Interactive effects of free-air CO2 enrichment and drought stress on maize growth

Europ. J. Agronomy 52 (2014) 11–21

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Interactive effects of free-air CO2 enrichment and drought stress on maize growth Remy Manderscheid ∗ , Martin Erbs, Hans-Joachim Weigel Institute of Biodiversity, Johann Heinrich von Thunen-Institute, Federal Research Institute for Rural Areas, Forestry and Fisheries, Bundesallee 50, D-38116 Braunschweig, Germany

a r t i c l e

i n f o

Article history: Received 31 August 2011 Received in revised form 8 December 2011 Accepted 19 December 2011 Keywords: CO2 concentration Climate change Growth Maize Radiation use efficiency Water use efficiency

a b s t r a c t Predicting future maize yields requires quantifying anticipated climate change impacts on maize growth and yield. In the present study, maize was grown over 2 years (2007 and 2008) under sufficient (WET) and reduced water supply (DRY) and under ambient (378 ␮l l−1 , AMB) and elevated (550 ␮l l−1 , FACE) atmospheric CO2 concentration ([CO2 ]) using free air CO2 enrichment (FACE). The objective of the present study was to test the hypothesis that maize growth does not respond to elevated [CO2 ] under WET but under DRY conditions due to an increase of water use efficiency (WUE) of biomass production realized through reduced transpiration. Moreover, in 2008 soil cover was varied to test whether mitigation of evaporation by straw mulch increases the CO2 effect on WUE. The DRY treatment received 12% and 48% less water than the WET treatment in 2007 and 2008, respectively, which was achieved with the aid of rainout shelters. In the first year, drought stress was insignificant and crop growth was similar among the two watering regimes. CO2 enrichment did not affect crop growth in 2007 and also in the WET treatment of 2008. In the second year, a pronounced drought stress decreased green leaf index, accumulated seasonal radiation absorption and radiation use efficiency (RUE) significantly. However, these effects were mitigated by CO2 enrichment and the decrease of RUE was higher under AMB (−18%) than under FACE (−2%) conditions. In the DRY treatment in 2008, CO2 enrichment significantly increased final biomass (+24%) and grain yield (+41%) as compared to the DRY AMB treatment. CO2 enrichment significantly increased soil water content under WET and DRY conditions but did not affect the soil water exploitation. There was a significant interaction of [CO2 ] and water supply on WUE with no (2007) or a small CO2 -response (+10% in 2008) under WET and a strong effect under DRY conditions in 2008 (+25%). Soil cover did not intensify the CO2 effect on WUE. It is concluded that maize will benefit from the increase in [CO2 ] only under drought but not under sufficient water supply. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Atmospheric CO2 concentration [CO2 ] has increased from about 280 ␮l l−1 in pre-industrial times to 385 ␮l l−1 today and is predicted to reach 550 ␮l l−1 in the middle of this century (Meehl et al., 2007). These changes are expected to rise air temperature and may increase the frequency of extremes, including drought conditions, which will have significant consequences for crop growth and food supply in the future (Easterling et al., 2007). Maize is the most important crop species in terms of global production and comes a close second after wheat in terms of globally cultivated area (FAOSTAT, 2009). By 2020, global demand for maize as a food supply is projected to exceed that for wheat or rice, making it the world’s most important crop (Pingali, 2001). Moreover, this crop is increasingly being used not only for food and feed but also to produce biofuels. Despite this importance of maize in global agricultural

∗ Corresponding author. Tel.: +49 (0)531 596 2579; fax: +49 (0)531 596 2599. E-mail addresses: [email protected] (R. Manderscheid), [email protected] (M. Erbs), [email protected] (H.-J. Weigel). 1161-0301/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.eja.2011.12.007

