Euxinic versus ferruginous anoxia before and during the Toarcian Oceanic Anoxic Event

Mesozoic oceanic anoxic events are recognized as widespread deposits of marine organic-rich mudrocks temporally associated with mass extinctions and large igneous province emplacement. The Toarcian Oceanic Anoxic Event (T-OAE) is one example during which expanded ocean anoxia is hypothesised in response to environmental perturbations associated with emplacement of the Karoo–Ferrar igneous province. However, the global extent of total sea�oor anoxia and the relative extent of ferruginous (anoxic and Fe2+-rich) versus euxinic (anoxic and H2S-rich) conditions during the T-OAE and other Mesozoic OAEs are poorly constrained. Here we present new estimates of the global anoxic and euxinic sea�oor area before and during the T-OAE based on rhenium and molybdenum enrichments in organic-rich mudrocks of the Fernie Formation (British Columbia, Canada). Trace metal concentrations and ratios, together with high organic carbon contents, indicate that this previously unstudied locality was minimally restricted from global ocean circulation, experienced deep-water nutrient upwelling, and had O2-decient bottom waters. Pronounced rhenium and molybdenum enrichments in mudrocks deposited from locally anoxic and euxinic waters, respectively, point to large global oceanic reservoirs of these metals. Mass balance models suggest that the T-OAE likely comprised a modest expansion of up to ~7% anoxic sea�oor dominated by euxinia. Hence, anoxic sea�oor was likely con�ned to epicontinental seaways, semi-restricted basins, and continental margin oxygen minimum zones during the T-OAE.

basins highly restricted from global ocean circulation have called these interpretations into question 8, 19−21 .Importantly, Mo isotope data do not reliably constrain the extent of ferruginous sea oor because the magnitude of isotope fractionation during Mo removal to sediments under Fe 2+ -rich bottom waters overlaps with fractionations observed for Mo burial in weakly euxinic to mildly oxygenated settings 22 .
Thallium isotope compositions (ε 205 Tl) from ORM have also been applied to reconstruct the global ocean redox landscape during the T-OAE.Preferential burial of isotopically heavy Tl adsorbed to Mn oxides deposited in well-oxygenated sea oor sediments shifts seawater ε 205 Tl towards lighter values, whereas limited areas of oxic sea oor will shift seawater to heavier values.In the early Toarcian, two distinctive shifts towards heavier ε 205 Tl are captured in ORM from western Canada, one ~500 kyr before a negative carbon isotope excursion (N-CIE) and another at the onset of the N-CIE, which are thought to indicate two expansions of ocean anoxia 23 .The highest ε 205 Tl values at the onset of the N-CIE indicate that burial of Mn oxides decreased by at least 50% during the T-OAE, suggesting an equivalent increase of weakly-oxygenated, ferruginous, and/or euxinic bottom waters 23 .However, the Tl isotope proxy does not deconvolve the relative sea oor areas covered by these three O 2 -de cient redox settings.
An alternative approach to quantify the overall extent of oceanic anoxia-including ferruginous sea oorduring the T-OAE is required.Here, we apply a recently developed elemental mass balance model 24 that uses rhenium and Mo enrichments from Pliensbachian to Toarcian ORM (Gordondale Member, Fernie Formation, British Columbia, Canada; Figure 1) to quantitatively estimate total anoxic sea oor area (euxinic plus ferruginous) and total euxinic sea oor area, respectively, before and during the T-OAE.Both Re and Mo are ideal trace metals to quantify the global redox conditions in the oceans due to their conservative behaviour in oxygenated seawater, long ocean residence time (130-440 kyr today) 25 , and low detrital background in organic-rich marine sediments 18,24 .High Re burial rates, and thus Re enrichments, in marine sediments occur in both ferruginous and euxinic environments via complexation of Re with organic matter and sul de minerals 26 , but negligible Re enrichment occurs in oxygenated sediments.Molybdenum preferentially forms thiomolybdate complexes in the presence of dissolved H 2 S and the burial e ciency of sulfurized Mo species in euxinic sediments is signi cantly elevated compared to Mo burial in non-euxinic settings.
