Simple sediment rheology explains the Ediacara biota preservation

Abstract

The soft-bodied Ediacara biota (571–541 million years ago) represents the oldest complex large organisms in the fossil record, providing a bridge between largely microbial ecosystems of the Precambrian and the animal-dominated world of the Phanerozoic, potentially holding clues about the early evolution of Metazoa. However, the nature of most Ediacaran organisms remains unresolved, partly due to their enigmatic non-actualistic preservation. Here, we show that Flinders-style fossilization of Ediacaran organisms was promoted by unusually prolonged conservation of organic matter, coupled with differences in rheological behaviour of the over- and underlying sediments. In contrast with accepted models, cementation of overlying sand was not critical for fossil preservation, which is supported by the absence of cement in unweathered White Sea specimens and observations of soft sediment deformation in South Australian specimens. The rheological model, confirmed by laboratory simulations, implies that Ediacaran fossils do not necessarily reflect the external shape of the organism, but rather the morphology of a soft external or internal organic ‘skeleton’. The rheological mechanism provides new constraints on biological interpretations of the Ediacara biota.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Styles of preservation of the Ediacara biota fossils.
Fig. 2: Evidence for the absence of early diagenetic cementation in the White Sea and South Australian Ediacaran sections.
Fig. 3: Taphonomic laboratory experiments testing the Rheological model.
Fig. 4: The Rheological model of preservation of Ediacaran macrofossils.
Fig. 5: Dickinsonia overlapping with a negative structure below a clay pebble within sandstone.
Fig. 6: Organically preserved Ediacaran fossils, and Dickinsonia transitional between Flinders- and Nama-style preservation.

Data availability

All materials are available within the main text and Supplementary Information files. Palaeontological specimens from South Australia are stored at the South Australian Museum. Specimens from the White Sea area are stored at the Borissiak Palaeontological Institute. Thin sections and higher-quality images are available from the corresponding authors on request.

References

  1. 1.

    Fedonkin, M. A. & Waggoner, B. M. The late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature 388, 868–871 (1997).

    CAS  Article  Google Scholar 

  2. 2.

    Ivantsov, A. Y. Paleontological evidence for the supposed Precambrian occurrence of mollusks. Paleontol. J. 44, 1552–1559 (2010).

    Article  Google Scholar 

  3. 3.

    Antcliffe, J. B., Gooday, A. J. & Brasier, M. D. Testing the protozoan hypothesis for Ediacaran fossils: a developmental analysis of Palaeopascichnus. Palaeontology 54, 1157–1175 (2011).

    Article  Google Scholar 

  4. 4.

    Seilacher, A., Grazhdankin, D. & Legouta, A. Ediacaran biota: the dawn of animal life in the shadow of giant protists. Paleontol. Res. 7, 43–54 (2003).

    Article  Google Scholar 

  5. 5.

    Kolesnikov, A. V. et al. The oldest skeletal macroscopic organism Palaeopascichnus linearis. Precambrian Res. 316, 24–37 (2018).

    CAS  Article  Google Scholar 

  6. 6.

    Bobrovskiy, I., Hope, J. M., Krasnova, A., Ivantsov, A. & Brocks, J. J. Molecular fossils from organically preserved Ediacara biota reveal cyanobacterial origin for Beltanelliformis. Nat. Ecol. Evol. 2, 437–440 (2018).

    Article  Google Scholar 

  7. 7.

    Ivantsov, A. Y., Gritsenko, V. P., Konstantinenko, L. I. & Zakrevskaya, M. A. Revision of the problematic Vendian macrofossil Beltanelliformis (=Beltanelloides, Nemiana). Paleontol. J. 48, 1415–1440 (2014).

    Article  Google Scholar 

  8. 8.

    Xiao, S. & Laflamme, M. On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol. Evol. 24, 31–40 (2009).

    Article  Google Scholar 

  9. 9.

    Budd, G. E. & Jensen, S. The origin of the animals and a ‘Savannah’ hypothesis for early bilaterian evolution. Biol. Rev. 92, 446–473 (2017).

    Article  Google Scholar 

  10. 10.

    Brasier, M. D. & Antcliffe, J. B. Dickinsonia from Ediacara: a new look at morphology and body construction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 270, 311–323 (2008).

    Article  Google Scholar 

  11. 11.

    Droser, M. L., Gehling, J. G. & Jensen, S. R. Assemblage palaeoecology of the Ediacara biota: the unabridged edition? Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 131–147 (2006).

    Article  Google Scholar 

  12. 12.

    Dzik, J. Organic membranous skeleton of the Precambrian metazoans from Namibia. Geology 27, 519–522 (1999).

    Article  Google Scholar 

  13. 13.

    Parry, L. A. et al. Soft-bodied fossils are not simply rotten carcasses—toward a holistic understanding of exceptional fossil preservation. Bioessays 40, 1700167 (2018).

    Article  Google Scholar 

  14. 14.

    Narbonne, G. M. The Ediacara biota: Neoproterozoic origin of animals and their ecosystems. Annu. Rev. Earth Planet. Sci. 33, 421–442 (2005).

