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- Materials and Methods
Stomata orchestrate one of plant biology’s greatest concerts; microscopic pores on the leaf surface through which, each year, pass 122 Gt of carbon and enough water vapor to more than equal the annual flow of all rivers on earth (Baumgartner & Reichel, 1975; Post et al., 1990). Given the magnitude of these fluxes, it is understandable that stomata have historically occupied a critical position in the study of plant responses to global environmental change, including many studies designed to quantify the responses of plants and ecosystems to elevated CO2 (Baker & Allen, 1994; Saxe et al., 1998; Norby et al., 1999). To the extent that stomatal responses are involved in determining CO2-induced enhancements of photosynthesis (Rey & Jarvis, 1998; Gunderson et al., 2002; Noormets et al., 2001), differences in stomatal conductance caused by CO2 have been of interest in the study of terrestrial carbon dynamics. Stomata and their response to elevated CO2 have also been the focus of multiscale investigations related to transpiration, water-use efficiency and ecosystem water use (Jackson et al., 1994; Tognetti et al., 1998; Eamus, 1999; Wullschleger et al., 2002). There was so much interest in the response of stomata to elevated CO2 in the mid-1990s that experimental observations that stomatal resistance might increase 50% with a doubling of atmospheric CO2 were quickly incorporated into land-surface models for addressing potential CO2-induced interactions between terrestrial ecosystems and climate (Henderson-Sellers et al., 1995; Pollard & Thompson, 1995; Sellers et al., 1996).
As the spatial and temporal scale of our measurements and experiments has increased, so too has our perception of how stomata are involved in regulating the carbon and water cycles at large spatial scales and over long periods of time (Field et al., 1995; Wilson et al., 1999). It is now generally recognized that while certain ecosystems are especially responsive to elevated CO2 concentrations (Bremer et al., 1996; Field et al., 1997), other systems are not (Ellsworth et al., 1995). Interestingly, this difference may not be directly dependent on whether elevated CO2 elicits a major response in stomatal conductance (Niklaus et al., 1998), and conclusions must inevitably account for higher-order changes in leaf area index and boundary layer considerations (Wilson et al., 1999). Physiological feedbacks are also important (Sellers et al., 1996; Wilson et al., 1999), as are interactions between climate (e.g. vapor pressure deficit) and stomatal conductance. Furthermore, the scale at which the relationships between CO2 concentration, stomatal conductance and ecosystem water use are observed may also shape our perspective of how one process affects the others.
We have previously reported for a 12-year-old sweetgum (Liquidambar styraciflua L.) plantation that canopy transpiration measured by sap-flow techniques is reduced at elevated CO2 concentration (Wullschleger & Norby, 2001). This response was less, however, than might be anticipated based solely on leaf-level measurements of stomatal conductance (Gunderson et al., 2002). Here, we expand these analyses to include processes that take place at spatial scales larger than individual leaves, and integrate insights from leaf and canopy measurements to assess how stomatal conductance, canopy transpiration and conductance, and evapotranspiration may be affected in a future, higher CO2 world. In keeping with previous theoretical and/or modeling discussions (Field et al., 1995; Raupach, 1998; Wilson et al., 1999), we explore the possibility that the hydrological response of a closed-canopy forest to elevated CO2 may depend on the scale of observation, and that interacting variables (e.g. radiation, vapor pressure deficit and soil water potential) and integration of processes over time and space will collectively act to reduce what at the leaf level might otherwise appear to be a large and significant response.
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- Materials and Methods
A common expectation from many, albeit not all, studies that address the physiological response of plants to elevated CO2 is that stomatal conductance will be reduced. In herbaceous species, these reductions can approach 27–40% (Morison, 1985; Field et al., 1995), whereas in some coniferous species the response may be considerably less (Ellsworth, 1999; Teskey, 1995; Tissue et al., 1997). In addition, stomata are also highly responsive to other environmental variables, such that high vapor pressure deficits, drying soils and low light may all act to reduce gs from its theoretical maximum. Within this matrix of interactions, the complex response of stomatal conductance to CO2 enrichment must be considered and integrated to understand the impacts of environmental change at higher scales. In this study, the mean 22–24% decrease in gs by elevated CO2 was comparable to means reported across multiple woody species, including appreciable variation within and among studies (e.g. 20–23%; Field et al., 1995; Drake et al., 1997; Medlyn et al., 2001). Although reductions in gs were smaller in magnitude and less statistically robust than concurrent increases in photosynthesis, they were similarly sustained over three growing seasons (Gunderson et al., 2002), indicating that stomatal sensitivity to elevated CO2 was not lost over time. Stomatal interactions with environmental variation over the course of the day and the growing season such as those we observed for sweetgum trees doubtlessly contributed to the lack of statistical significance on individual dates, and may contribute to the often ambiguous effects on gs observed in woody species (Curtis & Wang, 1998), where stomatal responses tend to be smaller than in herbaceous plants (Gunderson et al., 1993; Beerling et al., 1996; Heath, 1998; Rey & Jarvis, 1998; Saxe et al., 1998; Ellsworth, 1999; Norby et al., 1999).
