Full Paper
Journal of Agricultural Meteorology 71 (2): 98-105, 2015
Evaluation of the effects of increasing temperature on the transpiration rate and canopy conductance of soybean by using the sap flow method Satoshi NAKANO a , †, Custodio R. P. TACARINDUA b , Keiichiro NAKASHIMA b , Koki HOMMA b and Tatsuhiko SHIRAIWA b a
NARO Agricultural Research Center, 3-1-1 Kannondai, Tsukuba, Ibaraki 305-8666, Japan b Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
Abstract This study aimed to investigate the effects of increasing temperature on the transpiration rate and canopy conductance of soybean grown in temperature gradient chambers under drought and wet conditions. The heat balance method was used to measure the transpiration rate from sap flow; additionally, canopy conductance was continuously estimated from the transpiration rate and vapor pressure deficit (VPD). An increase of 3℃ in temperature resulted in an increased transpiration rate but decreased canopy conductance. Further, the differences in canopy conductance observed at high and low temperature treatments were more remarkable during the morning than around noon. This suggested that there was concomitant increase in VPD with increasing temperature when solar radiation was low during the morning. Although the transpiration rate and canopy conductance decreased during drought conditions, the overall tendency of the response to the changes in temperature and VPD was similar to those in the well-watered condition. The partial correlation coefficients between canopy conductance and VPD were negative when the temperature effect was held constant. However, those between canopy conductance and temperature showed opposite trends in the two years of study—negative in 2011 but positive in 2012. These results suggest that the decrease of canopy conductance in a high temperature treatment is more likely caused by increasing VPD than by increasing temperature itself. Key words: Canopy conductance, Sap flow, Temperature, Transpiration rate, Vapor pressure deficit.
1. Introduction Recent studies have revealed the impact of projected global warming on soybean production in Japan under field-like conditions by using temperature gradient chambers (TGCs). In the cooler regions of Japan, increasing temperature improved leaf area and photosynthesis and increased the number of flowers, pods, and seeds in the late-maturing cultivars because of the longer flowering period (Kumagai and Sameshima, 2014). On the other hand, in the warmer regions, increasing temperature decreased the number of pods and seeds and the size of seeds because of the decline in dry matter production (Tacarindua et al., 2013). Tacarindua et al. (2013) suggested that increasing temperature reduced photosynthetic rates by reducing stomatal conductance. However, they could not differentiate between the effects of the concomitant increase in vapor pressure deficit (VPD) with increased temperature on stomatal conductance. The responses of stomatal conductance to local environmental conditions have been extensively studied because stomatal regulation plays an important role in the adaption of plants to changing environmental conditions and stress. Stomatal conductance was shown to have a negative relationship with VPD (Bunce, 1998). The mechanisms of the responses of stomatal conductance to VPD were believed to involve feedforward (changed when stomata sensed an increasing VPD) or feedback (changed when the tranReceived; October 16, 2014. Accepted; January 29, 2015. Corresponding Author:
[email protected]
†
DOI: 10.2480/agrmet.D-14-00046
spiration rate increased) processes (Bunce, 1996; Monteith, 1995; Streck, 2003). Further, stomatal conductance was found to have a negative relationship with CO2 concentrations (Bernacchi et al., 2006). Mott (1998) reported that the response of stomatal conductance to CO2 concentration is associated with the intercellular CO2 concentrations rather than with the CO2 concentrations at the leaf surface or in the stomatal pores. In addition, the stomata were found to respond to a soil moisture deficit by producing rootoriginated abscisic acid that regulates stomatal apertures (Liu et al., 2005). Exposure to ozone and peroxides decreased stomatal conductance and thus the photosynthetic rate in soybean cultivars having different sensitivities to air pollution stress (Chutteang et al., 2013). However, few studies have evaluated the direct effect of increasing temperature on stomatal conductance, and the mechanism associated with the response of stomata to high temperatures remains unclear (Damour et al., 2010; Reynolds-Henne et al., 2010). This is because increasing temperature simultaneously increases VPD, making it difficult to differentiate between the effects of high temperature and those of VPD (Weber et al., 1985; Greer, 2012; Li et al., 2012). In this study, we estimated canopy conductance, including stomatal and aerodynamic conductance, of soybean grown in TGCs on the basis of transpiration rate and VPD (Kostner et al., 1992; Kostner et al., 1996; Braun et al., 2010; Du et al., 2011). The results of the study were analyzed to evaluate the direct effects of increasing temperature on stomatal conductance by eliminating the effects of VPD. Further, we determined the effects of high temperature under wet and drought conditions by using different soil moisture treatments.
