Deep-water first occurrences of Ediacara biota prior to the Shuram carbon isotope excursion in the Wernecke Mountains, Yukon, Canada.

Ediacara-type macrofossils appear as early as ~575 Ma in deep-water facies of the Drook Formation of the Avalon Peninsula, Newfoundland, and the Nadaleen Formation of Yukon and Northwest Territories, Canada. Our ability to assess whether a deep-water origination of the Ediacara biota is a genuine reflection of evolutionary succession, an artifact of an incomplete stratigraphic record, or a bathymetrically controlled biotope is limited by a lack of geochronological constraints and detailed shelf-to-slope transects of Ediacaran continental margins. The Ediacaran Rackla Group of the Wernecke Mountains, NW Canada, represents an ideal shelf-to-slope depositional system to understand the spatiotemporal and environmental context of Ediacara-type organisms' stratigraphic occurrence. New sedimentological and paleontological data presented herein from the Wernecke Mountains establish a stratigraphic framework relating shelfal strata in the Goz/Corn Creek area to lower slope deposits in the Nadaleen River area. We report new discoveries of numerous Aspidella hold-fast discs, indicative of frondose Ediacara organisms, from deep-water slope deposits of the Nadaleen Formation stratigraphically below the Shuram carbon isotope excursion (CIE) in the Nadaleen River area. Such fossils are notably absent in coeval shallow-water strata in the Goz/Corn Creek region despite appropriate facies for potential preservation. The presence of pre-Shuram CIE Ediacara-type fossils occurring only in deep-water facies within a basin that has equivalent well-preserved shallow-water facies provides the first stratigraphic paleobiological support for a deep-water origination of the Ediacara biota. In contrast, new occurrences of Ediacara-type fossils (including juvenile fronds, Beltanelliformis, Aspidella, annulated tubes, and multiple ichnotaxa) are found above the Shuram CIE in both deep- and shallow-water deposits of the Blueflower Formation. Given existing age constraints on the Shuram CIE, it appears that Ediacaran organisms may have originated in the deeper ocean and lived there for up to ~15 million years before migrating into shelfal environments in the terminal Ediacaran. This indicates unique ecophysiological constraints likely shaped the initial habitat preference and later environmental expansion of the Ediacara biota.

Lithium isotopic constraints on the evolution of continental clay mineral factory and marine oxygenation in the earliest Paleozoic Era.

The evolution of oxygen cycles on Earth's surface has been regulated by the balance between molecular oxygen production and consumption. The Neoproterozoic-Paleozoic transition likely marks the second rise in atmospheric and oceanic oxygen levels, widely attributed to enhanced burial of organic carbon. However, it remains disputed how marine organic carbon production and burial respond to global environmental changes and whether these feedbacks trigger global oxygenation during this interval. Here, we report a large lithium isotopic and elemental dataset from marine mudstones spanning the upper Neoproterozoic to middle Cambrian [~660 million years ago (Ma) to 500 Ma]. These data indicate a dramatic increase in continental clay formation after ~525 Ma, likely linked to secular changes in global climate and compositions of the continental crust. Using a global biogeochemical model, we suggest that intensified continental weathering and clay delivery to the oceans could have notably increased the burial efficiency of organic carbon and facilitated greater oxygen accumulation in the earliest Paleozoic oceans.

Constraining the oxygen requirements for modern microbial eukaryote diversity.

Eukaryotes originated prior to the establishment of modern marine oxygen (O2) levels. According to the body fossil and lipid biomarker records, modern (crown) microbial eukaryote lineages began diversifying in the ocean no later than ~800 Ma. While it has long been predicted that increasing atmospheric O2 levels facilitated the early diversification of microbial eukaryotes, the O2 levels needed to permit this diversification remain unconstrained. Using time-resolved geochemical parameter and gene sequence information from a model marine oxygen minimum zone spanning a range of dissolved O2 levels and redox states, we show that microbial eukaryote taxonomic richness and phylogenetic diversity remain the same until O2 declines to around 2 to 3% of present atmospheric levels, below which these diversity metrics become significantly reduced. Our observations suggest that increasing O2 would have only directly promoted early crown-eukaryote diversity if atmospheric O2 was below 2 to 3% of modern levels when crown-eukaryotes originated and then later met or surpassed this range as crown-eukaryotes diversified. If atmospheric O2 was already consistently at or above 2 to 3% of modern levels by the time that crown-eukaryotes originated, then the subsequent diversification of modern microbial eukaryotes was not directly driven by atmospheric oxygenation.

