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Biological pump Sensitivity and climate change: InterroGatiNg past environmentAL perturbations

Periodic Reporting for period 2 - BioSIGNAL (Biological pump Sensitivity and climate change: InterroGatiNg past environmentAL perturbations)

Reporting period: 2021-07-01 to 2022-06-30

Complex forms of animal Life, including the first representatives of most groups that we know today, appeared in the oceans around 550 million years ago. Paleontological data compilations show that marine Life subsequently diversified to eventually reach the highly diverse ecosystems that we know today. Yet, the evolution of biodiversity throughout geological times is complex, alternating rises and plateaus and sudden falls during the so-called mass extinctions. The drivers of these temporal trends have been the focus of many studies over many decades, but they remain largely unconstrained so far. The BioSIGNAL project aims at improving our understanding of the co-evolution of climate and the marine biosphere. The goal is to shed new light on and provide reading keys to understand the evolution of biodiversity through time.

Developing a mechanistic understanding of the response of biodiversity to environmental change is crucial for society. Marine species are an essential resource for human communities. They also constitute a key component of the Earth System and contribute to the regulation of climate at the global scale. But the response of the marine communities to ongoing climate change is uncertain. Studying the past is a key opportunity to gain knowledge that will ultimately permit to improve the next generation of models used to predict the consequences of climate change, hence providing more accurate predictions, and permitting to hopefully adopt the right measures.

The project focuses on a previously overlooked potential driver of marine biodiversity: the ocean dissolved oxygen concentration. Indeed, dissolved oxygen is necessary to complex animals. Studies of the present-day ocean confirm that biodiversity suddenly drops in poorly oxygenated regions. It is thus expected that the evolution of marine biodiversity at the geological timescale may have been driven by changes in ocean oxygenation, too. The goal of the BioSIGNAL project is to determine and quantify the relationship between ocean oxygenation and marine biodiversity over the last 550 million years.
In terms of numbers first, 6 rank-A papers have been published, 1 additional paper has been accepted, 5 others are under review and 4 are in preparation. These papers have been published in high-impact journals, including Nature Geoscience, Nature Communications, Science Advances and PNAS. Two manuscripts are in revisions for Nature (as 1st and 3rd author).

We notably demonstrated that the high extinction rates documented over the ca. 100 million years following the appearance of the main animal groups could be explained by the poor ocean oxygen concentration (Stockey, Pohl et al., PNAS 2021), which could be due, at least in part, to the very specific configuration of the continents at that time (Pohl et al., revised for Nature). We also focused on specific periods of time and constrained the position of the continents and climate at the period when Life diversified in the oceans (around 520 million years ago; Hearing, Pohl et al., Nature Communications 2021) and were able to develop a model reproducing with success the spatial patterns of phytoplankton diversity at that time (Zacaï, Monnet, Pohl et al., Science Advances 2021). We also studied with a level of detail that had never been reached so far, the changes in ocean oxygen concentrations during the first of the major mass extinctions of the last 550 million years, during the latest Ordovician (ca. 444 million years ago). We demonstrated that ocean deoxygenation expanded in the deep ocean in response to cooling due to changes in the ocean circulation, but also showed that this mechanism does not permit to explain the concomitant mass extinction and that other kills mechanisms must be found (including cooling) (Pohl et al., Nature Geoscience 2021).
The outputs of the BioSIGNAL project, after 2.5 years, go well beyond the state of the art. The modeling workflows that we developed, permitting to quantify the feedbacks between marine Life and the environment (Stockey, Pohl et al., PNAS 2021; Zacaï, Monnet, Pohl et al., Science Advances 2021) constitute a major step forward toward the mechanistic understanding of the co-evolution of Life and the physical environment through geological time. But of course, the robust understanding of such co-evolution largely relies on our capacity to reconstruct environmental changes in the deep time. To that purpose, we developed a dedicated workflow permitting to assimilate sparse geological data in a spatially-resolved, 3-dimensional numerical framework offering a coupled representation of climate and the biosphere. This workflow permitted to shed new light on the ocean oxygenation changes during the latest Ordovician mass extinction (Pohl et al., Nature Geoscience 2021) and on the geological record of ocean oxygenation over the last 550 million years (Pohl et al., revised for Nature). We are firmly convinced that such method, by permitting to reconcile data bearing conflicting signals into a physically consistent numerical framework, will pave the way for future work and should become a standard procedure.

We are now improving our understanding of the co-evolution of marine Life and the physical environment during key geological periods that witnessed significant changes in the trajectory of global biodiversity (Devonian, early Triassic). Our main objective consists in combining our model of marine biodiversity (Stockey, Pohl et al., PNAS 2021; Zacaï, Monnet, Pohl et al., Science Advances 2021) with our updated environmental reconstructions of the last 550 million years (Pohl et al., revised for Nature) in order to provide new insights into the trajectory that led biodiversity to its present-day state.
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