A decrease in gs with depth in the canopy is a common observation in trees growing in a closed-canopy forest or plantation (Whitehead, 1998). It reflects the fact that leaves in the lower canopy are older, often possess lower nitrogen concentrations and are, as a result, less physiologically active than are upper-canopy leaves (Warren & Adams, 2001). In addition, lower-canopy leaves are exposed to vastly different environmental conditions, including radiation, than are upper-canopy leaves and this too can preclude maximal stomatal function (Leuning et al., 1995). In the case of the closed-canopy sweetgum plantation studied here, our observation that gs decreases with depth in the canopy primarily reflects lower light availability (Gunderson et al., 2002). More interesting perhaps is the observation that not only was the absolute magnitude of gs dependent on canopy position, but so too was the relative difference in gs between CO2 treatments. Although variability was admittedly high and differences not always significant, marked reductions in gs observed in upper-canopy leaves at elevated CO2 were not typically seen at middle or lower canopy positions. Since so few studies have been conducted on closed-canopy stands exposed to atmospheric CO2 enrichment, the observation that the effect of elevated CO2 on gs is dependent on radiation regime is unique. Herrick & Thomas (1999, 2001) examined the effects of elevated CO2 on photosynthesis of sun and shade leaves in sweetgum trees at the Duke University FACE facility, and argued that conclusions about the response of plants to elevated CO2 must take into account the complex nature of the light environment within a canopy and how light interacts with CO2 to affect photosynthesis. We extend this argument to stomatal conductance and suggest that CO2-induced reductions in gs may also be dependent on canopy light environment. If this is shown to be true, such a response would have important implications for how effects of elevated CO2 on stomatal conductance measured on only upper-canopy leaves should be scaled throughout plant canopies. It would also have relevance to the sensitivity of understory vegetation to elevated CO2 (DeLucia & Thomas, 2000) where low light may limit some physiological responses of plants to CO2 enrichment.
Since stomatal conductance of upper-canopy leaves was sensitive to atmospheric CO2 enrichment, whereas mid- and lower-canopy leaves were less so, it is expected that only moderate effects of elevated CO2 would be observed on canopy conductance. Treatment differences in gc ranged from +6 to –34% and averaged –14% over the growing season. This agrees, as it should, with our previous findings that sap velocity and stand transpiration were only moderately responsive to elevated CO2 (Wullschleger & Norby, 2001). Ellsworth et al. (1995) reported no effect of elevated CO2 on sap velocity in loblolly pine (Pinus taeda L.) and others have reported that treatment differences in sap velocity or whole-tree water use are difficult to detect (Senock et al., 1996; Kellomäki & Wang, 1998). Such detection difficulties were attributed in our earlier paper to the dependency of stand transpiration on prevailing weather conditions, particularly vapor pressure deficit and radiation (Wullschleger & Norby, 2001). Others have drawn similar conclusions about whole-tree and canopy transpiration, but few studies have been conducted such that the response of canopy conductance to ambient and elevated CO2 could be explicitly compared. Pataki et al. (1998) reported an 8% reduction in sap velocity for 4-year-old loblolly pines exposed in open-top chambers to a +300 ppm increase in atmospheric CO2 and a similar, albeit highly variable, decrease in mean daily canopy conductance. Estimates of daily gc in the study of Pataki et al. (1998) varied between 9 and 16 mmol m−2 s−1 (all-sided leaf area) and all measurements were taken during periods of the year when mean daily air temperatures did not exceed 10°C. A combination of low temperatures and inherently low gc for small pine saplings, compared with the environmental and growth conditions of our study, may have limited a response to elevated CO2 in their study. Nonetheless, our results agree with the general conclusions drawn by Pataki et al. (1998) that canopy conductance in loblolly pine, and now in sweetgum, was only marginally affected by the CO2 treatments imposed.
