Implications for plants and for their environment of increased rooting depth by vascular plants during the Palaeozoic
The discussion of the biogeochemical content of the early embryophytes suggested that pre-embryophytic photosynthetic organisms on land, and associated microbial food webs, had significant effects in increasing the rate of weathering and the mobilization of plant nutrients from rocks, and in N2 fixation, leading to the production of a surface layer resembling soil. The evolution of embryophytes with roots (or with the antecedents, or functional analogues, of roots) increased this weathering activity. The larger and more structurally complex below-ground structures, involved in anchoring the plant and in taking up water and nutrients, were simultaneously permitted and required by larger and more structurally complex above-ground structures absorbing photons and CO2.
Chaloner and Sheerin show, in their text—Fig. 5 (see also Fig. 6.15 of Niklas, 1997) the maximum observed aerial axis diameter of vascular plant fossils from the late Silurian to the Devonian-Carboniferous boundary (Chaloner and Sheerin, 1979). The increase is from some 3 mm diameter in the latest Silurian, via an approximately linear increase in the logarithm of diameter with time, to almost 2 m at the end of the Devonian in the progymnosperm Archaeopteris (Callixylon). This progymnosperm has secondary thickening; the use of the relationships between height and basal stem diameter for organisms with secondary thickening (Fig. 5.9, Niklas, 1994; Figs 6.14, 6.15, Niklas, 1997) suggest a height for Archaeopteris of 10–30 m.
Corresponding to this increase in height is an increased plant biomass per unit land area and depth of penetration of roots sensu lato. While not suggesting that the depth and mass of below-ground parts of the plant increase in direct proportion to the height and mass of above-ground parts of the plant, there is independent evidence of an increasing depth of penetration of roots (Algeo et al., 1995; Algeo and Scheckler, 1998; Berner, 1990, 1993, 1994, 1997, 1998; Retallack, 1997; Elick et al., 1998) during the Devonian. Thus, dichotomous root traces up to 2 mm in diameter and up to 0.9 m long in the Emsian (late Early Devonian) have been found (Elick et al., 1998). An increasing area of land occupied by tracheophyte vegetation, and an increasing rooting depth in vegetated areas, meant an increasing volume of rock weathered throughout the Devonian. This permitted the ‘mining’ of more rock-derived nutrients which supplied the increasing biomass of plants, although the need per unit of added biomass for P, K, Fe and Mg does not increase in proportion to biomass in plants with extensive secondary thickening, since much of the biomass comprises non-living xylem which has much lower P, K, Fe and Mg (and N) content relative to the peripheral living tissue. This argument on mineral requirements requires that the P, K, Fe, Mg and N released can be recycled to growing peripheral tissue. A similar consideration applies to the recycling of P, K, Fe, Mg and N from relatively short-lived photosynthetic structures and nutrient and water-acquiring below-ground structures in long-lived plants (Addicott, 1982; Atkinson, 1992; Raven, 1986; Jackson et al., 1997; Robinson, 1990). Internal recycling from senescent short-lived structures into the perennial plant structures avoids the loss of these resources which have not been transported into the living core of the plant when the short-lived organ dies, regardless of whether it is abscissed. There are also considerations of how rapidly these mineral elements are recycled from dead plants (or abscissed or otherwise removed dead parts of plants) to the soil and hence to growing plants.
It has been pointed out that the increased weathering rate, as the volume of land surface impacted by root systems increased during the Devonian, was probably transient (Algeo and Scheckler, 1998). The argument contrasts to the high atmospheric CO2 with minimal (see above) biological pumping of CO2 into the land surface before the deep ‘rooting’ of embryophytes in the Devonian radiation with the low atmospheric CO2 (due to increased weathering on land) with higher CO2 in the land surface due to increased biological pumping as the volume of land surface impacted by root systems from the Carboniferous onwards. These two situations yield essentially identical rates of weathering (averaged over millions of years) before and after the Devonian radiation (Algeo and Scheckler, 1998). To recapitulate, the pre-Devonian high atmospheric CO2 and minimal biological CO2 pumping gave way to a post-Devonian lower CO2 atmospheric level with substantial biological CO2 pumping into the land surface and both scenarios are suggested to yield similar weathering rates. In the Devonian, as the area, and even more, the volume of biologically weathered land surface increased very significantly. This rapid weathering removed CO2 from the atmosphere and was maintained by the increased volume of land surface impacted by high CO2 produced from the biological pump. It has been suggested that CO2 in the land surface built up relative to the (decreasing) atmospheric CO2 in the Devonian so that the weathering rate was higher than before or after (Algeo and Scheckler, 1998). The argument of these authors suggests that there was a pulse of weathering of the land surface in the Devonian, whose extent has not been matched before (when weathering was predominantly a result of high atmospheric CO2) or since (when weathering was predominantly a result of high land surface CO2) (Algeo and Scheckler, 1998). It is possible that Algeo and Scheckler somewhat underestimated the pre-Devonian role of non-vascular terrestrial photosynthetic and other organisms in enhancing weathering (Algeo and Scheckler, 1998; Horodyski and Knauth, 1994; Yapp and Poths, 1992).