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S. Nakano et al.：Evaluation of increasing temperature on canopy conductance of soybean
2. Materials and Methods 2.1 Plant materials and growth condition Soybean (Glycine max (L.) Merr. cv. Enrei) was sown on 12 July in 2011 and 2012 in 0.25 m wide rows with an intra-row spacing of 0.25 m (plant density, 16 plant m-2) in the TGCs at the experimental farm of the Kyoto University, Kyoto City, Japan (35.0 °N, 135.5 °E). The TGCs were plastic-covered greenhouses (width, 2.5 m; height, 2.7 m; length, 25 m) with an air inlet at one end and exhaust fans at the other. The temperature gradients inside the TGCs were maintained along the longitudinal axis from near ambient temperature to several degrees higher by using solar radiation and an air heater. Two plots were set along the temperature gradient in each TGC: low (L) and high temperature (H). Soil moisture condition was controlled using a subsurface irrigation system to maintain well-watered (W) and drought (D) conditions. Drought was initiated at the early flowering stage (R1) by discontinuing irrigation around 6 August in 2011 and 2012. In 2011, three TGCs were used—two for W and the other for D. In 2012, two TGCs were used—one for W and the other for D. Temperature and relative humidity of each plot were measured using T-type thermocouples and a thin-film polymer humidity sensor (RTR-52; T & D, Matsumoto, Japan) under a force-ventilated radiation shield set at a height of 1.5 m. Although the wind speed in the TGCs was not measured, the design value of wind speed was calculated to be about 0.46 m s-1 on the basis of the ventilation fan capacity and the effective sectional area of the TGCs. Because our study was conducted on hot and sunny days in summer, the wind speed was adjusted to be close to the design value to maintain a temperature gradient in the TGCs. Solar radiation outside the TGCs was measured. The solar radiation transmittance into the TGCs was greater than at least 70%. The soil in the TGCs was classified as alluvial sandy loam, and the transpirable soil moisture was between 33% (field capacity) and 13% (Tacarindua et al., 2013). During the periods when transpiration was measured, the averages of soil moisture were about 25% in W and 15% in D treatments at 30 cm depth in both the years. After transpiration was measured, leaf area was measured using a leaf area meter (LI-3100; LI-COR, Lincoln, NE, USA), and the leaf area index (LAI) was calculated by multiplying the leaf area by canopy density. 2.2 Sap flow measurement and canopy conductance estimation Because the transpiration rate at the whole plant level could be measured continuously by using the sap flow method (Sakuratani, 1984; Sameshima et al., 1995; Nakano et al., 2010), canopy conductance was also estimated continuously. The whole plant transpiration rate was measured every 10 min and averaged for each hour by using sap flow measurements and the stem heat balance method. The sap flow sensors were mounted on the basal part of the stems of plants. For the stem heat balance method, a stem section was continuously heated, and the distribution of radial and vertical heat was measured. The convective heat transport by the sap stream and water flow in the sap was calculated from the thermal energy balance of the stem section (Sakuratani, 1984; Gerdes et al., 1994). All sensors were calibrated using the gravimetric balance method previously developed for potted soybean.
Additional details related to the measurement of sap flow have been reported by Nakano et al. (2010). Between 3 and 13 September 2011, sap flow was measured for four plants in W treatment and two plants in D treatment at H and L temperatures. Between 25 August and 11 September 2012, sap flow was measured at H and L temperatures for three plants each of W and D treatments. These periods corresponded approximately to the beginning of the seed filling stage of soybean. Canopy transpiration was estimated as follows (Sakuratani, 1987): Ec = E p × n ,
(1)
where Ec is the canopy transpiration rate (mm h-1), Ep is the whole plant transpiration rate measured using the sap flow method (mm plant-1 h-1), and n is the plant density. Canopy transpiration rate is known to be affected by the absorption of global solar energy by the canopy (Sakuratani, 1987). However, because the canopy coverage of soybean (cv. Enrei) almost reached 1.0 when LAI was 4.0 (Sameshima, 1995), the changes in LAI over 4.0 had little effect on canopy transpiration. Canopy conductance was estimated as follows (Kostner et al., 1996; Braun et al., 2010): gc =
P ρ G v Tk Ec × × a , D M w × 3600 Tk R
(2)
where gc is the canopy conductance for vapor (mol m−2 s−1), Ec is the canopy transpiration rate (mm h−1), D is VPD (kPa), ρ is the density of water (998 kg m−3), Gv is the gas constant for water vapor (0.462 m3 kPa kg-1 K-1), Tk is the air temperature on the absolute temperature scale (K), Mw is the molecular mass of water (18.02 g mol−1), 3,600 is obtained by the conversion of hours to seconds, Pa is the atmospheric pressure (101.3 kPa), and R is the gas constant (8.31 J mol-1 K-1). The third component involving Pa, Tk and R is obtained by the conversion of canopy conductance units from mm s−1 to mol m−2 s−1 (Monteith and Unsworth, 2008). Canopy conductance includes stomatal and aerodynamic conductance. However, because aerodynamic conductance is usually an order of magnitude larger than stomatal conductance, and the changes in aerodynamic conductance are relatively constant over time and temperature differences, the differences between canopy conductance and stomatal conductance are small (Kostner et al., 1996; Homma et al., 1999). Inoue (1987) showed that the transpiration rate divided by VPD reflected the corresponding changes in the photosynthetic rate under a wide range of environmental and crop conditions at the leaf chamber level. The partial correlation coefficient was calculated to assess the strength of the relationship between canopy conductance and meteorological factors after other variables were adjusted as follows (Stuart and Ord, 1991): rxy⋅ z =
rxy − rxz r yz 2 2 (1 − rxz ) (1 − r yz )
,
(3)
where rxy·z is the partial correlation coefficient, which indicates the strength of the relationship between x and y when the effect of z is held constant, and rxy, rxz, and ryz are simple correlation coefficients between x and y, x and z, and y and z, respectively.
