The mechanistic hypothesis of Beerling et al. (2001)
links the gap between the earliest vascular plants and the advent of large megaphylls with a dramatic 90 % drop in the atmospheric CO2 concentration during the late Palaeozoic (Berner, 2004). The large fall in CO2 corresponded with a marked rise in the stomatal density of vascular land plants, with densities increasing a 100-fold from 5–10 mm–2 on early vascular plant axes to 800–1000 mm–2 on the cuticles of late Carboniferous megaphylls (McElwain and Chaloner, 1995; Edwards, 1998). These evolutionary shifts in leaf anatomy are consistent with the effects of CO2 on stomatal development observed in modern plants cultivated in controlled conditions under different CO2 concentrations (Woodward, 1987).
According to theoretical calculations with a model of leaf biophysics and physiology, the rise in stomatal density held special significance for the evolution of leaves by permitting greater evaporative cooling and alleviating the requirement for convective heat loss (Beerling et al., 2001). Simulations indicate that archaic land plants with axial stems, few stomata, and low transpiration rates only avoided lethal overheating because they intercepted a minimal quantity of solar energy (Beerling et al., 2001; Roth-Nebelsick, 2001). In contrast, a megaphyll intercepting at least twice as much solar energy (per unit area of the photosynthetic organ) reached temperatures approaching the highly conserved lethal threshold of extant tropical taxa (Beerling et al., 2001) because the same limited evaporative cooling was inadequate to dissipate the absorbed thermal energy. Theoretical arguments therefore indicate that early vascular land plants were prevented from developing large laminate leaves because their low stomatal densities placed a tight constraint on evaporative cooling.
Even if the stomatal density of the early vascular land plants was not under the influence of atmospheric CO2, and megaphylls evolved a high density, the transpiration rates required to maintain cool temperatures (approx. 9–13 mmol H2O m–2 s–1) are calculated to outstrip the capacity of xylem to supply it by factor of ten, assuming the primitive stele of Psilotum nudum is a reasonable analogue for that of the early rhyniophytes (Schulte et al., 1987). In this case, dehydration precluded the evolution of large megaphylls with high stomatal densities in early land plants; no fossils of such an anatomically modified organ have yet been discovered.
By the time large laminate leaves became widespread in late Devonian/early Carboniferous fossil floras, the concentration of atmospheric CO2 had fallen, and stomatal densities had increased by up to a 100 times the value of early vascular land plant axes. Large leaves of late Devonian/early Carboniferous plants attained transpiration rates sufficiently high to maintain temperatures well below the lethal threshold, despite intercepting more solar energy (Beerling et al., 2001). Greater evaporative cooling also meant that large leaves stayed cool despite diminished convective heat loss, a flux that declines with increasing leaf size as friction across the surface slows the passage of air and the transfer of heat. Large-leaved perennials in today's deserts similarly rely on a high transpiration rate to prevent overheating and maintain leaf temperatures 8–18 °C below that of the air (Smith, 1978; Ehleringer, 1988), with some species in southern California even evolving a correspondingly lower temperature optimum for photosynthesis (Smith, 1978). For these large-leaved desert species, summertime precipitation permits high transpiration rates. But in the late Palaeozoic, the evolution of large leaves required the co-evolution of the root and vascular systems for improved water delivery and transport to sustain higher transpiration rates (Knoll et al., 1984; Raven and Edwards, 2001). Deeper roots accessed water and nutrients from a greater volume of soil, whilst xylem conduit enlargement and the appearance of secondary growth of xylem by the end of the Devonian increased the hydraulic conductance through stems and trunks to the leafy canopy, helping to maintain higher transpiration rates (Rowe and Speck, 2005).
The hypothesis of Beerling et al. (2001) makes the clear prediction that larger leaves gradually appeared as CO2 levels declined and stomatal numbers rose to increase evaporative cooling and ease the thermal burden of absorbed solar energy. Osborne et al. (2004a, b) achieved a successful test of this prediction with a morphometric analysis of 300 fossil specimens archived in major European collections. Their results showed a 25-fold enlargement of leaf blades as atmospheric CO2 fell during the late Palaeozoic (Fig. 2B). Leaf enlargement occurred first in the progymnosperms during the mid- to late-Devonian with the initial radiation of Archaeopteris and soon afterwards in the pteridosperms, a group attaining a larger maximum size coincident with a lower atmospheric CO2 concentration.
The consistent pattern of leaf blade enlargement seen in these two phylogenetically independent clades (Boyce and Knoll, 2002; Osborne et al., 2004a,b) is consistent with the argument that CO2 acted as an environmental driver for this aspect of plant evolution. But as the concentration of atmospheric CO2 declined to permit the evolution of leaves, competition for light and space between neighbouring plants intensified. Competition is therefore envisaged as providing a powerful selective force for plants to become leafier and taller. These shifting ecological interactions were most obviously manifested as the well-documented increase in plant size (Chaloner and Sheerin, 1979) that tracked historical patterns of leaf enlargement (Fig. 2C).
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