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Significance The decline in extinction rates through geologic time is a well-established but enigmatic feature of the marine animal fossil record. We hypothesize that this trend is driven largely by secular changes in the oxygenation of the atmosphere and oceans, as physiological principles predict that marine animals would have been more vulnerable to ocean warming during intervals of geological time with limited atmospheric oxygenation. We test this at a global oceanographic scale by combining models of ocean biogeochemistry and animal physiology. We show that atmospheric oxygen exerts a first-order control on the simulated extinction vulnerability of marine animals, highlighting its likely importance in controlling extinction trends through geologic time. 

Abstract 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 (δ³⁰Si) 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 δ³⁰Si and δ¹⁸O 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. 

It is clear from modern analogue studies that O2-deficient conditions favor preservation of organic matter (OM) in fine-grained sedimentary rocks (black shales). It is also clear that appreciable productivity and OM flux to the sediment are required to establish and maintain these conditions. However, debates regarding redox controls on OM accumulation in black shales have mainly focused on oxic versus anoxic conditions, and the implications of different anoxic redox states remain unexplored. Here, we present detailed multi-proxy sedimentary geochemical studies of major Paleozoic and Mesozoic North American black shale units to elucidate their depositional redox conditions. This is the first broad-scale study to use a consistent geochemical methodology and to incorporate data from Fe-speciation – presently the only redox proxy able to clearly distinguish anoxic depositional conditions as ferruginous (H2S-limited) or euxinic (H2S-replete, Fe-limited). These data are coupled with total organic carbon (TOC), programmed pyrolysis, and redox-sensitive trace element proxies, with almost all measurements analyzed using the same geochemical methodology. Consistent with expectations based on previous geochemical and paleontological/ichnological studies, these analyses demonstrate that the study units were almost exclusively deposited under anoxic bottom waters. These analyses also demonstrate that there is wide variance in the prevalence of euxinic versus ferruginous conditions, with many North American black shale units deposited under predominantly ferruginous or oscillatory conditions. TOC is significantly higher under euxinic bottom waters in analyses of both preserved (present day) TOC and reconstructed initial TOC values, although sediments deposited under both redox states do have economically viable TOC content. While this correlation does not reveal the mechanism behind higher organic enrichment in euxinic environments, which may be different in different basins, it does open new research avenues regarding resource exploration and the biogeochemistry of ancient reducing environments. 

Ocean warming is increasing organismal oxygen demand, yet at the same time the ocean’s oxygen supply is decreasing. For a patch of habitat to remain viable, there must be a minimum level of environmental oxygen available for an organism to fuel its metabolic demand—quantified as its critical oxygen partial pressure (pO_2crit). The temperature-dependence ofpO_2critsets an absolute lower boundary on aerobically viable ocean space for a species, yet whether certain life stages or geographically distant populations differ in their temperature-dependent hypoxia tolerance remains largely unknown. To address these questions, we used the purple sea urchinStrongylocentrotus purpuratusas a model species and measuredpO_2critfor 3 populations of adult urchins (Clallam Bay, WA [n = 39], Monterey Bay, CA [91], San Diego, CA [34]) spanning 5-22°C and for key embryonic and larval developmental phases (blastula [n = 11], gastrula [21], prism [31], early-pluteus [21], late-pluteus [14], settled [12]) at temperatures of 10-19°C. We found that temperature-dependent hypoxia tolerance is consistent among adult populations exposed to different temperature and oxygen regimes, despite variable basal oxygen demands, suggesting differential capacity to provision oxygen. Moreover, we did not detect evidence for a hypoxia tolerance bottleneck for any developmental phase. Earlier larval phases are associated with higher hypoxia tolerance and greater temperature sensitivity, while this pattern shifts towards lower hypoxia tolerance and reduced temperature sensitivity as larvae develop. Our results indicate that, at least forS. purpuratus,models quantifying aerobically viable habitat based onpO_2crit-temperature relationships from a single adult population will conservatively estimate viable habitat. 

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. 

Abstract 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 (Φ A ) 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 Φ A with physiological measurements for red abalone ( Haliotis rufescens ) and purple urchin ( Strongylocentrotus purpuratus ). Φ A 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 Φ A framework. 

Oxygen 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. 

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.