Abstract
The fossil record, including the record of Burgess Shale-type deposits, is biased towards late ontogenetic stages. Larval stages, juvenile and subadult specimens exist but are very rare and often preserved as phosphatic fossils, resulting in biased population structures. Here, we report a new Burgess Shale-type Lagerstätte from Haiyan, China. The Haiyan palaeocommunity is extraordinary in that it is rich in fossils of early and middle ontogenetic stages of various phyla, with eggs also commonly found in the studied interval. This Lagerstätte also hosts a considerable number of new taxa—many related to later biotas of Gondwana and Laurentia. We propose that the deposit may either preserve one of the earliest nurseries in the fossil record or, alternatively, records several attempted invasions. Our study highlights the complexity of biotas and their interactions in the lower Cambrian ocean and calls for a better understanding of the mechanisms responsible for the observed spatial variation of fossil community composition in the Cambrian.
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Data availability
All elements necessary to allow interpretation and replication of the results, including full datasets, are provided in Supplementary Tables 1–4. All specimens are kept at YKLP at Yunnan University. Photographic material of the studied material is available from the corresponding authors on request.
References
Zhao, F. et al. Diversity and species abundance patterns of the early Cambrian (Series 2, Stage 3) Chengjiang Biota from China. Paleobiology 40, 50–69 (2014).
Zhu, M.-Y., Zhang, J.-M. & Li, G.-X. Sedimentary environments of the early Cambrian Chengjiang biota: sedimentology of the Yu’anshan Formation in Chengjiang County, eastern Yunnan. Acta Palaeontol. Sin. 40, 80–105 (2001).
Hu, S.-X. Taphonomy and palaeoecology of the early Cambrian Chengjiang Biota from eastern Yunnan, China. Berl. Palobiologische Abhandlungen 7 (2005).
Hou, X. et al. The Cambrian Fossils of Chengjiang, China. The Flowering of Early Animal Life 2nd edn (John Wiley & Sons, 2017).
Zhang, W.-T. & Hou, X.-G. Preliminary notes on the occurrence of the unusual trilobite Naraoia in Asia. Acta Palaeontol. Sin. 24, 591–595 (1985).
Luo, H.-L, Hu, S.-X, Chen, L.-Z, Zhang, S.-S & Tao, Y.-H. Early Cambrian Chengjiang Fauna from Kunming Region, China (Yunnan Science and Technology Press, 1999).
Chen, J.-Y The Dawn of Animal World (Jiangsu Science and Technology Press, China, 2004).
Duan, Y. et al. Reproductive strategy of the bradoriid arthropod Kunmingella douvillei from the lower Cambrian Chengjiang Lagerstätte, South China. Gondwana Res. 25, 983–990 (2014).
Zhao, F.-C., Zhu, M.-Y. & Hu, S.-X. Community structure and composition of the Cambrian Chengjiang biota. Sci. China Earth Sci. 53, 1784–1799 (2010).
Liu, Y. et al. Three-dimensionally preserved minute larva of a great-appendage arthropod from the early Cambrian Chengjiang biota. Proc. Natl Acad. Sci. USA 113, 5542–5546 (2016).
Ou, Q. et al. Evolutionary trade-off in reproduction of Cambrian arthropods. Sci. Adv. 6, 33–76 (2020).
Dornbos, S. Q. & Chen, J.-Y. Community palaeoecology of the Early Cambrian Maotianshan Shale biota: ecological dominance of priapulid worms. Palaeogeogr. Palaeoclimatol. Palaeoecol. 258, 200–212 (2008).
Fu, D. et al. The Qingjiang biota—a Burgess Shale-type fossil Lagerstätte from the early Cambrian of South China. Science 363, 1338–1342 (2019).
Caron, J.-B. & Jackson, D. A. Paleoecology of the Greater Phyllopod Bed community, Burgess Shale. Palaeogeogr. Palaeoclimatol. Palaeoecol. 258, 222–256 (2008).