These distinctive redox characteristics mean that a predominantly well-oxygenated global ocean will have large dissolved reservoirs of Re and Mo sourced from rivers, and thus pronounced enrichments will occur in ORM that cover small areas of the open ocean within oxygen minimum zones on continental margins.By contrast, an expansion of anoxic and euxinic marine sediment sinks will draw down the dissolved oceanic Re and Mo reservoirs, respectively, leading to muted enrichments in ORM deposited in unrestricted marine settings 18,24 .Using these principles, Re and Mo oceanic mass balance models can be used to infer the extent of sea oor anoxia and euxinia, respectively, using their enrichments in locally anoxic or euxinic ORM deposited in unrestricted marine settings.The extent of ferruginous sea oor can be calculated as the difference between the total anoxic and euxinic sea oor areas.

Local paleoenvironmental setting of the T-OAE in British Columbia
The T-OAE is expressed globally by synchronous deposits of ORM recording a N-CIE in organic and carbonate carbon, embedded within a broader positive CIE [27][28][29][30][31][32][33] .The T-OAE was identi ed in the Red Deer Member (Fernie Formation) of Alberta, Canada in cores (1-35-62-5W6 and 6-32-75-20W5) and outcrop (Bighorn Creek East Tributary) by a N-CIE with a magnitude of -3‰ to -4‰ 27,34 .We report new elemental and organic carbon isotope data (δ 13 C org ) from a drill core (c-B6-A/94-B-8) in British Columbia, Canada, that hosts equivalent Fernie Formation strata (Gordondale Member).This core contains the N-CIE across a vertical interval of 7.1 m and has a magnitude of -2.0 to -2.4‰ (Figure 2).Using this δ 13 C org pro le, the Gordondale Member can be subdivided into Pre N-CIE (>1582.10m), N-CIE (1582.10-1575.00m) and Post N-CIE (< 1575.00 m) intervals.A second N-CIE is observed below 1587.00 m but may represent an older Sinemurian or Pliensbachian event 34,35 .Direct age constraints are not available within the study core, however, detailed litho-and chemostratigraphic correlations with Early Jurassic sections in Alberta containing ammonite biostratigraphy, Re-Os (ORM) and U-Pb (bentonite) ages constrain the age of the Toarcian N-CIE in the core to between ~185 and 182 Ma (see SI).
The Gordondale Member hosts elevated Re auth (207 ± 91 ng/g, 1 s.d.) and U auth (13 ± 8 µg/g, 1 s.d.), like many Phanerozoic ORM deposited from anoxic bottom waters 24,43 .By contrast, V auth (764 ± 568 µg/g, 1 s.d.), Mo auth (96 ± 88 µg/g, 1 s.d.), Re/Mo auth (4.Samples that were likely deposited under suboxic conditions (Re/Mo auth > 10) were not included in the mean calculations.The low Mo auth in the Upper Pre N-CIE and Lower N-CIE is probably not due to an expansion of global euxinia drawing down the oceanic Mo reservoir 18 because Re auth (and U auth ) should show a similar drawdown, which is not observed.Instead, the decline in Mo auth and increased U/Mo auth and Re/Mo auth in the middle portion of the core are interpreted as a transition from euxinic to ferruginous anoxia in the local depositional environment.
Covariations of Mo versus U and cadmium versus Mo can be used to determine paleohydrographic conditions during deposition of the Gordondale Member 47,48 (see discussion in SI).The Mo-U covariation trend for the Gordondale ORM suggests vigorous water-mass exchange with the open ocean 47 .The Cd-Mo covariation corroborates this interpretation, and the elevated Cd content further suggests an environment where upwelling of deep-water nutrients enhanced primary productivity 48 .Based on the local hydrographic regime and its deposition from ferruginous or euxinic bottom waters, the Gordondale Member core is ideal for estimating global ocean redox conditions from redox-sensitive metal concentrations.

