This Botanical Briefing reviews how the integration of palaeontology, geochemistry and developmental …

• Abstract
• Introduction
• Evolution of the leaf and atmosphere
• Genes, leaves and stomata
• Vegetation feedbacks and the long-term carbon cycle
• Conclusions
• Literature cited
• Figures

Biology Articles » Evolutionary Biology » Leaf Evolution: Gases, Genes and Geochemistry » Vegetation feedbacks and the long-term carbon cycle

Vegetation feedbacks and the long-term carbon cycle

- Leaf Evolution: Gases, Genes and Geochemistry

The realization that aspects of plant evolution may be directed by changes in atmospheric CO₂ gains greater significance when considered alongside the impact that plants themselves exert on the long-term carbon cycle. Before plants, Earth's global climate and atmospheric CO₂ were regulated on a multi-million year timescale by the inorganic carbon cycle, in which CO₂ is supplied to the atmosphere by volcanism and metamorphic degassing, and removed by the chemical weathering of Ca–Mg silicate rocks (Walker et al., 1981; Berner et al., 1983). The closed cycle can be represented as a simple systems diagram with arrows indicating a direct response (no bull's-eyes) or an inverse response (with bull's-eyes) (Fig. 3A). In these diagrams an even number of arrows with or without bull's-eyes defines a positive feedback and an odd number with bull's-eyes a negative feedback. The inorganic carbon cycle (Fig. 3A) is stabilized by a negative feedback loop because silicate-weathering rates increase with temperature (Walker et al., 1981; Berner et al., 1983). Rising CO₂ levels, for example, strengthen the greenhouse effect, warm the climate, accelerate the chemical weathering of Ca–Mg silicate rocks, remove CO₂ from the atmosphere and lead to a cooler climate (Fig. 3A).

 
The advent of rooted vascular land plants introduced a potent biotic feedback into the long-term carbon cycle (Berner, 2004). Plant activities greatly enhance silicate rock weathering rates through a wide variety of processes. Weathering proceeds as described by the overall reaction:

CO2 + (Ca, Mg) SiO3 --> (Ca, Mg) CO3 + SiO2

where Mg and Ca represent all calcium and magnesium silicates and carbonates (e.g. dolomite). Equation (1) summarizes the net result of a wide variety of processes, the most important being the secretion of organic acids and chelates by rootlets (and associated symbionts) and the generation of CO₂ by respiration of organic matter, both of which break down silicate minerals and produce bicarbonate ions (Berner et al., 2003). Plant roots are especially effective at accelerating chemical and physical weathering of rocks and soils (Raven and Edwards, 2001; Berner et al., 2003) by increasing the surface area of soil–root interface directly and by fracturing mineral grains (Fig. 4). Roots also anchor soils, and decelerate physical erosion, thus increasing the water contact time of primary minerals. At the regional scale, recirculation of precipitation by evapotranspiration dissolves minerals more efficiently and enhances transport of bicarbonate ions from soils into rivers (Berner et al., 2003). After transport to the oceans by rivers, weathering products are removed by the formation of carbonates. Plants are also the primary source of organic matter buried in sediments.  
For the past two decades, only two negative stabilizing feedbacks on the long-term carbon cycle involving plants, weathering and organic carbon cycle and have been identified (Volk, 1987, 1989). Recognizing CO₂ as a driver of plant evolution has revealed, through a systems analysis of the intricate web of interactions, several new positive feedback loops (PFLs) that operate only when plants encounter a warm climate (Beerling and Berner, 2005). These feedbacks operate whether CO₂ is rising or falling. However, in the context of this Briefing, my comments are confined to the late Palaeozoic (falling CO₂) situation.

The four most important PFLs involve the action of CO₂ on plant evolution and its feedback on rock weathering rates, and sedimentary organic carbon burial (Fig. 3). In the first PFL (Fig. 3B) a drop in the atmospheric CO₂ concentration and a rise in stomatal density permits the evolution of larger leaves through the mechanisms discussed earlier. Higher stomatal densities maximize CO₂ diffusion into the leaf under conditions favourable for photosynthesis, and larger leaves capture more solar energy; both traits promote primary production and leafier canopies (Beerling and Berner, 2005). Higher densities are also associated with smaller stomata that can open and close more rapidly helping to protect the xylem water pathway from cavitation and allowing taller plants (Hetherington and Woodward, 2003). Taller, leafier plants require deeper rooting systems and more symbionts, including mycorrhizae, for uptake of water and nutrients (Raven and Edwards, 2001). Deeper roots and more abundant mycorrhizae increase nutrient removal and the surface area of the soil–root interface, accelerating the chemical weathering of silicates and further enhancing the removal of CO₂ from the atmosphere (Berner et al., 2003).

In the second PFL, a similar chain of cause and effect follows a drop in atmospheric CO₂, but with larger more productive plants enhancing organic carbon burial, both in terrestrial wetlands and marine environments after transport to the sea by rivers. Increasing organic carbon burial with falling atmospheric CO₂ reflects a major evolutionary trend towards woody plants containing a high proportion of the relatively non-biodegradable compound lignin (Berner, 2004). An expanding terrestrial biomass, promoting CO₂ removal from the atmosphere, is recorded as an enormous increase in sedimentary organic carbon burial on land and in the sea (Fig. 2D), most obviously manifested as carboniferous coal deposits. Two further complementary PFLs to those already described operate through the direct action of CO₂ on climate, via the greenhouse effect (Fig. 3D and E).

The strengthening of this suite of PFLs during the late Palaeozoic evolution of the terrestrial flora, especially rooted forests, strongly amplified the extent and rate of both silicate weathering and sedimentary organic carbon burial. It was by way of these geochemical effects that plants brought about the precipitous decline in atmospheric CO₂ that led ultimately to the Permo-Carboniferous glaciation (Berner, 2004; Beerling and Berner, 2005). The accelerated removal of CO₂ from the atmosphere was only stabilized by the negative CO₂-climate feedback loop of the inorganic carbon cycle (Fig. 3A), as the climate cooled and decelerated rates of silicate weathering.

In the long term, plants brought about a gradual and continual alteration of the global environment that modified selection pressures on subsequent generations, effectively facilitating their own evolution through the process of niche construction (Odling-Smee et al., 2003). Moreover, plant activities appear to have caused rates of evolution in terrestrial animals to accelerate. Late Palaeozoic insect and tetrapod faunas diversified together with terrestrial plants, and enhanced burial of organic carbon raised global oxygen levels (Berner, 2004), fuelling a spectacular radiation of insect gigantism (Graham et al., 1995).