Possible links between extreme oxygen perturbations and the Cambrian radiation of animals

Abstract

The role of oxygen as a driver for early animal evolution is widely debated. During the 21 Cambrian explosion, episodic radiations of major animal phyla occurred coincident with 22 repeated carbon isotope fluctuations. However, the driver of these isotope fluctuations and 23 potential links to environmental oxygenation are unclear. Here, we report high-resolution 24 carbon and sulphur isotope data for marine carbonates from the southeastern Siberian 25 Platform that document the canonical explosive phase of the Cambrian radiation from ~524 26 to ~514 Myr ago. These analyses demonstrate a strong positive covariation between 27 carbonate  13 C and carbonate-associated sulphate  34 S through five isotope cycles. 28 Biogeochemical modelling suggests that this isotopic coupling reflects periodic oscillations 29 in atmospheric O2 and the extent of shallow ocean oxygenation. Episodic maxima in the 30 biodiversity of animal phyla directly coincided with these extreme oxygen perturbations. 31 Conversely, the subsequent Botoman Toyonian animal extinction events (~514 to ~512 32Myr ago) coincided with decoupled isotope records that suggest a shrinking marine 33 sulphate reservoir and expanded shallow marine anoxia. We suggest that fluctuations in 34 oxygen availability in the shallow marine realm exerted a primary control on the timing and 35 tempo of biodiversity radiations at a crucial phase in the early history of animal life. 36 37The early Cambrian witnessed a dramatic diversification of animal body plans and 38 behaviours 1 , as well as between-species interactions and palaeocommunity innovations 2,3 , 39 ultimately leading to modern animal ecosystems. Ocean oxygenation is a commonly invoked 40 environmental pre-requisite 4 6 . However, some recent studies suggest that despite probable 41 low-oxygen conditions, the oceans exceeded requisite oxygen thresholds for simple animals, 42 such as sponges, well before the Cambrian Period 7,8 . Many of the new animal body plans and 43 lifestyles that appeared during the early Cambrian were associated with considerably higher 44 oxygen demands 9,10 . Fluctuations in the maximum dissolved oxygen content of surface 45 waters, or the extent of shallow ocean oxygenation, could therefore have played an important 46 role in regulating the pattern of Cambrian radiations. This brings into question the role of 47 55 single, large oxidised oceanic reservoir (dissolved sulphate and inorganic carbon), the isotopic 56 composition of which is governed by isotope fractionation during microbially-mediated 57 reduction to sulphide (ultimately preserved as pyrite) and organic carbon. Burial of these 58 reduced species represents the two main net sources of oxygen to the surface environment 12 59 14 , and also imprints on both the seawater sulphate sulphur isotope ( 34 S, as recorded by 60 carbonate-associated sulphate) and carbon isotope ( 13 C, as recorded in carbonate) records, 61 allowing redox changes in the surface environment to be traced through geologic time.62 63 Here we present...

Dynamic and synchronous changes in metazoan body size during the Cambrian Explosion

“…5A). In contrast to 31 , biogeochemical modelling of these cycles suggests that each positive carbon isotope excursions represents a pulse of oxygenation within highly productive anoxic oceans with relatively low sulphate concentration 35 . Additional positive feedbacks between ocean ventilation, phosphorus retention in sediments, and biological ventilation behaviour, may have also driven rapid bottom-water oxygenation leading to the re-establishment of anoxia so potentially creating the repetitive cycles.…”

“…The early Cambrian record on the Siberian Platform shows transient (0.5-2 Myr) coupled carbonate δ 13 C and carbonate-associated sulphate δ 34 S cycles (III-VII) 35 (Fig. 5A).…”

“…Additional positive feedbacks between ocean ventilation, phosphorus retention in sediments, and biological ventilation behaviour, may have also driven rapid bottom-water oxygenation leading to the re-establishment of anoxia so potentially creating the repetitive cycles. These extreme oxygen perturbations would have created temporarily expanded shallow habitable shelves, and an increased diversity of metazoans is inferred to have coincided with these intervals 35 . The Sinsk Event coincided with decoupling of the isotope records, suggesting a further shrinking of the marine sulphate reservoir, as well as expanded shallow marine anoxia.…”

On the co‐evolution of surface oxygen levels and animals

“…For example, the “Canfield ocean” featured anoxic and euxinic (sulfide‐rich) deep‐ocean conditions through the Proterozoic, relieved only by a relatively unidirectional rise in oxygen during the late Ediacaran (Canfield, ). Broader stratigraphic and geographic coverage, including onshore–offshore transects, as well as new redox proxies have provided a more nuanced view of Proterozoic redox with much less stability (Diamond & Lyons, ; Doyle, Poulton, Newton, Podkovyrov, & Bekker, ; He et al, ; Li, Cheng, et al, ; Li, Zhang, et al, ; Planavsky, Cole, et al, ; Planavsky, Slack, et al, ; Sperling et al, ; Tang, Shi, Wang, & Jiang, ). Any attempts to model Proterozoic redox conditions are similarly left with the conclusion that the marine redox landscape was patchy and complicated (Reinhard, Planavsky, Olson, Lyons, & Erwin, ).…”

Desequilibrio del ciclo del azufre y cambio ambiental durante el Período Ediacárico

“…The absence of a large DOM buffer in the ocean, climate and oxygen levels would have been rendered more vulnerable to change. There are tantalising hints that this may have been the case after c.550 Ma (Tostevin et al, 2019), and that the ocean redox balance remained sensitively balanced throughout the Ediacaran-Cambrian transition interval (He et al, 2019). If exhaustion of the DOM pool occurred during the Shuram anomaly, it is plausible to suppose that the subsequent expansion of aerobic Ediacaran fauna was an opportunistic radiation in response to a transient oxidant surplus.…”