production there is a lack of experimental studies addressing the response of this crop to changes in atmospheric CO2 concentration and water availability (Leakey, 2009). The rise of [CO2 ] produces an increase of the intracellular CO2 concentration of the leaf which induces a decrease of stomatal conductance and an increase of photosynthesis in C3 plants (Ainsworth and Rogers, 2007). Photosynthesis of C4 species is CO2 saturated at the current [CO2 ], and thus, photosynthetic CO2 uptake theoretically should not respond to elevated [CO2 ] (Ghannoum, 2009). Several CO2 enrichment studies with maize done under controlled environment conditions showed an increase of C4 photosynthesis under sufficient water supply (Kang et al., 2002; Driscoll et al., 2006; Ziska and Bunce, 1997) while others did not (Rogers et al., 1983; Kim et al., 2007). Similar findings have been obtained with other C4 plants (Leakey, 2009). Up to now there have been free air CO2 enrichment (FACE) experiments with C4 crops only at two sites in the United States, in which sorghum (Arizona) and maize (Illinois) were cultivated in the field under different [CO2 ]. In the sorghum-FACE study CO2 enrichment produced an increase of the photosynthetic quantum efficiency in young leaves (Cousins et al., 2001) and in mature leaves net photosynthesis was strongly

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R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

increased (+23%) under drought but only slightly (+9%) under wet conditions (Wall et al., 2001). In the maize-FACE studies photosynthesis was increased by elevated [CO2 ] under summer drought (Leakey et al., 2004; Markelz et al., 2011) but was totally unaffected when the plant was not experiencing water deficit (Leakey et al., 2006; Markelz et al., 2011). With respect to biomass production many enclosure studies indicated an increase of maize growth under elevated [CO2 ] and well-watered conditions (Driscoll et al., 2006; Kang et al., 2002; King and Greer, 1986; Loomis and Lafitte, 1987; Morison and Gifford, 1984) while others reported on no CO2 effects (Bethenod et al., 2001; Kim et al., 2007; Rudorff et al., 1996; Samarakoon and Gifford, 1996). In the FACE experiments with C4 crops biomass of sorghum was only slightly increased by CO2 enrichment (Ottman et al., 2001), however biomass and grain yield of maize was totally unaffected under sufficient water availability (Leakey et al., 2006; Markelz et al., 2011). Under drought stress growth of maize was generally increased by CO2 enrichment and the relative CO2 effect was greater than under well-watered conditions (Kang et al., 2002; King and Greer, 1986; Loomis and Lafitte, 1987; Samarakoon and Gifford, 1996) and this was also observed in the FACE experiment with sorghum (Ottman et al., 2001). The CO2 fertilization effect of C4 crops under drought is attributed to decreased stomatal conductance, which may conserve the soil water and thus delay the onset of drought stress (Ghannoum, 2009). Improved soil moisture under high [CO2 ] has been found in FACE studies with sorghum and maize (Conley et al., 2001; Leakey et al., 2006). However, the CO2 effect on evapotranspiration, which amounted to 10–13% (Conley et al., 2001; Triggs et al., 2004), was much lower than the effect on stomatal conductance, which ranged between 30% and 40% (Leakey et al., 2006; Wall et al., 2001). The reasons for this difference are several feedback processes at the leaf and canopy level (Oliver et al., 2009). Wilson et al. (1999) have analysed these feedback processes for maize and soybean with a model approach in more detail. According to their study the soil evaporation feedback was most important in reducing the CO2 effect by 60%. The increased specific humidity deficit of the canopy airspace and the higher soil moisture content, which both result from the decrease of stomatal conductance under high [CO2 ], should contribute to an increase of evaporative loss throughout the season. Consequently, in the field much of the potential water saving under elevated [CO2 ] could be lost by evaporation and thus would not be available for mitigation of drought stress. Evaporation depends on the water content in the upper soil layer, surface net radiation and amounts to approximately 15% of total water flux at leaf area index of 4 for a maize crop (Villalobos and Fereres, 1990). Averaged over the season about one third of water consumption of a maize crop results from soil evaporation (Liu et al., 2002). This water loss can be decreased, for example, by soil cover and according to Bond and Willis (1969) a straw layer of 8 t ha−1 reduces evaporation by 80%. Consequently, soil cover by residue which is used to improve crop growth under limited water supply by conserving soil water might be even more advisable under elevated [CO2 ]. Insufficient precipitation decreases soil water content (SWC) which in turn first affects growth of plant tissue and at lower values also stomatal conductance and CO2 assimilation rate of the leaves (Sadras and Milroy, 1996). Moreover, water deficit can advance leaf senescence and reduce light absorption (Stone et al., 2001). Thus, drought stress impairs biomass production by decreasing the absorption of light by the green canopy and the efficiency with which absorbed light is used for photosynthesis and dry weight production, i.e. radiation use efficiency (RUE) (Earl and Davis, 2003; Stone et al., 2001). Previous CO2 enrichment studies have addressed some details of the processes involved in the decline of biomass production under

