Evolution of the global phosphorus cycle.

The macronutrient phosphorus is thought to limit primary productivity in the oceans on geological timescales. Although there has been a sustained effort to reconstruct the dynamics of the phosphorus cycle over the past 3.5 billion years, it remains uncertain whether phosphorus limitation persisted throughout Earth's history and therefore whether the phosphorus cycle has consistently modulated biospheric productivity and ocean-atmosphere oxygen levels over time. Here we present a compilation of phosphorus abundances in marine sedimentary rocks spanning the past 3.5 billion years. We find evidence for relatively low authigenic phosphorus burial in shallow marine environments until about 800 to 700 million years ago. Our interpretation of the database leads us to propose that limited marginal phosphorus burial before that time was linked to phosphorus biolimitation, resulting in elemental stoichiometries in primary producers that diverged strongly from the Redfield ratio (the atomic ratio of carbon, nitrogen and phosphorus found in phytoplankton). We place our phosphorus record in a quantitative biogeochemical model framework and find that a combination of enhanced phosphorus scavenging in anoxic, iron-rich oceans and a nutrient-based bistability in atmospheric oxygen levels could have resulted in a stable low-oxygen world. The combination of these factors may explain the protracted oxygenation of Earth's surface over the last 3.5 billion years of Earth history. However, our analysis also suggests that a fundamental shift in the phosphorus cycle may have occurred during the late Proterozoic eon (between 800 and 635 million years ago), coincident with a previously inferred shift in marine redox states, severe perturbations to Earth's climate system, and the emergence of animals.

Atmosphere-ocean oxygen and productivity dynamics during early animal radiations.

The proliferation of large, motile animals 540 to 520 Ma has been linked to both rising and declining O2 levels on Earth. To explore this conundrum, we reconstruct the global extent of seafloor oxygenation at approximately submillion-year resolution based on uranium isotope compositions of 187 marine carbonates samples from China, Siberia, and Morocco, and simulate O2 levels in the atmosphere and surface oceans using a mass balance model constrained by carbon, sulfur, and strontium isotopes in the same sedimentary successions. Our results point to a dynamically viable and highly variable state of atmosphere-ocean oxygenation with 2 massive expansions of seafloor anoxia in the aftermath of a prolonged interval of declining atmospheric pO2 levels. Although animals began diversifying beforehand, there were relatively few new appearances during these dramatic fluctuations in seafloor oxygenation. When O2 levels again rose, it occurred in concert with predicted high rates of photosynthetic production, both of which may have fueled more energy to predators and their armored prey in the evolving marine ecosystem.

Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation.

Sedimentary rocks deposited across the Proterozoic-Phanerozoic transition record extreme climate fluctuations, a potential rise in atmospheric oxygen or re-organization of the seafloor redox landscape, and the initial diversification of animals. It is widely assumed that the inferred redox change facilitated the observed trends in biodiversity. Establishing this palaeoenvironmental context, however, requires that changes in marine redox structure be tracked by means of geochemical proxies and translated into estimates of atmospheric oxygen. Iron-based proxies are among the most effective tools for tracking the redox chemistry of ancient oceans. These proxies are inherently local, but have global implications when analysed collectively and statistically. Here we analyse about 4,700 iron-speciation measurements from shales 2,300 to 360 million years old. Our statistical analyses suggest that subsurface water masses in mid-Proterozoic oceans were predominantly anoxic and ferruginous (depleted in dissolved oxygen and iron-bearing), but with a tendency towards euxinia (sulfide-bearing) that is not observed in the Neoproterozoic era. Analyses further indicate that early animals did not experience appreciable benthic sulfide stress. Finally, unlike proxies based on redox-sensitive trace-metal abundances, iron geochemical data do not show a statistically significant change in oxygen content through the Ediacaran and Cambrian periods, sharply constraining the magnitude of the end-Proterozoic oxygen increase. Indeed, this re-analysis of trace-metal data is consistent with oxygenation continuing well into the Palaeozoic era. Therefore, if changing redox conditions facilitated animal diversification, it did so through a limited rise in oxygen past critical functional and ecological thresholds, as is seen in modern oxygen minimum zone benthic animal communities.

Thallium isotopes reveal protracted anoxia during the Toarcian (Early Jurassic) associated with volcanism, carbon burial, and mass extinction.