A further effect of increased weathering and the production of soil concerns the increased storage capacity for water near the surface. This helps to tide homoiohydric plants over between stochastic rainfall events as photosynthesizing organisms rather than just permitting them to stay alive, as would be the case for poikilohydric, desiccation-tolerant organisms. This water storage, together with the moderating effect on rainfall of the above-ground plant canopy and the more extensive root system, can reduce soil erosion during rainstorms.
These effects of the increased rock weathering as a result of an increased volume of rock available to weathering by plants have been viewed until now as having essentially a positive feedback in plants, i.e. increasing the quantity and/or continuity of resource (water, pedosphere-derived nutrients) availability. However, plant-increased weathering also has an effect on the aerial environment of plants (discussed above in relation to the transitory increase in weathering rate) which can be considered as a negative feedback on the capacity for the rate of biomass increase. This relates to the removal of atmospheric CO2 in weathering of silicate minerals.
The mechanism whereby photosynthesis at the (rock or) soil surface and respiration below the photic zone (a concept borrowed from aquatic ecology) increase CO2 use in weathering, which was outlined earlier for algal mats as part of microbial food webs, is quantitatively accentuated for tracheophytes, and especially for deeper-rooting tracheophytes. The increased external (via a leaf area index in excess of one) and internal (via intercellular gas spaces in leaves) area involved in CO2 uptake permits the canopy-top photon flux density of up to 2000 µmol photon m-2 s-1 to be used effectively in photosynthesis, noting that the potential for CO2 fixation could be constrained with less appropriate geometry by diffusion of CO2 in solution to the carboxylase. This latter constraint might, with geometry of photosynthetic structures similar, in principle, to those of extant plants, in the Silurian and early Devonian with CO2 at 10–20 times the present level, permit C3 photosynthesis to occur at up to 6 µmol CO2 per m2 of area over which CO2 passes from the gas to the solution phase per second. This, with a photon yield of C3 photosynthesis in high CO2 of 0.1 mol CO2 fixed per mol photons absorbed or 0.08 mol CO2 fixed per mol incident photons (assuming an absorptance of 0.8), would permit a fixation of up to 75 µmol CO2 m-2 gas exchange surface s-1; this requires a gas-exchange surface area of 27 times the land area to effectively use 2000 µmol photon m-2 s-1 incident photon flux density. This could be accomplished by a leaf (axis) area index of three and an internal area exposed to a gas phase nine times the external (projected) area (see Raven, 1977, 1993, 1995a, 1997, 1998; Konrad et al., 2000).
Up to half of this productivity could be transported in phloem (or analogous) tissues to roots, where up to half of the transported organic carbon could be respired to CO2 by living plant cells. Dead roots, plus aerial plants parts mixed into soil by animals, could be respired by animals and, especially, microbes to produce CO2. This CO2 has two possible sinks. One sink is diffusion from the soil solution, via the soil gas phase to the atmosphere. The other sink is consumption in weathering. The low conductance for CO2 via the soil gas spaces resulting from the long linear diffusion path and tortuosity of the diffusion path, and the small fraction of the area parallel to the soil surface which is occupied by gas spaces, result in the build-up of CO2 in the rock/soil surface layers. This CO2 build-up increases the rate of weathering. The balance between CO2 evasion to the atmosphere and CO2 consumption in weathering as CO2 output into the rock/soil surface layers involves an increased rate of weathering with an increased rate of respiratory CO2 injection into the rock/soil surface. It is of interest that CO2 arises not only from respiration by below-ground plant organs, and by heterotrophs living on live or dead particulate plant material, but also from respiration of soluble organic solution. These organic acids can, before their conversion to inorganic carbon, increase the rate and pathway of weathering of silicates (Berner and Berner, 1996).
The occurrence of an increasing fraction of the area of the land surface colonized by tracheophytes, and an increasing depth of (rock) soil exploited by tracheophyte roots, tends to speed up the reactions in equation (1) relative to those of equation (3), but has a negligible effect on the rate of equation (5) (see above under The biogeochemical context of early embryophytes). This means that the expansion of tracheophytes, including the activities of their root systems, removes CO2 from the atmosphere. While the build-up of organic matter in biomass also removes CO2 from the atmosphere, the much more rapid turnover of the great majority of this material to regenerate CO2 (months to thousands of years, depending on the chemistry and structure of the material: Schlesinger, 1991; Berner and Berner, 1996) means that the impact on atmospheric CO2 over millions of years and longer comes more from the sedimentation, weathering and vulcanism of inorganic carbon than of organic carbon.
