Methanogenic burst in the end-Permian carbon cycle

The end-Permian extinction is associated with a mysterious disruption to Earth’s carbon cycle. Here we identify causal mechanisms via three observations. First, we show that geochemical signals indicate superexponential growth of the marine inorganic carbon reservoir, coincident with the extinction and consistent with the expansion of a new microbial metabolic pathway. Second, we show that the efficient acetoclastic pathway in Methanosarcina emerged at a time statistically indistinguishable from the extinction. Finally, we show that nickel concentrations in South China sediments increased sharply at the extinction, probably as a consequence of massive Siberian volcanism, enabling a methanogenic expansion by removal of nickel limitation. Collectively, these results are consistent with the instigation of Earth’s greatest mass extinction by a specific microbial innovation.The greatest rate of taxonomic loss during the end-Permian extinction—the most severe in the fossil record (1)—occurs within 20,000 y, beginning about 252.28 million years ago (Ma) (2) at a time precisely coincident (2) with geochemical signals indicating a severe and equally rapid perturbation to Earth’s carbon cycle (1–6). Although probably related, neither the cause of the extinction nor the origin of the change in the carbon cycle is known. One possible linkage derives from the observation that massive Siberian volcanism occurs at roughly the same time as the extinction (7, 8). However, quantitative estimates of direct volcanic outgassing are much too small to account for the changes in the carbon cycle (9). Secondary effects of Siberian volcanism, such as the combustion of huge deposits of coal (10) or other forms of organic carbon (11), are more attractive quantitatively but still difficult to reconcile with observed geochemical changes (1–6). Reports of marine anoxia in the Late Permian (5, 12, 13) also indicate changes in the carbon cycle. Moreover, the notion that a disturbance of the carbon cycle plays a significant role as a “kill mechanism” derives considerable support from observations of physiological differences between species that survived the extinction and those that did not (14–16).Here we relate the principal observations of end-Permian environmental change—massive volcanism and changes in marine CO₂ and O₂ levels—to the transfer of genetic material, from a cellulolytic bacterium to a methanogenic archaeon, that enabled efficient methanogenic degradation of organic carbon (17). Our analysis is constructed from three key observations. First, we show that the form of time-dependent changes in the carbon isotopic record indicates an instability within the carbon cycle that is inconsistent with volcanic combustion of organic sediments but consistent with the expansion of a new microbial metabolic pathway. Second, we identify this pathway with efficient acetoclastic methanogenesis and show that the age of the last common ancestor of Methanosarcina, the genus using this pathway, is consistent with the time of the extinction. Because methanogens are limited by nickel (18, 19), the third component of our study presents an analysis of nickel deposited in South China sediments. We find that nickel concentrations rose just before the extinction, presumably as a consequence of Siberian volcanism, providing a mechanism not only to enhance the methanogenic expansion and its perturbation to the carbon cycle but also to amplify the development of marine anoxia. Taken as a whole, these results reconcile an array of apparently disparate observations about the end-Permian event.     

Environmental mutagenesis during the end-Permian ecological crisis

During the end-Permian ecological crisis, terrestrial ecosystems experienced preferential dieback of woody vegetation. Across the world, surviving herbaceous lycopsids played a pioneering role in repopulating deforested terrain. We document that the microspores of these lycopsids were regularly released in unseparated tetrads indicative of failure to complete the normal process of spore development. Although involvement of mutation has long been hinted at or proposed in theory, this finding provides concrete evidence for chronic environmental mutagenesis at the time of global ecological crisis. Prolonged exposure to enhanced UV radiation could account satisfactorily for a worldwide increase in land plant mutation. At the end of the Permian, a period of raised UV stress may have been the consequence of severe disruption of the stratospheric ozone balance by excessive emission of hydrothermal organohalogens in the vast area of Siberian Traps volcanism.     