For this study, we generated thallium (Tl) isotope records from two anoxic basins to track the earliest changes in global bottom water oxygen contents over the Toarcian Oceanic Anoxic Event (T-OAE; ∼183 Ma) of the Early Jurassic. The T-OAE, like other Mesozoic OAEs, has been interpreted as an expansion of marine oxygen depletion based on indirect methods such as organic-rich facies, carbon isotope excursions, and biological turnover. Our Tl isotope data, however, reveal explicit evidence for earlier global marine deoxygenation of ocean water, some 600 ka before the classically defined T-OAE. This antecedent deoxygenation occurs at the Pliensbachian/Toarcian boundary and is coeval with the onset of initial large igneous province (LIP) volcanism and the initiation of a marine mass extinction. Thallium isotopes are also perturbed during the T-OAE interval, as defined by carbon isotopes, reflecting a second deoxygenation event that coincides with the acme of elevated marine mass extinctions and the main phase of LIP volcanism. This suggests that the duration of widespread anoxic bottom waters was at least 1 million years in duration and spanned early to middle Toarcian time. Thus, the Tl data reveal a more nuanced record of marine oxygen depletion and its links to biological change during a period of climatic warming in Earth's past and highlight the role of oxygen depletion on past biological evolution.

Geochemical evidence for widespread euxinia in the later Cambrian ocean.

Widespread anoxia in the ocean is frequently invoked as a primary driver of mass extinction as well as a long-term inhibitor of evolutionary radiation on early Earth. In recent biogeochemical studies it has been hypothesized that oxygen deficiency was widespread in subsurface water masses of later Cambrian oceans, possibly influencing evolutionary events during this time. Physical evidence of widespread anoxia in Cambrian oceans has remained elusive and thus its potential relationship to the palaeontological record remains largely unexplored. Here we present sulphur isotope records from six globally distributed stratigraphic sections of later Cambrian marine rocks (about 499 million years old). We find a positive sulphur isotope excursion in phase with the Steptoean Positive Carbon Isotope Excursion (SPICE), a large and rapid excursion in the marine carbon isotope record, which is thought to be indicative of a global carbon cycle perturbation. Numerical box modelling of the paired carbon sulphur isotope data indicates that these isotope shifts reflect transient increases in the burial of organic carbon and pyrite sulphur in sediments deposited under large-scale anoxic and sulphidic (euxinic) conditions. Independently, molybdenum abundances in a coeval black shale point convincingly to the transient spread of anoxia. These results identify the SPICE interval as the best characterized ocean anoxic event in the pre-Mesozoic ocean and an extreme example of oxygen deficiency in the later Cambrian ocean. Thus, a redox structure similar to those in Proterozoic oceans may have persisted or returned in the oceans of the early Phanerozoic eon. Indeed, the environmental challenges presented by widespread anoxia may have been a prevalent if not dominant influence on animal evolution in Cambrian oceans.

Proterozoic ocean redox and biogeochemical stasis.

The partial pressure of oxygen in Earth's atmosphere has increased dramatically through time, and this increase is thought to have occurred in two rapid steps at both ends of the Proterozoic Eon (∼2.5-0.543 Ga). However, the trajectory and mechanisms of Earth's oxygenation are still poorly constrained, and little is known regarding attendant changes in ocean ventilation and seafloor redox. We have a particularly poor understanding of ocean chemistry during the mid-Proterozoic (∼1.8-0.8 Ga). Given the coupling between redox-sensitive trace element cycles and planktonic productivity, various models for mid-Proterozoic ocean chemistry imply different effects on the biogeochemical cycling of major and trace nutrients, with potential ecological constraints on emerging eukaryotic life. Here, we exploit the differing redox behavior of molybdenum and chromium to provide constraints on seafloor redox evolution by coupling a large database of sedimentary metal enrichments to a mass balance model that includes spatially variant metal burial rates. We find that the metal enrichment record implies a Proterozoic deep ocean characterized by pervasive anoxia relative to the Phanerozoic (at least ∼30-40% of modern seafloor area) but a relatively small extent of euxinic (anoxic and sulfidic) seafloor (less than ∼1-10% of modern seafloor area). Our model suggests that the oceanic Mo reservoir is extremely sensitive to perturbations in the extent of sulfidic seafloor and that the record of Mo and chromium enrichments through time is consistent with the possibility of a Mo-N colimited marine biosphere during many periods of Earth's history.

