Temperature-driven nutrient recycling and euxinia as a marine mass extinction mechanism Dominik Hülse ( [email protected] ) University of California, Riverside https://orcid.org/0000-0001-5386-6746 Kimberly Lau The Pennsylvania State University Sebastiaan van de Velde University of California, Riverside Sandra Arndt University of Bristol Katja Meyer Willamette Andy Ridgwell University of California, Riverside https://orcid.org/0000-0003-2333-0128 Article Keywords: nutrient recycling, euxinia, temperature, microbial metabolism, ocean redox state, carbon cycling, end-Permian mass extinction Posted Date: November 30th, 2020 DOI: https://doi.org/10.21203/rs.3.rs-80350/v1 License: This work is licensed under a Creative Commons Attribution 4.0 International License. Read Full License 1 Temperature-driven nutrient recycling and euxinia as a 2 marine mass extinction mechanism 1 2,3 1 3 Dominik Hulse,¨ Kimberly V. Lau, Sebastiaan J. van de Velde, 4 5 1 4 Sandra Arndt, Katja Meyer, Andy Ridgwell 1 5 Department of Earth and Planetary Sciences, University of California, Riverside, CA, USA 2 6 Geosciences and Earth and Environmental Systems Institute, The Pennsylvania State University, 7 University Park, PA ,USA 3 8 Geology and Geophysics, University of Wyoming, WY, USA 4 9 Bgeosys, Geoscience, Environment & Society, Universite´ Libre de Bruxelles, Brussels, Belgium 5 10 Earth and Environmental Sciences, Willamette University, Salem, OR, USA 11 Extreme warming at the end-Permian induced profound changes in marine biogeochemical 12 cycling and animal habitability, leading to the largest extinction in Earth’s history. However, 13 a causal mechanism for the extinction that explains the different proxy evidence has yet to 14 be found. By combining recent modeling developments with global and local redox obser- 15 vations, we show that a temperature-driven increase in microbial respiration can reconcile 16 reconstructions of the spatial distribution of euxinia and seafloor anoxia spanning the Per- 17 mian/Triassic transition. We illustrate how enhanced metabolic rates would have strength- 18 ened upper ocean nutrient recycling, and thus shoaled and intensified the oxygen minimum 19 zones eventually causing euxinic waters to expand onto continental shelves, poisoning ben- 20 thic habitats. Finally, we find that the temperature effect on microbial activity can account 1 21 for some of the decline in carbon isotopes at the end-Permian with the implication that car- 22 bon release as inferred from those changes is likely overestimated. Our findings present 23 a novel view of the sensitive interconnections between temperature, microbial metabolism, 24 ocean redox state and carbon cycling during the end-Permian mass extinction with potential 25 far-ranging implications for the interpretation of carbon cycle perturbations during Earth 26 history. 27 Climate warming driven by volcanic greenhouse gas release is widely regarded as the under- 28 lying driver for the largest metazoan extinction event in Earth’s history at the end of the Permian 1, 2 29 Period when ∼90% of marine species were eliminated . Although the extinction event itself has 30 been intensely studied and is relatively well characterized, the specific physical and/or biogeo- 3 31 chemical environmental changes that drove biodiversity loss in the ocean are uncertain . Proxy ◦ 4–6 32 evidence reveals a 7-10 C increase in sea surface temperature occurring in as little as ∼39 kyr 7 33 (Fig. 1a+d), the development of (photic-zone) euxinia (waters containing sulphide ), an expan- 8, 9 34 sion in the extent of seafloor anoxia , and a decrease in the carbon isotopic signature recorded in 10 13 11 35 carbonates (δ Ccarb, Fig. 1e), all approximately reaching their nadir at the extinction horizon 36 (EH, ∼251.94 Ma). 37 Proposed explanations linking these observations with the extinction all require reduced oxy- 38 genation of the ocean, but fundamentally diverge at this point. In particular, previous 3D Earth 39 system model (ESM) studies have required either a sustained collapse of global ocean circulation 12 40 in conjunction with a much weaker biological pump , or a well ventilated end-Permian ocean 2 41 in conjunction with a much stronger biological pump driven by enhanced nutrient (phosphate) 13, 14 15 42 availability . However, other modelling work has demonstrated that increasing the ocean 43 phosphate inventory sufficiently to create widespread subsurface euxinia, not only requires an ex- 16 44 cessive increase in phosphate availability, but also results in near-global anoxia in the deep sea 9,17 45 which is in conflict with paleoredox estimates from uranium isotope records (Fig. 1b+c). Other 46 explanations focus on reducing oxygen availability throughout the ocean as a whole, either through 13 47 the oxidation of methane released from hydrates or of a massive reservoir of dissolved organic 18 19, 20 48 matter , or via warming driven by the CO2 release associated with volcanism . These car- 13 49 bon release mechanisms can also drive a pronounced decline in δ Ccarb. However, a gradient in 13 21 50 δ Ccarb from surface to subsurface records suggests a vertical partitioning in ocean geochem- 51 istry occurred and that there is much more to the event than carbon release and climate warming. 