Calcium isotope constraints on the end-Permian mass extinction

The end-Permian mass extinction horizon is marked by an abrupt shift in style of carbonate sedimentation and a negative excursion in the carbon isotope (δ¹³C) composition of carbonate minerals. Several extinction scenarios consistent with these observations have been put forward. Secular variation in the calcium isotope (δ^44/40Ca) composition of marine sediments provides a tool for distinguishing among these possibilities and thereby constraining the causes of mass extinction. Here we report δ^44/40Ca across the Permian-Triassic boundary from marine limestone in south China. The δ^44/40Ca exhibits a transient negative excursion of ∼0.3‰ over a few hundred thousand years or less, which we interpret to reflect a change in the global δ^44/40Ca composition of seawater. CO₂-driven ocean acidification best explains the coincidence of the δ^44/40Ca excursion with negative excursions in the δ¹³C of carbonates and organic matter and the preferential extinction of heavily calcified marine animals. Calcium isotope constraints on carbon cycle calculations suggest that the average δ¹³C of CO₂ released was heavier than -28‰ and more likely near -15‰; these values indicate a source containing substantial amounts of mantle- or carbonate-derived carbon. Collectively, the results point toward Siberian Trap volcanism as the trigger of mass extinction.An abrupt shift in style of carbonate sedimentation occurs across the end-Permian extinction horizon. Microbialites and oolites overlie diverse, fossiliferous limestones of the latest Permian age in carbonate strata deposited across the tropical Tethys (1–8) and in the Panthalassa Ocean (8, 9) (Fig. S1). The mass extinction and facies shift are associated with a large negative excursion in the carbon isotope (δ¹³C) composition of carbonate minerals.Geochemical and sedimentary observations have been used to support various causal mechanisms for the mass extinction. Three different scenarios have been put forth. First, the “Strangelove Ocean” scenario links mass extinction to collapse of the biological pump—the vertical separation in the water column of carbon fixation and respiration, which results from the sinking of organic matter out of the surface ocean (10). Under this scenario, an initial decrease in carbonate deposition would occur because of mixing of surface waters with CaCO₃-undersaturated deeper waters (assuming an oxygenated deep ocean); subsequent increase in alkalinity because of continental weathering would lead to enhanced carbonate deposition, explaining the deposition of microbialites and oolites (10). Second, the ocean overturn model proposes that extensive sulfate reduction in anoxic deep waters of the Permian oceans resulted in a buildup of carbonate alkalinity and hydrogen sulfide in deep water prior to the extinction event (11–14). Upwelling of these alkaline deep waters would have triggered carbonate precipitation on the shelves (2, 5, 15, 16) and caused mass extinction through combined stresses of hypercapnia, anoxia, and hydrogen sulfide poisoning (14, 15, 17). Third, the ocean acidification model proposes that massive release of ¹³C-depleted carbon from a reservoir in the crust (e.g., methane clathrates, coal, and magma) (18–22) acidified the ocean, reducing carbonate sedimentation and potentially leading to dissolution of carbonate sediments (8). Subsequently enhanced continental weathering and consequent delivery of carbonate alkalinity to the oceans would account for the widespread deposition of microbialites and oolites above the extinction horizon (8).One avenue for distinguishing among these hypotheses lies in their differing implications for the global cycling of calcium, an element with a residence time of approximately 600–1,000 ky and uniform isotope composition in the modern oceans (23, 24). Isotopes of calcium are fractionated during the precipitation of calcium carbonate (25–27): ⁴⁰Ca is preferentially incorporated into the solid phase, leaving seawater enriched in ⁴⁴Ca at steady state relative to the delivery and burial fluxes (24, 28). Consequently, scenarios that require imbalances between the delivery and burial fluxes of calcium in the oceans should impart changes in the calcium isotope