Stomatal behaviour, photosynthesis and transpiration under

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1 Plant, Cell and Environment (1999) 22, ORIGINAL ARTICLE OA 220 EN Stomatal behaviour, photosynthesis and transpiration under rising CO 2 A. J. JARVIS, T. A. MANSFIELD & W. J. DAVIES Institute of Environmental and Natural Sciences, Lancaster University, Lancaster, LA1 4YQ, UK ABSTRACT The literature reports enormous variation between species in the extent of stomatal responses to rising CO 2. This paper attempts to provide a framework within which some of this diversity can be explained. We describe the role of stomata in the short-term response of leaf gas exchange to increases in ambient CO 2 concentration by developing the recently proposed stomatal model of Jarvis & Davies (1998). In this model stomatal conductance is correlated with the functioning of the photosynthetic system so that the effects of increases in CO 2 on stomata are experienced through changes in the rate of photosynthesis in a simple and mechanistically transparent way. This model also allows us to consider the effects of evaporative demand and soil moisture availability on stomatal responses to photosynthesis and therefore provides a means of considering these additional sources of variation. We emphasize that the relationship between the rate of photosynthesis and the internal CO 2 concentration and also drought will have important effects on the relative gains to be achieved under rising CO 2. Key-words: drought, elevated CO 2, photosynthesis, stomatal conductance, transpiration. Abbreviations: Definitions of the variables used and the units are given in Table 1. INTRODUCTION An increase in the CO 2 concentration of the atmosphere in contact with vegetation acts to increase the CO 2 concentration gradient between the atmosphere and the air space within leaves. Given no adjustment to this change the rate of CO 2 diffusion through the stomatal pores would rise in proportion to the increase in ambient CO 2. It is clear from the contents of this issue, however, that a complex dynamic is initiated between plants and their environment following an imposed change in the atmospheric CO 2 concentration. In recognition of the importance of feedback within plant atmosphere interactions Monteith (1995a) referred to the continual dynamic adjustment of plants and environment as a process of accommodation. Understanding the nature of the accommodation Correspondence: A. J. Jarvis. A. Jarvis@lancaster.ac.uk 1999 Blackwell Science Ltd between plants and environment is a central requirement when forecasting the effects of elevated CO 2 on both vegetation and climate. For CO 2 responses, this dynamic occurs across a broad range of temporal and spatial scales affecting many processes including the aperture and distribution of stomatal pores. In a description of plant environment interactions under rising CO 2 several key processes can be broadly identified relating to a role for stomata (Eamus 1991). An increase in the ambient CO 2 concentration, c a, can cause net CO 2 assimilation, A N, to rise (Drake, Gonzàlez-Meler & Long 1997) despite reductions in stomatal aperture and frequency and hence stomatal conductance (to water vapour), g s (Morison 1987; Field, Jackson & Mooney 1995; Drake et al. 1997). Reductions in g s can cause reductions in the rate of transpiration, E. Reductions in E cause a partial desaturation of the air adjacent to vegetation and the decreased evaporative cooling of leaves results in increased leaf temperature; both factors increasing evaporative demand. In the absence of changes in the leaf area, reductions in E when integrated over time can result in an improved soil moisture availability (Field et al. 1995). Unless plants lose out to neighbours in the competition for soil water, improved soil moisture availability would allow the maintenance of g s and hence A N (Knapp Hamerlynck & Owensby 1993; Jackson et al. 1994; Owensby et al. 1997). Increases in A N increase the amount of carbon available for investment in foraging for water, thus further enhancing soil moisture availability (Eamus 1996). At the same time increases in the amount of carbon available for new leaves may enlarge the leaf area to an extent that offsets the imposed reductions in E (Heath & Kersteins 1997). Although this may suffice as a general description of some dominant processes relating to stomata under rising CO 2, a description of the individual processes described is required if we are to estimate the relative gains of each one, and integrate them to forecast the overall gain between our input, rising CO 2, and our chosen outputs. However, the mechanistic basis of the CO 2 response of some of these processes is obscure. Therefore, the focus of this paper will be restricted to describing the role of stomata in the short term response of leaf gas exchange to increases in c a by developing the recently proposed stomatal model of Jarvis & Davies (1998). The aim is to provide a speculative framework within which some of the diversity of observations on stomatal responses to rising CO 2 can be discussed. 639

