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.

Flat latitudinal diversity gradient caused by the Permian-Triassic mass extinction.

The latitudinal diversity gradient (LDG) is recognized as one of the most pervasive, global patterns of present-day biodiversity. However, the controlling mechanisms have proved difficult to identify because many potential drivers covary in space. The geological record presents a unique opportunity for understanding the mechanisms which drive the LDG by providing a direct window to deep-time biogeographic dynamics. Here we used a comprehensive database containing 52,318 occurrences of marine fossils to show that the shape of the LDG changed greatly during the Permian-Triassic mass extinction from showing a significant tropical peak to a flattened LDG. The flat LDG lasted for the entire Early Triassic (∼5 My) before reverting to a modern-like shape in the Middle Triassic. The environmental extremes that prevailed globally, especially the dramatic warming, likely induced selective extinction in low latitudes and accumulation of diversity in high latitudes through origination and poleward migration, which combined together account for the flat LDG of the Early Triassic.

Rapid enhancement of chemical weathering recorded by extremely light seawater lithium isotopes at the Permian-Triassic boundary.

Lithium (Li) isotope analyses of sedimentary rocks from the Meishan section in South China reveal extremely light seawater Li isotopic signatures at the Permian-Triassic boundary (PTB), which coincide with the most severe mass extinction in the history of animal life. Using a dynamic seawater lithium box model, we show that the light seawater Li isotopic signatures can be best explained by a significant influx of riverine [Li] with light δ7Li to the ocean realm. The seawater Li isotope excursion started ≥300 Ky before and persisted up to the main extinction event, which is consistent with the eruption time of the Siberian Traps. The eruption of the Siberian Traps exposed an enormous amount of fresh basalt and triggered CO2 release, rapid global warming, and acid rains, which in turn led to a rapid enhancement of continental weathering. The enhanced continental weathering delivered excessive nutrients to the oceans that could lead to marine eutrophication, anoxia, acidification, and ecological perturbation, ultimately resulting in the end-Permian mass extinction.

Redox chemistry changes in the Panthalassic Ocean linked to the end-Permian mass extinction and delayed Early Triassic biotic recovery.

The end-Permian mass extinction represents the most severe biotic crisis for the last 540 million years, and the marine ecosystem recovery from this extinction was protracted, spanning the entirety of the Early Triassic and possibly longer. Numerous studies from the low-latitude Paleotethys and high-latitude Boreal oceans have examined the possible link between ocean chemistry changes and the end-Permian mass extinction. However, redox chemistry changes in the Panthalassic Ocean, comprising ∼85-90% of the global ocean area, remain under debate. Here, we report multiple S-isotopic data of pyrite from Upper Permian-Lower Triassic deep-sea sediments of the Panthalassic Ocean, now present in outcrops of western Canada and Japan. We find a sulfur isotope signal of negative Δ33S with either positive δ34S or negative δ34S that implies mixing of sulfide sulfur with different δ34S before, during, and after the end-Permian mass extinction. The precise coincidence of the negative Δ33S anomaly with the extinction horizon in western Canada suggests that shoaling of H2S-rich waters may have driven the end-Permian mass extinction. Our data also imply episodic euxinia and oscillations between sulfidic and oxic conditions during the earliest Triassic, providing evidence of a causal link between incursion of sulfidic waters and the delayed recovery of the marine ecosystem.

Flourishing ocean drives the end-Permian marine mass extinction.

The end-Permian mass extinction, the most severe biotic crisis in the Phanerozoic, was accompanied by climate change and expansion of oceanic anoxic zones. The partitioning of sulfur among different exogenic reservoirs by biological and physical processes was of importance for this biodiversity crisis, but the exact role of bioessential sulfur in the mass extinction is still unclear. Here we show that globally increased production of organic matter affected the seawater sulfate sulfur and oxygen isotope signature that has been recorded in carbonate rock spanning the Permian-Triassic boundary. A bifurcating temporal trend is observed for the strata spanning the marine mass extinction with carbonate-associated sulfate sulfur and oxygen isotope excursions toward decreased and increased values, respectively. By coupling these results to a box model, we show that increased marine productivity and successive enhanced microbial sulfate reduction is the most likely scenario to explain these temporal trends. The new data demonstrate that worldwide expansion of euxinic and anoxic zones are symptoms of increased biological carbon recycling in the marine realm initiated by global warming. The spatial distribution of sulfidic water column conditions in shallow seafloor environments is dictated by the severity and geographic patterns of nutrient fluxes and serves as an adequate model to explain the scale of the marine biodiversity crisis. Our results provide evidence that the major biodiversity crises in Earth's history do not necessarily implicate an ocean stripped of (most) life but rather the demise of certain eukaryotic organisms, leading to a decline in species richness.