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Journal of Agricultural Meteorology 71 (2), 2015 even for D treatment. The differences between H and L temperatures were maintained at 2 – 3℃ throughout the day. The dynamics of VPD were reflected in those of temperature, but they were not completely synchronized in 2011. Although the canopy transpiration rate at H temperature was higher than that at L temperature, except for W treatment in 2011, the canopy conductance was lower at H temperature than at L temperature. Accordingly, the differences in canopy transpiration rate between H and L temperatures resulted from the difference in VPD between the two treatments. The trend of diurnal variation of canopy conductance was almost equal across both the years and water conditions; canopy conductance peaked during the morning
3. Results
Canopy transpiration (mm h-1)
3.1 Diurnal variation The diurnal courses of canopy transpiration rate, temperature, VPD, and canopy conductance in W and D treatments on average sunny days, which were selected for having daily solar radiation greater than 10 MJ m−2 d−1, are shown in Figs. 1 and 2 LAI at L and H temperatures were 10.1 and 8.0 in 2011 and 7.7 and 7.3 in 2012 for W treatment, and 6.0 and 5.7 in 2011 and 5.3 and 5.6 in 2012 for D treatment, respectively. Although water shortage caused the LAI for D treatment to be slightly smaller than that for W treatment, the LAI was high enough to reach canopy closure 2011 (n = 5)
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Fig. 1. Diurnal courses of canopy transpiration rate, temperature, vapor pressure deficit, and canopy conductance in well-watered treatment (W) on average sunny days when daily solar radiation was greater than 10 MJ m−2 d−1. Error bars represent standard errors for means. L: Low temperature, H: High temperature. n indicates the number of days for which data were averaged. * indicates the significant difference in canopy conductance between the L and H temperatures at the 5% level according to unpaired Student’s t-test.
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S. Nakano et al.：Evaluation of increasing temperature on canopy conductance of soybean
Canopy transpiration (mm h-1)
and then gradually decreased in the afternoon. In the morning, between 06:00 and 09:00 h, the difference in canopy conductance was 28% lower at the H temperature than at the L temperature across both the years and water conditions. However, at noon, when the temperature peaked and exceeded 35℃ in the H treatment, the differences in canopy conductance between H and L temperatures were smaller than those during the morning. The canopy transpiration rates in D treatment were 40.4% and 42.8% lower than those for W treatment at H and L temperatures, respectively. The canopy conductance in D treatment was 50.0% and 48.0% lower than that in W treatment at H and L temperatures, respectively. Changes in soil moisture, but not temperature, affected the transpiration rate and canopy conductance. 2011 (n = 5)
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3.2 Responses to meteorological factors The hourly canopy transpiration rate was associated more closely with the changes in solar radiation than with those in VPD in the W treatment in 2011 and 2012 (Fig. 3). Although the relationship between the canopy transpiration rate and solar radiation was linear, that between canopy conductance and solar radiation was non-linear and reached a plateau during the periods of high radiation of about more than 400 W m−2. The differences in canopy conductance between L and H temperatures were the largest when solar radiation was around 200 to 300 W m−2, but those differences diminished when the radiation level exceeded 500 W m−2. The upper limit of canopy conductance decreased when the VPD exceeded about 1 kPa. Although the canopy transpiration
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Fig. 2. Diurnal courses of canopy transpiration rate, temperature, vapor pressure deficit, and canopy conductance in drought treatment (D) on average sunny days when daily solar radiation was greater than 10 MJ m−2 d−1. Error bars represent standard errors for means. L: Low temperature, H: High temperature. n indicates average day number. * indicates the significant difference in canopy conductance between L and H temperatures at the 5% level according to unpaired Student’s t-test.