Nanglu, K., Caron, J.-B. & Gaines, R. R. The Burgess Shale paleocommunity with new insights from Marble Canyon, British Columbia. Paleobiology 46, 58–81 (2020).
Gaines, R. R. in Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization Vol. 20 (eds Laflamme, M. et al.) 123–146 (Paleontological Research Institution, 2014).
Zhai, D. et al. Variation in appendages in early Cambrian bradoriids reveals a wide range of body plans in stem-euarthropods. Commun. Biol. 2, 329 (2019).
Isaevaa, V. V., Ozernyukc, N. D. & Rozhnov, S. V. Evidence for evolutionary changes in ontogeny: paleontological, comparative morphological, and molecular aspects. Biol. Bull. 40, 243–252 (2013).
Liu, Y., Haug, J. T., Haug, C., Briggs, D. E. G. & Hou, X.-G. A 520 million-year-old chelicerate larva. Nat. Commun. 5, 4440 (2014).
Chipman, A. D. An embryological perspective on the early arthropod fossil record. BMC Evol. Biol. 15, 285 (2015).
Wolfe, J. M. Metamorphosis is ancestral for crown euarthropods, and evolved in the Cambrian or earlier. Integr. Comp. Biol. 57, 499–509 (2017).
Haug, T. J. Why the term “larva” is ambiguous, or what makes a larva? Acta Zool. 101, 167–188 (2018).
Fu, D., Zhang, X., Budd, G. E., Liu, W. & Pan, X. Ontogeny and dimorphism of Isoxys auritus (Arthropoda) from the Early Cambrian Chengjiang biota, South China. Gondwana Res. 25, 975–982 (2014).
Yang, X.-F., Kimmig, J., Lieberman, B. S. & Peng, S.-C. A new species of the deuterostome Herpetogaster from the early Cambrian Chengjiang biota of South China. Sci. Nat. 107, 37 (2020).
Zhai, D. Y. et al. Fine-scale appendage structure of the Cambrian trilobitomorph Naraoia spinosa and its ontogenetic and ecological implications. Proc. R. Soc. B 286, 20192371 (2019).
Hughes, N. C. et al. Articulated trilobite ontogeny: suggestions for a methodological standard. J. Paleont. 95, 298–304 (2021).
Chen, J.-Y. & Zhou, G.-Q. Biology of the Chengjiang fauna. Bull. Natl Mus. Nat. Sci. 10, 11–106 (1997).
Haug, J. T., Caron, J.-B. & Haug, C. Demecology in the Cambrian: synchronized moulting in arthropods from the Burgess Shale. BMC Biol. 11, 64 (2013).
Robison, R. A., Babcock, L. E. & Gunther, V. G. Exceptional Cambrian fossils from Utah: A Window into the Age of Trilobites (Utah Geological Survey, 2015).
Kimmig, J., Strotz, L. C., Kimmig, S. R., Egenhoff, S. O. & Lieberman, B. S. The Spence Shale Lagerstätte: an important window into Cambrian biodiversity. J. Geol. Soc. Lond. 176, 609–619 (2019).
Paterson, J. R. et al. The Emu Bay Shale Konservat-Lagerstätte: a view of Cambrian life from East Gondwana. J. Geol. Soc. Lond. 173, 3107 (2016).
Du, K. et al. A new early Cambrian Konservat-Lagerstätte expands the occurrence of Burgess Shale-type deposits on the Yangtze Platform. Earth Sci. Rev. 211, 103409 (2020).
Harper, D. A. T. et al. The Sirius Passet Lagerstätte of North Greenland: a remote window on the Cambrian explosion. J. Geol. Soc. Lond. 176, 1023–1037 (2019).
Chen, L. Z et al. Early Cambrian Chengjiang Fauna in Eastern Yunnan, China (Yunnan Science and Technology Press, 2002).
Zhao, F. C., Caron, J.-B., Hu, S. X. & Zhu, M. Y. Quantitative analysis of taphofacies and paleocommunities in the Early Cambrian Chengjiang Lagerstätte. PALAIOS 24, 826–839 (2009).