Pre- versus post-mass extinction divergence of Mesozoic marine reptiles dictated by time-scale dependence of evolutionary rates.

The fossil record of a major clade often starts after a mass extinction even though evolutionary rates, molecular or morphological, suggest its pre-extinction emergence (e.g. squamates, placentals and teleosts). The discrepancy is larger for older clades, and the presence of a time-scale-dependent methodological bias has been suggested, yet it has been difficult to avoid the bias using Bayesian phylogenetic methods. This paradox raises the question of whether ecological vacancies, such as those after mass extinctions, prompt the radiations. We addressed this problem by using a unique temporal characteristic of the morphological data and a high-resolution stratigraphic record, for the oldest clade of Mesozoic marine reptiles, Ichthyosauromorpha. The evolutionary rate was fastest during the first few million years of ichthyosauromorph evolution and became progressively slower over time, eventually becoming six times slower. Using the later slower rates, estimates of divergence time become excessively older. The fast, initial rate suggests the emergence of ichthyosauromorphs after the end-Permian mass extinction, matching an independent result from high-resolution stratigraphic confidence intervals. These reptiles probably invaded the sea as a new ecosystem was formed after the end-Permian mass extinction. Lack of information on early evolution biased Bayesian clock rates.

Organism activity levels predict marine invertebrate survival during ancient global change extinctions.

Multistressor global change, the combined influence of ocean warming, acidification, and deoxygenation, poses a serious threat to marine organisms. Experimental studies imply that organisms with higher levels of activity should be more resilient, but testing this prediction and understanding organism vulnerability at a global scale, over evolutionary timescales, and in natural ecosystems remain challenging. The fossil record, which contains multiple extinctions triggered by multistressor global change, is ideally suited for testing hypotheses at broad geographic, taxonomic, and temporal scales. Here, I assess the importance of activity level for survival of well-skeletonized benthic marine invertebrates over a 100-million-year-long interval (Permian to Jurassic periods) containing four global change extinctions, including the end-Permian and end-Triassic mass extinctions. More active organisms, based on a semiquantitative score incorporating feeding and motility, were significantly more likely to survive during three of the four extinction events (Guadalupian, end-Permian, and end-Triassic). In contrast, activity was not an important control on survival during nonextinction intervals. Both the end-Permian and end-Triassic mass extinctions also triggered abrupt shifts to increased dominance by more active organisms. Although mean activity gradually returned toward pre-extinction values, the net result was a permanent ratcheting of ecosystem-wide activity to higher levels. Selectivity patterns during ancient global change extinctions confirm the hypothesis that higher activity, a proxy for respiratory physiology, is a fundamental control on survival, although the roles of specific physiological traits (such as extracellular pCO2 or aerobic scope) cannot be distinguished. Modern marine ecosystems are dominated by more active organisms, in part because of selectivity ratcheting during these ancient extinctions, so on average may be less vulnerable to global change stressors than ancient counterparts. However, ancient extinctions demonstrate that even active organisms can suffer major extinction when the intensity of environmental disruption is intense.

Predator-prey interactions amongst Permo-Triassic terrestrial vertebrates as a deterministic factor influencing faunal collapse and turnover.

Unlike modern mammalian communities, terrestrial Paleozoic and Mesozoic vertebrate systems were characterized by carnivore faunas that were as diverse as their herbivore faunas. The comparatively narrow food base available to carnivores in these paleosystems raises the possibility that predator-prey interactions contributed to unstable ecosystems by driving populations to extinction. Here, we develop a model of predator-prey interactions based on diversity, abundance and body size patterns observed in the Permo-Triassic vertebrate fossil record of the Karoo Basin, South Africa. Our simulations reflect empirical evidence that despite relatively high carnivore: herbivore species ratios, herbivore abundances were sufficient for carnivores to maintain required intake levels through most of the Karoo sequence. However, high mortality rates amongst herbivore populations, even accounting for birth rates of different-sized species, are predicted for assemblages immediately preceding the end-Guadalupian and end-Permian mass extinctions, as well as in the Middle Triassic when archosaurs replaced therapsids as the dominant terrestrial fauna. These results suggest that high rates of herbivore mortality could have played an important role in biodiversity declines leading up to each of these turnover events. Such declines would have made the systems especially vulnerable to subsequent stochastic events and environmental perturbations, culminating in large-scale extinctions.