Mass Balance Modeling of Global Sea oor Total Anoxia and Euxinia
First-order approximations of global anoxic and euxinic sea oor area can be inferred from Re auth and Mo auth enrichments in ORM deposited in areas well-connected to global ocean circulation 18,24 .Modern seawater Re and Mo concentrations are regulated primarily by rivers with minor sea oor hydrothermal inputs 25 , and burial into sediments deposited from oxic, suboxic, and anoxic (Re) or euxinic (Mo) bottom waters 18,24 .Rhenium is removed most e ciently to the anoxic sink as indicated by an average burial rate of 1.3 ng/cm 2 yr, which is one to three orders of magnitude greater than suboxic (4.2 × 10 −1 ng/cm 2 yr) and oxic (1.6 × 10 −3 ng/cm 2 yr) settings 24 .Burial rates of Re into sediments beneath ferruginous and euxinic bottom waters are not signi cantly different because Re removal to organic-rich sediments depends on O 2 de ciency rather than H 2 S availability 24,40 .In contrast, Mo removal to these sediments hinges on the presence of free H 2 S in bottom waters 42 such that there is a large offset between average Mo burial rates in oxic (2.75 × 10 −3 µg/cm 2 yr) and suboxic (0.27 µg/cm 2 yr) versus euxinic (1.53 µg/cm 2 yr) sediments 18 .The high Re and Mo burial rates in anoxic and euxinic settings, respectively, means that a relatively minor expansion of anoxic or euxinic sea oor will result in substantial drawdown of these metals from seawater until a new steady state is reached.A smaller oceanic metal reservoir should lead to lower enrichments in marine ORM deposited from locally ferruginous or euxinic waters.
Hence, Re and Mo enrichments in ORM, coupled with a recently developed mass balance model 24 (Equations S2-S5) can be used to track changes in the extent of global ocean anoxia and euxinia associated with the T-OAE.
Application of the mass balance model to data from the Gordondale Member before and during the T-OAE requires samples selected from locally anoxic (Re) or euxinic (Mo) ORM 18,24 .Thus, the euxinic sea oor area from the Mo mass balance is not calculated for the locally non-euxinic Upper Pre N-CIE and Lower N-CIE intervals, but the anoxic sea oor area can be deduced from all four de ned Gordondale Member intervals.To produce a representative model of the change in global anoxic and euxinic sea oor area before and during the T-OAE, local spatiotemporal parameters were applied to these stratigraphic intervals.We assess the impact on mass-balance model solutions by local bulk sediment mass accumulation rate (Equation S6), thermal maturity (Equation S7), and Early Jurassic Re and Mo input uxes from rivers and hydrothermal sources.We present an environmentally realistic scenario, with further sensitivity analysis described in the SI.
The modern Re and Mo riverine uxes to the oceans are 4.29 × 10 5 mol/yr and 3.00 × 10 8 mol/yr, respectively 24,25 , which is the assumed baseline (pre N-CIE) ux given broadly similar atmospheric O 2 levels at that time compared to modern 49 .Riverine uxes scale with the rate of continental weathering, which is estimated to have increased by 215-530% over a 100-200 kyr period at the onset of the T-OAE based on Os and Ca isotope data 10,11 .The Os isotope data is from the Red Deer Member 10 , which is closely related to the Gordondale Member in the c-B6-A/94-B-8 core, however, a sill between the units may have created minor basin restriction during Red Deer Member deposition 50 .The c-B6-A/94-B-8 core contains consistently elevated authigenic Re (208 ± 91 ng/g, 1 s.d.) and total organic carbon (TOC) content (6.4 ± 2.2%, 1 s.d.), while the East Tributary section hosting the Red Deer Member contains variably low Re concentrations (52 ± 49 ng/g, 1 s.d.) 10 and moderate TOC content (3.9 ± 1.0%, 1 s.d.) 27 .
The lower Re contents at East Tributary is not a result of more oxygenated conditions because sedimentary Fe speciation data indicates deposition from locally euxinic bottom waters 51 .Hence, the minor hydrographic restriction at the Red Deer Member depositional locality could have caused local seawater 187 Os/ 188 Os to be higher than global seawater such that the weathering rate evaluation (215-530% increase) from the East Tributary section 10 may be a mild overestimation.Hence, we apply a conservative threefold increase of Re and Mo riverine ux at the onset of the N-CIE and maintain this ux through both Lower and Upper N-CIE intervals.