Beck, M. K. et al. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633–641 (2001).
Botton, M. L. & Loveland, R. E. Abundance and dispersal potential of horseshoe crab (Limulus polyphemus) larvae in the Delaware estuary. Estuar. Coasts 26, 1472–1479 (2003).
Watson, W. H. & Chabot, C. C. High resolution tracking of adult horseshoe crabs Limulus polyphemus in a New Hampshire estuary using a fixed array ultrasonic telemetry. Curr. Zool. 56, 599–610 (2010).
Perry, F. A. et al. Habitat partitioning in Antarctic krill: spawning hotspots and nursery areas. PLoS ONE 14, e0219325 (2019).
Nagelkerken, I. in Ecological Connectivity among Tropical Coastal Ecosystems (ed. Nagelkerken, I.) 357–399 (Springer, 2009).
Kanciruk, P. in The Biology and Management of Lobsters Vol. 2 (eds Cobb, J. S. & Phillips, B. F.) 59–96 (Academic Press, 1980).
Sandt, V. J. & Stoner, A. W. Ontogenetic shift in habitat by early juvenile queen conch, Strombus gigas: patterns and potential mechanisms. Fish. Bull. 91, 516–525 (1993).
Pedrotti, M. L. & Fenaux, L. Dispersal of echinoderm larvae in a geographical area marked by upwelling (Ligurian Sea, NW Mediterranean). Mar. Ecol. Prog. Ser. 87, 217–227 (1992).
Zhai, D. et al. Spatial heterogeneity of the population age structure of the ostracode Limnocythere inopinata in Hulun Lake, Inner Mongolia and its implications. Hydrobiologia 716, 29–46 (2013).
Baillon, S., Hamel, J. F., Wareham, V. E. & Mercier, A. Deep cold-water corals as nurseries for fish larvae. Front. Ecol. Environ. 10, 351–356 (2012).
Treude, T., Kiel, S., Linke, P., Peckmann, J. & Goedert, J. Elasmobranch egg capsules associated with modern and ancient cold seeps: a nursery for marine deep-water predators. Mar. Ecol. Prog. Ser. 437, 175–181 (2011).
Rooper, C. N., Boldt, J. L. & Zimmermann, M. An assessment of juvenile Pacific Ocean perch (Sebastes alutus) habitat use in a deepwater nursery. Estuar. Coast. Shelf Sci. 75, 371–380 (2007).
Pimiento, C., Ehret, D. J., MacFadden, B. J. & Hubbell, G. Ancient nursery area for the extinct giant shark Megalodon from the Miocene of Panama. PLoS ONE 5, e10552 (2010).
Villafaña, J. A. et al. First evidence of a palaeo-nursery area of the great white shark. Sci. Rep. 10, 8502 (2020).
Paterson, J. R., Jago, J. B., Brock, G. A. & Gehling, J. G. Taphonomy and palaeoecology of the emuellid trilobite Balcoracania dailyi (early Cambrian, South Australia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 249, 302–321 (2007).
Hartnoll, R. G. in Physiology and Behaviour of Marine Organisms (eds McLusky, D. S. & Berry, A. J.) 349–358 (Pergamon Press, 1978).
Hartnoll, R. G. & Bryant, A. D. Size-frequency distributions in decapod Crustacea—the quick, the dead and the cast-offs. J. Crust. Biol. 10, 14–19 (1990).
Sheldon, P. R. Trilobite size-frequency distributions, recognition of instars, and phyletic size changes. Lethaia 21, 293–306 (1988).
Herrnkind, W. F. in The Biology and Management of Lobsters Vol. 1 (eds Cobb, J. S. & Phillips B. F.) 349–407 (Academic Press, 1980)
Linnane, A., Dimmlich, W. & Ward, T. Movement patterns of the southern rock lobster, Jasus edwardsii, of South Australia. NZ J. Mar. Freshw. Res. 39, 335–346 (2005).