    CAS  Article  Google Scholar 

  15. 15.

    Waggoner, B. The Ediacaran biotas in space and time. Integr. Comp. Biol. 43, 104–113 (2003).

    Article  Google Scholar 

  16. 16.

    Grazhdankin, D. Patterns of distribution in the Ediacaran biotas: facies versus biogeography and evolution. Paleobiology 30, 203–221 (2004).

    Article  Google Scholar 

  17. 17.

    Boag, T. H., Darroch, S. A. F. & Laflamme, M. Ediacaran distributions in space and time: testing assemblage concepts of earliest macroscopic body fossils. Paleobiology 42, 574–594 (2016).

    Article  Google Scholar 

  18. 18.

    Wade, M. Preservation of soft-bodied animals in Precambrian sandstones at Ediacara, South Australia. Lethaia 1, 238–267 (1968).

    Article  Google Scholar 

  19. 19.

    Gehling, J. G. Microbial mats in terminal Proterozoic siliciclastics; Ediacaran death masks. Palaios 14, 40–57 (1999).

    Article  Google Scholar 

  20. 20.

    Liu, A. G. Framboidal pyrite shroud confirms the ‘death mask’ model for moldic preservation of Ediacaran soft-bodied organisms. Palaios 31, 259–274 (2016).

    Article  Google Scholar 

  21. 21.

    Gibson, B. M., Schiffbauer, J. D. & Darroch, S. A. F. Ediacaran-style decay experiments using mollusks and sea anemones. Palaios 33, 185–203 (2018).

    Article  Google Scholar 

  22. 22.

    Liu, A. G., McMahon, S., Matthews, J. J., Still, J. W. & Brasier, A. T. Petrological evidence supports the death mask model for the preservation of Ediacaran soft-bodied organisms in South Australia. Geology 47, 215–218 (2019).

    CAS  Article  Google Scholar 

  23. 23.

    Serezhnikova, E. A. in Advances in Stromatolite Geobiology 525–535 (Springer, Berlin & Heidelberg, 2011).

  24. 24.

    Tarhan, L. G., Hood, A. v. S., Droser, M. L., Gehling, J. G. & Briggs, D. E. G. Exceptional preservation of soft-bodied Ediacara biota promoted by silica-rich oceans. Geology 44, 951–954 (2016).

    CAS  Article  Google Scholar 

  25. 25.

    Callow, R. H. T. & Brasier, M. D. Remarkable preservation of microbial mats in Neoproterozoic siliciclastic settings: implications for Ediacaran taphonomic models. Earth Sci. Rev. 96, 207–219 (2009).

    Article  Google Scholar 

  26. 26.

    Gehling, J. G. & Droser, M. L. Textured organic surfaces associated with the Ediacara biota in South Australia. Earth Sci. Rev. 96, 196–206 (2009).

    CAS  Article  Google Scholar 

  27. 27.

    Seilacher, A. Biomat-related lifestyles in the Precambrian. Palaios 14, 86–93 (1999).

    Article  Google Scholar 

  28. 28.

    Dzik, J. Anatomical information content in the Ediacaran fossils and their possible zoological affinities. Integr. Comp. Biol. 43, 114–126 (2003).

    Article  Google Scholar 

  29. 29.

    Fedonkin, M. A. in Origin and Early Evolution of the Metazoa (eds Lipps, J. H. & Signor, P. W.) 87–129 (Springer, 1992).

  30. 30.

    Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Preservational modes in the Ediacaran Gaojiashan Lagerstätte: pyritization, aluminosilicification, and carbonaceous compression. Palaeogeogr. Palaeoclimatol. Palaeoecol. 326-328, 109–117 (2012).

    Article  Google Scholar 

  31. 31.

    Orr, P. J., Briggs, D. E. G. & Kearns, S. L. Cambrian Burgess Shale animals replicated in clay minerals. Science 281, 1173–1175 (1998).

    CAS  Article  Google Scholar 

  32. 32.

    Gehling, J., Droser, M., Jensen, S., Runnegar, B. & Briggs, D. Evolving form and function: fossils and development. In Proc. Symposium Honouring Adolf Seilacher for His Contributions to Paleontology, in Celebration of His 80th Birthday (ed. Briggs, D. E. G.) 43–66 (Yale Univ. Press, 2005).

  33. 33.

    Ivantsov, A. Y. Feeding traces of proarticulata—the Vendian metazoa. Paleontol. J. 45, 237–248 (2011).

    Article  Google Scholar 

  34. 34.

    Seilacher, A. Vendozoa: organismic construction in the Proterozoic biosphere. Lethaia 22, 229–239 (1989).

    Article  Google Scholar 

  35. 35.

    Evans, S. D., Droser, M. L. & Gehling, J. G. Dickinsonia liftoff: evidence of current derived morphologies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 434, 28–33 (2015).

    Article  Google Scholar 

  36. 36.

    Retallack, G. J. Were the Ediacaran fossils lichens? Paleobiology 20, 523–544 (1994).

