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Ecosystem CO2 Starvation and Terrestrial Silicate Weathering: Mechanisms and Global-Scale Quantification During the Late Miocene

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Ecosystem CO2 Starvation and Terrestrial Silicate Weathering: Mechanisms and Global-Scale Quantification During the Late Miocene Journal of Ecology 2012, 100, 31–41 doi: 10.1111/j.1365-2745.2011.01905.x CENTENARY SYMPOSIUM SPECIAL FEATURE Ecosystem CO2 starvation and terrestrial silicate weathering: mechanisms and global-scale quantification during the late Miocene David J. Beerling1*, Lyla L. Taylor1, Catherine D. C. Bradshaw2, Daniel J. Lunt2, Paul J. Valdes2, Steven A. Banwart3, Mark Pagani4 and Jonathan R. Leake1 1Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK; 2School of Geographical Sciences, University of Bristol, Bristol BS8 1SS, UK; 3Cell-Mineral Research Centre, Kroto Research Institute, Univer- sity of Sheffield, Sheffield S1 7HQ, UK; and 4Department of Geology and Geophysics, Yale University, New Haven, CT 06520, USA Summary 1. The relative constancy of the lower limit on Earth’s atmospheric CO2 concentration ([CO2]a) during major tectonic episodes over the final 24 million years (Ma) of the Cenozoic is surprising because they are expected to draw-down [CO2]a by enhancing chemical weathering and carbonate deposition on the seafloor. That [CO2]a did not drop to extremely low values suggests the existence of feedback mechanisms that slow silicate weathering as [CO2]a declines. One proposed mechanism is a negative feedback mediated through CO2 starvation of land plants in active orogenic regions compromising the efficiency of the primary carboxylating enzyme in C3 plants (Rubisco) and dimin- ishing productivity and terrestrial weathering. 2. The CO2 starvation hypothesis is developed further by identifying four key related mechanisms: decreasing net primary production leading to (i) decreasing below-ground C allocation, reducing the surface area of contact between minerals and roots and mycorrhizal fungi and (ii) reduced demand for soil nutrients decreasing the active exudation of protons and organic acids by fine roots and mycorrhizas; (iii) lower carbon cost-for-nutrient benefits of arbuscular mycorrhizas (AM) favouring AM over ectomycorrhizal root–fungal symbioses, which are less effective at mineral weathering, and (iv) conversion of forest to C3 and C4 grassland arresting Ca leaching from soils. 3. We evaluated the global importance of mechanisms 1 and 2 in silicate weathering under a chan- ging late Miocene [CO2]a and climate using a process-based model describing the effects of plants and mycorrhizal fungi on the biological proton cycle and soil chemistry. The model captures what we believe are the key processes controlling the pH of the mycorrhizosphere and includes numerical routines for calculating weathering rates on basalt and granite using simple yet rigorous equilibrium chemistry and rate laws. 4. Our simulations indicate a reduction in the capacity of the terrestrial biosphere to weather conti- nental silicate rocks by a factor of four in response to successively decreasing [CO2]a values (400, 280, 180 and 100 p.p.m.) and associated late Miocene (11.6–5.3 Ma) cooling. Marked reductions in terrestrial weathering could effectively limit biologically mediated long-term carbon sequestration in marine sediments. 5. These results support the idea of terrestrial vegetation acting as a negative feedback mechanism that counteracts substantial declines in [CO2]a linked to increased production of fresh weatherable minerals in warm, low-latitude, active orogenic regions. Key-words: biological weathering, Miocene, modelling, mycorrhiza, plant–climate interac- tions *Correspondence author. E-mail: d.j.beerling@sheffield.ac.uk Ó 2012 The Authors. Journal of Ecology Ó 2012 British Ecological Society 32 D. J. Beerling et al. Our paper is organized into three parts. First, we provide an Introduction overview of the proposed linkage between silicate weathering Paraphrasing Oscar Wilde, the gifted but controversial by terrestrial ecosystems, climate and [CO2]a during the late Oxford botanist and geneticist C. D. Darlington (1903–1981) Cenozoic (Pagani et al. 2009). Second, we critically review the scathingly described ecology during the 1950s as being the ‘the ecological literature to identify mechanisms by which changing pursuit of the incomprehensible by the incompetent’ (Harman [CO2]a influences terrestrial plants, their symbiotic fungal 2004). Darlington had evidently not yet absorbed the emerging partners and soil carbon cycle processes that contribute to the legacy of Sir Arthur Tansley, the father of British ecology and chemical weathering of Ca- and Mg-rich silicate minerals. Sili- one of the founders of the Journal of Ecology (Godwin 1957). cate mineral weathering is important because on a timescale of Tansley (1935) pioneered an enlightened approach to ecology millions of years, it acts as the long-term sink of [CO2]a (Berner by conceptualizing the ecosystem as a set of interacting compo- 2004). The overall process by which silicate weathering transfers nents, whereby plants, climate, soils and animals function as a Ca2+ ions into the oceans is given by the following