Blazejowski, B. et al. Ancient animal migration: a case study of eyeless, dimorphic Devonian trilobites from Poland. Palaeontology 59, 743–751 (2016).
Hughes, N. C., Kříž, J., Macquaker, J. H. S. & Huff, W. D. The depositional environment and taphonomy of the Homerian “Aulacopleura shales” fossil assemblage near Loděnice, Czech Republic (Prague Basin, Perunican microcontinent). Bull. Geosci. 89, 219–238 (2014).
Whitaker, A. F. & Kimmig, J. Anthropologically introduced biases in natural history collections, with a case study on the invertebrate paleontology collections from the middle Cambrian Spence Shale Lagerstätte. Palaeontol. Electron. 23, a58 (2020).
Conway Morris, S. The community structure of the Middle Cambrian phyllopod bed (Burgess Shale). Palaeontology 29, 423–467 (1986).
Caron, J.-B., Gaines, R. R., Aria, C., Mángano, M. G. & Streng, M. A new phyllopod bed-like assemblage on from the Burgess Shale of the Canadian Rockies. Nat. Commun. 5, 3210 (2014).
Ihaka, R. R. & Gentleman, R. A language for data analysis and graphics. J. Comput. Graph. Stat. 5, 299–314 (1996).
Acknowledgements
We thank M. Wilson and R. LaVine for comments on earlier versions of the manuscript. We thank N. Hughes and J. Schiffbauer for their reviews that improved the manuscript. This paper is a contribution to IGCP668, Equatorial Gondwanan History and Early Palaeozoic Evolutionary Dynamics. X.Y. was supported by the National Natural Science Foundation of China (grant nos. 41062001, 41562001) and the State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) (grant no. 103113). S.P. was supported by the State Key Laboratory of Palaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS) (grant no. 20191101). D.Z. was supported by Key Research Program of the Institute of Geology & Geophysics, Chinese Academy of Sciences (grant no. IGGCAS-201905).
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X.Y. designed and led the study. X.Y. and S.P. completed fieldwork and collected all specimens used in the study. X.Y. photographed the specimens and completed EDS analyses. X.Y. completed all the measurements. X.Y. and J.K. completed all analyses. X.Y., J.K. and S.R.K. created the figures. X.Y., J.K., S.R.K., S.P., D.Y. and Y.L. wrote the manuscript. All authors discussed and agreed in interpretation of the data.
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Peer review information Nature Ecology & Evolution thanks Nigel Hughes, James Schiffbauer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
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Extended data
Extended Data Fig. 1 Detailed stratigraphy of the Haiyan Lagerstätte.
Stratigraphic succession of the Cambrian Stage 3 Haiyan section with ranges of major fossil lineages preserved in the Haiyan Lagerstätte and the upper soft-bodied interval.
Extended Data Fig. 2 Taphonomy of the Haiyan Lagerstätte.
a–g, Soft-bodied tissue preservation of a new hemichordate, YKLP14443. a, Microprobe EDS spectrum of the matrix. b, Stereo microscope image. c, Backscatter electron (BSE) image showing pyrite on the surface of fossil, black arrow indicates the boundary of the fossil and the matrix. d, Elemental map overlay, including silicon (Si), aluminium (Al), oxygen (O), potassium (K), iron (Fe). e–j, individual elemental maps e, Iron. f, Silicon. g, Aluminium. h, Carbon (C). i, Sulfur (S). j, Oxygen. k, Unpolished mudstone from the lower level of the Haiyan Lagerstätte. l, Polished mudstone from the lower level of the Haiyan Lagerstätte. Scale bars, 200 μm (c–i), 1 mm (b),10 mm (k, l).