2 640 A. J. Jarvis et al. Symbol Definition Units Table 1. Abbreviations A Gross CO 2 fixation rate mol m 2 s 1 A m Gross CO 2 fixation capacity mol m 2 s 1 A N Net CO 2 fixation rate mol m 2 s 1 A Nm Net CO 2 fixation capacity mol m 2 s 1 c a Ambient CO 2 mole fraction mol mol 1 c i Leaf air space CO 2 mole fraction mol mol 1 c s Leaf surface CO 2 mole fraction mol mol 1 D H 2 O concentration gradient mol mol 1 E Transpiration rate mol m 2 s 1 E m Local maximum transpiration rate mol m 2 s 1 G A Stomatal photosynthesis gain mol m 2 s 1 G E Stomatal transpiration gain G α Stomatal photosynthesis gain at constant c i /c a g m Local maximum stomatal conductance to water vapour mol m 2 s 1 g mx Maximum stomatal conductance to water vapour mol m 2 s 1 g s Stomatal conductance to water vapour mol m 2 s 1 g tc Total gas phase conductance to CO 2 mol m 2 s 1 R Respiration rate mol m 2 s 1 S Soil moisture availability index m 2 s mol 1 V Slope of relationship between A and c c i = 0 mol m 2 s 1 α c i /c. THE EFFECTS OF CO 2 ON STOMATAL CONDUCTANCE Since the early work of Heath & Russell (1954) it has become obvious that c a has a powerful effect on stomatal aperture and hence g s. For example, Snaith & Mansfield (1982) found reductions in aperture of over 80% in 700 p.p.m. compared with zero CO 2 in the incubated epidermis of Commelina communis. The cellular mechanisms of reversible responses of stomatal guard cells to CO 2 have not yet been identified (Assmann 1993) although new information has recently become available (e.g. Webb et al. 1996; Zeiger & Zhu 1998). It is generally, but not universally, observed that if the growth CO 2 concentration is doubled then g s falls by between 20 (Drake et al. 1997) and 40 (Morison 1987) per cent. This is attributable to changes in both stomatal frequency and aperture. Mott (1988) demonstrated that g s responds to a disturbance in the intercellular CO 2 concentration, c i, rather than c a, and the conservation of proportionality between c i and c a (Wong, Cowan & Farquhar 1978) facilitated by the response of g s to CO 2 provides us with information on the mechanism behind the stomatal response to CO 2 in intact leaves. This proportionality appears to change with factors that affect water loss, such as humidity (Morison & Gifford 1983; Zhang & Nobel 1996) and particularly soil moisture availability (Brodribb 1996) but is largely unaffected by nutrient status (Wong, Cowan & Farquhar 1985), irradiance above the light compensation point (Wong et al. 1978), temperature (Ball, Woodrow & Berry 1987) and persistent exposure to elevated CO 2 (Drake et al. 1997). The observed regulation of c i is a manifestation of an equilibrium state between stomatal responses to CO 2 and the factors affecting the diffusion of CO 2 into the leaf; that is, gas phase resistances and the biochemical CO 2 demand. These processes are intimately related through the effects of numerous feedbacks. To account for the role of stomata in the observed regulation of c i a physiological description of fluxes of CO 2 and water vapour into and out of leaves is required, of which there are three central components: descriptions of the diffusion process itself, of the processes determining the demand for the gas fluxes and of the stomatal control of these fluxes. For water vapour and to a lesser extent for CO 2, mechanistic descriptions of diffusion and demand processes are well developed. In contrast, although a theory that may explain patterns of stomatal behaviour has been presented (Cowan & Farquhar 1977) the mechanistic basis of this theory remains unresolved. The reason for this is that while diffusion is a welldefined physical process, and photosynthesis is essentially a reaction involving identifiable molecular components including CO 2, stomatal function is a control process, itself comprised of numerous feedbacks between poorly defined physiological and biochemical processes. Therefore, initially