simplified system and emphasizing investigation of processes that link expression representative of all calcium silicates (Berner 2004): them. Consequently, over the past five decades, ecosystems CO2½atm þ CaSiO3½continent ! SiO2½continentþocean have become increasingly recognized as playing a central role eqn 1 CaCO in Earth’s environmental history, through their effects on þ 3½ocean the major cycles of elements, the fate of sediments, and Mg ions liberated from Mg silicates exchange with calcium atmospheric and ocean chemistry (Knoll 2003; Berner 2004; in marine basalts (Berner 2004), leading to the deposition of Beerling 2007). CaCO3 rather than MgCO3. The weathering of Ca and Mg 2+ Our contribution to the Centenary celebration of the carbonates releases both Ca and CO2, resulting in no net Journal of Ecology develops this theme by investigating change in [CO2]a on timescales of millions of years, and places the interplay between the terrestrial biosphere, climate and the the emphasis on continental silicate rocks in controlling long- geosphere in the context of Earth’s atmospheric CO2 history term CO2 sequestration in the oceans. over the past 24 million years (Ma) (Pagani et al. 2009; Beer- In the third part of the paper, we report results from global ling & Royer 2011) (Fig. 1). We adopt a process-based simulations analysing how declining [CO2]a and climatic cool- approach to terrestrial ecosystem functioning, and its chemical ing in the late Miocene (11.6–5.3 Ma) alters biological weath- interaction with the regolith (weathering), by investigating its ering of silicate rocks by terrestrial ecosystems (Taylor et al. hypothesized role in regulating Earth’s lower limit of atmo- 2011, 2012). Our approach uses a process-based model describ- spheric concentration ([CO2]a) during major orogenic events ing the effects of plants and mycorrhizal fungi on mineral (Pagani et al. 2009) (Fig. 1). weathering via their influence on the ‘biological proton cycle’ 2500 High elevations for southern Tibetan Plateau ??? ??? 2000 Crustal-scale thrusting and denudation Early Tibetan-Himalayan collision: of the Himalayas and southern Tibet weaker evidence for extensive uplift Lateral growth of Tibetan Rapid crustal 1500 Plateau thickening in southern Tibet (p.p.m.v) 2 Deformation/exhumation Surface uplift of the in the Eastern Cordillera northern Altipano central Andes 1000 Surface uplift of southern Deformation and Pantogonian Andes surface uplift of Atmospheric CO Surface Exhumation western N. America uplift of of New Guinea 500 Southern Alps arc New Zealand Miocene Oligocene Eocene 0 0 5 10 15 20 25 30 35 40 45 50 Age (Ma) Fig. 1. Earth’s atmospheric CO2 and tectonic history over the past 50 Ma. Shaded bands indicate [CO2]a estimates from the alkenone proxy and circles from the boron isotope proxy (redrawn after Pagani et al. 2009). Ó 2012 The Authors. Journal of Ecology Ó 2012 British Ecological Society, Journal of Ecology, 100,31–41 CO2 starvation and ecosystem weathering 33 in soils (Banwart, Berg & Beerling 2009; Taylor et al. 2011, and global temperatures well below average pre-industrial 2012). We focus on the late Miocene because it represents a levels (Berner & Kothavala 2001; Pagani et al. 2005). Indeed, a time of global warmth, relative to now, and encompasses inter- very small, sustained imbalance in the carbon cycle results in vals of mountain building, including the uplift of the Hima- very large changes in [CO2]a (Berner & Caldeira 1997). For layas and the Alps between 14 and 8 Ma (Jime´nez-Moreno, example, the substantial [CO2]a fall at c. 34 Ma (Fig. 1) only Fauquette & Suc 2008). Global-scale analyses are achieved required a sustained <0.01 PgC year)1 offset between carbon with a well-defined modelling strategy (Taylor et al. 2011, input and output (Kerrick & Caldeira 1998). But this is not 2012) using late Miocene (11.6–5.3 Ma) climates simulated for observed for the past 24 Ma, suggesting that other strong feed- four [CO2]a values (400, 280, 180 and 100 p.p.m.) by the Had- backs maintain the balance of the geochemical carbon cycle ley Centre coupled ocean–atmosphere general circulation over this long interval of time. model, HadCM3L (C. D. Bradshaw, D. J. Lunt, R. Flecker, To explain these observations, a mechanistic ‘Earth system’ U. Salzmann, A. M. Haywood, M. J. Pound unpubl. data). hypothesis postulates that a lower limit of [CO2]a is buffered Overall, these simulations provide a rigorous basis for addres- by a strong negative feedback, caused by a diminished capacity sing the combined effects of [CO2]a and climate on terrestrial of land plants to weather Ca- and Mg-bearing silicates as silicate weathering by plants (Godde´ris & Donnadieu 2009). [CO2]a falls to critically low ‘starvation’ levels (Pagani et al. 2009). Vascular plants, and their symbiotic mycorrhizal fungal partners, accelerate rates of chemical weathering by a factor of Ecosystem CO starvation and the late 2 1.5 to <10 (Berner, Berner & Moulton 2003). Roots fracture Cenozoic carbon cycle rocks and increase the mineral surface area, soil pH is lowered Polar ice-core records indicate that Earth’s [CO2]a varied by root-respired CO2 and organic carbon oxidation, organic between c.180 and 300 p.p.m.
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