Origin of animals at a time of chaotic oxygen levels

Every organism that you can easily see is a eukaryote, the vast majority of which depend on the availability of oxygen molecules. The range of genetic variation in a wide variety of eukaryotes suggests, using a molecular ‘clock’, that the first of them arose between 2000 to 1000 Ma ago. It possibly originated as a symbiotic assemblage of earlier prokaryote cells ‘bagged-up’ within a single cell wall: Lynn Margulis’s hypothesis of endosymbiosis. It had to have happened after the Great Oxygenation Event (GOE 2.4 to 2.2 Ga), before which free oxygen was present in the seas and atmosphere only at vanishingly small concentrations. Various single-celled fossil possibilities have been suggested to be the oldest members of the Eukarya but are not especially prepossessing, except for one bizarre assemblage in Gabon. The first inescapable sign that eukaryotes were around is the appearance of distinctive organic biomarkers in sediments about 720 Ma old. The Neoproterozoic is famous for its Snowball Earth episodes and the associated multiplicity of large though primitive animals during the Ediacaran Period (see: The rise of the eukaryotes; December 2017).

The records of carbon- and sulfur isotopes in Neo- and Mesoproterozoic sedimentary rocks are more or less flat lines after a mighty hiccup in the carbon and sulfur cycles that followed the GOE and the earliest recorded major glaciation of the Earth. The time between 2.0 and 1.0 Ga has been dubbed ‘the Boring Billion’. At about 900 Ma, both records run riot. Sulfur isotopes in sediments reveal the variations of sulfides and sulfates on the seafloor, which signify reducing and oxidising conditions respectively.  The δ13C record charts the burial of organic carbon and its release from marine sediments related to reducing and oxidising conditions in deep water. There were four major ‘excursions’ of δ13C during the Neoproterozoic, which became increasingly extreme. From constant anoxic, reducing conditions throughout the Boring Billion the Late Neoproterozoic ocean-floor experienced repeated cycles of low and high oxygenation reflected in sulfide and sulfate precipitation and by fluctuations in trace elements whose precipitation depends on redox conditions. By the end of the Cambrian, when marine animals were burgeoning, deep-water oxic-anoxic cycles had been smoothed out, though throughout the Phanerozoic eon anoxic events crop up from time to time.

Atmospheric levels of free oxygen relative to that today (scale is logarithmic) computed using combined carbon- and sulfur isotope records from marine sediments since 1500 Ma ago. The black line is the mean of 5,000 model runs, the grey area represents ±1 standard deviations. The pale blue area represents previous ‘guesstimates’. Vertical yellow bars are the three Snowball Earth events of the Late Neoproterozoic (Sturtian, Marinoan and Gaskiers). (Credit: Krause et al., Fig 1a)

The Late Neoproterozoic redox cycles suggest that oxygen levels in the oceans may have fluctuated too. But there are few reliable proxies for free oxygen. Until recently, individual proxies could only suggest broad, stepwise changes in the availability of oxygen: around 0.1% of modern abundance after the GOE until about 800 Ma; a steady rise to about 10% during the Late Neoproterozoic; a sharp rise to an average of roughly 80% at during the Silurian attributed to increased photosynthesis by land plants. But over the last few decades geochemists have devised a new approach based on variations on carbon and sulfur isotope data from which powerful software modelling can make plausible inferences about varying oxygen levels. Results from the latest version have just been published (Krause, A.J. et al. 2022. Extreme variability in atmospheric oxygen levels in the late Precambrian. Science Advances, v. 8, article 8191; DOI: 10.1126/sciadv.abm8191).

Alexander Krause of Leeds University, UK, and colleagues from University College London, the University of Exeter, UK and the Univerisité Claude Bernard, Lyon, France show that atmospheric oxygen oscillated between ~1 and 50 % of modern levels during the critical 740 to 540 Ma period for the origin and initial diversification of animals. Each major glaciation was associated with a rapid decline, whereas oxygen levels rebounded during the largely ice-free episodes. By the end of the Cambrian Period (485 Ma), by which time the majority of animal phyla had emerged, there appear to have been six such extreme cycles.

Entirely dependent on oxygen for their metabolism, the early animals faced periodic life-threatening stresses. In terms of oxygen availability the fluctuations are almost two orders of magnitude greater than those that animal life faced through most of the Phanerozoic. Able to thrive and diversify during the peaks, most animals of those times faced annihilation as O2 levels plummeted. These would have been periods when natural selection was at its most ruthless in the history of metazoan life on Earth. Its survival repeatedly faced termination, later mass extinctions being only partial threats. Each of those Phanerozoic events was followed by massive diversification and re-occupation of abandoned and new ecological niches. So too those Neoproterozoic organism that survived each massive environmental threat may have undergone adaptive radiation involving extreme changes in their form and function. The Ediacaran fauna was one that teemed on the sea floor, but with oxygen able to seep into the subsurface other faunas may have been evolving there exploiting dead organic matter. The only signs of that wholly new ecosystem are the burrows that first appear in the earliest Cambrian rocks. Evolution there would have ben rife but only expressed by those phyla that left it during the Cambrian Explosion.