drought. As already mentioned [CO2 ] effects on maize were higher under drought than under sufficient water supply. In addition, CO2 enrichment increased leaf area more under dry than wet conditions (Kang et al., 2002; King and Greer, 1986; Samarakoon and Gifford, 1996). Most of the CO2 enrichment studies with maize have been done in chambers and with artificial root environment in pots. There was only one FACE site, at which the growth response of maize to elevated [CO2 ] was investigated over three seasons with different precipitation regimes (Leakey et al., 2006; Markelz et al., 2011). It turned out that water supply to the crop was slightly insufficient in 2 years and but not in 1 year, when no CO2 effect on photosynthesis and biomass production was detected. As there are no other CO2 enrichment studies with maize under conditions of controlled water supply, there is a need for FACE experiments with maize, in which water supply is included as an additional factor in order to determine the interaction of [CO2 ] and water supply more precisely (Leakey, 2009; Oliver et al., 2009). The present FACE experiment with maize was carried under field conditions over two growing seasons. We combined the FACE technique with a large-scale rain exclusion system (Erbs et al., 2011) to study the effect of CO2 enrichment simultaneously under wellwatered and drought stress conditions. The main objectives of the study were to quantify the effects of CO2 and water supply on the primary processes responsible for biomass and yield production of maize, i.e. temporal changes in green leaf area index, the resulting radiation absorption by the canopy and the radiation and water use efficiencies. Moreover, in the second growing year soil cover was included as an additional subplot treatment to test whether straw mulching as compared to bare soil increases the CO2 fertilization effect under drought by lessening evaporative water loss and enhancing water usage for plant growth. This is the first FACE study to address comprehensively the interactions of elevated CO2 and water in maize.

2. Materials and methods 2.1. Field conditions and experimental treatments The experiment was conducted on an experimental field site (10 ha) of the Johann Heinrich von Thunen-Institute. The soil at the experimental area is a luvisol of a loamy sand texture in the plough horizon (0–40 cm) and the subsoil consists of a mixture of gravel and sand. It has a pH of 6.5, a mean organic matter content of 1.4% and a comparatively shallow rooting zone (0–60 cm). The drained upper (0.01 MPa soil water tension) and lower limits (1.5 MPa soil water tension) of plant available volumetric SWC within the 0.6 m soil profile were approximately 23% and 5%, respectively. Based on expert knowledge the rooting depth for maize at the study site is assumed to be approximately 0.6 m. The estimated plant available water capacity within the root zone of 0.6 m was 108 mm. A FACE system engineered by Brookhaven National Laboratory and previously used for C3 crops (Weigel et al., 2005) was modified for the maize experiments. Three circular plots were equipped with FACE rings each with a diameter of 20 m. The 32 vertical vent pipes of each FACE ring had a height of 3.2 m compatible to the maximal height of 3 m of the maize crop. The three rings comprised what was termed the FACE treatment. Three circular plots without CO2 enrichment and without venting were used as control treatment (=AMB treatment). The target CO2 concentration in the FACE rings was set to 550 ␮l l−1 during daylight hours. CO2 enrichment was interrupted at high wind speed (>5.5 m s−1 ). At the field site, wind speed was low during the night but increased during the day with a maximum in early afternoon. So the effect of venting on canopy climate was exceeded by the wind effect. This was confirmed by data of canopy air temperature recorded in AMB and FACE plots

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

Sowing Emergence Start of CO2 enrichment Start of irrigation Anthesis stage Final harvest End of CO2 enrichment