composition in the oceans and associated sediments.We constructed a one-box, isotope mass-balance model of the global calcium cycle (see Methods and SI Discussion) to generate quantitative predictions for marine calcium isotopes and concentrations associated with the various Permian-Triassic (P/T) boundary scenarios. Fig. 1 illustrates the predictions for these scenarios as well as two alternative possibilities requiring a shift in calcium isotopes only. Both the Strangelove Ocean and acidification scenarios predict an initial decrease in the carbonate depositional flux followed by an increase in carbonate deposition to return the system to steady state, but the perturbation is potentially much larger under the acidification scenario. In contrast, under the ocean overturn scenario one would expect a positive excursion in δ^44/40Ca because of the stimulation of carbonate precipitation by upwelling of alkaline deep water (2, 5, 15). Oceanographic mechanisms allowing for the overturn scenario have been debated (29–31); here we consider its implications for calcium isotopes irrespective of its feasibility from an oceanographic standpoint. A permanent global shift from calcite- to aragonite-dominated carbonate deposition across the extinction horizon is capable of producing δ^44/40Ca variation similar to that predicted under the acidification scenario; it causes no change in the calcium concentration of the ocean. A global shift in the isotope composition of the calcium delivery flux within the range of likely values would cause a much smaller and more gradual change in δ^44/40Ca and no change in the marine calcium concentration (Fig. 1 and Fig. S2).Open in a separate windowFig. 1.Output from calcium cycle model under scenarios proposed to explain the P/T boundary δ¹³C excursion and associated deposition of carbonate microbialites and oolites. (A) δ^44/40Ca in carbonate rocks. (B) Calcium concentration in seawater. The overturn and acidification scenarios are shown under an assumption of a 100-ky perturbation. Also shown are δ^44/40Ca predictions for a permanent increase by 50% in the proportion of aragonite in carbonate sediment and a 100-ky decrease in the δ^44/40Ca of the river calcium flux by 0.3‰. Modeled calcium concentrations do not change under these last two scenarios. Additional output and sensitivity tests are presented in Fig. S2.To constrain changes in global calcium cycling across the P/T transition, we analyzed the δ^44/40Ca of the micritic fraction of limestone samples from a P/T boundary section at Dajiang, in Guizhou Province, China. P/T boundary strata at Dajiang were deposited above the storm wave base on the Great Bank of Guizhou (GBG), an isolated carbonate platform within the Nanpanjiang Basin (32). The Nanpanjiang Basin is a deep-marine embayment in the Yangtze Block, which was located at approximately 12°N in the eastern Tethys during Early Triassic time (33). The section contains more than 50 m of diverse, fossiliferous packstone and grainstone of the Upper Permian Wujiaping Formation, which contains fusulinid and nonfusulinid foraminifers, calcareous green and red algae, rugose corals, crinoids, brachiopods, calcareous sponges, and gastropods (5, 34). The Wujiaping Formation is overlain by a 15-m-thick thrombolitic microbialite deposited in the immediate aftermath of the mass extinction (Hindeodus parvus conodont zone) (35), which contains a low-diversity assemblage of foraminifers, gastropods, and bivalves with rare echinoderms and calcitic and phosphatic brachiopods (4, 5). The microbialite is overlain by 1–2 m of molluscan and brachiopod packstone with rare echinoderms. Above the thin packstone interval are 47 m of thinly bedded, poorly bioturbated micritic limestone. The Lower Triassic section continues with 95 m of dolomite and dolomitized ooid-bearing cryptalgal laminate overlain by 225 m of peritidal limestone cycles (5, 36). Carbonate sediments continued to accumulate on the GBG through Middle Triassic time, reaching a total thickness of nearly 2 km before the platform drowned early in the Late Triassic (32). The GBG was buried in siliciclastic sediments during Late Triassic time, reaching a maximum burial depth of 2.5–3 km (37). Representative P/T boundary facies are illustrated in Fig. S1.     