Extended Data Fig. 3 Exceptionally preserved new specimens of rare Chengjiang biota taxa in the Haiyan Lagerstätte.
a, Larva of the deuterostome Yunnanozoon sp., YKLP14449. b, New ctenophore, YKLP14450. c, A juvenile of the problematicum Archotuba elongata, YKLP14451. d, A juvenile specimen of the sipunculan worm Cambrosipunculus sp., YKLP14452. e, Priapulid worm Anningvermis multispinosa, YKLP14453. f, Vetulicolian Heteromorphus confusus, YKLP14454. g, Priapulid worm Acosmia maotiania, YKLP14455. h, Phoronid Iotuba chengjiangensis, YKLP14456. i, Arthropod Urokodia aequalis, YKLP14457. j, The problematicum Eldonia eumorpha, YKLP14458, preserved with a priapulid worm Maotianshania cylindrica and the brachiopod Longtancunella chengjiangensis. k, The problematicum Archotuba elongata, YKLP14459, preserved together with specimens of the palaeoscolecid worm Maotianshania cylindrica, the entoproct Cotyledion tylodes and the priapulid worm Paraselkirkia sinica. Scale bars, 500 μm (c,), 1 mm (a, b, d), 5 mm (e, g, i), 10 mm (f, h, k), 20 mm (j). df = dorsal fin.
Extended Data Fig. 4 Further elements of the Haiyan Lagerstätte biota.
a, A probable juvenile specimen of the mollusk Wiwaxia sp., YKLP14473. b, A juvenile specimen of the problematicum Eldonia eumorpha, YKLP14474. c, A juvenile specimen of the chancelloriid Allonnia phrixothrix, YKLP14475. d, The cnidarian Xianguangia sinica, YKLP14476. e, A new ctenophoran, YKLP14477. f, The brachiopod Diandongia pista, YKLP14478. g, The brachiopod Lingulellotreta malongensis, YKLP14479. h, An indeterminate juvenile sponge, YKLP14480. i–k, Hyolithids. i, Ambrolinevitus ventricosus, YKLP14481. j, Burithes yunnanensis, YKLP14482, k, Burithes yunnanensis, YKLP14483. l, The cnidarian Archisaccophyllia kunmingensis, YKLP14484. m–p, Sponges. m, A new sponge, YKLP14485. n, Crumillospongia biporosa, YKLP144486. o, Choiaella radiata, YKLP14487. p, A new sponge, YKLP14488. q, The brachiopod Heliomedusa orienta, YKLP14489. r, The alga Fuxianospira gyrata, YKLP14490. Scale bars, 500 μm (e), 1 mm (c, n), 2 mm (a), 5 mm (b, d–m, o, q), 10 mm (p, r).
Extended Data Fig. 5 Further elements of the Haiyan Lagerstätte biota.
a, Molt of an indeterminate vetulicolian, YKLP14523. b, Molt of the deuterostome Yunnanozoon lividum, YKLP14524. c, Cluster of juvenile bivalved arthropods, recording possible gregarious behaviour, YKLP14525. d, Cluster of hemichordate fossils, recording possible gregarious behaviour, YKLP14526. e, Circular aggregate of trilobite and hyolith shell fragments, possibly a coprolite, YKLP14527. f, Burrows under the carapace of an indeterminate bivalved arthropod, YKLP14528. Scale bars, 5 mm (f), 10 mm (a, b), 20 mm (c–e).
Extended Data Fig. 6 Further arthropods from the Haiyan Lagerstätte.
a, Missizhouia longicaudata, YKLP14491. b, An uncertain juvenile arthropod, YKLP14492. c, A juvenile specimen of Tanglangia sp., YKLP14493. d, Kunmingella douvillei, YKLP14494. e, Primicaris larvaformis, YKLP 14495. f, Chuandianella ovata, YKLP14496. g, Fortiforceps foliosa, YKLP14497. h, Sunella sp., YKLP14498. i, Pectocaris sp., YKLP14499. j, Eoredlichia intermedia, YKLP14500. k, Naraoia spinosa, YKLP14501. l, Acanthomeridion sp., YKLP14502. m, Yunnanocephalus yunnanensis., YKLP14503. n, Isoxys auritus, YKLP14504. o, Chengjiangocaris sp., YKLP14505. p, Combinivalvula chengjiangensis, YKLP14506. q, A juvenile specimen of Chengjiangocaris sp., YKLP14507. Scale bars, 500 μm (b), 1 mm (e), 2 mm (a, d, n, p, q), 5 mm (b, c, f–l, o), 10 mm (m).