Hydrothermal Re and Mo uxes to modern seawater are poorly constrained but are likely minor compared to riverine ux 24,25 .Sensitivity analyses of hydrothermal uxes demonstrate that its subordinate contribution compared to river ux obviate its impact on the Re and Mo mass balance (see SI), thus the hydrothermal ux was excluded from the mass-balance model.

Maximum Extent of Anoxia at the Onset of the T-OAE
The Re model yields the proportion of total sea oor area covered by anoxic sediments (A anoxic ).The results fall within a narrow range for the Lower Pre N-CIE (0.14-2.5%),Upper Pre N-CIE (1.1-8.2%) and Upper N-CIE (2.9-6.4%)intervals (Figure 3A,B).The Lower N-CIE interval has the greatest uncertainty in A anoxic (3.9-100%) due to the asymptotic nature of the model when A anoxic is less than 1% or greater than 10% total sea oor area.Variation in A anoxic is rooted in the Re auth variance for each interval, which likely re ects, at least in part, changes in local depositional conditions such as uctuating redox conditions, host phase availability/composition or sedimentation rates 52 , rather than global redox changes.It is important to note that lower Re concentrations, caused by local depositional factors, do not actually convey meaningful information about the global extent of ocean anoxia.Hence, mean Re concentrations are a more robust global redox indicator and were used to calculate mean anoxic sea oor areas of 0.84%, 2.6%, 6.9% and 4.1% of the global sea oor area for the respective stratigraphic intervals.These estimates may re ect maximum constraints for the extent of sea oor anoxia because Re concentrations higher than the means suggest lower extents of sea oor anoxia.
The areas of euxinic sea oor from the Mo mass balance model (A euxinic ) also fall within a narrow range for the Lower Pre N-CIE (0.15-1.4%) and Upper N-CIE (3.9-6.2%)intervals and are independently stratigraphically consistent with A anoxic (Figure 3C,D).Mean A euxinic estimates are 0.47% and 4.8% for the Lower Pre N-CIE and Upper N-CIE intervals, respectively.As a subclass of anoxia, euxinia should cover a sea oor area equal to or less than total sea oor anoxia.The range of A euxinic falls within the range of A anoxic for both Lower Pre N-CIE and Upper N-CIE intervals, and the mean A euxinic for both intervals is not appreciably different considering model uncertainties (p-values > 0.16 for paired t-tests).
The Re mass balance model yields a maximum area of sea oor anoxia at the onset of the N-CIE and a contraction of anoxic sea oor area towards the conclusion of the N-CIE.An areal decrease of globally anoxic bottom waters through the T-OAE is consistent with other global redox reconstructions from Europe and Canada 16,51 .The Pre N-CIE interval exhibits global ocean redox conditions similar to modern, however, a minor expansion of sea oor anoxia directly preceding the N-CIE suggests that the T-OAE began prior to the classically recognized δ 13 C expression of the event.A similar observation was noted in the Tl isotope record from another Canadian T-OAE section 51 .This early expansion was not documented in global redox reconstructions from Europe because pre-N-CIE bottom water conditions recorded in those sections are thought to have been generally oxic 15,16 .
Combining the ndings from the Re and Mo models illuminates the redox structure of the global ocean before and during the T-OAE.The offset between mean A anoxic and A euxinic in the Lower Pre N-CIE and Upper N-CIE intervals are not statistically different, suggesting euxinic rather than ferruginous conditions covered most of the anoxic sea oor, as observed in modern anoxic environments.