Explosive eruption of coal and basalt and the end-Permian mass extinction

The end-Permian extinction decimated up to 95% of carbonate shell-bearing marine species and 80% of land animals. Isotopic excursions, dissolution of shallow marine carbonates, and the demise of carbonate shell-bearing organisms suggest global warming and ocean acidification. The temporal association of the extinction with the Siberia flood basalts at approximately 250 Ma is well known, and recent evidence suggests these flood basalts may have mobilized carbon in thick deposits of organic-rich sediments. Large isotopic excursions recorded in this period are potentially explained by rapid venting of coal-derived methane, which has primarily been attributed to metamorphism of coal by basaltic intrusion. However, recently discovered contemporaneous deposits of fly ash in northern Canada suggest large-scale combustion of coal as an additional mechanism for rapid release of carbon. This massive coal combustion may have resulted from explosive interaction with basalt sills of the Siberian Traps. Here we present physical analysis of explosive eruption of coal and basalt, demonstrating that it is a viable mechanism for global extinction. We describe and constrain the physics of this process including necessary magnitudes of basaltic intrusion, mixing and mobilization of coal and basalt, ascent to the surface, explosive combustion, and the atmospheric rise necessary for global distribution.Recent studies have brought the Great Dying at the end of the Permian Period into focus. Up to 95% of shell-bearing marine species and 80% of land animals perished (1, 2). The temporal association of the extinction with the Siberia flood basalts at approximately 250 Ma is well known (1–7), but a causal mechanism connecting the flood basalts to global extinction is not evident. The flows directly killed only those biota in their path, and basalt is not a massive source of greenhouse gases such as CO₂ (8). Recent studies suggest flood basalts may have mobilized carbon in thick deposits of organic-rich sediments, resulting in global climate change and extinction (4, 5, 7, 9–13). New work also suggests magmatic release of CO₂ from mantle-derived eclogite as a potential extinction mechanism (14).Svensen et al. (15) were the first to discuss the mechanism by which basaltic interaction with organic sediments may cause mass extinction through explosive release of methane. McElwain et al. (16) expanded on this idea by linking the intrusion of Karoo–Ferrar magmas into coal with the 183 Ma Toarcian oceanic anoxic event. In this model, basaltic intrusions metamorphosed sediments driving off hydrocarbons, including methane, which quickly oxidized to carbon dioxide (CO₂) and water. This sudden release of organic carbon acidified the ocean and caused a ∂¹³C excursion in the sedimentary record.Retallack and Jahren (5) applied a similar idea linking basaltic intrusion of coal seams in Siberia to the late Permian extinction. Their study focused on this mechanism as an explanation for the large, short-term carbon isotopic excursions observed during this time. In their model, basaltic dikes feeding flood basalts repeatedly intrude and heat coal seams, causing mobilization and release of methane into the atmosphere. The low carbon isotopic value of coal-derived methane makes it a plausible source for the large isotopic excursions. Other carbon sources have much higher isotopic ratios and would require much larger releases in order to cause the observed excursions (5).In addition to these mechanisms for carbon release, fly ash recently documented in contemporaneous sediments in northern Canada suggest explosive combustion of coal by mafic intrusion (17). This paper explores the physical mechanism by which coal and basalt may have erupted and contributed to the end-Permian mass extinction along with other previously proposed mechanisms.The process begins with a massive mafic sill preferentially intruding, heating, and mixing with thick coal seams in Siberia (Fig. 1). This mechanism is far more efficient than dikes in quickly delivering heat to coal. The hot coal–basalt mixture extrudes at numerous surface locations. The physical mechanism behind this process of pipe initiation and fracturing would be similar to that described by Jamtveit et al. (18). The coal in the mixture ignites on contact with the air, causing pyroclastic fly ash, soot, sulfate, and basaltic dust to ascend into the stratosphere.Open in a separate windowFig. 1.Schematic of coal–basalt volcanism leading to mass extinction.Acceleration of extinction by massive coal–basalt eruption is particularly attractive because it has the virtue of changing the environment within a generation time of many of the organisms that became extinct. Detailed ecology, ocean, and climate modeling are beyond the scope of this paper, but we note potential adverse effects on biota. Large injections of dust, CO₂ and methane into the atmosphere may have generated a highly unstable climate, driving extinctions of land biota. Ocean acidification may have resulted from the sudden addition of CO₂ to the shallow mixed layer on the scale of months to years, driving extinction of marine organisms and formation of the observed dissolution horizon (2).     