Sulfur isotopes track the global extent and dynamics of euxinia during Cretaceous Oceanic Anoxic Event 2.

The Mesozoic Era is characterized by numerous oceanic anoxic events (OAEs) that are diagnostically expressed by widespread marine organic-carbon burial and coeval carbon-isotope excursions. Here we present coupled high-resolution carbon- and sulfur-isotope data from four European OAE 2 sections spanning the Cenomanian-Turonian boundary that show roughly parallel positive excursions. Significantly, however, the interval of peak magnitude for carbon isotopes precedes that of sulfur isotopes with an estimated offset of a few hundred thousand years. Based on geochemical box modeling of organic-carbon and pyrite burial, the sulfur-isotope excursion can be generated by transiently increasing the marine burial rate of pyrite precipitated under euxinic (i.e., anoxic and sulfidic) water-column conditions. To replicate the observed isotopic offset, the model requires that enhanced levels of organic-carbon and pyrite burial continued a few hundred thousand years after peak organic-carbon burial, but that their isotope records responded differently due to dramatically different residence times for dissolved inorganic carbon and sulfate in seawater. The significant inference is that euxinia persisted post-OAE, but with its global extent dwindling over this time period. The model further suggests that only ~5% of the global seafloor area was overlain by euxinic bottom waters during OAE 2. Although this figure is ~30× greater than the small euxinic fraction present today (~0.15%), the result challenges previous suggestions that one of the best-documented OAEs was defined by globally pervasive euxinic deep waters. Our results place important controls instead on local conditions and point to the difficulty in sustaining whole-ocean euxinia.

Pulse of atmospheric oxygen during the late Cambrian.

A rise in atmospheric O(2) has been linked to the Cambrian explosion of life. For the plankton and animal radiation that began some 40 million yr later and continued through much of the Ordovician (Great Ordovician Biodiversification Event), the search for an environmental trigger(s) has remained elusive. Here we present a carbon and sulfur isotope mass balance model for the latest Cambrian time interval spanning the globally recognized Steptoean Positive Carbon Isotope Excursion (SPICE) that indicates a major increase in atmospheric O(2). We estimate that this organic carbon and pyrite burial event added approximately 19 × 10(18) moles of O(2) to the atmosphere (i.e., equal to change from an initial starting point for O(2) between 10-18% to a peak of 20-28% O(2)) beginning at approximately 500 million years. We further report on new paired carbon isotope results from carbonate and organic matter through the SPICE in North America, Australia, and China that reveal an approximately 2‰ increase in biological fractionation, also consistent with a major increase in atmospheric O(2). The SPICE is followed by an increase in plankton diversity that may relate to changes in macro- and micronutrient abundances in increasingly oxic marine environments, representing a critical initial step in the trophic chain. Ecologically diverse plankton groups could provide new food sources for an animal biota expanding into progressively more ventilated marine habitats during the Ordovician, ultimately establishing complex ecosystems that are a hallmark of the Great Ordovician Biodiversification Event.

Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish.

The evolution of Earth's biota is intimately linked to the oxygenation of the oceans and atmosphere. We use the isotopic composition and concentration of molybdenum (Mo) in sedimentary rocks to explore this relationship. Our results indicate two episodes of global ocean oxygenation. The first coincides with the emergence of the Ediacaran fauna, including large, motile bilaterian animals, ca. 550-560 million year ago (Ma), reinforcing previous geochemical indications that Earth surface oxygenation facilitated this radiation. The second, perhaps larger, oxygenation took place around 400 Ma, well after the initial rise of animals and, therefore, suggesting that early metazoans evolved in a relatively low oxygen environment. This later oxygenation correlates with the diversification of vascular plants, which likely contributed to increased oxygenation through the enhanced burial of organic carbon in sediments. It also correlates with a pronounced radiation of large predatory fish, animals with high oxygen demand. We thereby couple the redox history of the atmosphere and oceans to major events in animal evolution.

A sedimentary record of the evolution of the global marine phosphorus cycle.