we will represent the stomatal CO 2 response empirically by c i = αc a (Ball & Berry 1982), where α is approximately 0 7 for C3 plants and 0 4 for C4 plants under well-watered conditions (Wong, Cowan & Farquhar 1979), and incorporate this response into equations describing the biochemical demand for and diffusion of CO 2 to provide an insight into the nature of the stomatal CO 2 response in leaves. The net rate of CO 2 diffusion, A N, is assumed to be linearly related to the total gas phase conductance to CO 2, g tc, and the CO 2 concentration gradient c a c i where c i and c a are the CO 2 mole fractions in the intercellular air spaces of the leaf and the ambient air, respectively. A N =(c a c i )g tc. (1)

3 Stomatal behaviour, photosynthesis and transpiration under rising CO For simplicity Eqn 1 ignores the small effect of E on A N (Jarman 1974) and a finite mesophyll resistance (Farquhar & Sharkey 1982). Here, we will describe the biochemical demand for CO 2 by just two parameters accounting for the initial slope, V, and saturation level, A m, of the relationship between the gross rate of assimilation, A, and c i A m c i A = (2) A m /V + c i A N is the difference between the gross CO 2 fixation rate, A, and the rate of CO 2 evolution by respiration, R (A N = A R). At small scales, such as patches of young leaves, Eqn 2 will give an incomplete description of the response of A to increasing c i since such responses are invariably observed as being biphasic (Farquhar, von Caemmerer & Berry 1980). However, with increasing scale, spatial heterogeneity in the carboxylation processes masks the biphasic nature of this response therefore improving the descriptive power of Eqn 2. Substituting αc a for c i in Eqns 1 and 2 gives A N =(1 α)c a g tc (3) and A m α c a A = (4) A m /V + α c a α is approximately constant providing A N >> R (Farquhar & Wong 1984). Therefore, assuming A N A and combining Eqns 3 and 4 by eliminating c a we derive a single expression between A and g tc which describes how A and g tc co-vary when c i = αc a g tc = G α (A m A). (5) G α is given by (V/A m )α/(1 α). g tc is expressed as the dependent term since we now see that increases in A are associated with linear decreases in g tc which is obviously at variance with Eqn 1 and must therefore be indicative of a potential control mechanism resulting in the observed regulation of c i. Observations of c i are made using gas exchange systems where high boundary layer conductances are imposed. As a result c a is approximately equal to the leaf surface CO 2 concentration, c s, and g tc is approximately equal to g s /1 6. From Eqn 5 we conclude that a simple explanation of the observed regulation of c i by stomatal movements lies not with the direct effects of c i on stomata (Raschke 1975) which are generally non-linear, but rather with a linear relationship between increases in A and reductions in g s when the photosynthetic properties of the leaf remain constant (Jarvis & Davies 1998). Under such circumstances c i is an intermediary variable since A = f(c i ) (compare with Eqn 2). The now apparently fortuitous regulation of c i enabled Wong et al. (1979) to identify stomatal responses to photosynthetic capacity, A m, since at constant c a the manipulation of the photosynthetic properties of leaves led to near linear variations in both A N and g s because, providing α remains approximately constant, the CO 2 concentration gradient at the leaf surface (1 α)c s, must also. A m A is analogous to the degree to which the photosynthetic capacity of the leaf is satisfied and can be interpreted as a pool of a carbon-fixing substrate consumed in proportion to A to which stomata appear to respond (Jarvis & Davies 1998). In the analysis of published data presented by Jarvis & Davies (1998) the measured net rates, A N, were used. Provided the CO 2 -saturated rate of CO 2 fixation associated with A N is also net (A Nm ) then A m A A Nm A N. Here, the gross rate difference, A m A, will be preferred to A Nm A N to simplify the integration of stomatal responses into the closed loop description of the response of g s and A to c s. A similar theory to that of Jarvis & Davies (1998) was initially formalized in a simulation model of stomatal function presented by Farquhar & Wong (1984) but became discredited due to an over-emphasis on stomatal CO 2 responses to mesophyll photosynthetic properties. As a result of the non-acceptance of the ideas of Farquhar & Wong (1984), the short-term response of g s to variations in c a have