Rapid expansion of oceanic anoxia immediately before the end-Permian mass extinction

Periods of oceanic anoxia have had a major influence on the evolutionary history of Earth and are often contemporaneous with mass extinction events. Changes in global (as opposed to local) redox conditions can be potentially evaluated using U system proxies. The intensity and timing of oceanic redox changes associated with the end-Permian extinction horizon (EH) were assessed from variations in (238)U/(235)U (δ(238)U) and Th/U ratios in a carbonate section at Dawen in southern China. The EH is characterized by shifts toward lower δ(238)U values (from -0.37‰ to -0.65‰), indicative of an expansion of oceanic anoxia, and higher Th/U ratios (from 0.06 to 0.42), indicative of drawdown of U concentrations in seawater. Using a mass balance model, we estimate that this isotopic shift represents a sixfold increase in the flux of U to anoxic facies, implying a corresponding increase in the extent of oceanic anoxia. The intensification of oceanic anoxia coincided with, or slightly preceded, the EH and persisted for an interval of at least 40,000 to 50,000 y following the EH. These findings challenge previous hypotheses of an extended period of whole-ocean anoxia prior to the end-Permian extinction.     

Marine anoxia and delayed Earth system recovery after the end-Permian extinction

Delayed Earth system recovery following the end-Permian mass extinction is often attributed to severe ocean anoxia. However, the extent and duration of Early Triassic anoxia remains poorly constrained. Here we use paired records of uranium concentrations ([U]) and ²³⁸U/²³⁵U isotopic compositions (δ²³⁸U) of Upper Permian−Upper Triassic marine limestones from China and Turkey to quantify variations in global seafloor redox conditions. We observe abrupt decreases in [U] and δ²³⁸U across the end-Permian extinction horizon, from ∼3 ppm and −0.15‰ to ∼0.3 ppm and −0.77‰, followed by a gradual return to preextinction values over the subsequent 5 million years. These trends imply a factor of 100 increase in the extent of seafloor anoxia and suggest the presence of a shallow oxygen minimum zone (OMZ) that inhibited the recovery of benthic animal diversity and marine ecosystem function. We hypothesize that in the Early Triassic oceans—characterized by prolonged shallow anoxia that may have impinged onto continental shelves—global biogeochemical cycles and marine ecosystem structure became more sensitive to variation in the position of the OMZ. Under this hypothesis, the Middle Triassic decline in bottom water anoxia, stabilization of biogeochemical cycles, and diversification of marine animals together reflect the development of a deeper and less extensive OMZ, which regulated Earth system recovery following the end-Permian catastrophe.The end-Permian mass extinction—the most severe biotic crisis in the history of animal life—was followed by 5 million years of reduced biodiversity (1, 2), limited ecosystem complexity (3), and large perturbations in global biogeochemical cycling (4, 5). Ocean anoxia has long been invoked both as a cause of the extinction (6–8) and as a barrier to rediversification (9). Numerous lines of evidence demonstrate widespread anoxic conditions around the time of the end-Permian mass extinction (e.g., refs. 6 and 10–12). In contrast, the prevalence of anoxia during the 5- to 10-million-year recovery interval remains poorly constrained (13, 14).Reconstructing paleoredox conditions is challenging because some indicators of anoxia characterize only the local conditions of the overlying water column, whereas other indicators may be influenced by confounding factors, such as weathering rates on land. Here, we use paired measurements of [U] and δ²³⁸U in marine carbonate rocks to differentiate changes in weathering of U from variations in global marine redox conditions. Microbially mediated reduction of U(VI) to U(IV) under anoxic conditions at the sediment−water interface results in a substantial decrease in uranium solubility and a measureable change in ²³⁸U/²³⁵U (15–18). Because ²³⁸U is preferentially reduced and immobilized relative to ²³⁵U, the δ²³⁸U value of seawater U(VI) decreases as the areal extent of bottom water anoxia increases (Fig. S1). Consequently, a global increase in the extent of anoxic bottom waters will cause simultaneous decreases in [U] and δ²³⁸U of carbonate sediments. A previous study of δ²³⁸U variations at one stratigraphic section through the immediate extinction interval (∼40,000 y) (11) suggested a rapid onset of anoxia coincident with the loss of marine diversity. However, with only a single site, it is unclear if the signal is globally representative; moreover, the lack of data for all but the lowest biostratigraphic zone of the Triassic leaves the pattern and timing of environmental amelioration during the recovery interval unconstrained.Open in a separate windowFig. S1.Study materials and methods. (A) Paleogeographic map showing locations of Turkey and South China, modified from ref. 19. (B) Schematic cross section and studied stratigraphic sections of the GBG, modified after ref. 20. (C) Inputs and outputs of the modern uranium cycle.To develop a quantitative, global reconstruction of seawater redox conditions for the entire 15-million-year interval of mass extinction and subsequent Earth system recovery, we measured 58 Upper Permian (Changhsingian) through Upper Triassic (Carnian) limestone samples from three stratigraphic sections (Dajiang, Dawen, and Guandao) arrayed along a depth transect on the Great Bank of Guizhou (GBG), an isolated carbonate platform in the Nanpanjiang Basin of south China (eastern Tethys). To test the extent to which variations in [U] and δ²³⁸U within the GBG reflect global uranium cycling, we also analyzed 28 limestone samples from the Taşkent section, Aladag Nappe, Turkey, located in the western Tethys (Fig. S1). We focused our measurements on samples deposited in shallow marine environments (<100 m water depth, i.e., Dajiang, Dawen, and Taşkent) likely to have remained oxygenated. Variations in [U] and δ²³⁸U in these samples should reflect changes in global, rather than local, redox conditions.     

Massive and rapid predominantly volcanic CO2 emission during the end-Permian mass extinction

The end-Permian mass extinction event (∼252 Mya) is associated with one of the largest global carbon cycle perturbations in the Phanerozoic and is thought to be triggered by the Siberian Traps volcanism. Sizable carbon isotope excursions (CIEs) have been found at numerous sites around the world, suggesting massive quantities of ¹³C-depleted CO₂ input into the ocean and atmosphere system. The exact magnitude and cause of the CIEs, the pace of CO₂ emission, and the total quantity of CO₂, however, remain poorly known. Here, we quantify the CO₂ emission in an Earth system model based on new compound-specific carbon isotope records from the Finnmark Platform and an astronomically tuned age model. By quantitatively comparing the modeled surface ocean pH and boron isotope pH proxy, a massive (∼36,000 Gt C) and rapid emission (∼5 Gt C yr⁻¹) of largely volcanic CO₂ source (∼−15%) is necessary to drive the observed pattern of CIE, the abrupt decline in surface ocean pH, and the extreme global temperature increase. This suggests that the massive amount of greenhouse gases may have pushed the Earth system toward a critical tipping point, beyond which extreme changes in ocean pH and temperature led to irreversible mass extinction. The comparatively amplified CIE observed in higher plant leaf waxes suggests that the surface waters of the Finnmark Platform were likely out of equilibrium with the initial massive centennial-scale release of carbon from the massive Siberian Traps volcanism, supporting the rapidity of carbon injection. Our modeling work reveals that carbon emission pulses are accompanied by organic carbon burial, facilitated by widespread ocean anoxia.

