Biodiversity and Global Change: From Creator to Victim to a new Revolution Tim Lenton, University of Exeter, UK [Note to the reader: This is a preliminary work-in-progress, put together in haste, with incomplete and uneven referencing. I am unsure whether the scope is too broad or the level too elementary and whether large sections are superfluous. The last section on the projected consequences of climate change for biodiversity is at a very early stage of writing. Hence I welcome any frank feedback.] Introduction The premise of this paper is that we owe our very existence to the activities of past and present life forms, which have created a world that we could inhabit.1 This is true not just in the evolutionary sense that we are descended from earlier life forms, but in the Earth system sense that the atmosphere would be unbreathable and the climate intolerable were it not for the accumulated actions of other members of the biosphere, past and present.1 This fundamental role of biodiversity in maintaining our life support system is strangely under- recognised by utilitarian arguments for preserving nature. Hence the first section briefly reviews which life forms and which functions they perform have been particularly important in creating a world we could inhabit in the first place. We are part of biodiversity and have been born out of this world, only to be transforming it now in ways that are bad for us and bad for much of the rest of life. As the first section reviews, this is not the first time that life has radically transformed the planet with damaging consequences.1 However, it is the first time that a single animal species has wielded such world changing power. Past revolutionary transformations of the biosphere took life to the brink of total extinction in events such as ‘snowball Earth’. Our very existence dictates that life survived such past scrapes with disaster1 – but the flipside is that there is no guarantee that the biosphere will necessarily survive what is unfolding now. After past close shaves, it typically took millions of years for the slow workings of Earth system dynamics and the blind watchmaker of natural selection to restore a well-functioning, self-regulating biosphere.1 We don’t have the luxury of waiting that long. We are meant to be Homo sapiens – wise man (sic) – instead we are practicing an act of cosmic stupidity: In extinguishing biodiversity we are eroding our own life-support system. The irony of this would surely not be lost on any watching deity. The second section reviews how we came to be planet changers and how climate change interacting with other global changes is predicted to impact biodiversity. This turns to some critical reflection on just how big a threat the unfolding extinction could be to the core functioning of the biosphere, or conversely whether the organisms that really run the planet can acclimate and adapt to the global changes we are causing. Finally, rather than just chart the biodiversity dimensions of our demise, the aim here is to leave the reader with a chink of light to cling to – to consider how if we really are wise, and we learned to properly value biodiversity, could we become good citizens of a flourishing future biosphere? If so, what might that revolution look like? How life created a world we could inhabit The aim of this section is to sketch in broad terms how the past evolution of life has created a world that we could inhabit in the first place.1 Along the way we identify some crucial roles of different types of life – from prokaryotes to fellow multicellular eukaryotes – in creating and maintaining a habitable biosphere for advanced multicellular life forms including ourselves. The perspective here is that life and the Earth have co-evolved in the sense that the evolution of life has shaped the planet, changes in the planetary environment have shaped life, and together this can be viewed as one process.2 When we look at this co-evolution over Earth history, a relatively few revolutionary changes leap out, in which the Earth system was radically transformed.1 Each of these revolutionary changes depended on the previous one, and without them we would not be here – and nor would much of the biodiversity that is currently described and projected to be under threat (i.e. complex eukaryote life forms). To help orientate the reader, Figure 1 provides a timeline of major events in Earth history. Origins of the biosphere - 1 - The most fundamental change in the history of the Earth system started with the origin of life, which appeared on Earth remarkably soon after our planet became continuously habitable. The formation of the solar system is dated from the oldest meteoritic material at 4.567 billion years ago. The Earth and the other planets are younger than this, because they had to form from the gravitational collisions and accumulation of material spinning around the early Sun – in a process called accretion. During the accretion of the Earth there were some truly massive collisions, one (or several) of which formed the Moon 4.470 billion years ago. Whilst the Earth was still forming, the gas giants Jupiter and Saturn had finished accreting. Their gravitational pull disrupted the band of asteroids between Mars and Jupiter, sending some of them off on elliptical orbits that crossed the inner Solar System. Crucially, this brought water and other volatile substances, including nitrogen and carbon dioxide, to the early Earth. Remarkably, some tiny bits of the Earth’s crust from this time are still present at the surface today, in the form of grains of the mineral zircon that can be precisely dated. The oldest is 4.374 billion years old and was originally part of a granite rock, indicating that the continental crust had started to form in the first 100 million years of the planet’s history. Even more remarkably the isotopic composition of oxygen in the zircon suggests that oceans of liquid water were present on the Earth at that early time. However, the onslaught from outer space was not over. The Earth and all the inner Solar System suffered a ‘Late Heavy Bombardment’ by asteroids between about 4.1 and 3.9 billion years ago. Some of these impacts were large enough to have evaporated the early oceans and thus temporarily rendered the planet uninhabitable. Thus the Earth did not become ‘continuously habitable’ until the end of this bombardment around 3.85 billion years ago. Remarkably the first tentative evidence for life on Earth comes within ~50 million years of the end of the Late Heavy Bombardment, 3.8 billion years ago. As soon as there are sedimentary rocks that could record the presence of life they suggest it is there. Some of the first evidence takes the form of small particles of graphite – organic carbon – with an isotopic composition (d13C) consistent with carbon fixation by some form of chemosynthesis or photosynthesis.3,4 Putative microbial structures have also been described from the same rock sequence5. By 3.5 billion years ago the first putative microscopic fossils of life appear,6,7 although not everyone is convinced the fossil structures were made by biology.8,9 There are also more convincingly biogenic sedimentary structures formed by microbial mats.10 By 3.26 billion years ago there are microfossils of cells caught in the act of division.11 The earliest biosphere was made up exclusively of prokaryotes – bacteria and archaea – two kingdoms of life which divided very early. Metabolically the earliest life forms may have consumed compounds in their environment that could be reacted to release chemical energy, but a shortage of chemical energy on a global scale would have severely restricted the productivity of such a biosphere. One possibility is that early archaea consumed hydrogen from the atmosphere and carbon dioxide to make methane, but such a methanogen- based biosphere would have been restricted to around a thousandth of the productivity of the modern marine biosphere.12,13 A more productive global biosphere would have arisen when early life began to harness the most abundant energy source on the planet – sunlight. Photosynthesis fixing carbon dioxide from the atmosphere appears to have evolved very early in the history of life. Whilst the ~3.8 billion year old graphite has a carbon isotopic composition consistent with photosynthesis, some scientists argue that there are non-biological ways to make graphite with this isotopic signature. However, 3.5 billion years ago the earliest carbonate sediments have an isotopic signature that suggests significant organic carbon burial globally, which must have been supported by photosynthesis. The first photosynthesis was not the kind we are familiar with, which splits water and spits out oxygen as a waste product. Instead, early photosynthesis was ‘anoxygenic’ – meaning it didn’t produce oxygen. It could have used a range of compounds, in place of water, as a source of electrons with which to fix carbon from carbon dioxide and reduce it to sugars, including hydrogen (H2) or hydrogen sulphide (H2S) in the atmosphere, or ferrous iron (Fe2+) dissolved in the ancient oceans. The early biosphere fuelled by anoxygenic photosynthesis would have been limited by the supplies of these electron donors, all of which are a lot less abundant than water. In fact, shortage of materials would have posed a more general problem for life within the early Earth system: The fluxes of materials coming into the surface Earth system from volcanic and metamorphic processes today are many orders of magnitude less than the fluxes due to life at the surface of the Earth today, indicating that today’s biosphere is a phenomenal recycling system (Figure 2).