The oldest record of Saurosphargiformes (Diapsida) from South China could fill an ecological gap in the Early Triassic biotic recovery.

Diversification following the end-Permian mass extinction marks the initiation of Mesozoic reptile dominance and of modern marine ecosystems, yet major clades are best known from the Middle Triassic suggesting delayed recovery, while Early Triassic localities produce poorly preserved specimens or have restricted diversity. Here we describe Pomolispondylus biani gen. et sp. nov. from the Early Triassic Nanzhang-Yuan'an Fauna of China assigned to Saurosphargiformes tax. nov., a clade known only from the Middle Triassic or later, which includes Saurosphargidae, and likely is the sister taxon to Sauropterygia. Pomolispondylus biani is allied to Saurosphargidae by the extended transverse processes of dorsal vertebrae and a low, table-like dorsal surface on the neural spine; however, it does not have the typical extensive osteoderms. Rather an unusual tuberous texture on the dorsal neural spine and rudimentary ossifications lateral to the gastralia are observed. Discovery of Pomolispondylus biani extends the known range of Saurosphargiformes and increases the taxic and ecological diversity of the Nanzhang-Yuan'an Fauna. Its small size fills a different ecological niche with respect to previously found species, but the overall food web remains notably different in structure to Middle Triassic and later ecosystems, suggesting this fauna represents a transitional stage during recovery rather than its endpoint.

The main stage of recovery after the end-Permian mass extinction: taxonomic rediversification and ecologic reorganization of marine level-bottom communities during the Middle Triassic.

The recovery of marine life from the end-Permian mass extinction event provides a test-case for biodiversification models in general, but few studies have addressed this episode in its full length and ecological context. This study analyses the recovery of marine level-bottom communities from the end-Permian mass extinction event over a period of 15 Ma, with a main focus on the previously neglected main phase during the Middle Triassic. Our analyses are based on faunas from 37 lithological units representing different environmental settings, ranging from lagoons to inner, mid- and outer ramps. Our dataset comprises 1562 species, which belong to 13 higher taxa and 12 ecological guilds. The diversification pattern of most taxa and guilds shows an initial Early Triassic lag phase that is followed by a hyperbolic diversity increase during the Bithynian (early middle Anisian) and became damped later in the Middle Triassic. The hyperbolic diversity increase is not predicted by models that suggest environmental causes for the initial lag phase. We therefore advocate a model in which diversification is primarily driven by the intensity of biotic interactions. Accordingly, the Early Triassic lag phase represents the time when the reduced species richness in the wake of the end-Permian mass extinction was insufficient for stimulating major diversifications, whereas the Anisian main diversification event started when self-accelerating processes became effective and stopped when niche-crowding prevented further diversification. Biotic interactions that might drive this pattern include interspecific competition but also habitat construction, ecosystem engineering and new options for trophic relationships. The latter factors are discussed in the context of the resurgence of large carbonate platforms, which occurred simultaneously with the diversification of benthic communities. These did not only provide new hardground habitats for a variety of epifaunal taxa, but also new options for grazing gastropods that supposedly fed from microalgae growing on dasycladaceans and other macroalgae. Whereas we do not claim that changing environmental conditions were generally unimportant for the recovery of marine level-bottom communities, we note that their actual role can only be assessed when tested against predictions of the biotic model.

The paleobiology and paleoecology of South African Lystrosaurus.