The end-Permian mass extinction (EPME) that occurred at 251.941 ± 0.037 Mya is considered the most severe biodiversity loss in Earth history (1, 2). The EPME coincides with the eruption of the Siberian Traps, a voluminous large igneous province (LIP) that occupies 6 million square kilometers (km²) in Siberia, Russia (3–5). The volcanic activity of this LIP is linked to SO₂ and CO₂ degassing generated by sill intrusion (6–10). The large amount of CO₂ injected into the atmosphere is thought to have led to severe global warming (11–14), catastrophic ocean anoxia (15, 16), and extreme ocean and terrestrial acidification (17–21) being lethal for life on land and in the sea (22). To date, no agreement has been reached regarding the source of the ¹³C-depleted carbon that triggered the global carbon cycle perturbation, the decrease in ocean pH, and the global warming across the EPME. Additionally, atmospheric CO₂ levels following the initial pulse of Siberian Traps volcanism and across the EPME remain poorly known (23, 24), limiting our understanding of the climate feedbacks that occur upon greenhouse gas release during this time.To address this critical gap in our knowledge, we constrain the source, pace and total amount of CO₂ emissions using an Earth system model of intermediate complexity (i.e., carbon centric-Grid Enabled Integrated Earth system model [cGENIE]; SI Appendix) forced by new astronomically tuned δ¹³C records from well-preserved lipid biomarkers preserved in sediments from the Finnmark Platform, Norway. The Finnmark Platform is located offshore northern Norway on the Eastern Barents Sea shelf, hosting an expanded shallow marine section (paleo-water depth roughly 50 to 100 m) where two drill cores were collected (7128/12-U-01 and 7129/10-U-01) spanning the Permian–Triassic transition (Fig. 1). A previously generated bulk organic carbon isotope record (δ¹³C_org) from the same core shows a two-step decline with a total carbon isotope excursion (CIE) magnitude of ∼4‰ (25). Although the sedimentary organic carbon was considered primarily of terrestrial origin, small contributions from marine organic carbon production could not be excluded. Here, we use compound-specific carbon isotope analysis of both long-chain and short-chain n-alkanes preserved in marine sediments in the Finnmark Platform to generate separate yet directly comparable records of δ¹³C for the terrestrial and the marine realm, respectively, across the EPME. Long-chain n-alkanes with a strong odd-over-even predominance (n-C₂₇ and n-C₂₉) are produced by higher plant leaf waxes, and their isotopic composition (δ¹³C_wax) relates to their main carbon source (i.e., atmospheric CO₂) (26). On the other hand, short-chain alkanes (n-C₁₇ and n-C₁₉) are derived from marine algae, and their δ¹³C values (δ¹³C_algae) represent carbon in the marine realm (27, 28). To date, only a few EPME compound-specific carbon isotope studies have been reported, all of which are limited by unfavorable sedimentary facies or high thermal maturity of the organic matter (29, 30). In the present study, the exceptionally low thermal maturity of the organic matter is evident from the yellow color of pollen and spores, indicating a color index 2 out of 7 on the thermal alteration scale of Batten (31), which is equivalent to a vitrinite reflectance R₀ of 0.3%. Moreover, the high sedimentation rate (discussed in Carbon Cycle Quantification Using Astrochronology and Earth System Model) of the siliciclastic sediments at the study site allows for studying both marine and terrestrial CIE across the EPME in unprecedented detail. Taken together, the Finnmark sedimentary records enable the reconstruction of individual yet directly comparable carbon isotope records for the terrestrial and the marine realm that can be astronomically tuned and used to quantitatively assess the source, pace, and total amount of ¹³C-depleted carbon released during the Siberian Traps eruption that led to the EPME. Using our new compound-specific carbon isotope records, rather than marine carbonates, has several advantages: 1) new astrochronology enables a 10⁴-year temporal resolution for our paired marine and terrestrial carbon isotope records; 2) we do not need to assume a constant sedimentation rate between tie point or using diachronous biozones to compare age like those used in global compilations (24) (see Fig. 4A); 3) the δ¹³C_algae data are not artificially smoothed as in ref. 32 to avoid underestimation of the CIE magnitude; and 4) our records are not affected by dissolution or truncation, a phenomenon common to shallow marine carbonates due to the presumed ocean acidification occurred during the EPME (18, 33). In addition, the directly comparable records of δ¹³C for the atmosphere and the ocean offer further insights into the size of the true CIE and rate and duration of carbon emissions.Open in a separate windowFig. 1.(A) Paleogeographical map of the Late Permian, with former and current coastlines. Indicated are 1) the location of Finnmark cores 7128/12-U-01 and 7129/10-U-01, 2) the East Greenland site at Kap Stosch discussed in ref. 52, 3) the GSSP site for the base of the Triassic at Meishan, China, and 4) the Kuh-e-Ali Bashi site of Iran (66, 107). The map was modified after ref. 61. (B) Paleogeography and paleobathymetry of the Late Permian used in cGENIE.Open in a separate windowFig. 4.Synthesized proxy records of carbon isotopes from marine carbonates and fossil C₃ land plants remains, sea surface temperature, and pH. (A) Comparison between δ¹³C_algae and global marine carbonate carbon isotopes from sites at Abadeh, Kuh-e-Ali Bashi, Shahreza, and Zal in Iran, Meishan, Wenbudangsang, and Yanggou in South China, at Bálvány North in Hungary, and at Nhi Tao in Vietnam (24). (B) Comparison between δ¹³C_leaf wax and the δ¹³C of sedimentary leaf cuticles and wood of C₃ land plants from South China (24). (C) Reconstructed sea surface temperature data using conodont fossils (circles) (24) and brachiopods (triangles) (14). The conodont-based temperature data are from sites in the Paleo-Tethys, including Chanakhchi, Kuh-e Ali Bashi, Meishan, Shangsi, and Zal. (D) Relative changes in sea surface pH based on boron isotope proxy from ref. 17 and ref. 20. Pink and red circles are data from scenario 1 and scenario 2 in ref. 17, and green and blue diamonds are data from scenario 1 and scenario 2 in ref. 20.     