52 Here we reconcile the varying proxy observations and provide new insights into the controls on 53 subsurface euxinia and hence marine extinction mechanisms, by recognising the important role of 54 temperature in stimulating microbial respiration and thus dictating the redox profile in the water 55 column. 56 Oxygen availability in the water column generally decreases from well-mixed surface waters 57 (few tens of meters), to the oxygen minimum zone (OMZ, typically at a depth of a few hundreds 58 of meters). Along with vertical ocean mixing, this gradient is controlled by the remineralization 59 of particulate organic matter (POM) which consumes oxygen and releases inorganic nutrients (and 22 60 carbon) that can be returned to the surface to fuel new primary productivity . Critical here is the 61 interplay between reactivity and sinking rate of POM, as it controls the shape of the remineraliza- 3 62 tion rate depth profile (i.e. the scale depth of POM remineralization) and, thus, the intensity and 16, 23 63 depth of OMZs . We posit that a further factor, and the key to understanding how the marine 24 64 environment changed across the Permian/Triassic boundary (P/Tr), is ocean temperature . 65 A mechanistic representation of the biological pump 66 To demonstrate the importance of a warming ocean in driving subsurface euxinia and potentially 67 widespread extinction across shallow marine environments, we simulate redox distributions for a 25, 26 68 range of P/Tr conditions using the cGENIE ESM . We modify the widely used ’static’ represen- 27 69 tation of the biological pump (i.e. an invariant POM remineralization depth profile ), to allow us 70 to explicitly account for the impact of ocean warming at the end-Permian on POM remineralization 71 (SI). In addition, to reflect the shallower remineralization profile inferred prior to the rise of pelagic 23 72 calcifiers in the early Mesozoic , we decrease the sinking rate of POM in the model by ∼22% – 28 73 scaled to the smaller mean animal biovolume at the end-Permian ( , SI). Finally, we account for 74 changes in POM remineralization as reactive POM compounds react with sulphide (H2S) and be- 29 75 come less susceptible to bacterial remineralization (SI), in a process known as “sulfurization” . 76 Because the time-scale of warming leading up to the P/Tr boundary is slow relative to the adjust- 77 ment time-scale of large-scale ocean circulation (i.e. warming likely occurred over ∼39 kyr or 6, 11 78 more, starting in the C. meishanensis biostratigraphic zone ), a series of (10 kyr) steady-state 79 simulations is appropriate for simulating the biogeochemical response to warming. In these, we 80 prescribe a range of atmospheric pCO2 (1 – 30 × pre-industrial pCO2, i.e. 280–8400 ppmv) chosen 81 to span the increase in tropical Tethys ocean temperatures reconstructed from proxy records (∼22 ◦ 82 – 35 C, Fig. 1a+d, SI). Simultaneously, we explore the importance of 1 – 2.5× modern ocean 4 83 phosphate inventories to represent the potential net impact of increased weathering and sediment 30–32 84 regeneration rates as the climate warms and ocean anoxia increases, respectively – thus, creat- 85 ing model ensembles of varying climate vs. ocean nutrient state. Atmospheric oxygen is fixed at 86 modern. 87 Constraining model results with global and local redox proxies 88 Uranium isotopes can provide powerful constraints on ocean models via the reconstructed extent 89 of seafloor anoxia (fanox) . To quantitatively compare the ESM results with a compilation of car- 238 90 bonate δ U data over the P/Tr transition (SI), we use a forward box model that encapsulates the 9 91 uncertainties in the U isotope budget (adapted from Lau et al. ). According to our U-model results, 238 92 the δ U data can be best explained by an abrupt increase in fanox that either coincided with the 93 EH, or preceded it by much less than the onset of the warming event (Fig. 1 b+c). An increase 94 of fanox from a modern value of 0.6% to about 30% (i.e. a factor of 50) represents our preferred 95 scenario as other perturbations fail to simulate the rate of change and magnitude of the shift in the 238 96 δ U data (Extended Data Fig. 4). 97 We also ground-truth the ESM results with a new compilation of local redox proxies (Ex- 98 tended Data Fig. 1 and Extended Data Table 2). The data-set consists of geochemical, lithologic, 99 sedimentologic, and biomarker evidence for water-column euxinia and bottom water anoxia and 100 distinguishes three phases of the P/Tr transition (Late Permian background, Start Warming and 101 Main Extinction, Extended Data Table 2).