30th April 10th May 11th June 20th July 18th July 1st October 2nd October

9th May 16th May 9th June 27th June 25th July 29th September 30th September

over the whole season. CO2 enrichment started at a leaf area index of about 0.5 in early June, since crop water dynamics for the time LAI < 0.5 have little effects on the remainder of the growing season, and lasted until final harvest at the end of September (Table 1). Mean seasonal [CO2 ] during daylight hours in the AMB treatment was 378 ␮l l−1 (2007: 377.2 ␮l l−1 , 2008: 378.5 ␮l l−1 ). In order to test the CO2 response of maize under two levels of water supply each of the six circular main plots was split into a well-watered (WET) and a dry (DRY) semicircular subplot. In the WET subplots water content in the 0.6 m soil profile was kept above 50% of maximum plant available SWC. In the DRY treatment it was intended to reduce SWC in the 0.6 m soil profile below 50% of maximum plant available SWC during midsummer. Based on long-term data from the Agrometeorological Research Station of the German Weather Service at Braunschweig maize suffers more than 20 days from drought stress in every second summer (July–August) at our experimental field site. Drip irrigation lines were installed along the maize rows, which enabled to establish the WET treatment by drip irrigation or the DRY treatment by omitting water supply depending on the climatic conditions during summer. To induce drought also in summer with high rainfall, we tested different rain exclusion systems. In 2007, wooden racks equipped with PVC shelves (0.6 m width) were positioned in every second inter row area and the rain intercepted was drained to the outside area of the plots. The racks were operated from the end of August until the end of September, but only 11% of the total precipitation could be excluded during this time. In 2008, the designated DRY subplots were equipped with aluminium frames of tents with a ground area of 20 m × 12 m each as described by Erbs et al. (2011). The frames were covered with transparent PVC tarpaulins during periods of forecasted rainfall >10 mm day−1 . The frames reduced incident photosynthetic active radiation (PAR) by 6.6% without tarpaulins based on the exposed horizontal area and by 24.1% with tarpaulins. The tarpaulins were installed during three periods (3rd to 4th July, 17th to 22nd July, and 22nd to 25th August) resulting in rain exclusion of 12, 16 and 29 mm, respectively (Fig. 1). Two sensors for PAR (BF2 sunshine sensor, Delta-T Devices, UK) operated from mid of June until final harvest in the DRY and WET areas yielded amounts of incident radiation of 812 and 872 MJ m−2 , respectively, Thus, the incident radiation over the season was reduced by 7% in the dry plots as compared to the wet plots. Apart from the reduction in incident PAR, the rain shelter equipment had no substantial influence on the environmental conditions (Erbs et al., 2011). In 2008 each semicircle of the WET and DRY treatments was additionally divided in a quarter without soil cover (BARE) and a quarter in which the soil surface was covered at the 1st July by hand with 7 t ha−1 barley straw (MULCH). Such an amount of residue on the soil surface reduces the rate of evaporative water loss by ca. 80% as compared to the bare soil (Bond and Willis, 1969). The objective of this additional treatment was to test whether the effect of CO2 enrichment on plant growth under drought can be advanced by minimizing the evaporative water flux.

30

25

30

20 20 15

10

10

rainfall, irrigation (mm d )

Second growing season

rainfall irrigation radiation temperature

5

0 1-Jun

0 22-Jun

13-Jul

3-Aug

24-Aug

14-Sep

35

40 2008

rainfall irrigation radiation temperature

30

25

30

20 20 15

10

10

rainfall, irrigation (mm d )

First growing season

2007 radiation (MJ m d ), temperature (°C)

Event

40

35

radiation (MJ m d ), temperature (°C)

Table 1 Timetable of agricultural measures carried out in the first (2007) and second (2008) season.

13

5

0 1-Jun

0 22-Jun

13-Jul

3-Aug

24-Aug

14-Sep

Fig. 1. Mean daily air temperature and total daily global radiation, rainfall and irrigation over the growing seasons of 2007 and 2008. The operation time of the tarpaulins of the rain-shelter in 2008 is shown by grey bars. The DRY plots were not irrigated except of one event at 30th July 2008 (20 mm). (Notes: *: Wet plots with FACE were not irrigated. **: For one time dry plots were also irrigated at this date with 20 mm. ***: Wet plots with FACE and mulch layer were excluded from irrigation.)