Thermal optima in the hypoxia tolerance of marine ectotherms: Physiological causes and biogeographic consequences.

The minimum O2 needed to fuel the demand of aquatic animals is commonly observed to increase with temperature, driven by accelerating metabolism. However, recent measurements of critical O2 thresholds ("Pcrit") reveal more complex patterns, including those with a minimum at an intermediate thermal "optimum". To discern the prevalence, physiological drivers, and biogeographic manifestations of such curves, we analyze new experimental and biogeographic data using a general dynamic model of aquatic water breathers. The model simulates the transfer of oxygen from ambient water through a boundary layer and into animal tissues driven by temperature-dependent rates of metabolism, diffusive gas exchange, and ventilatory and circulatory systems with O2-protein binding. We find that a thermal optimum in Pcrit can arise even when all physiological rates increase steadily with temperature. This occurs when O2 supply at low temperatures is limited by a process that is more temperature sensitive than metabolism, but becomes limited by a less sensitive process at warmer temperatures. Analysis of published species respiratory traits suggests that this scenario is not uncommon in marine biota, with ventilation and circulation limiting supply under cold conditions and diffusion limiting supply at high temperatures. Using occurrence data, we show that species with these physiological traits inhabit lowest O2 waters near the optimal temperature for hypoxia tolerance and are restricted to higher O2 at temperatures above and below this optimum. Our results imply that hypoxia tolerance can decline under both cold and warm conditions and thus may influence both poleward and equatorward species range limits.

Oxygen availability and body mass modulate ectotherm responses to ocean warming.

In an ocean that is rapidly warming and losing oxygen, accurate forecasting of species' responses must consider how this environmental change affects fundamental aspects of their physiology. Here, we develop an absolute metabolic index (ΦA) that quantifies how ocean temperature, dissolved oxygen and organismal mass interact to constrain the total oxygen budget an organism can use to fuel sustainable levels of aerobic metabolism. We calibrate species-specific parameters of ΦA with physiological measurements for red abalone (Haliotis rufescens) and purple urchin (Strongylocentrotus purpuratus). ΦA models highlight that the temperature where oxygen supply is greatest shifts cooler when water loses oxygen or organisms grow larger, providing a mechanistic explanation for observed thermal preference patterns. Viable habitat forecasts are disproportionally deleterious for red abalone, revealing how species-specific physiologies modulate the intensity of a common climate signal, captured in the newly developed ΦA framework.

Mesoproterozoic surface oxygenation accompanied major sedimentary manganese deposition at 1.4 and 1.1 Ga.

Manganese (Mn) oxidation in marine environments requires oxygen (O2 ) or other reactive oxygen species in the water column, and widespread Mn oxide deposition in ancient sedimentary rocks has long been used as a proxy for oxidation. The oxygenation of Earth's atmosphere and oceans across the Archean-Proterozoic boundary are associated with massive Mn deposits, whereas the interval from 1.8-1.0 Ga is generally believed to be a time of low atmospheric oxygen with an apparent hiatus in sedimentary Mn deposition. Here, we report geochemical and mineralogical analyses from 1.1 Ga manganiferous marine-shelf siltstones from the Bangemall Supergroup, Western Australia, which underlie recently discovered economically significant manganese deposits. Layers bearing Mn carbonate microspheres, comparable with major global Mn deposits, reveal that intense periods of sedimentary Mn deposition occurred in the late Mesoproterozoic. Iron geochemical data suggest anoxic-ferruginous seafloor conditions at the onset of Mn deposition, followed by oxic conditions in the water column as Mn deposition persisted and eventually ceased. These data imply there was spatially widespread surface oxygenation ~1.1 Ga with sufficiently oxic conditions in shelf environments to oxidize marine Mn(II). Comparable large stratiform Mn carbonate deposits also occur in ~1.4 Ga marine siltstones hosted in underlying sedimentary units. These deposits are greater or at least commensurate in scale (tonnage) to those that followed the major oxygenation transitions from the Neoproterozoic. Such a period of sedimentary manganogenesis is inconsistent with a model of persistently low O2 throughout the entirety of the Mesoproterozoic and provides robust evidence for dynamic redox changes in the mid to late Mesoproterozoic.