There is a clear, empirical link between redox shifts and very large-scale glacial and deglaciation events. Seeking a cause for the dramatic cycles of climate, oxygen and life is not easy. The main drivers of the greenhouse effect COand methane had to have been involved, i.e. the global carbon cycle. But what triggered the instability after the ‘Boring Billion’? The modelled oxygen record first shows a sudden rise to above 10% of modern levels at about 900 Ma, with a short-lived tenfold decline at 800 Ma. Could the onset have had something to do with a hidden major development in the biosphere: extinction of prokaryote methane generators; explosion of reef-building and oxygen-generating stromatolites? How about a tectonic driver, such as the break-up of the Rodinia supercontinent? Then there are large extraterrestrial events … Maybe the details provided by Krause et al. will spur others to imaginative solutions. See also: How fluctuating oxygen levels may have accelerated animal evolution. Science Daily, 14 October 2022

A Lower Jurassic environmental crisis

Curiously, one of the largest environmental disruptions during the Phanerozoic Eon (i.e. since 541 Ma ago) does not stand out in the way that the ‘Big Five’ mass extinctions do. Each of them killed off between 70 and 95% of all marine species. The Jurassic was a period of biological recovery from the End-Triassic extinction 201 Ma ago. Throughout its ~50 Ma duration extinction rates were below the average for the Phanerozoic, and they remained relatively low until the K-Pg mass extinction that drew the Mesozoic Era to a close at 66 Ma. Nevertheless, there were significant extinctions, such as the demise of several lineages of herbivorous dinosaurs towards the end of the Early Jurassic followed by the rise of the familiar, long-necked variety of eusauropods. Marine organisms that secreted hard parts made of calcium carbonate also experienced a collapse then. From time to time during the Jurassic and Cretaceous Periods the oceans lost a great deal of dissolved oxygen, increasing the chances of organic carbon being buried in marine sediments. Such oceanic anoxia resulted in the widespread deposition of hydrocarbon source rocks in the form of black bituminous muds. Overall, both the Jurassic and Cretaceous experienced  greenhouse climatic conditions, with  atmospheric CO2 levels rising to almost 3000 ppm and oxygen levels significantly lower than the modern 21%. Sea levels rose by up to 200 metres, thought to be due to fast sea-floor spreading and large areas of warm, buoyant oceanic lithosphere.

A notable ocean-anoxia event took place during the Lower Jurassic, around 183 Ma ago at the start of the Toarcian Age. This stratigraphic level was penetrated by a 1.5 km borehole sunk in 2015-2016 at Mochras in North Wales, UK, on the shore of Cardigan Bay. The core provided the thickest and most complete record ever recovered for this event, and has been analysed in exquisite detail using many techniques. The most revealing data have been published by a multinational team led by scientists from Trinity College, Dublin (Ruhl, M. et al. 2022. Reduced plate motion controlled timing of Early Jurassic Karoo-Ferrar large igneous province volcanism. Science Advances, v. 8, article eabo0866; DOI: 10.1126/sciadv.abo0866).

Plate boundaries around Gondwanaland and the Karoo-Ferrar large igneous province in the Early Jurassic (small yellow dots show dated localities) . Large pink dots: positions of Tristan de Cunha and Bouvet hotspots at the time (Credit: Ruhl et al. Fig 1A)

At the start of the Toarcian (183.7 Ma) the 187Os/186Os ratio of the samples begins to rise from 0.3 to almost 0.8 to fall back to 0.3 by 180.8 Ma. Osmium isotopes are a measure of continental weathering, and this ‘excursion’ surely signifies significant global warming and increases in atmospheric humidity and acidity that broke down rocks at the continental surface. Over the same period δ13C rises, decreases to by far the lowest value in the Lower Jurassic, rises again to gradually fall back. The start of the Toarcian seems to have experienced a major release of carbon then a profound sequestration of organic carbon, presumably through burial of dead organisms in the black mudstones that signify anoxic conditions. Remarkably, the 95 m thick Toarcian black-mudstone sequence also reveals a tenfold increase in its content of the element mercury, from 20 to 200 parts per billion (ppb), peaking at the same time (~182.8 Ma) as the most negative δ13C value was reached: the acme of carbon sequestration. A coincidence of massive organic carbon burial and increased mercury in marine sediments also happened at the time of the end-Permian mass extinction, although that does not necessarily imply exactly the same mechanism.

The early Toarcian geochemical trends, however, coincide with the initiation and duration of the Karoo-Ferrar large igneous province, which formed flood basalts, igneous dyke swarms and large volcanic centres in South Africa and Antarctica. That LIP may have emitted mercury, but so too may have increased chemical weathering of the land surface. Whichever, mercury forms an organic compound (methyl mercury) in water bodies. Readily incorporated into living organisms, that could explain the close parallel between the δ13C and Hg records in the Jurassic sediment core from Wales. The Karoo-Ferrar igneous activity itself presents a bit of a conundrum, as suggested by Ruhl et al. It happened at the very time that there was a 120° change in the direction of motion of the tectonic plate carrying along Africa and, indeed, the Gondwanaland supercontinent during the Jurassic. The directional change also involved local plate movement stopping for a while. According to the authors, it wasn’t a fortuitous coincidence of two mantle plumes from the core-mantle boundary hitting the bottom of the continental lithosphere below Africa and Antarctica at this tectonic ‘U-turn’. It is more likely that the pause gave existing plumes the opportunity and time to ‘erode’ the base of the continental lithosphere and rise. Decompression melting would then have produced the voluminous magmas. The two plumes were in place for a very long time and created seamount chains as plates moved over them. Both are still volcanically active: Tristan de Cunha on the mid-Atlantic Ridge, and Bouvet Island at a triple junction between South Africa and Antarctica.

So, a venture to unravel a period of profound environmental change during the Early Jurassic, which didn’t result in mass extinction, may well have spawned a new model for massive igneous events that did. Ruhl et al. suggest that the short-lived Siberian, North Atlantic and East African Rift LIPs each seem to have coincided with short episodes of tectonic slowing-down: LIPs may result in dramatic environmental change, but at the whim of plate tectonics.

See also: https://scitechdaily.com/surprising-discovery-shows-how-slowing-of-continental-plate-movement-controlled-earths-largest-volcanic-events/