2.2. Crop culture and management Agricultural management measures of the 10 ha field and the experimental plots were carried out according to local farm practices. Maize (Zea mays L., cv. ‘Romario’) was sown with a row distance of 0.75 m and a seeding density of 10 plants m−2 (Table 1). Weed control was done by application of herbicides in May and hand weeding in the experimental rings. Mineral nutrients were added according to local fertilizing practices based on soil analysis in early springtime. The following amounts of fertilizers were applied: 2007: 171 kg N ha−1 , 92 kg P2 O5 ha−1 , 200 kg K2 O ha−1 , and 36 kg S ha−1 ; 2008: 198 kg N ha−1 , 92 kg P2 O5 ha−1 , 25 kg MgO ha−1 , and 20 kg S ha−1 . Anthesis stage was reached at 18th and 25th of July in 2007 and 2008, respectively, and did not significantly differ between the treatments. 2.3. Measurements of soil water content and climatic conditions, and water supply Volumetric SWCs were measured by time domain reflectometry (TDR) sensors approximately twice per week from 12th of June until final harvest. To account for spatial variation in SWC due to the drip irrigation and the discharge of precipitation to the plant row area, soil moisture measurements were done at different positions. This was especially considered in the DRY treatment to quantify average SWC conditions. In the top soil layer (0–0.2 m) water content was measured by a hand-held TDR probe at three positions from

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

the plant row up to the centre between two rows. In each of the six WET plots two TDR probes were installed in 0.3 m soil depth with a horizontal distance of 0.2 m from the plant rows with one probe in the BARE and MULCH quarter, respectively, in 2008. A similar positioning was used for the DRY treatment in 2007, while in 2008 an additional probe was installed in the BARE quarter. The records were used for the quantification of SWC in the 0.2–0.4 m soil layer. Values in the 0.4–0.6 m layer were obtained by one (2007) or two probes (2008, in BARE and MULCH) installed in the DRY plots only. Plant available water (PAW) in the 0.6 m rooting depth was calculated from the data of the TDR probes. For the WET treatment it was assumed that water content in the 0.4–0.6 m layer remained constant at a high level as measured in the DRY plots during June before applying the different watering regime. Data on climatic conditions (global radiation, rainfall, air temperature measured 2 m above ground level) were obtained from the nearby Agrometeorological Research Station of the German Weather Service located 500 m apart from the experimental site. Irrigation of the experimental plots was controlled by manual application based on records of SWC.

120

RWC =

FW − DW × 100 TW − DW

(1)

2.5. Plant growth analysis Four (2007) or five (2008) destructive harvests were carried out from June until end of September and samples were taken from each quarter per ring. The size of the sampling area amounted to 1 m2 and 2 m2 at the intermediate and final harvest, respectively. The major fraction (ca. 70%) of the total above ground biomass was dried and the dry weight was determined. The remaining sub-sample was used for estimation of green area and biomass partitioning. Area of green leaves was measured with a leaf area meter (Model LI-3100, LICOR) and used to calculate green leaf area index. Dry weights of leaves, stems, husks and cobs were determined after drying at 105 ◦ C. At maturity yield components (grain number, mean grain weight and grain yield) were measured. Fraction of PAR absorbed by the green canopy (fapar ) was measured at noon (±2 h) similar to the procedure done by Earl and Davis (2003) and approximately once per week starting in the middle of June when fapar reached a value of 0.3–0.4. The measurements were carried out with the SUNSCAN system (Delta-T Devices, Cambridge, UK) and included the radiation incident on the canopy (J0 ), reflected by the canopy (Jr ), and the radiation at the lower limit of the green canopy (Jc ), which was estimated by eye. Jr and Jc were measured two to four times per semicircle in 2007 and per quarter in 2008 and averaged. fapar was calculated using the following equation: fapar =

J0 − Jr − Jc J0

(2)

80

60

40

DRY AMB DRY FACE WET AMB WET FACE

20

0 1-Jun

120

22-Jun

13-Jul

3-Aug

24-Aug

14-Sep

13. Jul

03. Aug

24. Aug

14. Sep

2008

100

PAW (mm)