    Article  Google Scholar 

  37. 37.

    Jeong, S. W., Locat, J., Leroueil, S. & Malet, J.-P. Rheological properties of fine-grained sediment: the roles of texture and mineralogy. Can. Geotech. J. 47, 1085–1100 (2010).

    CAS  Article  Google Scholar 

  38. 38.

    Darroch, S. A. F., Laflamme, M., Schiffbauer, J. D. & Briggs, D. E. G. Experimental formation of a microbial death mask. Palaios 27, 293–303 (2012).

    Article  Google Scholar 

  39. 39.

    Verruijt, A. An Introduction to Soil Mechanics Vol. 30 (Springer, 2018).

  40. 40.

    Panagiotopoulos, I., Voulgaris, G. & Collins, M. B. The influence of clay on the threshold of movement of fine sandy beds. Coast. Eng. 32, 19–43 (1997).

    Article  Google Scholar 

  41. 41.

    Tarhan, L. G., Droser, M. L., Gehling, J. G. & Dzaugis, M. P. Taphonomy and morphology of the Ediacara form genus Aspidella. Precambrian Res. 257, 124–136 (2015).

    CAS  Article  Google Scholar 

  42. 42.

    Burzynski, G., Narbonne, G. M., Alexander Dececchi, T. & Dalrymple, R. W. The ins and outs of Ediacaran discs. Precambrian Res. 300, 246–260 (2017).

    CAS  Article  Google Scholar 

  43. 43.

    Ivantsov, A. Y. Reconstruction of Charniodiscus yorgensis (Macrobiota from the Vendian of the White Sea). Paleontol. J. 50, 1–12 (2016).

    Article  Google Scholar 

  44. 44.

    Noffke, N. The criteria for the biogeneicity of microbially induced sedimentary structures (MISS) in Archean and younger, sandy deposits. Earth Sci. Rev. 96, 173–180 (2009).

    CAS  Article  Google Scholar 

  45. 45.

    Bobrovskiy, I. et al. Ancient steroids establish the Ediacaran fossil Dickinsonia as one of the earliest animals. Science 361, 1246–1249 (2018).

    CAS  Article  Google Scholar 

  46. 46.

    Steiner, M. & Reitner, J. Evidence of organic structures in Ediacara-type fossils and associated microbial mats. Geology 29, 1119–1122 (2001).

    Article  Google Scholar 

  47. 47.

    Kenchington, C. G. & Wilby, P. R. in Reading and Writing of the Fossil Record: Preservational Pathways to Exceptional Fossilization (eds Laflamme, M., Darroch, S. A. F. & Schiffbauer, J. D.) 101–122 (Cambridge Univ. Press, 2017).

  48. 48.

    Liu, A. G., McIlroy, D., Antcliffe, J. B. & Brasier, M. D. Effaced preservation in the Ediacara biota and its implications for the early macrofossil record. Palaeontology 54, 607–630 (2011).

    Article  Google Scholar 

  49. 49.

    Fedonkin, M. A., Simonetta, A. & Ivantsov, A. Y. New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. Geol. Soc. Lond. Spec. Publ. 286, 157–179 (2007).

    Article  Google Scholar 

  50. 50.

    Dzik, J. & Ivantsov, A. Y. Internal anatomy of a new Precambrian dickinsoniid dipleurozoan from northern Russia. Neues Jahrb. Geol. Palaontol. Monatsh. 385–396 (2002).

Download references

Acknowledgements

The study was funded by Australian Research Council grants DP160100607 and DP170100556 (to J.J.B.) and Russian Foundation for Basic Research project number 17-05-02212A (to I.B., A.K. and A.I). I.B. acknowledges an Australian Government Research Training Program stipend scholarship. The authors are grateful to A. Nagovitsyn, P. Rychkov, V. Rychkov, S. Rychkov, T. Rychkova and A. Makushkina for help in the field, L. Zaytseva for help with scanning electron microscopy imaging, J. M. Hope, J. Wurtzel, S. Eggins, A. Rummery and R. Kerr for providing materials for the taphonomic experiments, M.-A. Binnie and J. G. Gehling for providing access to the South Australian Museum collections, and N. J. Butterfield and A. G. Liu for helpful comments on this study.

Author information

Affiliations

Authors

Contributions

I.B. designed the study, studied the collections and developed the model. A.K. and I.B. performed the thin-section and scanning electron microscopy analyses. I.B., A.K., A.I. and E.L. participated in the field expeditions. A.I. and E.L. provided samples from the Borissiak Paleontological Institute (RAS) collections. I.B. and J.J.B. designed the taphonomic laboratory experiments. I.B. and J.J.B. wrote the paper with contributions from all authors.

Corresponding authors

Correspondence to Ilya Bobrovskiy or Jochen J. Brocks.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–6

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bobrovskiy, I., Krasnova, A., Ivantsov, A. et al. Simple sediment rheology explains the Ediacara biota preservation. Nat Ecol Evol 3, 582–589 (2019). https://doi.org/10.1038/s41559-019-0820-7

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing