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Oxygen requirements for the Cambrian explosion

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Abstract

Hypoxic tolerance experiments may be helpful to constrain the oxygen requirement for animal evolution. Based on literature review, available data demonstrate that fishes are more sensitive to hypoxia than crustaceans and echinoderms, which in turn are more sensitive than annelids, whilst mollusks are the least sensitive. Mortalities occur where O2 concentrations are below 2.0 mg/L, equivalent to saturation with oxygen content about 25% PAL (present atmospheric level). Therefore, the minimal oxygen requirement for maintaining animal diversity since Cambrian is determined as 25% PAL. The traditional view is that a rise in atmospheric oxygen concentrations led to the oxygenation of the ocean, thus triggering the evolution of animals. Geological and geochemical studies suggest a constant increase of the oxygen level and a contraction of anoxic oceans during Ediacaran–Cambrian transition when the world oceans experienced a rapid diversification of metazoan lineages. However, fossil first appearances of animal phyla are obviously asynchronous and episodic, showing a sequence as: basal metazoans>lophotrochozoans>ecdysozoans and deuterostomes. According to hitherto known data of fossil record and hypoxic sensitivity of animals, the appearance sequence of different animals is broadly consistent with their hypoxic sensitivity: animals like molluscs and annelids that are less sensitive to hypoxia appeared earlier, while animals like echinoderms and fishes that are more sensitive to hypoxia came later. Therefore, it is very likely that the appearance order of animals is corresponding to the increasing oxygen level and/or the contraction of anoxic oceans during Ediacaran–Cambrian transition.

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References

  • Antcliffe, J. B., Callow, R. H. T., Brasier, M. D., 2014. Giving the Early Fossil Record of Sponges A Squeeze. Biological Reviews, 89: 972–1004

    Article  Google Scholar 

  • Berkner, L. V., Marshall, L. C., 1965. On the Origin and Rise of Oxygen Concentration in the Earth’s Atmosphere. Journal of Atmospheric Sciences, 22: 225–261

    Article  Google Scholar 

  • Blair, J. E., 2009. Animals (Metazoa). In: Hedges, S. B., Kumar, S., eds., The Timetree of Life. Oxford University Press, Oxford. 223–230

    Google Scholar 

  • Braddy, S. J., Poschmann, M., Tetlie, O. E., 2008. Giant Claw Reveals the Largest Ever Arthropod. Biology Letter, 4: 106–109

    Article  Google Scholar 

  • Butterfield, N. J., 2009. Oxygen, Animals and Oceanic Ventilation: An Alternative View. Geobiology, 7: 1–7

    Article  Google Scholar 

  • Campbell, I. H., Allen, C. M., 2008. Formation of Supercontinents Linked to Increases in Atmospheric Oxygen. Nature Geoscience, 1: 554–558

    Article  Google Scholar 

  • Campbell, I. H., Squire, R. J., 2010. The Mountains that Triggered the Late Neoproterozoic Increase in Oxygen: the Second Great Oxidation Event. Geochimica et Cosmochimica Acta, 74: 4187–4206

    Article  Google Scholar 

  • Canfield, D. E., 2005. The Early History of Atmospheric Oxygen: Homage to Robert M. Garrels. Annual Review of Earth and Planetary Science, 33: 1–36

    Article  Google Scholar 

  • Canfield, D. E., Poulton, S. W., Narbonne, G. M., 2007. Late-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life. Science, 315: 92–95

    Article  Google Scholar 

  • Catling, D. C., Glein, C. R., Zahnle, K. J., et al., 2005. Why O2 Is Required by Complex Life on Habitable Planets and the Concept of Planetary “Oxygenation Time”. Astrobiology, 5: 415–438

    Article  Google Scholar 

  • Chen, X., Ling, H. F., Vance, D., et al., 2015. Rise to Modern Levels of Ocean Oxygenation Coincided with the Cambrian Radiation of Animals. Nature Communications, 6:7142 (DOI: 10.1038/ncomms8142)

    Article  Google Scholar 

  • Cloud, P. E Jr., 1948. Some Problems and Patterns of Evolution Exemplified by Fossil Invertebrates. Evolution, 2: 322–350

    Article  Google Scholar 

  • Cloud, P. E., 1976. Beginnings of Biospheric Evolution and Their Biogeochemical Consequences. Paleobiology, 2: 351–387

    Google Scholar 

  • Conway M. S., Peel, J. S., 2008. The Earliest Annelids: Lower Cambrian Polychaetes from the Sirius Passet Lagerstätte, Peary Land, North Greenland. Acta Palaeontologica Polonica, 53: 137–148

    Article  Google Scholar 

  • Danovaro, R., Dell’Anno, A., Pusceddu, A., Gambi, C., Heiner, I., Kristensen, R.M., 2010. The First Metazoa Living in Permanently Anoxic Conditions. BMC Biology, 8: 30.

    Article  Google Scholar 

  • Decker, H., van Holde, K. E., 2011. Oxygen and the Evolution of Life. Springer, Berlin. 172

    Book  Google Scholar 

  • Diaz, R. J., Rosenberg, R., 1995. Marine Benthic Hypoxia: A Review of Its Ecological Effects and the Behavioural Responses of Benthic Macrofauna. Oceanography and Marine Biology: An Annual Review, 33: 245–303

    Google Scholar 

  • Dries, R. R., Theede, H., 1974. Sauerstoffmangelresistenz Mariner Bodenvertebraten aus der Westlichen Ostsee. Marine Biology, 25: 327–333

    Article  Google Scholar 

  • Erwin, D. H., Laflamme, M., Tweedt, S. M., et al. 2011. The Cambrian Conundrum: Early Divergence and Later Ecological Success in the Early History of Animals. Science, 334: 1901–1907

    Article  Google Scholar 

  • Erwin, D. H., Tweedt, S., 2012. Ecological Drivers of the Ediacaran-Cambrian Diversification of Metazoa. Evolutionary Ecology, 26: 417–433

    Article  Google Scholar 

  • Erwin, D. H., Valentine, J. W., 2013. The Cambrian Explosion: the Construction of Animal Biodiversity. Roberts and Company Publishers, Inc., Greenwood Village. 406

    Google Scholar 

  • Fedonkin, M. A., Waggoner, B. M., 1997. The Late Precambrian Fossil Kimberella Is a Mollusc-Like Bilaterian Organism. Nature, 388: 868–871

    Article  Google Scholar 

  • Feng, L. J., Li, C., Huang, J., et al., 2014. A sulfate Control on Marine Mid-Depth Euxinia on the Early Cambrian (Ca. 529-521 Ma) Yangtze Platform, South China. Precambrian Research, 246: 123–133

    Google Scholar 

  • Gray, J. S., Wu, R. S., Or, Y. Y., 2002. Effects of Hypoxia and Organic Enrichment on the Coastal Marine Environment. Marine Ecology Progress Series, 238: 249–270

    Article  Google Scholar 

  • Henriksson, R., 1969. Influence of Pollution on the Bottom Fauna of the Sound (Öresund). Oikos, 20: 507–523

    Article  Google Scholar 

  • Hua, H., Chen, Z., Yuan, X. L., et al., 2005. Skeletogenesis and Asexual Reproduction in the Earliest Biomineralizing Animal Cloudina. Geology, 33: 277–280

    Article  Google Scholar 

  • Jin, C. S., Li, C., Peng, X. F., et al., 2014. Spatiotemporal Variability of Ocean Chemistry in the Early Cambrian, South China. Science China: Earth Science, 57: 579–591

    Article  Google Scholar 

  • Kasting, J. F., 1993. Earth’s Early Atmosphere. Science, 259: 920–926

    Article  Google Scholar 

  • Kendall, B., Anbar, A. D., Kappler, A., et al., 2012. The Global Iron Cycle. In: Knoll, A. H., Canfield, D. E., Konhauser, K. O., eds., Fundamentals of Geobiology. Wiley-Blackewll, Oxford. 65–92

    Chapter  Google Scholar 

  • Knoll, A. H., Sperling, E. A., 2014. Oxygen and Animals in Earth History. Proceedings of the National Academy of Sciences of the United States of America, 111: 3907–3908

    Article  Google Scholar 

  • Knoll, A.H., Carroll, S.B., 1999. Early Animal Evolution: Emerging Views from Comparative Biology and Geology. Science, 284: 2129–2137

    Article  Google Scholar 

  • Knoll, A. H., Walter, M. R., 1992. Latest Proterozoic Stratigraphy and Earth History. Nature, 356: 673–678

    Article  Google Scholar 

  • Kouchinsky, A., Bengtson, S., Clausen, S., et al., 2015. A Lower Cambrian Fauna of Skeletal Fossils from the Emyaksin Formation, Northern Siberia. Acta Palaeontologica Polonica (in press).

    Google Scholar 

  • Kouchinsky, A., Bengtson, S., Runnegar, B., et al., 2012. Chronology of Early Cambrian Biomineralization. Geological Magazine, 149: 221–251

    Article  Google Scholar 

  • Kump, L. R., 2008. The Rise of Atmospheric Oxygen. Nature, 451: 277–278

    Article  Google Scholar 

  • Landing, E., Geyer, G., Brasier, M. D., et al., 2013. Cambrian Evolutionary Radiation: Context, Correlation, and Chronostratigraphy—Overcoming Deficiencies of the First Appearance Datum (FAD) Concept. Earth-Science Reviews, 123: 133–172

    Article  Google Scholar 

  • Li, C., Love, G. D., Lyons, T. W., et al., 2010. A Stratified Redox Model for the Ediacaran Ocean. Science, 328: 80–83

    Article  Google Scholar 

  • Li, Z. X., Powell, C. M., 2001. An Outline of the Palaeongeographic Evolution of the Australasian Region since the Beginning of the Neoproterozoic. Earth-Science Review, 53: 237–277

    Article  Google Scholar 

  • Ling, H. F., Chen, X., Li, D., et al., 2013. Cerium Anomaly Variations in Ediacaran–Earliest Cambrian Carbonates from the Yangtze Gorges Area, South China: Implications for Oxygenation of Coeval Shallow Seawater. Precambrian Research, 225: 110–127

    Article  Google Scholar 

  • Love, G. D., Grosjean, E., Fike, D. A., et al., 2009. Fossil Steroid Record the Appearance of Demospongiae during the Cryogenian Period. Nature, 457: 718–721

    Article  Google Scholar 

  • Lyons, T. W., Reinhard, C. T., Love, G. D., et al., 2012. Geobiology of the Proterozoic Eon. In: Knoll, A. H., Canfield, D. E., Konhauser, K. O., eds., Fundamentals of Geobiology. Wiley-Blackewll, Oxford. 371–402

    Chapter  Google Scholar 

  • Mángano, M. G., Buatois, L. A., 2014. Decoupling of Body-Plan Diversification and Ecological Structuring during the Ediacaran–Cambrian Transition: Evolutionary and Geobiological Feedbacks. Proceedings of the Royal Society B 281, 20140038.

    Article  Google Scholar 

  • Meert, J. G., 2003. Proterozoic East Gondwana: Supercontinent Assembly and Breakup. Special Publication 206, Eos, Transactions American Geophysical Union, 84: 372

    Article  Google Scholar 

  • Meert, J. G., 2011. Gondwanaland, Formation. In: Reitner, J., Thiel, V., eds., Encyclopedia of Geobiology, Springer, Berlin. 434–436

    Chapter  Google Scholar 

  • Mentel, M., Martin, W., 2010. Anaerobic Animals from an Ancient, Anoxic Ecological Niche. BMC Biology, 8: 32

    Article  Google Scholar 

  • Miller D. C., Poucher SL., Coiro L., et al., 1995. Effects of Hypoxia on Growth and Survival of Crustaceans and Fishes of Long Island Sound. In: McElroy A., Zeidner J., eds., Proceedings of the Long Island Sound Research Conference: Is the Sound Getting Better or Worse. New York Sea Grant Institute, Stony Brook, NY, p1–92

    Google Scholar 

  • Mills, D. B, Ward, L. M., Jones, C. A., et al., 2014. Oxygen Requirements of the Earliest Animals. Proceedings of the National Academy of Sciences of the United States of America, 111: 4168–4172

    Article  Google Scholar 

  • Nielsen, C., 2012 (3rd edition). Animal Evolution: Interrelationships of the Living Phyla. Oxford University Press, Oxford. 402

    Google Scholar 

  • Papineau, D., 2010. Global Biogeochemical Changes at Both Ends of the Proterozoic: Insights from Phosphorites. Astrobiology, 10: 165–181

    Article  Google Scholar 

  • Partin, C. A., Bekker, A., Planavsky, N. J., et al., 2013. Large-Scale Fluctuations in Precambrian Atmospheric and Oceanic Oxygen Levels from the Record of U in Shales. Earth and Planetary Science Letter, 369–370: 284–293

    Article  Google Scholar 

  • Petsch, S. T., 2004. The Global Oxygen Cycle. In: Schlesinger, W. H., ed., Biogeochemistry. Treatise on Geochemistry, 8: 515–555

    Google Scholar 

  • Planavsky, N. J., Rouxel, O. J., Bekker, A., et al., 2010. The Evolution of the Marine Phosphate Reservoir. Nature, 467: 1088–1090

    Article  Google Scholar 

  • Rhoads, D. C., Morse, J. W., 1971. Evolutionary and Ecological Significance of Oxygen-Deficient Marine Basins. Lethaia, 4: 413–428

    Article  Google Scholar 

  • Rogers, J. J. W., Santosh, M., 2004. Continents and Supercontinents. Oxford University Press, Oxford. 289

    Google Scholar 

  • Rosenberg, R., 1972. Benthic Faunal Recovery in a Swedish Fjord Following the Closure of a Sulphite Pulp Mill. Oikos, 23: 92–108

    Article  Google Scholar 

  • Runnegar, B., 1982. Oxygen Requirements, Biology and Phylogenetic Significance of the Late Precambrian Worm Dickinsonia, and the Evolution of the Burrowing Habit. Alcheringa, 6: 223–239

    Article  Google Scholar 

  • Runnegar, B., 1991. Precambrian Oxygen Levels Estimated from the Biochemistry and Physiology of Early Eukaryotes. Global and Planetary Change, 97: 97–111

    Article  Google Scholar 

  • Shu, D. G., Luo, H. L., Conway Morris, S., et al., 1999. Lower Cambrian Vertebrates from South China. Nature, 402: 42–46

    Article  Google Scholar 

  • Shu, D. G., Isozaki, Y., Zhang, X. L., et al., 2014. Birth and Early Evolution of Metazoans. Gondwana Research, 25: 884–895

    Article  Google Scholar 

  • Skovsted, C., B., Peel, J. S., 2011. Hyolithellus in life position from the Lower Cambrian of North Greenland. Journal of Paleontology, 85: 37–47

    Article  Google Scholar 

  • Sperling, E. A., Frieder, C. A., Raman, A. V., 2013a. Oxygen, Ecology, and the Cambrian Radiation of Animals. Proceedings of the National Academy of Sciences of the United States of America, 110: 13446–13451

    Article  Google Scholar 

  • Sperling, E. A., Halverson, G. P., Knoll., A. H., et al., 2013b. A Basin Redox Transect at the Dawn of Animal Life. Earth and Planetary Science Letter, 371–372: 143–155

    Article  Google Scholar 

  • Wang, J. G., Chen, D. Z., Yan, D. T., et al., 2012. Evolution from An Anoxic to Oxic Deep Ocean during the Ediacaran–Cambrian Transition and Implications for Bioradiation. Chemical Geology, 306: 129–138

    Article  Google Scholar 

  • Wang, H., Li, C., Hu, C., et al., 2015. Spurious Thermoluminescence Characteristics of the Ediacaran Doushantuo Formation (Ca. 635–551 Ma) and Its Implications for Marine Dissolved Organic Carbon Reservoir. Journal of Earth Science, 26(6): 883–892

    Google Scholar 

  • Wen, H. J., Carignan, J., Chu, X. L., et al., 2014. Selenium Isotopes Trace Anoxic and Ferruginous Seawater Conditions in the Early Cambrian. Chemical Geology, 390: 164–172

    Article  Google Scholar 

  • Wang, Y., Wang, X. L., Wang, Y., 2015. Cambrian Ichnofossils from the Zhoujieshan Formation (Quanji Group) Overlying Tillites in the Northern Margin of the Qaidam Basin, NW China. Journal of Earth Science, 26(2): 203–210

    Article  Google Scholar 

  • Wray, G. A., 2015. Molecular Clocks and the Early Evolution of Metazoan Nervous Systems. Philosophical Transactions of the Royal Society Series B, 370 (150046), 1–11

    Google Scholar 

  • Yang, B., Steiner, M., Li, G. X., et al., 2014. Terreneuvian Small Shelly Faunas of East Yunnan (South China) and Their Biostratigraphic Implications. Palaeogeography, Palaeoclimatology, Palaeoecology, 398: 28–58

    Article  Google Scholar 

  • Yin, Z. J., Zhu, M. Y., Davidson, E. H., et al., 2015. Sponge Grade Body Fossil with Cellular Resolution Dating 60 Myr before the Cambrian. Proceedings of the National Academy of Sciences of the United States of America, 112: E1453–1460

    Google Scholar 

  • Zhang, X. L., Shu, D. G., 2014. Causes and Consequences of the Cambrian Explosion. Science China—Earth Sciences, 57: 930–942

    Google Scholar 

  • Zhang, X., Shu, D., Han, J., et al., 2014. Triggers for the Cambrian Explosion: Hypotheses and Problems. Gondwana Research, 25: 896–909

    Article  Google Scholar 

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  1. Early Life Institute and State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University, Xian, 710069, China

    Xingliang Zhang & Linhao Cui

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Zhang, X., Cui, L. Oxygen requirements for the Cambrian explosion. J. Earth Sci. 27, 187–195 (2016). https://doi.org/10.1007/s12583-016-0690-8

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