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Journal of Agricultural Meteorology 71 (2), 2015 both the years and soil moisture conditions. On the other hand, although the partial correlation coefficients between canopy conductance and VPD remained constant, those between canopy conductance and temperature exhibited contrasting results in both the years. The values of the partial correlation coefficients between canopy conductance and temperature were smaller in D treatment than in W treatment, but the tendency of the coefficients did not change with the difference in soil moisture conditions. The relationship between canopy conductance and temperature is shown in Fig. 5 The effect of the change in VPD was reduced
Canopy conductance (mol m-2 s-1)
Canopy transpiration (mm h-1)
rate and canopy conductance in D treatment were restricted due to the low soil moisture, the responses to solar radiation and VPD exhibited the same tendency as those in the W treatment as mentioned above (Fig. 4). Correlation analysis was conducted between canopy conductance and the meteorological factors of temperature and VPD (Table 1). The effect of the changes in solar radiation were reduced by selecting data that had been collected when the solar radiation exceeded 500 W m−2. The correlation coefficients between canopy conductance and both temperature and VPD were negative for
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Fig. 3. Relationships between canopy transpiration rate, canopy conductance, and meteorological factors in well-watered treatment (W) on average sunny days when daily solar radiation was greater than 10 MJ m−2 d−1. L: Low temperature, H: High temperature.
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Fig. 4. Relationships between canopy transpiration rate, canopy conductance, and meteorological factors in drought treatment (D) on average sunny days when daily solar radiation was greater than 10 MJ m−2 d−1. L: Low temperature, H: High temperature.
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S. Nakano et al.：Evaluation of increasing temperature on canopy conductance of soybean
Table 1. Correlation coefficient between canopy conductance and temperature and vapor pressure deficit (VPD) when solar radiation was abundant, i.e., exceeded 500 W m−2. W: Well-watered, D: Drought. n indicates the number of data points. Canopy conductance Partial correlation coefficient to VPD canopy conductance1 2011[W](n = 30) Temperature 0.798** -0.581** -0.871** VPD -0.909** -0.724** -0.466** 2012[W](n = 72) Temperature 0.949** 0.608** VPD -0.646** -0.729** 2011[D](n = 30) Temperature 0.914** -0.383* -0.719** VPD -0.658** -0.005 -0.512** 2012[D](n = 72) Temperature 0.957** 0.483** VPD -0.646** -0.628** 1 Partial Correlation coefficients for the temperature values indicate the relationship between canopy conductance and temperate with the effect of VPD held constant. ‘*’and‘**’ indicate that the slopes of the correlation coefficients are significant at the 5 and 1% levels, respectively.
Canopy conductance (mol m-2 s-1)
and the effect of temperature was directly elucidated by conducting linear regression analysis between canopy conductance and temperature by categorizing VPD into five classes by 0.5 kPa (Fig. 5). Although increasing temperature decreased the canopy conductance irrespective of the difference in VPD, an opposite relation was obtained for W treatment in 2012; that is, increasing temperature resulted in increased canopy conductance at high temperatures of over 30℃ at VPD of 2.0 – 2.5 kPa. These results were consistent with those of the partial correlation coefficient for canopy conductance, as shown in Table 1.
2.0 1.5
This study investigated whether canopy conductance was affected by increasing temperature irrespective of the changes in VPD. Although several studies have shown that increasing VPD results in decreased stomatal or canopy conductance, data related to the direct effects of temperature on stomata are lacking, especially, at the whole plant level. Differentiating between the effects of these two factors has been difficult because temperature and VPD usually change simultaneously under field-like conditions (Weber et al., 1985; Okada et al., 1995). Although even our data
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4. Discussion
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Fig. 5. Relationships between canopy conductance and temperature revealed by categorizing vapor pressure deficit (VPD) into five classes by 0.5 kPa when solar radiation was abundant, i.e., exceeded 500 W m−2. Regression lines are included and points are enlarged when the slopes of the correlation coefficients are significant at the 5% level. W: Well-watered, D: Drought. n indicates data number. * and ** indicate significant correlations at the 5 and 1% levels, respectively.
