Possible evolution of mobile animals in association with microbial mats

Journal name:
Nature Geoscience
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Complex animals first evolved during the Ediacaran period, between 635 and 542 million years ago, when the oceans were just becoming fully oxygenated. In situ fossils of the mobile forms of these animals are associated with microbial sedimentary structures1, 2, 3, and the animal’s trace fossils generally were formed parallel to the surface of the seabed, at or below the sediment–water interface4, 5. This evidence suggests the earliest mobile animals inhabited settings with high microbial populations, and may have mined microbially bound sediments for food resources6, 7, 8. Here we report the association of mobile animals—insect larvae, oligochaetes and burrowing shore crabs—with microbial mats in a modern hypersaline lagoon in Venezuela. The lagoon is characterized by low concentrations of dissolved O2 and pervasive biomats dominated by oxygen-producing cyanobacteria, both analogous to conditions during the Ediacaran. We find that, during the day, O2 levels in the biomats are four times higher than in the overlying water column. We therefore conclude that the animals harvest both food and O2 from the biomats. In doing so, the animals produce horizontal burrows similar to those found in Ediacaran-aged rocks. We suggest that early mobile animals may have evolved in similar environments during the Ediacaran, effectively exploiting oases rich in O2 that formed within low oxygen settings.

At a glance


  1. Clark-type microelectrodes (50[thinsp][mu]M tip diameter) were used to measure the in situ[thinsp] O2 and H2S partial pressures in the bottom water, biomat and underlying sediment.
    Figure 1: Clark-type microelectrodes (50μM tip diameter) were used to measure the in situ O2 and H2S partial pressures in the bottom water, biomat and underlying sediment.

    Shown here are daytime profiles of dissolved O2 and H2S in the water above, and in the biolaminated sediments, at a, Augustana Lagoon and b, Pirata Lagoon. In both examples, O2 concentrations within the biomat (0 to −4mm) are substantially higher than the O2 concentrations in the overlaying water. In a, the H2S-producing zone is deeper than the probe’s terminal position. Night-time measurements are shown in Supplementary Fig. S3.

  2. Schematic showing behaviours associated with oxygen oases.
    Figure 2: Schematic showing behaviours associated with oxygen oases.

    a, Modern animal–biomat associations from Los Roques. b, Potential Upper Ediacaran and Lower Cambrian associations. Various lifestyles are illustrated: (i) free swimming animals that dive into zones of higher oxygen content; (ii) animals that reside in burrows isolated from the water column; (iii) open, branching networks provide access to the sediment–water interface and permit sub-mat feeding and exploitation of O2 above and below the biomat; (iv) burrows that maximize their surface area below biomats stand to increase O2 flux through the burrow wall; and (v) bottom-hugging animals residing within the oxycline.

  3. Examples of undermat trace fossils.
    Figure 3: Examples of undermat trace fossils.

    aOldhamia-like trace fossil preserved beneath biomat lamination; Ediacaran Rawnsley Quartzite, S. Australia (11cm wide). bEochondrites showing substantial below-mat exploitation. Back-fill structures are visible (indicated by ellipse). Upper Cambrian of Huquf, Oman (28cm wide). c, Back-filled tunnel mantled by biomat wrinkle structures; Early Cambrian Harkless Formation, California. As a result of back-filling during construction, animals associated with such traces would have drawn O2 from the biomat. d, Back-filled trace fossil associated with Kinneyia structures, which only form beneath biomats25, 26; Silurian Acacus Sandstone, Libya (cm scale lower right). a: bed sole; bd: bed tops.