2.4. Measurement of leaf relative water content (RWC) Leaf relative water content (RWC) was measured according to the method described by Schonfeld et al. (1988). In each quarter circle of the six rings four sun exposed leaves (5th and 6th leaf counted from the top and from two plants) were sampled within 1 h at 2 p.m. From the total leaf the tip and the base were abscised to obtain a middle segment of ca. 20 cm length. The four segments were put in a plastic bag and stored at 0 ◦ C until the measurement of the fresh weight (FW) within 2 h. Subsequently, the leaf segments were soaked over night in distilled water at room temperature. The leaf samples were carefully blotted dry with filter paper and the turgid weight (TW) was determined. Dry weights (DWs) of the leaf segments were obtained after drying at 105 ◦ C. RWC was calculated using the following equation:

2007

100

PAW (mm)

14

80

60

40

20

0 01. Jun

DRY AMB DRY FACE WET AMB WET FACE 22. Jun

Fig. 2. Seasonal changes in plant available soil water content (PAW) of maize grown over 2 years (2007, 2008) under different levels of water (WET, DRY) and CO2 supply (AMB, FACE). Values are given with standard error (n = 3 in 2007 and n = 6 in 2008).

Accumulated seasonal (from mid June until final harvest) radiation absorbed by the canopy (AR) was estimated as the sum of the daily values, which represent the product of fapar and incident global radiation multiplied by 0.5 to account for the fraction of PAR. Data from intervening days were obtained by linear interpolation of the fapar readings. The reduction in PAR by the tents in the DRY treatment in 2008 was accounted for by multiplying results for the DRY subplots with a factor of 0.76 and 0.93, respectively, when tarpaulins were installed or not. RUE was derived as the slope of the regression lines between the aboveground biomass per treatment replicate at different harvests plotted against the respective accumulated sums of AR. The water use efficiency was calculated by dividing the aboveground biomass (WUEb ) or grain yield (WUEy ) at final harvest by the respective amount of water used by the plants ranging from 12th June, when CO2 enrichment had started and measurement of SWC was initiated, until final harvest. Water use was calculated as quantity of water applied (precipitation and irrigation) minus the increase in SWC over this period. In 2007, there was a heavy rainfall (75 mm) during the last 4 days before final harvest, when the soil was already water saturated (Figs. 1 and 2). These 75 mm were omitted for calculation of water use. 2.6. Statistical analysis Data were analysed as completely randomized design with ambient CO2 (n = 3) and elevated CO2 (n = 3) treatments each split for water supply (n = 12) with the R statistical software package (R 2.12.0, The R Foundation for Statistical Computing). For the mulching treatment in 2008 additional treatment subplots were

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21 24

12

ANOVA results CO2 - SC - + CxS - -

4 11-Jun

24

During the growing seasons, CO2 enrichment was interrupted for 1.1% of the operational time in 2007 and for 2.5% in 2008 due to high wind speeds or system failures of the CO2 enrichment. The target concentration of 550 ␮l l−1 was reached within thresholds of ±10% of the average 1-min [CO2 ] at the FACE plots for 94.1% and 95.0% of the operational time in the 2007 and 2008 growing season, respectively. The weather conditions during the two experimental seasons were typical for this site (Fig. 1) except of the extraordinary amount of rainfall in 2007, which was nearly twice the amount of the longterm mean over the last 30 years.

20 soil water content (Vol%)