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Journal of Agricultural Meteorology 71 (2), 2015 could not completely differentiate the effects of changing temperature and VPD under field-like conditions, we attempted to evaluate the direct effect of temperature on canopy conductance by using continuous data related to canopy conductance obtained under variable meteorological conditions. Our results showed that canopy conductance peaked during the morning, and the differences between L and H treatments were more remarkable during the morning than around noon (Figs. 1 and 2). The restriction of the increasing canopy conductance at H temperature was likely caused by the environment during not only the morning but also the previous night, because VPD and temperature remained higher at H temperature during the night in the TGCs. Although we could not identify whether the morning or the previous night environment had more effect on canopy conductance, our results suggested that stomatal apertures are susceptible to high temperature or VPD during the morning. The relationships between canopy conductance and meteorological factors, such as solar radiation and VPD, were obtained continuously for a broad range of conditions from the canopy transpiration rate measured using the sap flow method (Figs. 3 and 4). The non-linear relationship between canopy conductance and solar radiation was similar to that suggested by Munkhtsetseg et al. (2008) for field measurement of soybean. The response of canopy conductance to solar radiation showed that the differences between L and H temperatures were more remarkable at low radiation (200 – 300 W m–2) than at high radiation (over 500 W m–2). The solar radiation from 200 to 300 W m–2 corresponds to the time from 07:00 to 08:00 h in the morning or from 14:00 to 15:00 h in the afternoon, and 500 W m–2 corresponds to the time from 11:00 to 12:00 h noon. Because the differences in canopy conductance between L and H temperatures were more remarkable during the morning than during the afternoon even under similar radiation conditions, solar radiation was thought to have little effect on the difference of canopy conductance between L and H temperatures. The response of canopy conductance to VPD was largely scattered and was not clearly differentiated between L and H temperatures. Wilson and Bunce (1997) reported that the sensitivity of stomatal conductance to VPD decreased from 25 to 30℃, but remained constant from 30 to 35℃. Because the temperature exceeded 30℃ even at the L temperature around noon (Figs. 1 and 2), there were no differences in sensitivity of canopy conductance to VPD between L and H temperatures. The canopy transpiration rate and canopy conductance in D treatment were smaller than those in W treatment. However, the diurnal variation and the response to meteorological factors mentioned above were not remarkably different between the two treatments; there was no interaction between high temperature and drought stress in our study. In our study, canopy conductance decreased with increasing temperature and VPD, although the partial correlation coefficient between temperature and canopy conductance indicated contrasting relationships for the two years despite the drought stress (Table 1 and Fig. 5). If increasing temperature has a certain direct effect on canopy conductance, interpreting the change in the partial correlation coefficient between temperature and canopy conductance from negative in 2011 to positive in 2012 is difficult. The partial correlation coefficient between VPD and canopy con-
ductance indicated that there is a constant negative relationship regardless of the change in temperature. These results suggest that increasing temperature has no direct effect on canopy conductance even under changing VPD conditions. The influence of increasing temperature on both canopy and stomatal conductance under high temperature conditions has not been clearly understood. Stomatal opening and decrease in stomatal resistance, which implies the reciprocal of stomatal conductance, were observed under high temperatures, allowing the plants to avoid heat stress (Homma et al., 1999; Reynolds-Henne et al., 2010). In contrast, increasing temperature did not have a significant impact on stomatal conductance (Greer, 2012; Li et al., 2012). Seversike et al. (2013) showed that the slope of transpiration response to VPD, which somewhat corresponded to canopy conductance, decreased when the VPD increased above 1.9 kPa at 25℃ at the whole plant level in soybean. However, transpiration was not restricted at higher VPD when the temperature was over 30℃. They suggested that this response was caused by the change in plant hydraulic conductance controlled by an aquaporin that is sensitive to temperature. In our study, the positive relationship between canopy conductance and temperature noted in 2012 can be thought to have been caused by the lowering of the restriction of canopy conductance at higher VPD by high temperature, because the temperature in 2012 was higher than that in 2011, i.e., exceeded 30℃ (Fig. 5). In conclusion, canopy conductance of soybean decreases in response to a slight increase in temperature in summer in Kyoto, a warm region of Japan. This response is associated with an increase in VPD rather than because of an increase in temperature itself. Our results suggested that the reduction of stomatal conductance, as indicated by Tacarindua et al. (2013), might have resulted from the concomitant increase in VPD with increased temperature. On the other hand, the decrease in seed size because of the reduced number of cells per cotyledon (Tacarindua et al., 2012) was likely caused by increasing temperature. Because controlling VPD when temperature gradient is the primary variable in a TGC is difficult (Okada et al., 1995), distinguishing between the effects of increasing temperature and VPD to assess the impacts of global warming under field-like conditions, especially for VPD-sensitive factors such as stomatal conductance, is difficult although necessary.
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