The increase in sea oor area covered by euxinic conditions likely played a role in the extinctions that occurred during the T-OAE.Several studies have invoked anoxia, and speci cally sul dic anoxia, as a likely kill mechanism for marine fauna during other mass extinctions [53][54][55] .The modern continental shelf and slope where biota is most heavily concentrated account for 3.6% and 5.6% of the global ocean area, respectively, totalling 9.2% 56 .If the area of Toarcian continental shelf and slope were not substantially different from the present, then our model suggests that the maximum expansion of anoxia (primarily as euxinia) in the early portion of the T-OAE did not extend into the deep ocean but remained within the continental margins (e.g., Panthalassa ocean margins) 27,30−33 or epicontinental seas (e.g., Tethys sea sub-basins) [15][16][17][19][20][21]28,29 . The Re mass-balance model results suggest that the open deep oceans away from continental margins likely remained predominantly oxygenated during the T-OAE, although potentially below modern levels 57 , contrasting with past statements suggesting "widespread" anoxia 1,15 . Our resuts align with estimates from previous Mo isotope studies which suggested euxinia covered < 10% of the global sea oor 16,17 .Our novel approach of using Re and Mo mass-balance models to independently estimate the total anoxic sea oor and euxinic sea oor areas show that even modest expansions of anoxia expressed as euxinia can be associated with catastrophic marine die-offs, as reported for the Toarcian 2 .
Our approach towards inferring global ocean redox conditions may be applicable to other intervals of the Phanerozoic characterized by severe mass extinctions, or in forecasting changes to the modern world.The modern Earth is likely experiencing dramatic surface changes such as an enhanced greenhouse atmosphere spurred by industrial, rather than volcanic, activity.The resulting environmental feedbacks associated with the accumulation of anthropogenic greenhouse gases is leading to species loss akin to those of past climate events 58 .Application of the coupled Re-Mo paleoredox proxy may improve understanding of the magnitude of ocean redox changes during ancient expansions of oceanic anoxia and euxinia and their effects on biodiversity, and thus may enable prediction of the results of human impacts on the biosphere.The coupled Re-Mo paleoredox proxy may also help track longer-term changes in the distribution of euxinic versus ferruginous sea oor throughout the Phanerozoic Eon.

Methods
Trace Metals.Sample preparation and analysis for trace metal content was performed at the Metal Isotope Geochemistry Laboratory, University of Waterloo.Samples without secondary features (e.g., fossils, veins, macroscopic pyrite nodules) were chosen for analysis.Samples were crushed without metal contact and powdered in a Retsch ball mill with agate grinding jars.Approximately 100 mg of powder was ashed overnight at 550°C to oxidize organic matter.Ashed powders were digested at 110°C in 2.5 ml concentrated HNO 3 and 0.5 ml concentrated HF for 48 h, followed by digestion in 4 ml aqua regia for 48 h and nally in 2 ml concentrated HCl for 24 h.Digested solutions were diluted 400-fold for Re and Cd, and 6000-fold for other elements by 2% HNO 3 and trace HF was added to ensure sample stability.Elemental concentrations were measured on an Agilent 8800 triple-quadrupole inductively coupled plasma mass spectrometer calibrated against standard solutions containing metal concentrations designed to be similar to the matrix of ORM.Internal standards Sc, Ge, In and Bi were used to correct for instrument drift.Instrument accuracy was veri ed by analyzing United States Geological Survey ORM standards SBC-1 59 and SGR-1b 60 multiple times during each analytical session to ensure accuracy.Concentration reproducibility was typically better than 5%.Organic Carbon Isotopes.Organic C analysis was performed at the Environmental Isotope Laboratory, University of Waterloo.Sample powders were subjected to two rounds of 10% HCl acidi cation at 50°C to leach carbonate, followed by rinsing with NanoPure water to remove excess acid.Approximately 1-10 mg of leached powder was placed in a foil cup for analysis on a Costech Instruments 4010 Elemental Analyzer coupled to a Thermo-Finnigan Delta Plus XL continuous-ow isotope ratio mass spectrometer.Carbon isotope ratios are reported against international and in-house standard reference materials calibrated to PeeDee Belemnite.Analytical precision was ± 0.2‰.

Declarations
Figure 1 Global Toarcian paleogeography.Negative carbon isotope excursion locations 27 used to identify the Toarcian Oceanic Anoxic Event are shown.The core used in this study was deposited along the western margin of Laurasia (proto-North America), and was connected to the Panthalassa ocean.