Extended Data Fig. 7 Vermiform fossils from the Haiyan Lagerstätte.
a–d, Priapulid worms. a, Palaeopriapulites parvus, YKLP14508. b, Sicyophorus rara, YKLP14509. c, Indeterminate priapulid worm, YKLP14510. d, Cricocosmia jinningensis, YKLP14511. e, Indeterminate vermiform fossil, YKLP14512. f–i, Priapulid worms f, Anningvermis multispinosa, YKLP14513. g, Xiaoheiqingella peculiaris, YKLP14514. h, Maotianshania cylindrica, YKLP14515. i, Yunnanpriapulus sp., YKLP14516. j, The lobopod Onychodictyon ferox, YKLP14517. k, The lobopod Hallucigenia fortis, YKLP14518. l, The priapulid worm Eximipriapulus sp., YKLP14519. m, Indeterminate vermiform fossil, YKLP14520. n, The priapulid worm Sicyophorus rara, YKLP14521. o, The lobopod Cardiodictyon catenulum, YKLP14522. Scale bars, 500 μm (k), 1 mm (a, m), 2 mm (b, c, i, j, l, n), 5 mm (e–h, o), 10 mm (d).
Extended Data Fig. 8 Exceptionally preserved new species from the Haiyan Lagerstätte.
a, A new Amiskwia sagittiformis-like animal, YKLP14435. b, close-up of the fin of (a). c, New chancelloriid sp. A., YKLP14436. d, New chancelloriid, sp. B., YKLP14437. e, The holotype of the deuterostome Herpetogaster haiyanensis, YKLP14404. f, New frond-like taxon, YKLP14438. g, New chaetognath preserving the gut with some gut content, YKLP14439. h, A new colonial hydroid, YKLP14440. i, Early ontogenetic stage of the new chaetognath, YKLP14441 j, k, New hemichordate, extending the range of the range of the Enteropneusta into the lower Cambrian. j, YKLP14442. k, YKLP14443. l, New wiwaxiid, preserving detailed sclerites, YKLP14444. m, New arthropod, YKLP14445. n, A new problematic taxon preserving fine spines (arrows), YKLP14446. o, New sponge, preserving detailed spicules, YKLP14447. p, New lophophorate preserving internal soft tissues, YKLP14448. Scale bars, 5 mm (a, e–i), 2 mm (b–d, l, k, m–p), 500 μm (j).
Extended Data Fig. 9 Adult arthropods from the Haiyan Lagerstätte.
a, A juvenile specimen of Saperion glumaceum, YKLP14460. b, Indeterminate bivalved arthropod, YKLP14461. c, Missizhouia longicaudata, YKLP14462. d, Pectocaris sp., YKLP14463. e, Parapaleomerus sp., YKLP14464. f, Posterior portion of thorax of an indeterminate arthropod, YKLP14465. g, Leanchoilia illecebrosa, YKLP14466. h, Isoxys paradoxus, YKLP14467. i, Indeterminate arthropod, YKLP14468. j, Amplectobelua symbrachiata, YKLP14469. k, Naraoia spinosa, YKLP14470. l, Haifengella corona, YKLP14471. m, Branchiocaris yunnanensis, YKLP14472. Scale bars, 1 mm (a), 5 mm (c, f), 10 mm (b, e, g, i, k, m), 20 mm (d, h, j, l).
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Yang, X., Kimmig, J., Zhai, D. et al. A juvenile-rich palaeocommunity of the lower Cambrian Chengjiang biota sheds light on palaeo-boom or palaeo-bust environments. Nat Ecol Evol 5, 1082–1090 (2021). https://doi.org/10.1038/s41559-021-01490-4
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DOI: https://doi.org/10.1038/s41559-021-01490-4
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