generally been presented as non-linear functions of c i rather than linear functions of A m or A (Schulze & Hall 1982; Jarvis & Davies 1998). It is well known that stomatal CO 2 responses comparable to those in the intact leaf are observed in detached epidermis. Changes in CO 2 concentration can induce increases in cytosolic calcium in guard cells on detached epidermis (Webb et al. 1996; see Assmann 1998), providing strong evidence that a signal transduction system for sensing CO 2 is present in the guard cell and that it is able to function independently of inputs from other leaf tissues. Nevertheless, the observed proportionality between c i and c a suggests that in whole leaves this process is somehow tightly coupled to mesophyll photosynthetic performance. Since c i can be common to both guard and mesophyll cells, information on the availability of CO 2 to both cell types is shared in the intact leaf (Raschke 1975) and easy to synthesize in experiments with detached epidermis. However, for guard cells to respond in accord with CO 2 utilization by the mesophyll information relating to mesophyll photosynthetic performance (crudely described here by A m and V) would also need to be shared between both cell types. How this is achieved is not known, but emphasizes the need to interpret mechanisms elucidated in detached epidermis within the context of the functioning of the whole leaf/plant. A parallel can be drawn here with the regulation of stomatal behaviour by the plant hormone abscisic acid (ABA). Stomata in detached epidermis can show a significant response to an ABA treatment, but to understand the role of ABA in regulating stomatal behaviour in whole plants one has to understand the synthesis and modulation of ABA signals prior to arrival at the stomatal complex. In the present context, the effect of an increase in c a is to increase c i and hence A, reducing A m A and g s. Therefore, Eqn 5 is describing negative feedback between A and g s which acts to ensure that g s is regulated in order to increase the use of leaf photosynthetic capacity. Jarvis & Davies (1998) re-analysed published data on the response of both A N and g s to variations in c a and found that a relationship between A N and g s consistent with Eqn 5 was invariably

4 642 A. J. Jarvis et al. observed providing that account was also taken of the effects of concomitant losses of water vapour on g s. If stomata close as c a increases, E will fall to a degree dependent on evaporative demand. The observed departure from a strict linearity between A N and g s as c a is increased could be explained if there was a similar negative feedback between E and g s (Jarvis et al. 1998), namely, as E increased g s tended to decrease linearly (Monteith 1995b), g s = g m (1 E/E m ). (6) g m and E m are the local maximum values of g s and E, respectively, which Monteith (1995b) estimated from experiments where humidity had been varied and found them to be functions of CO 2, temperature and soil moisture content. Combining Eqns 5 and 6 Jarvis & Davies (1998) proposed the following model of stomatal function to factors which affect both A and E g s = G A G E, (7) where G A = A m A and G E = G SE. G is the maximum sensitivity of stomatal conductance to A m A, which scales for stomatal characteristics and the proportionality between mesophyll CO 2 metabolism and guard cell carbon signalling. S is the sensitivity of G E to E which Jarvis & Davies (1998) speculated was closely related to soil moisture availability since the product SE can describe either hydraulic (Jones 1998) or hormonal (Jarvis & Davies 1997) mass balances in the proximity of the guard cells. Equation 7 is at best a gross simplification, ignoring any direct effects of light (Sharkey & Raschke 1981) and humidity (Farquhar 1978) on g s as well as the ubiquitous effects of temperature. However, of the 140 individual measurements analysed by Jarvis & Davies (1998) relating to the effects of short-term changes in c a on g s, 136 fitted the general pattern of Eqn 7 although the parameter estimates for G and S varied greatly between species and were particularly affected by variations in irradiance reflecting the effects of light on guard cells which were independent of mesophyll photosynthesis (Sharkey & Raschke 1981). Comparing Eqns 6 and 7, g m is given by (A m A)G and E m is given by G/S. Monteith (1995b) observed that the ratio g m /E m was somewhat independent of c a for the C4 grasses Maize and Paspalum which is inconsistent with Eqn 7 unless A m also varies