, H. L., Zhao, F. C. & Liu, Q. 2010. Biodiversity and taphonomy of the early Cambrian Guanshan biota, eastern Yunnan. SCIENCE CHINA Earth Sciences 53, 1765–73.CrossRefGoogle Scholar
Hughes, N. C. 2003. Trilobite tagmosis and body patterning from morphological and developmental perspectives. Integrative and Comparative Biology 43, 185–206.CrossRefGoogle ScholarPubMed
Hughes, N. C. 2007. The evolution of trilobite body patterning. Annual Review of Earth and Planetary Sciences 35, 401–34.CrossRefGoogle Scholar
Legg, D. A. 2014. Sanctacaris uncata: the oldest chelicerate (Arthropoda). Naturwissenschaften 101, 1065–73.CrossRefGoogle ScholarPubMed
Legg, D. A., Sutton, M. D. & Edgecombe, G. D. 2013. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nature Communications 4, 2485. doi: 10.1038/ncomms3485.CrossRefGoogle ScholarPubMed
Legg, D. A., Sutton, M. D., Edgecombe, G. D. & Caron, J.-B. 2012. Cambrian bivalved arthropod reveals origin of arthrodization. Proceedings of the Royal Society B: Biological Sciences 279, 4699–704.CrossRefGoogle ScholarPubMed
McHenry, B. & Yates, A. 1993. First report of the enigmatic metazoan Anomalocaris from the southern hemisphere and a trilobite with preserved appendages from the Early Cambrian of Kangaroo Island, South Australia. Records of the South Australian Museum 26, 77–86.Google Scholar
Müller, K. J. & Walossek, D. 1987. Morphology, ontogeny, and life habit of Agnostus pisiformis from the Upper Cambrian of Sweden. Fossils and Strata 19, 1–124.CrossRefGoogle Scholar
Ortega-Hernández, J., Legg, D. A. & Braddy, S. J. 2013. The phylogeny of aglaspidid arthropods and the internal relationships within Artiopoda. Cladistics 29, 15–45.CrossRefGoogle ScholarPubMed
Owens, R. M. 2003. The stratigraphical distribution and extinctions of Permian trilobites. Special Papers in Palaeontology 70, 377–97.Google Scholar
Ramsköld, L., Chen, J. Y., Edgecombe, G. D. & Zhou, G. Q. 1996. Preservational folds simulating tergite junctions in tegopeltid and naraoiid arthropods. Lethaia 29, 15–20.CrossRefGoogle Scholar
Ramsköld, L. & Edgecombe, G. D. 1996. Trilobite appendage structure – Eoredlichia reconsidered. Alcheringa 20, 269–76.CrossRefGoogle Scholar
Raymond, P. E. 1920. The appendages, anatomy, and relationships of trilobites. Memoirs of the Connecticut Academy of Arts and Sciences 7, 1–169.Google Scholar
Ross, R. J. 1979. Additional trilobites from the Ordovician of Kentucky. United States Geological Survey Professional Paper 1066D, 1–13.Google Scholar
Scholtz, G. & Edgecombe, G. D. 2005. Heads, Hox and the phylogenetic position of trilobites. Crustacean Issues 16, 139–65.CrossRefGoogle Scholar
Scholtz, G. & Edgecombe, G. D. 2006. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Development Genes and Evolution 216, 395–415.CrossRefGoogle ScholarPubMed
Shu, D. G., Geyer, G., Chen, L. & Zhang, X. L. 1995. Redlichiacean trilobites with preserved soft-parts from the lower Cambrian Chengjiang fauna (South China). Beringeria Special Issue 2, 203–41.Google Scholar
Stein, M. 2013. Cephalic and appendage morphology of the Cambrian arthropod Sidneyia inexpectans . Zoologischer Anzeiger 253, 164–78.CrossRefGoogle Scholar
Stein, M., Budd, G. E., Peel, J. S. & Harper, D. A. T. 2013. Arthroaspis n. gen., a common element of the Sirius Passet Lagerstätte (Cambrian, North Greenland), sheds light on trilobite ancestry. BMC Evolutionary Biology 13. doi: 10.1186/1471-2148-13-99, 99 pp.CrossRefGoogle Scholar
Stein, M. & Selden, P. A. 2012. A restudy of the Burgess Shale (Cambrian) arthropod Emeraldella brocki and reassessment of its affinities. Journal of Systematic Palaeontology 10, 361–83.CrossRefGoogle Scholar
Størmer, L. 1939. Studies on trilobite morphology, Part I, The thoracic appendages and their phylogenetic significance. Norsk Geologisk Tidsskrift 19, 143–273.Google Scholar
Størmer, L. 1951. Studies on trilobite morphology, Part III, The ventral cephalic sutures with remarks on the zoological position of the trilobites. Norsk Geologisk Tidsskrift 29, 108–58.Google Scholar
Strausfeld, N. J. 2016. Waptia revisited: intimations of behaviors. Arthropod Structure & Development 45, 173–84.CrossRefGoogle ScholarPubMed
Stürmer, W. & Bergström, J. 1973. New discoveries on trilobites by X-rays. Paläontologische Zeitschrift 47, 104–41.CrossRefGoogle Scholar
Tanaka, G., Hou, X. G., Ma, X. Y., Edgecombe, G. D. & Strausfeld, N. J. 2013. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502, 364–67.CrossRefGoogle Scholar