Breathless through Time: Oxygen and Animals across Earth's History.

AbstractOxygen levels in the atmosphere and ocean have changed dramatically over Earth history, with major impacts on marine life. Because the early part of Earth's history lacked both atmospheric oxygen and animals, a persistent co-evolutionary narrative has developed linking oxygen change with changes in animal diversity. Although it was long believed that oxygen rose to essentially modern levels around the Cambrian period, a more muted increase is now believed likely. Thus, if oxygen increase facilitated the Cambrian explosion, it did so by crossing critical ecological thresholds at low O2. Atmospheric oxygen likely remained at low or moderate levels through the early Paleozoic era, and this likely contributed to high metazoan extinction rates until oxygen finally rose to modern levels in the later Paleozoic. After this point, ocean deoxygenation (and marine mass extinctions) is increasingly linked to large igneous province eruptions-massive volcanic carbon inputs to the Earth system that caused global warming, ocean acidification, and oxygen loss. Although the timescales of these ancient events limit their utility as exact analogs for modern anthropogenic global change, the clear message from the geologic record is that large and rapid CO2 injections into the Earth system consistently cause the same deadly trio of stressors that are observed today. The next frontier in understanding the impact of oxygen changes (or, more broadly, temperature-dependent hypoxia) in deep time requires approaches from ecophysiology that will help conservation biologists better calibrate the response of the biosphere at large taxonomic, spatial, and temporal scales.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

Eukaryogenesis and oxygen in Earth history.

The endosymbiotic origin of mitochondria during eukaryogenesis has long been viewed as an adaptive response to the oxygenation of Earth's surface environment, presuming a fundamentally aerobic lifestyle for the free-living bacterial ancestors of mitochondria. This oxygen-centric view has been robustly challenged by recent advances in the Earth and life sciences. While the permanent oxygenation of the atmosphere above trace concentrations is now thought to have occurred 2.2 billion years ago, large parts of the deep ocean remained anoxic until less than 0.5 billion years ago. Neither fossils nor molecular clocks correlate the origin of mitochondria, or eukaryogenesis more broadly, to either of these planetary redox transitions. Instead, mitochondria-bearing eukaryotes are consistently dated to between these two oxygenation events, during an interval of pervasive deep-sea anoxia and variable surface-water oxygenation. The discovery and cultivation of the Asgard archaea has reinforced metabolic evidence that eukaryogenesis was initially mediated by syntrophic H2 exchange between an archaeal host and an α-proteobacterial symbiont living under anoxia. Together, these results temporally, spatially and metabolically decouple the earliest stages of eukaryogenesis from the oxygen content of the surface ocean and atmosphere. Rather than reflecting the ancestral metabolic state, obligate aerobiosis in eukaryotes is most probably derived, having only become globally widespread over the past 1 billion years as atmospheric oxygen approached modern levels.

Marine sponges in the once and future ocean.

Animals originated under hypoxia-low-oxygen conditions that are currently expanding throughout the global ocean. How marine sponges respond to hypoxia is both relevant to reconstructing early animal evolution and for forecasting the fate of modern marine ecosystems. In a new effort, multiple sponge species from two different oceans were found to tolerate hypoxia in the lab, revealing a more general capacity for hypoxia tolerance across sponges with implications for both the deep past and near future of animal life.

Decreasing Phanerozoic extinction intensity as a consequence of Earth surface oxygenation and metazoan ecophysiology.

