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The Impacts of Land Plant Evolution on Earth's Climate and Oxygenation State – an Interdisciplinary Review

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The Impacts of Land Plant Evolution on Earth's Climate and Oxygenation State – an Interdisciplinary Review The impacts of land plant evolution on Earth's climate and oxygenation state – An interdisciplinary review Dahl, Tais W.; Arens, Susanne K.M. Published in: Chemical Geology DOI: 10.1016/j.chemgeo.2020.119665 Publication date: 2020 Document version Publisher's PDF, also known as Version of record Document license: CC BY-NC-ND Citation for published version (APA): Dahl, T. W., & Arens, S. K. M. (2020). The impacts of land plant evolution on Earth's climate and oxygenation state – An interdisciplinary review. Chemical Geology, 547, [119665]. https://doi.org/10.1016/j.chemgeo.2020.119665 Download date: 10. Sep. 2020 Chemical Geology 547 (2020) 119665 Contents lists available at ScienceDirect Chemical Geology journal homepage: www.elsevier.com/locate/chemgeo Invited research article The impacts of land plant evolution on Earth's climate and oxygenation state T – An interdisciplinary review ⁎ Tais W. Dahl , Susanne K.M. Arens GLOBE Institute, University of Copenhagen, 1350 Copenhagen K, Denmark ARTICLE INFO ABSTRACT Keywords: The Paleozoic emergence of terrestrial plants has been linked to a stepwise increase in Earth's O2 levels and a Early land plants cooling of Earth's climate by drawdown of atmospheric CO2. Vegetation affects the Earth's2 O and CO2 levels in Terrestrialization multiple ways, including preferential organic carbon preservation by decay-resistant biopolymers (e.g. lignin) Climate and changing the continental weathering regime that governs oceanic nutrient supply and marine biological Oxygenation production. Over shorter time scales (≤1 Myr), land plant evolution is hypothesized to have occasionally en- Soils hanced P weathering and fertilized the oceans, expanding marine anoxia and causing marine extinctions. Earth history Oceanic anoxia would eventually become limited by oceanic O2 uptake as oxygen accumulates in the atmo- sphere and surface oceans when excess organic carbon is buried in marine sediments. Here, we review hy- potheses and evidence for how the evolving terrestrial ecosystems impacted atmospheric and oceanic O2 and CO2 from the Ordovician and into the Carboniferous (485–298.9 Ma). Five major ecological stages in the ter- restrial realm occurred during the prolonged time interval when land was colonized by plants, animals and fungi, marked by the evolution of 1) non-vascular plants, 2) vascular plants with lignified tissue, 3) plants with shallow roots, 4) arborescent and perennial vegetation with deep and complex root systems, and 5) seed plants. The prediction that land vegetation profoundly impacted the Earth system is justified, although it is still debated how the individual transitions affected the Earth's2 O and CO2 levels. The geological record preserves multiple lines of indirect evidence for environmental transitions that can help us to reconstruct and quantify global controls on Earth's oxygenation and climate state. 1. Introduction ‘Devonian cooling hypothesis’, posits that early afforestation enhanced atmospheric CO2 removal via enhanced silicate weathering, which led In this review we look at terrestrial plants as a geobiological agent Earth to transit from a hot greenhouse climate into a glaciated icehouse and their possible imprints on Earth's climate and oxygenation state (Berner, 1993). This hypothesis is commonly accepted (e.g., Algeo and during their emergence on the continents. Land plants affect our planet Scheckler, 1998; Morris et al., 2015), although recent studies challenge in a multitude of ways in particular through the hydrological cycle, the temporal correlation between the Late Devonian spread of vascular Earth's surface energy budget, and the global biogeochemical cycles. plants with deep roots (~380–360 million years ago, Ma) and the main Vegetation changes the water cycling, rainfall, runoff, and soil prop- phase of the Late Paleozoic Ice Age (335–260 Ma) (Goddéris et al., erties, harvesting nutrients for biological production that, in turn, 2017; Montañez and Poulsen, 2013). drives carbon sequestration and storage in terrestrial deposits and A more recent hypothesis states that the Late Ordovician climatic marine sediments. At the crux of this is how plants modify the physical cooling also resulted from colonization by non-vascular, rootless plants and chemical weathering processes of the land surface with lasting (Lenton et al., 2012). Both the Ordovician and Devonian transition have impacts on the global element cycles. The modifications by land plants also been linked to rises of atmospheric oxygen (Berner, 2006; Edwards are carried out in networks of interactions with