From the Cover: Evidence from South Africa for a protracted end-Permian extinction on land

Earth’s largest biotic crisis occurred during the Permo–Triassic Transition (PTT). On land, this event witnessed a turnover from synapsid- to archosauromorph-dominated assemblages and a restructuring of terrestrial ecosystems. However, understanding extinction patterns has been limited by a lack of high-precision fossil occurrence data to resolve events on submillion-year timescales. We analyzed a unique database of 588 fossil tetrapod specimens from South Africa’s Karoo Basin, spanning ∼4 My, and 13 stratigraphic bin intervals averaging 300,000 y each. Using sample-standardized methods, we characterized faunal assemblage dynamics during the PTT. High regional extinction rates occurred through a protracted interval of ∼1 Ma, initially co-occurring with low origination rates. This resulted in declining diversity up to the acme of extinction near the Daptocephalus–Lystrosaurus declivis Assemblage Zone boundary. Regional origination rates increased abruptly above this boundary, co-occurring with high extinction rates to drive rapid turnover and an assemblage of short-lived species symptomatic of ecosystem instability. The “disaster taxon” Lystrosaurus shows a long-term trend of increasing abundance initiated in the latest Permian. Lystrosaurus comprised 54% of all specimens by the onset of mass extinction and 70% in the extinction aftermath. This early Lystrosaurus abundance suggests its expansion was facilitated by environmental changes rather than by ecological opportunity following the extinctions of other species as commonly assumed for disaster taxa. Our findings conservatively place the Karoo extinction interval closer in time, but not coeval with, the more rapid marine event and reveal key differences between the PTT extinctions on land and in the oceans.

Mass extinctions are major perturbations of the biosphere resulting from a wide range of different causes including glaciations and sea level fall (1), large igneous provinces (2), and bolide impacts (3, 4). These events caused permanent changes to Earth’s ecosystems, altering the evolutionary trajectory of life (5). However, links between the broad causal factors of mass extinctions and the biological and ecological disturbances that lead to species extinctions have been difficult to characterize. This is because ecological disturbances unfold on timescales much shorter than the typical resolution of paleontological studies (6), particularly in the terrestrial record (6–8). Coarse-resolution studies have demonstrated key mass extinction phenomena including high extinction rates and lineage turnover (7, 9), changes in species richness (10), ecosystem instability (11), and the occurrence of disaster taxa (12). However, finer time resolutions are central to determining the association and relative timings of these effects, their potential causal factors, and their interrelationships. Achieving these goals represents a key advance in understanding the ecological mechanisms of mass extinctions.The end-Permian mass extinction (ca. 251.9 Ma) was Earth’s largest biotic crisis as measured by taxon last occurrences (13–15). Large outpourings from Siberian Trap volcanism (2) are the likely trigger of calamitous climatic changes, including a runaway greenhouse effect and ocean acidification, which had profound consequences for life on land and in the oceans (16–18). An estimated 81% of marine species (19) and 89% of tetrapod genera became extinct as established Permian ecosystems gave way to those of the Triassic. In the ocean, this included the complete extinction of reef-forming tabulate and rugose corals (20, 21) and significant losses in previously diverse ammonoid, brachiopod, and crinoid families (22). On land, many nonmammalian synapsids became extinct (16), and the glossopterid-dominated floras of Gondwana also disappeared (23). Stratigraphic sequences document a global “coral gap” and “coal gap” (24, 25), suggesting reef and forest ecosystems were rare or absent for up to 5 My after the event (26). Continuous fossil-bearing deposits documenting patterns of turnover across the Permian–Triassic transition (PTT) on land (27) and in the oceans (28) are geographically widespread (29, 30), including marine and continental successions that are known from China (31, 32) and India (33). Continental successions are known from Russia (34), Australia (35), Antarctica (36), and South Africa’s Karoo Basin (Fig. 1 and 37–40), the latter providing arguably the most densely sampled and taxonomically scrutinized (41–43) continental record of the PTT. The main extinction has been proposed to occur at the boundary between two biostratigraphic zones with distinctive faunal assemblages, the Daptocephalus and Lystrosaurus declivis assemblage zones (Fig. 1), which marks the traditional placement of the Permian–Triassic geologic boundary [(37) but see ref. 44]. Considerable research has attempted to understand the anatomy of the PTT in South Africa (38, 39, 45–52) and to place it in the context of biodiversity changes across southern Gondwana (53, 54) and globally (29, 31, 32, 44, 47, 55).Open in a separate windowFig. 1.Map of South Africa depicting the distribution of the four tetrapod fossil assemblage zones (Cistecephalus, Daptocephalus, Lystrosaurus declivis, Cynognathus) and our two study sites where fossils were collected in this study (sites A and B). Regional lithostratigraphy and biostratigraphy within the study interval are shown alongside isotope dilution–thermal ionization mass spectrometry dates retrieved by Rubidge et al., Botha et al., and Gastaldo et al. (37, 44, 80). The traditional (dashed red line) and associated PTB hypotheses for the Karoo Basin (37, 44) are also shown. Although traditionally associated with the PTB, the Daptocephalus–Lystrosaurus declivis Assemblage Zone boundary is defined by first appearances of co-occurring tetrapod assemblages, so its position relative to the three PTB hypotheses is unchanged. The Ripplemead member (*) has yet to be formalized by the South African Committee for Stratigraphy.Decades of research have demonstrated the richness of South Africa’s Karoo Basin fossil record, resulting in hundreds of stratigraphically well-documented tetrapod fossils across the PTT (37, 39, 56). This wealth of data has been used qualitatively to identify three extinction phases and an apparent early postextinction recovery phase (39, 45, 51). Furthermore, studies of Karoo community structure and function have elucidated the potential role of the extinction and subsequent recovery in breaking the incumbency of previously dominant clades, including synapsids (11, 57). Nevertheless, understanding patterns of faunal turnover and recovery during the PTT has been limited by the scarcity of quantitative investigations. Previous quantitative studies used coarsely sampled data (i.e., assemblage zone scale, 2 to 3 Ma time intervals) to identify low species richness immediately after the main extinction, potentially associated with multiple “boom and bust” cycles of primary productivity based on δ¹³C variation during the first 5 My of the Triassic (41, 58). However, many details of faunal dynamics in this interval remain unknown. Here, we investigate the dynamics of this major tetrapod extinction at an unprecedented time resolution (on the order of hundreds of thousands of years), using sample-standardized methods to quantify multiple aspects of regional change across the Cistecephalus, Daptocephalus, and Lystrosaurus declivis assemblage zones.     