Lystrosaurus was one of the few tetrapods to survive the end-Permian mass extinction (EPME), the most catastrophic biotic crisis in Phanerozoic history. The significant increased abundance of this genus during the post-extinction Early Triassic recovery period has made Lystrosaurus an iconic survivor taxon globally and ideal for studying changes in growth dynamics during a mass extinction. There is potential evidence of a Lilliput effect in Lystrosaurus in South Africa as the two Triassic species that became highly abundant after the EPME are relatively smaller than the two Permian species. In order to test this hypothesis a detailed examination of the body size and life history of Permo-Triassic Lystrosaurus is required. In this study, the basal skull length and growth patterns of the four South African Lystrosaurus species from the Karoo Basin, L. maccaigi, L. curvatus, L. murrayi and L. declivis, were examined using cranial measurements and bone histology. The basal skull length measurements show that the Triassic species are smaller than the Permian species and supports previous studies. The osteohistology examination of all four species reveal rapidly forming fibrolamellar bone tissues during early to mid-ontogeny. Growth marks are common in L. maccaigi and L. curvatus, but rare and inconsistent in the purely Triassic L. murrayi and L. declivis. The inconsistency of the growth marks in these latter two taxa suggests the presence of developmental plasticity. This feature may have been advantageous in allowing these species to alter their growth patterns in response to environmental cues in the post-extinction Early Triassic climate. An overall transition to slower forming parallel-fibered bone is observed in the largest individuals of L. maccaigi, but absent from the limb bones of the other species. The absence of such bone tissue or outer circumferential lamellae in L. curvatus, L. murrayi and L. declivis indicates that even the largest collected specimens do not represent fully grown individuals. Although L. murrayi and L. declivis are smaller in size, the lack of a growth asymptote in the largest specimens indicates that adult individuals would have been notably larger and may have been similar in size to large L. maccaigi and L. curvatus when fully grown. Thus, the previously described Lilliput effect, recognized by some authors in the Karoo fossil record (such as the therocephalian Moschorhinus kitchingi), may be a product of high juvenile excess mortality in the Triassic rather than a strict "dwarfing" of Lystrosaurus species. The lifestyle of Lystrosaurus was also re-examined. Although previous studies have proposed an aquatic lifestyle for the genus, the similar morphology and bone microanatomy to several other large terrestrial Permo-Triassic dicynodonts supports a fully terrestrial mode of life.

Taxonomic and ecomorphological diversity of temnospondyl amphibians across the Permian-Triassic boundary in the Karoo Basin (South Africa).

Temnospondyl amphibians experienced a geologically brief interval of success in the wake of the end-Permian mass extinction. This study examines the relationship between taxonomic and ecological diversity of temnospondyls across the Permian-Triassic boundary in the Karoo Basin of South Africa. Ecomorphological diversity, as implied by differences in cranial shape, was incorporated into the study by the use of a landmark-based geometric morphometric analysis. Both taxonomic diversity and cranial disparity are low during the Permian and increase across the Permian-Triassic boundary. Taxonomic diversity is stable through the Triassic, but disparity shows subsequent increases during the Olenekian and Anisian. Temnospondyls are restricted in size immediately following the extinction, but size range fully rebounds by the Olenekian. Cranial shape is heavily influenced by phylogenetic relatedness, and the observed increases in disparity may be partly the result of decreases in the net relatedness of coeval Karoo stereospondylomorph temnospondyls in younger faunas. The increase in community level taxonomic diversity for temnospondyls in the Karoo following the end-Permian mass extinction was likely facilitated by an influx of distantly related and ecologically distinct species.

Unexpected Early Triassic marine ecosystem and the rise of the Modern evolutionary fauna.

In the wake of the end-Permian mass extinction, the Early Triassic (~251.9 to 247 million years ago) is portrayed as an environmentally unstable interval characterized by several biotic crises and heavily depauperate marine benthic ecosystems. We describe a new fossil assemblage-the Paris Biota-from the earliest Spathian (middle Olenekian, ~250.6 million years ago) of the Bear Lake area, southeastern Idaho, USA. This highly diversified assemblage documents a remarkably complex marine ecosystem including at least seven phyla and 20 distinct metazoan orders, along with algae. Most unexpectedly, it combines early Paleozoic and middle Mesozoic taxa previously unknown from the Triassic strata, among which are primitive Cambrian-Ordovician leptomitid sponges (a 200-million year Lazarus taxon) and gladius-bearing coleoid cephalopods, a poorly documented group before the Jurassic (~50 million years after the Early Triassic). Additionally, the crinoid and ophiuroid specimens show derived anatomical characters that were thought to have evolved much later. Unlike previous works that suggested a sluggish postcrisis recovery and a low diversity for the Early Triassic benthic organisms, the unexpected composition of this exceptional assemblage points toward an early and rapid post-Permian diversification for these clades. Overall, it illustrates a phylogenetically diverse, functionally complex, and trophically multileveled marine ecosystem, from primary producers up to top predators and potential scavengers. Hence, the Paris Biota highlights the key evolutionary position of Early Triassic fossil ecosystems in the transition from the Paleozoic to the Modern marine evolutionary fauna at the dawn of the Mesozoic era.