with c a in these species (see Morison & Gifford 1983; Fig. 2a). Monteith (1995b) also observed that the data of Turner, Schulze & Gollan (1985) for sunflower demonstrated that g m remained constant with falling volumetric soil moisture content until a critical level of 8% was reached, whilst E m varied approximately linearly with volumetric soil moisture content. From the equivalence between Eqns 6 and 7 one can see why g m might have remained constant until significant reductions in A m A were incurred through drought-induced stomatal limitations to CO 2 supply whilst E m would vary approximately linearly with volumetric soil moisture content if S 1 acted to linearize the effects of the soil moisture content/potential relationship (see Monteith (1995b) Fig. (3)), assuming S is linearly related to soil matric potential (Schurr & Schulze 1996; Jarvis & Davies 1997). Equation 7 formalizes the conceptual hypothesis that stomata balance the biochemical demand for CO 2 with the evaporative demand for water relative to the availability of water to the plant. Here, this balance is represented by the product of the sensitivities of g s to carbon gain, G A, and water loss, G E. The product G A G E suggests that at some point the H 2 O and CO 2 signals to stomata must converge since the response of stomata to the one signal is dependent on the degree of response of stomata to the other. Taking a factor of S from G E gives g s =(A m A)(E m E)S, (8) which would suggest a degree of similarity in the nature of the response of g s to both E and A. CLOSURE FOR DIFFUSION, DEMAND AND STOMATAL CONTROL Having identified a relationship between g s and the quantity A m A we are interested in describing the magnitude of the resultant changes in A and hence A m A, g s and E, given a rise in c a. For simplicity we will consider the situation at the leaf surface (c a = c s, g tc = g s /1 6) and assume that the variations in leaf temperature arising from changes in latent heat flux are too small to affect A m, V and R. Noting E Dg s where D is the leaf surface H 2 O concentration gradient we derive the following quadratic in g s from Eqns 1, 2 and 7. ag 2 s + bg s + c = 0, (9) where a = SD((SDA m +1)A m + Vc s ), b = 2(A 2 m + GSD) (c s V+A m )G + 1 6((A m R)SD+1)Vand c = 1 6(A m R)GV +(A m G) 2. The minimum root of Eqn 9 yields the appropriate solution for g s. Interestly we note that equations 2 and 7 can be written A = V(A m A)c i /A m and (A m A) =g s /(G SDg s ), respectively, and combining these with eqn 1 gives V (g s c s + 1.6R)/A m A = (10) G + 1.6V/A m SDg s. Re-arranging eqn 10 for g s gives (G + 1.6V/A m ) A 1.6VR/A m g s = (11) c s V/A m + SDA which is similar to Ball et al. s (1987) widely applied model of stomatal response to environment. However, Eqn 11 is not a model of stomatal function but rather a model of covariance of g s and A with environment (Aphalo & Jarvis 1993) which would be inappropriately coupled to Eqn 2 or the like since it is derived in part from that expression. The variable V describes the degree of curvature of the A c i relationship and therefore how rapidly A m A tends to A m with increasing c i. When V is small A/ c i is near constant and the gain of the relationship between A and c s may

5 Stomatal behaviour, photosynthesis and transpiration under rising CO be approximated by V/(1 + V/g s ), namely, a doubling in c s will result in a doubling in A across a large range of g s and that this response will be relatively unaffected by any feedback arising from stomatal responses to changes in A until g s becomes small. In contrast when V is large, variations in A/ c i with c s may be significant so that the gain of the relationship between A and c s varies significantly with both g s and c s. Therefore, V has the potential to play an important role in determining differences in the response of A and g s to rising CO 2. Two scenarios will be explored here using Eqns 9 and 10. Firstly, the effect of V on the response of A and g s to c s alone. Secondly, the effects of the curvature introduced by V on the alleviation of CO 2 supply limitations when c s is doubled during soil drying. THE EFFECTS OF CO 2 ON A AND g S Equations 9 and 10 form the basis of the simulation in Fig. 1 which shows the effects of increasing c s on the relationship between g s and A for two values of V (see legend to Fig. 1 for parameter values). The effect of increasing V is to shift photosynthesis closer to CO 2 saturation and hence to determine where equilibrium lies on the relationship between g