3.1. Performance of the FACE system and environmental conditions over the two seasons

Due to the huge rainfall in 2007, the total amount of plant available water in the rooting zone (0.0–0.6 m, PAW) stayed at a high level and showed only a slight and temporary decrease towards the end of July, which was mitigated in the WET plots by 34 mm irrigation from late July to early August (Fig. 2). Thus, water supply was quite high in both DRY and WET treatment, and the seasonal water use hardly differed between the two watering regimes in 2007 (Table 2). In 2008, PAW decreased at the end of June (Fig. 2). Therefore, irrigation was started at this time in all WET plots to raise SWC (Fig. 1). Water supply to the WET FACE plots was reduced as compared to the WET AMB treatment (at the 1st August, 4th and 16th September) to prevent water logging (Fig. 1). PAW was significantly different (p < 0.001) between WET and DRY since the beginning of July. Elevated [CO2 ] resulted in a significant increase of PAW on several dates (p < 0.10: 7th and 10th July; 7th, 11th and 25th August; p < 0.05: 18th, 21st and 28th August), and there was no significant interaction of the CO2 and water supply on this variable. Soil cover affected SWC only in the top soil layer (Fig. 3). SWC was found to be increased (WET: 28th July, 7th August; DRY: 21st July, 31st July, 21st August) and decreased by the straw layer (WET: 24th July; DRY: 10th July). There was a positive interaction of CO2 enrichment and soil cover on several dates (WET: 14th July, 11th August; DRY: 17th July, 24 July). However, in the DRY treatment water content was also found to be less stimulated by CO2 enrichment in MULCH than in BARE subplots on two dates (17th July, 24th July). The seasonal rainfall in 2008 amounted to 208 mm and 151 mm for the WET and DRY plots, respectively, due to the operation of the rain exclusion system (Table 2). The quantity of water applied by rain and irrigation was ca. 330 mm and 170 mm for the WET and DRY treatment, respectively (Table 2). The difference in PAW between early June and end of September depended on the watering regime but was neither affected by CO2 enrichment nor

WET

16

8

3. Results

3.2. Soil water content and seasonal water use

AMB MUL AMB BARE FACE MUL FACE BARE

20 soil water content (Vol%)

established in each quarter of the ring halves and were included in the statistical analysis as additional splitting factor. Plants grown under the rain shelter in 2008 received 7% less incident PAR than plants from the WET plots. This should have decreased plant growth, since it is directly related to incident PAR. To exclude these differences in the radiation environment and to allow for a direct comparison of the growth data from the WET and DRY areas, a rough approximation was used and growth data obtained under the rain shelter in 2008 were corrected by multiplication of the measured values with 1.07. These corrected values are presented in Table 3 and in Figs. 5 and 6. Calculation of the resource use efficiency of biomass production was done with the uncorrected values (Table 4).

15

** - - -

1-Jul

ANOVA results CO2 SC CxS -

* -

- - * -

- - + - -

- ** - -

21-Jul

** * - + - -

* *** - + * **

* * -

-

+ -

- - + -

-

-

10-Aug

* +

+ - * - -

- ** - - -

** * - - -

-

30-Aug

* + + + * -

* * - - -

DRY 16

12

8

4 11-Jun

AMB MUL AMB BARE FACE MUL FACE BARE 1-Jul

21-Jul

10-Aug

30-Aug

Fig. 3. Seasonal changes in water content of the upper soil layer (0–0.2 m depth) of maize in 2008 under different levels of water (WET, DRY) and CO2 supply (AMB, FACE) and soil cover (BARE and MULCH). Values are given with standard error (n = 3). + p < 0.10; *p < 0.05; **p < 0.01; ***p < 0.001.

by soil cover. Thus, CO2 enrichment did not increase soil water exploitation even if the water supply was reduced to half of the amount added to the well-watered treatment. 3.3. Leaf relative water content and radiation absorption during a strong drought period At the end of July 2008, PAW decreased to a minimum of ca. 10 mm and 20 mm in the DRY AMB and DRY FACE treatment, respectively (Fig. 2). Moreover, in the upper soil layer SWC was close to the permanent wilting point (Fig. 3). This coincided with hot summer weather (Fig. 1) with daily maximum temperatures above 30 ◦ C. During this period leaf RWC was analysed as an indicator of the plant water status. At the 28th July, RWC was unaffected in WET plots but significantly decreased in DRY FACE and even more in DRY AMB plots (Fig. 4). Moreover, plants showed visible symptoms of drought stress, i.e. leaf curling, on 28th and 29th July, which increased during the day and resulted in a short-term decline of fapar . Therefore, additional recordings of fapar were made and not only before noon but also later in the day (Fig. 4). There was a significant effect of water supply on fapar at 28th July, which was mitigated by CO2 enrichment. This effect was primarily due to leaf curling, which partially ceased over night and then increased again as indicated by the fapar readings taken at the morning and noon of the next day. At 30th of July, all dry plots were irrigated with 20 mm to mitigate the severe drought stress (Fig. 2), which is confirmed by the data on RWC measured on 31st July and 4th August. Subsequently, on 7th August RWC of the leaves of the DRY AMB plots again were more affected by drought than those of the DRY FACE plots. Moreover, there was a persistent long-term decline of