心血管病患者院内死亡分析

目的　较准确地认识心血管病患者死亡的多见和少见病种及其危害程度 ;了解在直接死因中 ,心力衰竭及心脏猝死的构成。方法　本所心内科 1993年 7月 1日至 1998年 6月 3 0日五年内死亡总病例数 2 3 3例 ,回顾性分析每种疾病致死的人数及其构成比 ,并计算心力衰竭及心脏猝死在直接死因中的构成比。结果　第一位致死疾病为急性心肌梗死 ( AMI) ,构成比 2 5 .75 % ( 60 /2 3 3 ) ;第二位致死疾病为风湿性心脏病 ( RHD) ,构成比 2 0 .60 % ( 4 8/2 3 3 ) ;并列第三位是冠心病 ( CHD) (急性心肌梗死另计 )和感染性心内膜炎 ( IE) ,构成比均为 12 .0 2 % ( 2 8/2 3 3 ) ;其它依次为扩张型心肌病 ( 5 .15 % )、成人先天性心脏病 ( 3 .86% )、原发性肺动脉高压 ( 3 .43 % )和主动脉瘤 ( 3 .43 % )、高血压性心脏病 ( 3 .0 0 % )、肺源性心脏病 ( 2 .15 % ) ,……。另外 ,在直接死因中 ,心力衰竭占72 .5 3 % ( 169/2 3 3 ) ,心脏猝死占 11.5 9% ( 2 7/2 3 3 )。结论　急性心肌梗死、风湿性心脏病、冠心病 (急性心肌梗死另计 )、感染性心内膜炎、扩张型心肌病是主要的引起死亡的心血管病 ;心力衰竭是心血管病患者最多见的直接死因 ,(院内 )心脏猝死不容忽视     

Characteristics of the washout dead space.

The dead space volume was reproducibly measured in normal and diseased lungs by analysis of an inert gas washout. This washout dead space was appreciably larger than that measured by the Fowler technique. In the patients, the washout dead space (VD(0)) formed 72% of the physiological dead space volume, while the Fowler (VD(F)) method accounted for only 50%. The VD(O) increased significantly with age in males, but not in females. VD(F) was not well related to age in this population. VD(O) and VD(F) did not relate to lung volume in these subjects. Although that portion of the dead space delivered in Phase I was significantly greater in males than in females, it was not responsible for the difference in dead space measured by the two techniques. This volume difference was found in that portion delivered late in the breath (Phase III). The nature of this volume is speculative, but may involve a parallel dead space that is measured in addition to the series dead space.