s and A (Fig. 1 inset). As a result, the effect of increasing V in the present context is to shift photosynthesis closer to CO 2 saturation thereby reducing A m -A and hence g s (Fig. 1 inset). When c s is increased the comparative gains in A fall whilst the comparative reductions in g s rise with increasing V (Fig. 1), despite no change in the stomatal control law (Fig. 1 inset). Consistent with these predictions Ham et al. (1995) observed no effect of doubled c s on net canopy CO 2 exchange for a C4 dominated prairie whilst evapotranspiration was reduced by 22% following a 41% reduction in canopy conductance. Also, Wong (1979) observed that doubling growth c a at high nitrogen supply resulted in a 1 5-fold increase in A N and a 1 2-fold decrease in E in cotton compared with a 1 2-fold increase in A N and 1 5-fold decrease in E in maize. This high- Figure 1. The relationship between g s and A derived from solving Eqns 9 and 10 for two different values of V (1 0 and 0 1 mol m 2 s 1 ). Values of both g s and A are normalized to 350 p.p.m. levels. Therefore, to the left of (1,1) c s < 350 p.p.m., that is, pre-present day, whilst to the right of (1,1) c s > 350 p.p.m., that is, post-present day. Contours join values of g s and A at particular values of c s in 100 p.p.m. increments. The following parameter values were used: A m =50µmol m 2 ; D = 20 mmol mol 1 ; R =0µmol m 2 s 1 ; G = 0 1 mol µmol 1 ; S =10m 2 s µmol 1. The inset figure shows the corresponding relationship between the absolute values of g s and A. The marked points correspond to c s = 350 p.p.m., V = 1 0 or 0 1 mol m 2 s 1.

6 644 A. J. Jarvis et al. lights some ambiguity in using water use efficiency to describe the response of gas exchange to increasing c s since this parameter makes no distinction between the source of changes in efficiency. THE IMPORTANCE OF DROUGHT Both c i and A may be reduced as a result of the closure of stomata during soil drying (Brodribb 1996), and also to a lesser extent when evaporative demand increases (Morison & Gifford 1983). The effect of increasing c s under these conditions can then be the alleviation of CO 2 supply limitations leading to the maintenance of physiological activity (Idso & Idso 1994). Consistent with this effect are the findings of Clifford et al. (1993). Working with peanut growing under a 300-p.p.m. elevation in c a these authors observed an increase of 16% in dry matter accumulation under well-watered conditions compared with an increase of 112% under water limitation. In Fig. 2 variations in g s and A are simulated during soil drying by increasing S in Eqn 9. Again, for simplicity variations in leaf temperature arising from changes in latent heat flux are assumed to be too small to affect A m, V and R significantly. This is now a somewhat less robust approximation since the large reductions in latent heat flux experienced as soils dry can result in significant increases in surface temperature in still air. However, since the variation in A m, V and R with both surface temperature and soil drying are poorly defined, the implications of these sources of variation will not be considered. As the soil dries, g s falls (Fig. 2 inset). When V is small the magnitude of the CO 2 supply alleviation with a doubling in c s is evenly distributed across a broad range of soil moisture due to the degree of linearity in the relationship between A and c i (Fig. 2). In contrast, when V is large the magnitude of the CO 2 supply alleviation with a doubling in c s is unevenly distributed across a range of soil moisture due to the degree of curvature in the relationship between A and c i (Fig. 2). From Fig. 2 we might conclude that plants characterized by a low V would benefit more from rising CO 2 under well-watered conditions whereas plants characterized by high V would be favoured by a degree of soil moisture deficit. Consistent with this suggestion Owensby et al. (1997) observed increased primary productivity from C4 grassland at elevated CO 2 only in dry years. Also, Campbell et al. (1995) observed a Figure 2. The relationship between the difference in A (normalized to A m ) at c s = 700 and 350 p.p.m. and S as described by Eqns 9 and 10. The inset graph is of the corresponding relationship between the g s and S at c s = 350 (solid lines) and 700 (dashed lines) p.p.m. used to derive the main figure. The broad lines relate to V = 1 0 mol m 2 s 1 whilst all thin lines relate to V = 0 1 mol m 2 s 1. A m =50µmol m 2 s 1 ; D = 20 mmol mol 1 ; R = 0 µmol mol 2 s 1 ; G = 0 1 mol µmol 1.