Vapor pressure deficit was the most significant environmental influence on leaf gas exchange and gs in both CO2 treatments of this study, explaining more variation than either temperature, radiation, or soil water potential (Gunderson et al., 2002). A similar observation was made for canopy conductance, as daily variability in δe explained approximately 75% of total variation in measured canopy conductance. Our observation that gs and gc decline exponentially with increasing δe is consistent with relationships found in a variety of leaf, whole-tree and stand-level studies (Köstner et al., 1992; Granier et al., 1996; Köstner et al., 1996). It is interesting that based on our data, the equations and associated parameters used to describe the dependency of both gs and gc on δe (i.e. Oren et al., 1999) were different between leaves and trees measured in the two CO2 treatments. Application of Eqn 3 to available data sets indicated that the sensitivity of both gs and gc to increasing δe was, on average, 20% lower at elevated than it was at ambient CO2 concentration, as were estimates of gs and gc at a reference δe of 1.0 kPa. Tognetti et al. (1999) and Heath (1998) both reported reduced sensitivity of stomata to δe for trees growing in CO2-enriched atmospheres, whereas Kellomäki & Wang (1998) suggested that a decrease in sap flow at elevated CO2 was largely due to a CO2-induced increase in stomatal sensitivity to high vapor pressure deficit. Morison (1998) points out that the response of stomata to elevated CO2 is important in understanding not only stomatal physiology, but also in understanding plant–atmosphere interactions at scales from the individual plant to global vegetation. Unfortunately, few studies have addressed stomatal acclimation to elevated CO2 or examined the specific sensitivity of either gs or gc to δe (Drake et al., 1997). Despite this lack of information, our data suggest that the sensitivity of gs and gc to δe, at least as defined in Oren et al. (1999), does decline with atmospheric CO2 enrichment. Such leaf- and canopy-scale observations are in general agreement with conclusions drawn from a variety of studies (Hollinger, 1987; Will & Teskey, 1997; Heath, 1998; Tognetti et al., 1998).
Estimates of gs and gc obtained across a range of vapor pressure deficits and soil water potentials indicated that the effects of elevated CO2 on these parameters becomes less as gs and gc are reduced in absolute magnitude. Differences between treatments that were 25–35% at low δe and ample soil moisture, were more typically less than 10% under conditions of high δe and drought. Comparatively small CO2-induced reductions in gs have elsewhere been associated with species having intrinsically lower gs (Morison, 1985; Saxe et al., 1998), with dry season conditions, when δe was high and gs was low (Goodfellow et al., 1997), and with warm sunny days with high δe (Beerling et al., 1996; Heath, 1998). All of these results are consistent with the observation by Curtis (1996) that reductions in gs due to CO2 tend to be less in stressed plants. Pataki et al. (2000) observed that stomatal conductance in plants at a free-air CO2 enrichment experiment in an undisturbed Mojave Desert ecosystem was reduced in the high CO2 treatment, although the effect was apparent only under conditions of ample soil moisture. Similarly, Ellsworth et al. (1995) suggested that stomatal closure in Pinus taeda under high CO2 concentration, which was found to be minimal under drought conditions, may be more pronounced when soil moisture is abundant. Although this conclusion was refuted by Pataki et al. (1998) our results suggest that as gs and gc become less, so too does the magnitude of the CO2 affect. Stratification of available data indicated that the per cent change in gc due to elevated CO2 for conditions where gc was > 150 mmol m−2 s−1 was –28%, whereas within the range of 50–150 mmol m−2 s−1 it was roughly –15% and at < 50 mmol m−2 s−1 it was only −10%. We conclude that any condition that decreases the absolute magnitude of stomatal or canopy conductance, including vapor pressure deficit, soil water availability, or canopy position, will also reduce the effect that elevated CO2 has on these exchange processes.
Changes in whole-plant water use under high CO2 are of interest for predictions of large-scale water vapor fluxes, as well as stand growth and composition under future elevated concentrations of atmospheric CO2 (Pataki et al., 1998). In canopies with high leaf area index, boundary layer and aerodynamic conductance may exert a stronger control on water vapor exchange than stomatal conductance, so that any change in gs induced by elevated CO2 may only marginally affect transpiration and hence, stand water use. Niklaus et al. (1998) reported that ecosystem-level controls of the water balance can, in responsive systems such as grasslands, far outweigh the physiological effects of elevated CO2 observed at the leaf level. Our observation that the daily decoupling coefficient or Ω was high during mid-summer suggests that changes in gs due to elevated CO2 may lead to only marginal reductions in transpiration. For example, for a closed-canopy forest with an Ω of 0.5, a 24% change in stomatal conductance for leaves exposed to CO2 enrichment would result in only a 12% change in transpiration. Such a partial uncoupling of CO2-induced effects on gs at the level of individual leaves from associated impacts on transpiration at the scale of the canopy were, in our study, the result of low wind speeds that contributed to relatively low estimates of aerodynamic conductance.