the terrestrial fauna and et al., 2017; Lenton et al., 2016). In addition, the evolution of early fungi that co-evolved with the emergence of plants. lignified plants with shallow roots in the Late Silurian to Early Devo- The mid-Paleozoic colonization of land offers a unique opportunity nian (427.4–393.3 Ma) also changed the terrestrial ecosystems and soil to study how the terrestrial biosphere affected the Earth's climate and properties, as might the emergence of seed plants in drier upland en- oxygenation state in the past. A noteworthy hypothesis, known as the vironments. Each one of these events could have affected atmospheric ⁎ Corresponding author. E-mail address: [email protected] (T.W. Dahl). https://doi.org/10.1016/j.chemgeo.2020.119665 Received 27 December 2019; Received in revised form 2 May 2020; Accepted 9 May 2020 Available online 13 May 2020 0009-2541/ © 2020 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). T.W. Dahl and S.K.M. Arens Chemical Geology 547 (2020) 119665 CO2 and O2 levels on Earth, but the governing processes are poorly Paleozoic (Nelsen et al., 2019). However, algae-fungal symbioses have understood. emerged multiple times in Earth history and the fungal tree of life is still Although the interplay between the evolving terrestrial ecosystems less well constrained than the plant tree of life (Gargas et al., 1995; and atmospheric composition continued long after the mid-Paleozoic Hibbett et al., 2007; Lutzoni et al., 2018). The fossil record of lichens is (Ordovician–Devonian) and plant evolution modulated climate both sparse with putative representatives in the Ediacaran and Early Devo- during the Late Paleozoic Ice Age and during the Cretaceous rise of nian (Taylor et al., 1995; Yuan, 2005). Today, lichens account for 7% of flowering plants (angiosperms) (Boyce and Lee, 2017; Montañez and Earth's net terrestrial productivity (Elbert et al., 2012). The absence of Poulsen, 2013), we focus this review on the environmental impact of lichens and non-vascular plants in the early terrestrial ecosystems the early history of land plants. We highlight five major ecological would likely have resulted in drier, shallower and less stable soil eco- transitions that distinguish the terrestrial ecosystem at different times systems with lower productivity. (Le Hir et al., 2011), including 1) the invasion of rootless plants, 2) the Fossil soils (paleosols) are preserved throughout the geologic record invasion of vascular plants with lignified tissue, 3) the invasion of (Driese and Mora, 2001; Mángano and Buatois, 2016; Retallack, 2003; vascular plants with shallow roots, 4) the invasion of tall, perennial Sheldon and Tabor, 2009). Soils are altered surficial rock or sediment, trees with deep root systems, and 5) the invasion of seed plants in drier composed of mixtures of organic matter, minerals, fluids, and organ- upland environments. isms that develop through chemical weathering and deposition of litter This review aims to provide an all-round perspective on how the (Amundson, 2014). The earliest soils experienced limited hydrolytic early terrestrial biota has transformed Earth's climate and oxygenation alteration and contained little humic material and bio-essential ele- state. In Section 2 we review the history of early land plants and ancient ments (e.g. N, P), which would have posed a serious challenge to plant soils (paleosols). In Section 3, the obstacles and biological innovations colonization. In addition, Precambrian paleosols differ from Silurian during terrestrialization are summarized. In Section 4, we discuss the and younger paleosols by the lack of animal burrows (Driese and Mora, various effects of terrestrial vegetation on Earth's global biogeochem- 2001). ical cycles with specific focus on consequences to atmospheric2 O and CO2 levels. Section 5 deals with hypotheses for long-term climate and 2.2. Colonization by non-vascular, rootless land plants (~515–470 Ma) O2 regulation on Earth and how the evolving flora may have played into this. Section 6 summarizes key lines of evidence for mid-Paleozoic en- Early land plants reproduced solely by spores (cryptogamic). Seed vironmental transitions and discuss links between evolving terrestrial plants (spermatophytes) evolved later, and flowering plants (angios- ecosystems and Earth's climate and oxygenation state. In Section 7, we perms) much later in the Cretaceous (Fig. 1). The origin of land plants conclude with an outlook for future research. (embryophytes) is estimated to have occurred in the middle Cam- brian–Early Ordovician, 515.2–473.5 Ma, based on phylogenomic data 2. History of early land plants and terrestrial ecosystems encompassing the diversity of embryophytes and utilizing a Bayesian relaxed molecular clock analysis (Morris et al., 2018). The timeline for terrestrialization by land plants builds
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