Phosphorus (P) is typically considered to be the ultimate limiting nutrient for Earth's biosphere on geologic timescales. As P is monoisotopic, its sedimentary enrichment can provide some insights into how the marine P cycle has changed through time. A previous compilation of shale P enrichments argued for a significant change in P cycling during the Ediacaran Period (635-541 Ma). Here, using an updated P compilation-with more than twice the number of samples-we bolster the case that there was a significant transition in P cycling moving from the Precambrian into the Phanerozoic. However, our analysis suggests this state change may have occurred earlier than previously suggested. Specifically in the updated database, there is evidence for a transition ~35 million years before the onset of the Sturtian Snowball Earth glaciation in the Visingsö Group, potentially divorcing the climatic upheavals of the Neoproterozoic from changes in the Earth's P cycle. We attribute the transition in Earth's sedimentary P record to the onset of a more modern-like Earth system state characterized by less reducing marine conditions, higher marine P concentrations, and a greater predominance of eukaryotic organisms encompassing both primary producers and consumers. This view is consistent with organic biomarker evidence for a significant eukaryotic contribution to the preserved sedimentary organic matter in this succession and other contemporaneous Tonian marine sedimentary rocks. However, we stress that, even with an expanded dataset, we are likely far from pinpointing exactly when this transition occurred or whether Earth's history is characterized by a single or multiple transitions in the P cycle.

A long-term record of early to mid-Paleozoic marine redox change.

The extent to which Paleozoic oceans differed from Neoproterozoic oceans and the causal relationship between biological evolution and changing environmental conditions are heavily debated. Here, we report a nearly continuous record of seafloor redox change from the deep-water upper Cambrian to Middle Devonian Road River Group of Yukon, Canada. Bottom waters were largely anoxic in the Richardson trough during the entirety of Road River Group deposition, while independent evidence from iron speciation and Mo/U ratios show that the biogeochemical nature of anoxia changed through time. Both in Yukon and globally, Ordovician through Early Devonian anoxic waters were broadly ferruginous (nonsulfidic), with a transition toward more euxinic (sulfidic) conditions in the mid-Early Devonian (Pragian), coincident with the early diversification of vascular plants and disappearance of graptolites. This ~80-million-year interval of the Paleozoic characterized by widespread ferruginous bottom waters represents a persistence of Neoproterozoic-like marine redox conditions well into the Phanerozoic.

Evidence for the development of local anoxia during the Cambrian SPICE event in eastern North America.

The later Cambrian Steptoean Positive Carbon Isotope Excursion (SPICE) event was an episode marked by pronounced changes to the global biogeochemical cycles of carbon and sulfur and significant extinctions on several paleocontinents including Laurentia (North America). While the exact cause(s) of these events remains debated, various lines of evidence suggest an increase in the areal extent of anoxia at the seafloor was a likely feature. Here, we explore whether changes in local oxygenation accompanied the onset of the SPICE in southern Laurentia using cores of the Nolichucky and Eau Claire Formations from Ohio and Kentucky, USA, that represent a transect into the Rome Trough/Conasauga intrashelf basin. At our study locations, the initial positive δ13 C shift of the SPICE occurs in conjunction with increases in the abundance and δ34 S of sedimentary pyrite. Further local redox conditions, tracked using iron speciation analysis, indicate anoxic conditions developed at the two proximal locations after the start of the paired isotopic excursions. However, the location near the basin center shows no indication for anoxia before or during the onset of the SPICE. While this signal may reflect the structure of local redox conditions within the basin, with the development of anoxia limited to the basin margins, we argue that authigenic iron enrichments were muted by sedimentary dilution and/or the enhanced authigenesis of iron-bearing sheet silicates near the basin center, masking the signal for anoxia there. Regardless of the areal extent of anoxia within the basin, in either scenario the timing of the development of anoxic bottom waters was concurrent with local faunal turnover, features broadly consistent with a global expansion of anoxia playing a role in driving the isotopic trends and extinctions observed during the event.

Sulphur and carbon cycling in the subduction zone mélange.

Subduction zones impose an important control on the geochemical cycling between the surficial and internal reservoirs of the Earth. Sulphur and carbon are transferred into Earth's mantle by subduction of pelagic sediments and altered oceanic lithosphere. Release of oxidizing sulphate- and carbonate-bearing fluids modifies the redox state of the mantle and the chemical budget of subduction zones. Yet, the mechanisms of sulphur and carbon cycling within subduction zones are still unclear, in part because data are typically derived from arc volcanoes where fluid compositions are modified during transport through the mantle wedge. We determined the bulk rock elemental, and sulphur and carbon isotope compositions of exhumed ultramafic and metabasic rocks from Syros, Greece. Comparison of isotopic data with major and trace element compositions indicates seawater alteration and chemical exchange with sediment-derived fluids within the subduction zone channel. We show that small bodies of detached slab material are subject to metasomatic processes during exhumation, in contrast to large sequences of obducted ophiolitic sections that retain their seafloor alteration signatures. In particular, fluids circulating along the plate interface can cause sulphur mobilization during several stages of exhumation within high-pressure rocks. This takes place more pervasively in serpentinites compared to mafic rocks.