The decline in background extinction rates of marine animals through geologic time is an established but unexplained feature of the Phanerozoic fossil record. There is also growing consensus that the ocean and atmosphere did not become oxygenated to near-modern levels until the mid-Paleozoic, coinciding with the onset of generally lower extinction rates. Physiological theory provides us with a possible causal link between these two observations-predicting that the synergistic impacts of oxygen and temperature on aerobic respiration would have made marine animals more vulnerable to ocean warming events during periods of limited surface oxygenation. Here, we evaluate the hypothesis that changes in surface oxygenation exerted a first-order control on extinction rates through the Phanerozoic using a combined Earth system and ecophysiological modeling approach. We find that although continental configuration, the efficiency of the biological carbon pump in the ocean, and initial climate state all impact the magnitude of modeled biodiversity loss across simulated warming events, atmospheric oxygen is the dominant predictor of extinction vulnerability, with metabolic habitat viability and global ecophysiotype extinction exhibiting inflection points around 40% of present atmospheric oxygen. Given this is the broad upper limit for estimates of early Paleozoic oxygen levels, our results are consistent with the relative frequency of high-magnitude extinction events (particularly those not included in the canonical big five mass extinctions) early in the Phanerozoic being a direct consequence of limited early Paleozoic oxygenation and temperature-dependent hypoxia responses.

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.

Isotopic analyses of Ordovician-Silurian siliceous skeletons indicate silica-depleted Paleozoic oceans.

The Phanerozoic Eon marked a major transition from marine silica deposition exclusively via abiotic pathways to a system dominated by biogenic silica sedimentation. For decades, prevailing ideas predicted this abiotic-to-biogenic transition were marked by a significant decrease in the concentration of dissolved silica in seawater; however, due to the lower perceived abundance and uptake affinity of sponges and radiolarians relative to diatoms, marine dissolved silica is thought to have remained elevated above modern values until the Cenozoic radiation of diatoms. Studies of modern marine silica biomineralizers demonstrated that the Si isotope ratios (δ30 Si) of sponge spicules and planktonic silica biominerals produced by diatoms or radiolarians can be applied as quantitative proxies for past seawater dissolved silica concentrations due to differences in Si isotope fractionations among these organisms. We undertook 446 ion microprobe analyses of δ30 Si and δ18 O of sponge spicules and radiolarians from Ordovician-Silurian chert deposits of the Mount Hare Formation in Yukon, Canada. These isotopic data showed that sponges living in marine slope and basinal environments displayed small Si isotope fractionations relative to coeval radiolarians. By constructing a mathematical model of the major fluxes and reservoirs in the marine silica cycle and the physiology of silica biomineralization, we found that the concentration of dissolved silica in seawater was less than ~150 µM during early Paleozoic time-a value that is significantly lower than previous estimates. We posit that the topology of the early Paleozoic marine silica cycle resembled that of modern oceans much more closely than previously assumed.

Calibrating the coevolution of Ediacaran life and environment.

The rise of animals occurred during an interval of Earth history that witnessed dynamic marine redox conditions, potentially rapid plate motions, and uniquely large perturbations to global biogeochemical cycles. The largest of these perturbations, the Shuram carbon isotope excursion, has been invoked as a driving mechanism for Ediacaran environmental change, possibly linked with evolutionary innovation or extinction. However, there are a number of controversies surrounding the Shuram, including its timing, duration, and role in the concomitant biological and biogeochemical upheavals. Here we present radioisotopic dates bracketing the Shuram on two separate paleocontinents; our results are consistent with a global and synchronous event between 574.0 ± 4.7 and 567.3 ± 3.0 Ma. These dates support the interpretation that the Shuram is a primary and synchronous event postdating the Gaskiers glaciation. In addition, our Re-Os ages suggest that the appearance of Ediacaran macrofossils in northwestern Canada is identical, within uncertainty, to similar macrofossils from the Conception Group of Newfoundland, highlighting the coeval appearance of macroscopic metazoans across two paleocontinents. Our temporal framework for the terminal Proterozoic is a critical step for testing hypotheses related to extreme carbon isotope excursions and their role in the evolution of complex life.

Ediacaran reorganization of the marine phosphorus cycle.

