Research Article

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

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Science  07 Dec 2018:
Vol. 362, Issue 6419, eaat1327
DOI: 10.1126/science.aat1327
  • Schematic illustration of temperature-dependent hypoxia as a driver of the end-Permian marine mass extinction.

    Greenhouse gas forcing in a model of Earth’s climate at the end of the Permian drives ocean warming (contours) and oxygen loss that match geochemical proxy data. Ocean warming raises the organismal O2 demand amid declining supply. The resulting loss of aerobic habitat for diverse physiologies induces a mass extinction in model animal types (line) whose geographic signature—increased severity outside of the tropics—is consistent with reconstructions from the marine fossil record (circles).

    ILLUSTRATION BY J. PENN AND C. DEUTSCH; FOSSIL DRAWINGS BY E. HAECKEL; PHOTOS BY W. KAVENEY (BLUE CRAB), H. FJELD (ATLANTIC COD), J. WHITE (CHAMBERED NAUTILUS)
  • Fig. 1 Permian/Triassic ocean temperature and O2.

    (A) Map of near-surface (0 to 70 m) ocean warming across the Permian/Triassic (P/Tr) transition simulated in the Community Earth System Model. The region in gray represents the supercontinent Pangaea. (B) Simulated near-surface ocean temperatures (red circles) in the eastern Paleo-Tethys (5°S to 20°N) and reconstructed from conodont δ18Oapatite measurements (black circles) (4). The time scale of the δ18Oapatite data (circles) has been shifted by 700,000 years to align it with δ18Oapatite calibrated by U-Pb zircon dates (open triangles) (1), which also define the extinction interval (gray band). Error bars are 1°C. (C) Simulated zonal mean ocean warming (°C) across the P/Tr transition. (D) Map of seafloor oxygen levels in the Triassic simulation. Hatching indicates anoxic regions (O2 < 5 mmol/m3). (E) Simulated seafloor anoxic fraction ƒanox (red circles). Simulated values are used to drive a published one-box ocean model of the ocean’s uranium cycle (8) and are compared to δ238U isotope measurements of marine carbonates formed in the Paleo-Tethys (black circles). Error bars are 0.1‰. (F) Same as in (C) but for simulated changes in O2 concentrations (mmol/m3).

  • Fig. 2 Physiological and ecological traits of the Metabolic Index (Φ) and its end-Permian distribution.

    (A) The critical O2 pressure (pO2crit) needed to sustain resting metabolic rates in laboratory experiments (red circles, Cancer irroratus) vary with temperature with a slope proportional to Eo from a value of 1/Ao at a reference temperature (Tref), as estimated by linear regression when Φ = 1 (19). Energetic demands for ecological activity increase hypoxic thresholds by a factor Φcrit above the resting state, a value estimated from the Metabolic Index at a species’ observed habitat range limit. (B) Zonal mean distribution of Φ in the Permian simulation for ecophysiotypes with average 1/Ao and Eo (~4.5 kPa and 0.4 eV, respectively). (C and D) Variations in Φ for an ecophysiotype with weak (C) and strong (D) temperature sensitivities (Eo = 0 eV and 1.0 eV, respectively), both with 1/Ao ~ 4.5 kPa. Example values of Φcrit (black lines) outline different distributions of available aerobic habitat for a given combination of 1/Ao and Eo.

  • Fig. 3 Aerobic habitat during the end-Permian and its change under warming and O2 loss.

    (A) Percentage of ocean volume in the upper 1000 m that is viable aerobic habitat (Φ ≥ Φcrit) in the Permian for ecophysiotypes with different hypoxic threshold parameters 1/Ao and temperature sensitivities Eo. (B) Relative (percent) change in Permian aerobic habitat volume (ΔVi, where i is an index of ecophysiotype) under Triassic warming and O2 loss. Colored contours are for ecophysiotypes with Φcrit = 3. Measured values of 1/Ao and Eo in modern species are shown as black symbols, but in (B) these are colored according to habitat changes at a species’ specific Φcrit where an estimate of this parameter is available. The gray region at upper left indicates trait combinations for which no habitat is available in the Permian simulation.

  • Fig. 4 Global and regional extinction at the end of the Permian.

    (A) Global extinction versus latitude, as predicted for model ecophysiotypes and observed in marine genera from end-Permian fossil occurrences in the Paleobiology Database (PBDB). Model extinction is calculated from the simulated changes in Permian global aerobic habitat volume (ΔVi) under Triassic warming and O2 loss (19). The maximum depth of initial habitat and fractional loss of habitat resulting in extinction (Vcrit) are varied from 500 to 4000 m (colors) and from 40 to 95% (right-axis labels), respectively. The observed extinction of genera combines occurrences from all phyla in the PBDB (points). Error bars are the range of genera extinction across two taxonomic groupings: phyla multiply sampled in the modern physiology data (arthropods, chordates, and mollusks) and all other phyla. Latitude bands with fewer than five Permian fossil collections are excluded. The average range is used for latitude bands missing extinction estimates from both taxonomic groupings (i.e., 80°S, 30°S, and 40°N). The main latitudinal trend—increased extinction away from the tropics—is found when including all data together and when restricting to the best-sampled latitude bands (fig. S14). In all panels, model values are averaged across longitude and above 500 m. (B) Average hypoxic threshold and Φcrit across ecophysiotypes versus latitude in the Permian. In (B) to (D), shading represents the 1σ standard deviation at each latitude. (C) Regional extinction (i.e., extirpation) versus latitude for model ecophysiotypes, with individual contributions from warming and the loss of seawater O2 concentration. Extirpation occurs in locations where the Metabolic Index meets the active demand of an ecophysiotype in the Permian (Φ ≥ Φcrit) but falls below this threshold in the Triassic (Φ < Φcrit). (D) Same as (C) but including globally extinct ecophysiotypes (using a maximum habitat depth of 1000 m and Vcrit = 80%), and as observed in marine genera from end-Permian and early Triassic fossil occurrences of all phyla in the PBDB. Observed extirpation magnitudes are averaged across tropical and extratropical latitude bands (red points and horizontal lines). Regional 1σ standard deviations are shown as vertical lines.

Supplementary Materials

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

    Justin L. Penn, Curtis Deutsch, Jonathan L. Payne, Erik A. Sperling

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods 
    • Supplementary Text
    • Figs. S1 to S15
    • Tables S1 to S3 
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