Late inception of a resiliently oxygenated upper ocean.

Rising oceanic and atmospheric oxygen levels through time have been crucial to enhanced habitability of surface Earth environments. Few redox proxies can track secular variations in dissolved oxygen concentrations around threshold levels for metazoan survival in the upper ocean. We present an extensive compilation of iodine-to-calcium ratios (I/Ca) in marine carbonates. Our record supports a major rise in the partial pressure of oxygen in the atmosphere at ~400 million years (Ma) ago and reveals a step change in the oxygenation of the upper ocean to relatively sustainable near-modern conditions at ~200 Ma ago. An Earth system model demonstrates that a shift in organic matter remineralization to greater depths, which may have been due to increasing size and biomineralization of eukaryotic plankton, likely drove the I/Ca signals at ~200 Ma ago.

Evidence for rapid weathering response to climatic warming during the Toarcian Oceanic Anoxic Event.

Chemical weathering consumes atmospheric carbon dioxide through the breakdown of silicate minerals and is thought to stabilize Earth's long-term climate. However, the potential influence of silicate weathering on atmospheric pCO2 levels on geologically short timescales (103-105 years) remains poorly constrained. Here we focus on the record of a transient interval of severe climatic warming across the Toarcian Oceanic Anoxic Event or T-OAE from an open ocean sedimentary succession from western North America. Paired osmium isotope data and numerical modelling results suggest that weathering rates may have increased by 215% and potentially up to 530% compared to the pre-event baseline, which would have resulted in the sequestration of significant amounts of atmospheric CO2. This process would have also led to increased delivery of nutrients to the oceans and lakes stimulating bioproductivity and leading to the subsequent development of shallow-water anoxia, the hallmark of the T-OAE. This enhanced bioproductivity and anoxia would have resulted in elevated rates of organic matter burial that would have acted as an additional negative feedback on atmospheric pCO2 levels. Therefore, the enhanced weathering modulated by initially increased pCO2 levels would have operated as both a direct and indirect negative feedback to end the T-OAE.

Uranium isotopes distinguish two geochemically distinct stages during the later Cambrian SPICE event.

Anoxic marine zones were common in early Paleozoic oceans (542-400 Ma), and present a potential link to atmospheric pO2 via feedbacks linking global marine phosphorous recycling, primary production and organic carbon burial. Uranium (U) isotopes in carbonate rocks track the extent of ocean anoxia, whereas carbon (C) and sulfur (S) isotopes track the burial of organic carbon and pyrite sulfur (primary long-term sources of atmospheric oxygen). In combination, these proxies therefore reveal the comparative dynamics of ocean anoxia and oxygen liberation to the atmosphere over million-year time scales. Here we report high-precision uranium isotopic data in marine carbonates deposited during the Late Cambrian 'SPICE' event, at ca. 499 Ma, documenting a well-defined -0.18‰ negative δ238U excursion that occurs at the onset of the SPICE event's positive δ13C and δ34S excursions, but peaks (and tails off) before them. Dynamic modelling shows that the different response of the U reservoir cannot be attributed solely to differences in residence times or reservoir sizes - suggesting that two chemically distinct ocean states occurred within the SPICE event. The first ocean stage involved a global expansion of euxinic waters, triggering the spike in U burial, and peaking in conjunction with a well-known trilobite extinction event. During the second stage widespread euxinia waned, causing U removal to tail off, but enhanced organic carbon and pyrite burial continued, coinciding with evidence for severe sulfate depletion in the oceans (Gill et al., 2011). We discuss scenarios for how an interval of elevated pyrite and organic carbon burial could have been sustained without widespread euxinia in the water column (both non-sulfidic anoxia and/or a more oxygenated ocean state are possibilities). Either way, the SPICE event encompasses two different stages of elevated organic carbon and pyrite burial maintained by high nutrient fluxes to the ocean, and potentially sustained by internal marine geochemical feedbacks.