The increased weathering due to more widespread and deeper-rooting tracheophytes is thought to be a major cause of the decrease in atmospheric CO2 during the Devonian to a minimum (until the recent Pleistocene glacial maxima) value in Carboniferous (Berner, 1990, 1993, 1994, 1997, 1998; Berner and Berner, 1996). However, it is noted that the enhanced weathering due to tracheophytes is (rightly) incorporated in the biogeochemical models which predict atmospheric CO2 levels, so that these values of atmospheric CO2 are not obtained independently of assumptions about plant behaviour in increasing the rate of weathering.
This largely vascular land plant-induced decrease in atmospheric CO2 in the Devonian had important implications for performance of the aerial shoots in photosynthesis. Lower CO2 partial pressures decrease the rates of C3 photosynthesis over a range of photon flux densities if the anatomical and biochemical characteristics of the shoot are not modified and the near-extant O2 partial pressures in the Devonian is considered (Beerling et al., 1998). Increased stomatal indices and/or densities with decreasing CO2 partial pressures, as a result of adaptive or acclimatory processes, can partially offset the decreased CO2 fixation rate, but at the expense of an increased rate of H2O loss in transpiration per unit CO2 fixed.
What evidence is there as to evolutionary changes inplant shoots in the Devonian in parallel with the tracheophyte (root)-induced drawdown of atmospheric CO2? One change in shoot morphology through the Devonian which may be related to the decreased atmospheric CO2 level (Chaloner, 1999) is the evolution of planate branch systems, and of ‘webbing’ of photosynthetic tissues between the ultimate ramuli of the branches (Gensel and Andrews, 1984; Stewart and Rothwell, 1993; Taylor and Taylor, 1993). Chaloner suggests that the decrease in mean diffusion pathlength for CO2 in the gas phase of the intercellular gas spaces in the planate webbed structures than in the cylindrical photosynthetic structures can be related to the decreasing atmospheric CO2 level through the Devonian (Chaloner, 1999). This could be related to the mechanical constraints on the dimensions of cylindrical as opposed to planar structures with a density of 106 g m-3 in at atmosphere with a density of 103 g m-3. At all events, the radius of cylindrical plant structures is greater than the smallest half-thickness of a laminar organ, a comparison which relates the maximum possible CO2 diffusion pathlength from stomata to photosynthetic cells in the smallest diameter of cylindrical organ with that of the shortest CO2 diffusion pathlength from stomata to photosynthetic cells in an amphistomatous planar structure. The decreased capacity for use of light energy in CO2 fixation per unit projected area in a thin laminar structure relative to a small-diameter cylindrical organ can be countered at a whole-canopy level by increasing the number of layers (leaf area index: Raven, 1997, 1984a, b, 1993, 1994a, b, 1995a, 1997). Constraints on the structure of laminar organs in relation to the maximum possible distance between vascular tissue and the most distant photosynthetic cells have been discussed previously (Raven, 1994a). Clearly there are vascular plants today (when CO2 levels in the atmosphere are similar to the lowest values seen in the Palaeozoic (Carboniferous)) which have cylindrical photosynthetic structures, frequently co-existing with tracheophytes with laminar photosynthetic structures so, as with so much in biology, there may be more than one structural type working well in performing a given function.
The other evolutionary change which occurred between the Silurian and the Carboniferous is an increase in stomatal density (Chaloner and Collinson, 1975; McElwain and Chaloner, 1995, 1996; Chaloner, 1999). The very wide genotypic range in stomatal densities among extant plants (Chaloner and Collinson, 1975), as judged from the wide stomatal density range for organisms all living in the same CO2 environment means that extant comparators (NLE or nearest living equivalents) are needed in interpreting the fossil stomatal density values. This question has been addressed (McElwain, 1998; McElwain and Chaloner, 1995, 1996). This problem of NLEs occurs even for the recent past (Tertiary, and even the Mesozoic) when there were fossil plants with close phylogenetic similarity to extant plants (even extending to con-generics such as Ginkgo species from the recent and Mesozoic) as well as life-form and habitat similarities. For the Palaeozoic, close phylogenetic similarities do not occur, so the NLE comparators are largely those organisms with similar life forms and habitats.
With these provisos in mind (Edwards, 1998; McElwain, 1998; McElwain and Chaloner, 1995, 1996) a number of Palaeozoic plants have been analysed and a very significant decline in stomatal density between the Silurian and the Carboniferous shown. This is consistent with the decrease in CO2 suggested by the Geocarb II model (Berner, 1994) and the theoretical and observed acclimatory effects of growth CO2 on stomatal density in extant plants (Woodward, 1987; Woodward and Bazzaz, 1988; Woodward and Kelly, 1995; Beerling et al., 1998). The stomatal density changes over geological time have also been used to hindcast CO2 levels (McElwain, 1998); this contrasts with the way they are used here.
These two examples, i.e. the evolution of laminar photosynthetic structures and of decreasing stomatal density in the Devonian, show the likely feedback of root activities, via atmospheric CO2 drawdown, on shoot evolution.