The Ediacaran Period (635 to 541 Ma) marks the global transition to a more productive biosphere, evidenced by increased availability of food and oxidants, the appearance of macroscopic animals, significant populations of eukaryotic phytoplankton, and the onset of massive phosphorite deposition. We propose this entire suite of changes results from an increase in the size of the deep-water marine phosphorus reservoir, associated with rising sulfate concentrations and increased remineralization of organic P by sulfate-reducing bacteria. Simple mass balance calculations, constrained by modern anoxic basins, suggest that deep-water phosphate concentrations may have increased by an order of magnitude without any increase in the rate of P input from the continents. Strikingly, despite a major shift in phosphorite deposition, a new compilation of the phosphorus content of Neoproterozoic and early Paleozoic shows little secular change in median values, supporting the view that changes in remineralization and not erosional P fluxes were the principal drivers of observed shifts in phosphorite accumulation. The trigger for these changes may have been transient Neoproterozoic weathering events whose biogeochemical consequences were sustained by a set of positive feedbacks, mediated by the oxygen and sulfur cycles, that led to permanent state change in biogeochemical cycling, primary production, and biological diversity by the end of the Ediacaran Period.

Persistent global marine euxinia in the early Silurian.

The second pulse of the Late Ordovician mass extinction occurred around the Hirnantian-Rhuddanian boundary (~444 Ma) and has been correlated with expanded marine anoxia lasting into the earliest Silurian. Characterization of the Hirnantian ocean anoxic event has focused on the onset of anoxia, with global reconstructions based on carbonate δ238U modeling. However, there have been limited attempts to quantify uncertainty in metal isotope mass balance approaches. Here, we probabilistically evaluate coupled metal isotopes and sedimentary archives to increase constraint. We present iron speciation, metal concentration, δ98Mo and δ238U measurements of Rhuddanian black shales from the Murzuq Basin, Libya. We evaluate these data (and published carbonate δ238U data) with a coupled stochastic mass balance model. Combined statistical analysis of metal isotopes and sedimentary sinks provides uncertainty-bounded constraints on the intensity of Hirnantian-Rhuddanian euxinia. This work extends the duration of anoxia to >3 Myrs - notably longer than well-studied Mesozoic ocean anoxic events.

On the co-evolution of surface oxygen levels and animals.

Few topics in geobiology have been as extensively debated as the role of Earth's oxygenation in controlling when and why animals emerged and diversified. All currently described animals require oxygen for at least a portion of their life cycle. Therefore, the transition to an oxygenated planet was a prerequisite for the emergence of animals. Yet, our understanding of Earth's oxygenation and the environmental requirements of animal habitability and ecological success is currently limited; estimates for the timing of the appearance of environments sufficiently oxygenated to support ecologically stable populations of animals span a wide range, from billions of years to only a few million years before animals appear in the fossil record. In this light, the extent to which oxygen played an important role in controlling when animals appeared remains a topic of debate. When animals originated and when they diversified are separate questions, meaning either one or both of these phenomena could have been decoupled from oxygenation. Here, we present views from across this interpretive spectrum-in a point-counterpoint format-regarding crucial aspects of the potential links between animals and surface oxygen levels. We highlight areas where the standard discourse on this topic requires a change of course and note that several traditional arguments in this "life versus environment" debate are poorly founded. We also identify a clear need for basic research across a range of fields to disentangle the relationships between oxygen availability and emergence and diversification of animal life.

Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction.

Rapid climate change at the end of the Permian Period (~252 million years ago) is the hypothesized trigger for the largest mass extinction in Earth's history. We present model simulations of the Permian/Triassic climate transition that reproduce the ocean warming and oxygen (O2) loss indicated by the geologic record. The effect of these changes on animal survival is evaluated using the Metabolic Index (Φ), a measure of scope for aerobic activity governed by organismal traits sampled in diverse modern species. Modeled loss of aerobic habitat predicts lower extinction intensity in the tropics, a pattern confirmed with a spatially explicit analysis of the marine fossil record. The combined physiological stresses of ocean warming and O2 loss can account for more than half the magnitude of the "Great Dying."