In speculating about the effects of elevated CO2 on forest hydrology and evapotranspiration (ET), it is important to consider that not all components of ET will be affected in a CO2-enriched atmosphere. Interception losses and soil evaporation might not change with rising CO2 concentration, particularly in a closed-canopy plantation such as the one we studied where leaf area index was not different between ambient and elevated CO2 (Norby et al., 2001). Using estimates of annual transpiration from Wullschleger & Norby (2001) and modeled estimates of interception losses and soil evaporation, we calculate that annual ET would be 745 mm and 689 mm for the ambient and elevated CO2 treatments, respectively (Table 3): a difference of only 7% for the year. Wilson et al. (1999) emphasized in a modeling study that feedbacks associated with changing leaf area and soil moisture due to elevated CO2 were important considerations in understanding effects of CO2 enrichment on ET and showed that the impact of these factors on ET for agricultural crops could be significant. There has been a trend for slightly higher soil water potential (and content) in the elevated CO2 plots of our study (Gunderson et al., 2002), but differences between treatments have not been significant. Although our calculations, as presented in Table 3 are speculative, we suspect that feedbacks associated with leaf area and soil moisture will play only minor roles in determining annual rates of ET for closed-canopy forests exposed to elevated CO2 concentration. Nonetheless, future studies should (as best they can) include efforts to monitor all components of ET (Field et al., 1995).
Table 3. Estimated rates of annual evapotranspiration for a closed-canopy sweetgum stand exposed to ambient and elevated CO2 concentration
|Treatment||Transpiration (mm)||Interception (mm)||Evaporation (mm)||Evapotranspiration (mm)|
|Change (%)|| −10||–||–|| −7|
Decreases in estimated ET at elevated CO2 are theoretically less than decreases in single-leaf gs not only because of canopy decoupling, but also because of negative feedbacks associated with in-canopy vapor pressure deficit (Jarvis & McNaughton, 1986). As the spatial scale increases from stomata to canopy, and atmospheric transport processes become more limiting, thermodynamic considerations suggest that the lower gs at elevated CO2 will result in higher leaf temperatures and lower humidity in the canopy. This feedback acts to increase the driving force for transpiration (δe) and partly counteracts decreases in stomatal conductance. Midseason values of the decoupling coefficient of 0.5, which are an indication of the magnitude of this feedback, suggest that canopy transpiration rates may only be 50% as large as a change in stomatal conductance. Although the use of the ‘decoupling coefficient’ is not strictly valid for small plots, such as the FACE rings, feedbacks associated with canopy temperature and humidity are nonetheless likely. It is also likely that the feedback associated with Ω is smaller in the FACE plots than it would be in more extensive canopy. As a result, CO2-induced decreases in ET would be even less in more natural settings. Similar feedbacks at even larger scales, such as in a region with a diameter of several kilometers that is mostly forested, would further diminish the CO2 effect on ET (Jacobs & De Bruin, 1997; Wilson et al., 1999).
Finally, natural ecosystems provide a critical biotic feedback between the Earth’s terrestrial vegetation and our ever-changing climatic system. One is very much dependent on the other, and large-scale studies that examine the dynamic and often complex interaction between vegetative surfaces and the atmosphere are needed. A feedback of critical importance to the study of climate change is the hydrological response of forests to rising CO2 concentration. Few studies, however, have investigated this response at relevant temporal and spatial scales. Our results show that the response of gs to elevated CO2 in a fluctuating environment is indeed complex, and that simple reductions in gs with rising CO2 are dampened or accentuated depending on canopy location and interactions with vapor pressure deficit, soil water potential and canopy position. It is also clear that as the scale of observation increased, there was a general decline in the relative magnitude to which elevated CO2 impacts processes related to forest water use. Thus, we conclude that despite large effects of elevated CO2 on stomatal conductance, the influence of these effects on ET and larger-scale patterns of water use are likely to be minimal in forests that approximate conditions of the sweetgum plantation studied in this investigation.