7 Stomatal behaviour, photosynthesis and transpiration under rising CO competitive advantage of C3 over C4 species under wellwatered conditions but noted that the situation was reversed by water stress. Any savings in evaporative water loss arising from stomatal closure as c s increases will be integrated over time, extending the period under which a particular water availability persists thereby acting to amplify these effects (Field et al. 1997; Owensby et al. 1997). This will particularly be the case for ecological units where individual species are hydraulically isolated. Here, we have assumed that increases in A are beneficial per se. However, there may be situations where translation of increases in A into increased leaf area may result in higher total rates of water loss than can be sustained by water transport mechanisms (Heath & Kerstiens 1997). Stomatal limitations of CO 2 supply as a result of soil drying can give rise to the need for the down-regulation of photosynthesis to avoid photo-inhibitory damage (Osmond 1994). In arguing for stomatal responses coupled to residual photosynthetic capacity (A m A) a parallel between stomatal function and photoinhibition can be made since both can be viewed as control loops operating to ensure A m A is maintained within acceptable limits, stomata controlling CO 2 supply and hence A while photoinhibition controls A m biochemically. Reductions in A m A brought about by increases in c a reduce the need for the down-regulation of photosynthetic capacity under drought conditions. As a result, reductions in A m, and hence A, g s and E, to facilitate photoprotection may occur at lower soil moisture availability with increasing c a. Plants characterized by low V will experience increases in A m A and the need to inhibit photosynthesis ahead of high V neighbours for a given soil moisture regime, again enhancing differences in plant behaviour with rising CO 2. ACCLIMATION OF STOMATAL RESPONSES TO CO 2 In the current context stomatal acclimation to rising CO 2 would be manifest through changes in G (and S at fixed soil moisture) since this would be equivalent to changes in the relationship between A m A and guard cell carbon signal transduction. Figure 3 shows data taken from S antru c ek & Sage (1996). If g s were some direct function of c i then the relationship in Fig. 3(a) would lead to the conclusion that growth in 750 p.p.m. CO 2 reduced stomatal sensitivity to CO 2 since no change in stomatal frequency was observed. However, we see from Fig. 3(b) that if the observed reduction in A m at the higher growth c a is accounted for in the data, then a single unique relationship between A m A and g s results. This indicates that the acclimation that has occurred is photosynthetic rather than stomatal and highlights the need for a full analysis of the photosynthetic properties of the leaf before identification of any stomatal acclimation can be made (Morison 1998). ACCLIMATION OF STOMATAL CHARACTERISTICS The upper limit on stomatal conductance, g mx, is determined by the spacing, dimensions and maximum aperture of the stomatal pores. Expanding Eqn 7 gives, g s =A m G GA A m SE + SEA. (12) Assuming g s = g mx is achieved when A m is at a true maximum, E = 0 and A = 0 then, g mx = A m G. (13) Figure 3. The relationship between (a) g s and c i and (b) g s and A m A for Chenopodium alba L. grown at 34 C and 350 ( ) or 750 ( ) p.p.m. and measured at 35 C. Data taken from Figs 3(b) &(c) and 4(b) &(c) of S antru c ek & Sage (1996). The fitted line in b is g s = 0 12/(15 3D +(A m A) 1 ) (see Eqn 5 in Jarvis & Davies (1998)) where D is the leaf surface H 2 O concentration gradient which was taken to be constant at 7 mmol mol 1. A m was initially estimated as 55 8 and 51 7 µmol m 2 s 1 for 350 and 750 p.p.m., respectively, again using the above equation. Since there was negligible difference in the fitted parameters between the two treatments other than A m, single estimates were derived for both data sets having taken into account changes in A m.

