Why the Early Paleozoic was intrinsically prone to marine extinction.

The geological record of marine animal biodiversity reflects the interplay between changing rates of speciation versus extinction. Compared to mass extinctions, background extinctions have received little attention. To disentangle the different contributions of global climate state, continental configuration, and atmospheric oxygen concentration (pO2) to variations in background extinction rates, we drive an animal physiological model with the environmental outputs from an Earth system model across intervals spanning the past 541 million years. We find that climate and continental configuration combined to make extinction susceptibility an order of magnitude higher during the Early Paleozoic than during the rest of the Phanerozoic, consistent with extinction rates derived from paleontological databases. The high extinction susceptibility arises in the model from the limited geographical range of marine organisms. It stands even when assuming present-day pO2, suggesting that increasing oxygenation through the Paleozoic is not necessary to explain why extinction rates apparently declined with time.

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.

Continental configuration controls ocean oxygenation during the Phanerozoic.

The early evolutionary and much of the extinction history of marine animals is thought to be driven by changes in dissolved oxygen concentrations ([O2]) in the ocean1-3. In turn, [O2] is widely assumed to be dominated by the geological history of atmospheric oxygen (pO2)4,5. Here, by contrast, we show by means of a series of Earth system model experiments how continental rearrangement during the Phanerozoic Eon drives profound variations in ocean oxygenation and induces a fundamental decoupling in time between upper-ocean and benthic [O2]. We further identify the presence of state transitions in the global ocean circulation, which lead to extensive deep-ocean anoxia developing in the early Phanerozoic even under modern pO2. Our finding that ocean oxygenation oscillates over stable thousand-year (kyr) periods also provides a causal mechanism that might explain elevated rates of metazoan radiation and extinction during the early Palaeozoic Era6. The absence, in our modelling, of any simple correlation between global climate and ocean ventilation, and the occurrence of profound variations in ocean oxygenation independent of atmospheric pO2, presents a challenge to the interpretation of marine redox proxies, but also points to a hitherto unrecognized role for continental configuration in the evolution of the biosphere.

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.

Metabolic tradeoffs control biodiversity gradients through geological time.

The latitudinal gradient of increasing marine biodiversity from the poles to the tropics is one of the most conspicuous biological patterns in modern oceans.1-3 Low-latitude regions of the global ocean are often hotspots of animal biodiversity, yet they are set to be most critically affected by anthropogenic climate change.4 As ocean temperatures rise and deoxygenation proceeds in the coming centuries, the volume of aerobically viable habitat is predicted to decrease in these zones.5,6 In contrast to the slightly asymmetrical modern latitudinal biodiversity gradient,7 compilations of fossil occurrences indicate peaks in biodiversity may have existed much further away from the equator in the past, with transitions between climate states hypothesized to explain this trend.8-13 We combine a new compilation of fossil mollusc occurrences, paleotemperature proxies, and biogeographic data to reveal a non-monotonic relationship between temperature and diversity in the paleontological record over the last 145 million years. We derive a metabolic model that integrates the kinetic effects of temperature on biodiversity14 with the recently described Metabolic Index that calculates aerobic habitat availability based on the effect of temperature on hypoxia sensitivity.5,15,16 Although factors such as coastal habitat area and homeothermy are important,17,18 we find strong congruence between our metabolic model and our fossil and paleotemperature meta-analysis. We therefore suggest that the effects of ocean temperature on the aerobic scope of marine ectotherms is a primary driver of migrating biodiversity peaks through geologic time and will likely play a role in the restructuring of biodiversity under projected future climate scenarios.

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.

The Temporal and Environmental Context of Early Animal Evolution: Considering All the Ingredients of an "Explosion".

Animals originated and evolved during a unique time in Earth history-the Neoproterozoic Era. This paper aims to discuss (1) when landmark events in early animal evolution occurred, and (2) the environmental context of these evolutionary milestones, and how such factors may have affected ecosystems and body plans. With respect to timing, molecular clock studies-utilizing a diversity of methodologies-agree that animal multicellularity had arisen by ∼800 million years ago (Ma) (Tonian period), the bilaterian body plan by ∼650 Ma (Cryogenian), and divergences between sister phyla occurred ∼560-540 Ma (late Ediacaran). Most purported Tonian and Cryogenian animal body fossils are unlikely to be correctly identified, but independent support for the presence of pre-Ediacaran animals is recorded by organic geochemical biomarkers produced by demosponges. This view of animal origins contrasts with data from the fossil record, and the taphonomic question of why animals were not preserved (if present) remains unresolved. Neoproterozoic environments demanding small, thin, body plans, and lower abundance/rarity in populations may have played a role. Considering environmental conditions, geochemical data suggest that animals evolved in a relatively low-oxygen ocean. Here, we present new analyses of sedimentary total organic carbon contents in shales suggesting that the Neoproterozoic ocean may also have had lower primary productivity-or at least lower quantities of organic carbon reaching the seafloor-compared with the Phanerozoic. Indeed, recent modeling efforts suggest that low primary productivity is an expected corollary of a low-O2 world. Combined with an inability to inhabit productive regions in a low-O2 ocean, earliest animal communities would likely have been more food limited than generally appreciated, impacting both ecosystem structure and organismal behavior. In light of this, we propose the "fire triangle" metaphor for environmental influences on early animal evolution. Moving toward consideration of all environmental aspects of the Cambrian radiation (fuel, heat, and oxidant) will ultimately lead to a more holistic view of the event.

Oxygen, temperature and the deep-marine stenothermal cradle of Ediacaran evolution.

Ediacaran fossils document the early evolution of complex megascopic life, contemporaneous with geochemical evidence for widespread marine anoxia. These data suggest early animals experienced frequent hypoxia. Research has thus focused on the concentration of molecular oxygen (O2) required by early animals, while also considering the impacts of climate. One model, the Cold Cradle hypothesis, proposed the Ediacaran biota originated in cold, shallow-water environments owing to increased O2 solubility. First, we demonstrate using principles of gas exchange that temperature does have a critical role in governing the bioavailability of O2-but in cooler water the supply of O2 is actually lower. Second, the fossil record suggests the Ediacara biota initially occur approximately 571 Ma in deep-water facies, before appearing in shelf environments approximately 555 Ma. We propose an ecophysiological underpinning for this pattern. By combining oceanographic data with new respirometry experiments we show that in the shallow mixed layer where seasonal temperatures fluctuate widely, thermal and partial pressure ( pO2) effects are highly synergistic. The result is that temperature change away from species-specific optima impairs tolerance to low pO2. We hypothesize that deep and particularly stenothermal (narrow temperature range) environments in the Ediacaran ocean were a physiological refuge from the synergistic effects of temperature and low pO2.