Van Roy, P., Orr, P. J., Botting, J. P., Muir, L. A., Vinther, J., Lefebvre, B., Hariri, K. E. & Briggs, D. E. G. 2010. Ordovician faunas of Burgess Shale type. Nature 465, 215–8.CrossRefGoogle ScholarPubMed
Walcott, C. D. 1881. The trilobite, new and old evidence relating to its organization. Bulletin of the Museum of Comparative Zoology at Harvard College 8, 190–242.Google Scholar
Walcott, C. D. 1884. Appendages of the trilobite. Science 3, 279–81.CrossRefGoogle ScholarPubMed
Walcott, C. D. 1912. Cambrian Geology and Paleontology II. No. 6. Middle Cambrian Branchiopoda, Malacostraca, Trilobita and Merostomata. Smithsonian Miscellaneous Collections 57, 145–228.Google Scholar
Walcott, C. D. 1918. Cambrian Geology and Paleontology IV. No. 4. Appendages of trilobites. Smithsonian Miscellaneous Collections 67, 115–216.Google Scholar
Walcott, C. D. 1921. Cambrian Geology and Paleontology IV. No. 7. Notes on structure of Neolenus . Smithsonian Miscellaneous Collections 67, 365–456.Google Scholar
Walossek, D. & Müller, K. J. 1990. Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus . Lethaia 23, 409–27.CrossRefGoogle Scholar
Walossek, D. & Müller, K. J. 1998. Cambrian ‘Orsten’-type arthropods and the phylogeny of Crustacea. In Arthropod Relationships (eds Fortey, R. A. & Thomas, R. H.), pp. 139–53. London: Chapman & Hall.CrossRefGoogle Scholar
Whittington, H. B. 1975. Trilobites with appendages from the Middle Cambrian Burgess Shale, British Columbia. Fossils and Strata 4, 97–136.CrossRefGoogle Scholar
Whittington, H. B. 1980. Exoskeleton, moult stage, appendage morphology, and habits of the Middle Cambrian trilobite Olenoides serratus . Palaeontology 23, 171–204.Google Scholar
Whittington, H. B. 1993. Anatomy of the Ordovician trilobite Placoparia . Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 339, 109–18.Google Scholar
Whittington, H. B. & Almond, J. E. 1987. Appendages and habits of the Upper Ordovician trilobite Triarthrus eatoni . Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 317, 1–46.Google Scholar
Whittington, H. B., Chatterton, B. D. E., Speyer, S. E., Fortey, R. A., Owens, R. M., Chang, W. T., Dean, W. T., Geyer, G., Jell, P. A., Laurie, J. R., Palmer, A. R., Repina, L. N., Rushton, A. W. A., Shergold, J. H., Clarkson, E. N. K., Wilmot, N. V. & Kelly, S. R. A. 1997. Part O Trilobita Revised Volume 1. Boulder, Colorado: The Geological Society of America; and Lawrence, Kansas: University of Kansas Press, 530 pp.Google Scholar
Wolff, C. & Scholtz, G. 2008. The clonal composition of biramous and uniramous arthropod limbs. Proceedings of the Royal Society B: Biological Sciences 275, 1023–8.CrossRefGoogle ScholarPubMed
Yang, J., Ortega-Hernández, J., Butterfield, N. J. & Zhang, X. G. 2013. Specialized appendages in fuxianhuiids and the head organization of early euarthropods. Nature 494, 468–71.CrossRefGoogle ScholarPubMed
Zeng, H., Zhao, F. C., Yin, Z. J., Li, G. X. & Zhu, M. Y. 2014. A Chengjiang type fossil assemblage from the Hongjingshao Formation (Cambrian Stage 3) at Chenggong, Kunming, Yunnan. Chinese Science Bulletin 59, 3169–75.CrossRefGoogle Scholar
Zhang, Z. Q. 2013. Phylum arthropoda. In Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness (addenda 2013) (ed. Zhang, Z. Q.). Zootaxa 3703, 17–26.CrossRefGoogle Scholar
Zhang, X. L., Han, J., Zhang, Z. F., Liu, H. Q. & Shu, D. G. 2004. Redescription of the Chengjiang arthropod Squamacula clypeata Hou and Bergström, from the Lower Cambrian, south west China. Palaeontology 47, 605–17.CrossRefGoogle Scholar
Zhang, W. T., Lu, Y. H., Zhu, Z. L., Qian, Y. Y., Lin, H. L., Zhou, Z. Y., Zhang, S. G. & Yuan, J. L. 1980. Cambrian Trilobite Faunas of Southwestern China. Beijing: Science Press, 497 pp. (in Chinese with English summary).Google Scholar
Zhang, X. L. & Shu, D. G. 2005. A new arthropod from the Chengjiang Lagerstätte, Early Cambrian, southern China. Alcheringa 29, 185–94.CrossRefGoogle Scholar
Zhang, X. L., Shu, D. G. & Erwin, D. H. 2007. Cambrian naraoiids (Arthropoda): morphology, ontogeny, systematics, and evolutionary relationships. Journal of Paleontology 81, 1–52.CrossRefGoogle Scholar
Zhu, M. Y., Li, G. X., Zhang, J. M., Steiner, M., Qian, Y. & Jiang, Z. W. 2001. Early Cambrian stratigraphy of east Yunnan, southwestern China: a synthesis. Acta Palaeontologica Sinica 40, 4–39.Google Scholar
Zhu, M. Y., Babcock, L. E. & 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
Supplementary material: File

Zeng supplementary material

Table S1

Download Zeng supplementary material(File)
File 350.2 KB