8 646 A. J. Jarvis et al. The conditions necessary for this state would be achieved when plants were placed under conditions of saturating light, optimal temperatures and when the gradients in CO 2 and water vapour concentration above the leaf are equal to zero. Under these conditions A m will be limited only by the photosynthetic biochemistry of the leaf. Equation 13 suggests a coupling between the upper limit of photosynthetic capacity and the stomatal characteristics of the leaf, namely, that the stomatal and photosynthetic apparatus develop in unison (Körner, Scheel & Bauer 1979). In the context of rising CO 2 any long-term changes in the photosynthetic properties of leaves will result in changes in stomatal dimensions and/or frequencies. Drake et al. (1997) have concluded that the observed reductions in photosynthetic capacity resulting from persistent exposure to a doubling of c a are of the order of 15%. Woodward & Kelly (1995) report an average reduction in stomatal frequency of 9% associated with an increase in growth of c a from 350 to 700 p.p.m. RESPIRATION AND STOMATA So far we have ignored the effects of respiratory CO 2. From Eqn 1 we see that increasing R acts to increase c i which in turn will increase A and reduce g s. In reviewing the published literature Drake et al. (1997) found that a doubling in c a reduces R by 20% on average. Therefore, one might expect a slight offset in the reductions in g s as c a increases, although the effect will be marginal during conditions when A m is significantly greater than R. However, when A m R at dawn/dusk or during severe stress this effect will become more pronounced. Considering an extreme case in terms of the system behaviour we have proposed, when A N 0 and A m R then A m A = A m R which is tending to zero. Therefore g s 0 and c i c a 0/0 or + in this case. Obviously, there must be physical upper limits on c i, but we see that all the biochemical demand for CO 2 is being met by respiration with no water loss. The condition A m R, g s 0, c i + represents an instability boundary in the system where the effects of additional control laws would come into play. The effect of a 20% reduction in R will be to shift this instability boundary to lower photosynthetic capacities. CONCLUSIONS In studies of the effects of c a on g s the convention has been to regard c i as a controlling variable. A simpler analysis would suggest that increases in A elicited by increasing c a are associated with linear decreases in g s indicating the operation of a negative feedback between the photosynthetic operation of the leaf and stomatal behaviour. The above conclusion suggests that while studies with isolated guard cells may reveal important components of the CO 2 response, interpretation of patterns of stomatal behaviour in a changing environment requires an understanding of the functioning of whole leaves and indeed whole plants since the correct synthesis of the inputs to this mechanism may be difficult to attain in vitro. We identify the importance of the quantity A m A in determining g s. The issue with regard to the effects of rising c a on g s is to predict the magnitudes of the resultant changes in c i and A and hence A m A, g s and E given a rise in c a. This analysis requires information on the shape of the A c i relationship. Under both present and elevated CO 2 this relationship will depend upon a broad range of environmental and plant factors including photosynthetic acclimation. Soil moisture availability can have significant effects on the relative gains to be achieved under rising CO 2. We predict that in wet soil, plants characterized by low V (C3) profit most in terms of carbon and water balance from a rise in c a. In drying soils, plants characterized by high V (C4) profit most in terms of carbon and water balance from a rise in c a. Such responses can potentially give rise to important changes in plant community structure. There are relatively few reports in the literature which suggest stomatal acclimation to rising CO 2 although it is now commonly accepted that photosynthetic acclimation will take place (Drake et al. 1997). We suggest that the observed dependence of stomatal behaviour on photosynthetic performance is likely to account for much apparent stomatal acclimation. This again highlights the need for a full analysis of the photosynthetic properties of the leaf before identification of any stomatal acclimation can be made. 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