  1. Droser, M. L., Gehling, J. G. & Jensen, S. R. Assemblage palaeoecology of the Ediacara biota: The unabridged edition?. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 131147 (2006).
  2. Fedonkin, M. A., Simonetta, A. & Ivantsov, A. Y. in The Rise and Fall of the Ediacaran Biota 157179 (Special Publications Vol. 286, Geological Society, 2007).
  3. Gehling, J. G. & Droser, M. L. Textured organic surfaces associated with the Ediacara biota in South Australia. Earth Sci. Rev. 96, 196206 (2009).
  4. Jensen, S., Droser, M. L. & Gehling, J. G. Trace fossil preservation and the early evolution of animals. Palaeogeogr. Palaeoclimatol. Palaeoecol. 220, 1929 (2005).
  5. Jensen, S., Droser, M. L. & Gehling, J. G. A critical look at the Ediacaran trace fossil record. Top. Geobiol. 27, 115157 (2006).
  6. Seilacher, A. & Pflüger, F. in Biostabilization of Sediments (eds Krumbein, W., Paterson, D. M. & Stal, L. J.) 97105 (Bibliotheks und Informationssystem der Universität Oldenburg, 1994).
  7. Gehling, J. G. Microbial mats in terminal Proterozoic siliciclastics; Ediacaran death masks. Palaios 14, 4057 (1999).
  8. Seilacher, A., Buatois, L. A. & Mangano, M. G. Trace fossils in the Ediacaran–Cambrian transition: Behavioural diversification, ecological turnover and environmental shift. Palaeogeogr. Palaeoclimatol. Palaeoecol. 227, 323356 (2005).
  9. Canfield, D. E. & Teske, A. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382, 127132 (1996).
  10. Canfield, D. E., Poulton, S. W. & Narbonne, G. M. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 9295 (2007).
  11. Canfield, D. E. & Des Marais, D. J. Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim. Cosmochim. Acta 57, 39713984 (1993).
  12. Martin, M. W. et al. Age of Neoproterozoic bilatarian body and trace fossils, White Sea, Russia: implications for metazoan evolution. Science 288, 841845 (2000).
  13. Liu, A. G., Mcllroy, D. & Brasier, M. D. First evidence for locomotion in the Ediacara biota from the 565ma Mistaken Point Formation, Newfoundland. Geology 38, 123126 (2010).
  14. Gehling, J. G. Taphonomy of the Terminal Proterozoic Ediacara Biota, South Australia. Doctoral, Univ. of California at Los Angeles, Univ. Microfilms (1996).
  15. Fedonkin, M. A. & Setoguchi, T. The origin of the Metazoa in the light of the Proterozoic fossil record. Paleontol. Res. 7, 941 (2003).
  16. Seilacher, A. & Hagadorn, J. W. Early molluscan evolution: evidence from the trace fossil record. Palaios 25, 565575 (2010).
  17. Seilacher, A. Biomat-related lifestyles in the Precambrian. Palaios 14, 8693 (1999).
  18. Jensen, S., Saylor, B. Z., Gehling, J. G. & Germs, G. J. B. Complex trace fossils from the terminal Proterozoic of Namibia. Geology 28, 143146 (2000).
  19. Brasier, M. D. Background to the Cambrian explosion. J. Geol. Soc. 149, 585587 (1992).
  20. McIlroy, D. & Logan, G. A. The impact of bioturbation on infaunal ecology and evolution during the Proterozoic–Cambrian transition. Palaios 14, 5872 (1999).
  21. Nagell, B. & Landahl, C. C. Resistance to anoxia of Chironomus plumosus and Chironomus anthracinus (Diptera) larvae. Ecography 1, 333336 (1978).
  22. Plotnick, R. E. Chemoreception, odor landscapes, and foraging in ancient marine landscapes. Palaeontol. Electron. 10, 11 (2007).
  23. Fossing, H. et al. Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374, 713715 (2002).
  24. Peterson, K. J., Cotton, J. A., Gehling, J. G. & Pisani, D. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Phil. Trans. R. Soc. B 363, 14351443 (2008).
  25. Pflüger, F. Matground structures and redox facies. Palaios 14, 2539 (1999).
  26. Porada, H., Ghergut, J. & Bouougri, E. H. Kinneyia-type wrinkle structures—critical review and model of formation. Palaios 23, 6577 (2008).

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  1. Department of Earth and Atmospheric Science, 1-26 Earth Science Building, University of Alberta, Edmonton, Alberta, T6G 2E3, Canada

    • Murray Gingras,
    • Ernesto Pecoits,
    • Daniel Petrash &
    • Kurt O. Konhauser
  2. Department of Earth Sciences, Denver Museum of Nature and Science, Denver, Colorado 80205, USA

    • James W. Hagadorn
  3. Department of Geology and Geophysics, Yale University, New Haven, Connecticut 06520, USA

    • Adolf Seilacher
  4. Laboratoire Domaines Océaniques, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, Place Nicholas Copernic, Technopôle Brest-Iroise, 29280 Plouzané, France

    • Stefan V. Lalonde


M.G. and K.O.K. conceived the study and led field operations: S.V.L., E.P. and D.P. executed different aspects of the data gathering and data analysis: J.W.H. and A.S. provided ancient rock-record examples. All of the authors contributed to the writing of the final manuscript.

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