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R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

Table 2 Summary of seasonal water use (WU) of maize grown under different CO2 (AMB, FACE) and water supply (WET, DRY) during 2007 and 2008. In 2008 plants were also grown under different soil cover (BARE, MULCH). WU was made up of precipitation (Prec), excluded precipitation (Precex ), irrigation (Irr) and the changes in plant available soil water content (dPAW) over the period (12th June–1st October in 2007, 12th June–29th September in 2008). Values are given as means ± standard error (n = 3). Year

Soil cover

CO2

H2 O

Prec (mm)

2007

BARE

AMB AMB FACE FACE

WET DRY WET DRY

309 309 309 309

0 −9 0 −9

34 0 34 0

−23 −23 −16 −24

± ± ± ±

6 5 1 13

320 277 327 277

± ± ± ±

6 5 1 7

2008

BARE

AMB AMB FACE FACE AMB AMB FACE FACE

WET DRY WET DRY WET DRY WET DRY

208 208 208 208 208 208 208 208

0 −57 0 −57 0 −57 0 −57

119 20 94 20 119 20 89 20

−27 27 −29 30 −35 30 −30 26

± ± ± ± ± ± ± ±

1 5 0 5 3 3 3 6

300 198 273 201 292 201 267 197

± ± ± ± ± ± ± ±

1 5 0 5 5 3 3 6

Mulch

the fapar values predominantly in the DRY AMB plots, which was not due to leaf curling but caused by accelerated leaf senescence and a decrease in green leaf area index (Fig. 5). 3.4. Green leaf area index and total biomass production In 2007, when water availability to the crop was abundant in both WET and DRY plots, the course of green leaf area index was similar among both of two the water and CO2 levels, respectively 120

110

ANOVA results CO2 n.s. H2O *** CxH (*)

n.s. ** n.s.

n.s. *** n.s.

* *** *

Precex (mm)

Irr (mm)

dPAW (mm)

WU (mm)

(Fig. 5). The same applied to the total above ground biomass produced over the vegetation period in 2007 (Fig. 6). In the 2nd season, when PAW decreased to 10% of the maximum value until the end of July, leaf area index was significantly decreased under reduced water supply in early August. This effect persisted until autumn. CO2 enrichment firstly increased leaf index as observed in late August. However, in late September a slight interaction of water and CO2 supply was detected and CO2 enrichment had a positive effect under dry and a negative effect under wet conditions, respectively. In 2008, seasonal progress of above ground biomass production was again unaffected by CO2 enrichment in the WET

n.s. n.s. n.s.

8

2007 7 green leaf area index (m m )

leaf RWC (%)

100

90

80

70

dry amb dry FACE wet amb wet FACE

60

5 4 3 2

DRY AMB DRY FACE WET AMB WET FACE

1

Jul 28th

Jul 31st

Aug 4th

Aug 7th

Aug 11th 0 1-Jun

110

100

6

ANOVA results CO2 H2O n.s. CxH n.s.

*** **

* *

*** **

*** *

*** *

*** **

green leaf area index (m m )

fapar (%)

80

dry amb dry FACE wet amb wet FACE

70 Jul 23th

Jul 28th

Jul 29th

Jul 29th

Jul 31st

Aug 7th

Aug 13th

13-Jul

3-Aug

n.s. n.s. n.s.

n.s. *** n.s.

ANOVA results CO n.s. water n.s. CxW n.s.

6

14-Sep

* ** n.s.

n.s. *** (*)

5 4 3 2

DRY AMB DRY FACE WET AMB WET FACE

1

2008

Fig. 4. Effect of different water (WET, DRY) and CO2 supply (AMB, FACE) during a hot summer period on leaf relative water content (RWC) and on changes in radiation absorption of the canopy (fapar ). The short-term changes within a 24 h period resulted from leaf curling induced by drought stress. fapar was regularly measured in the morning at about 10 o’clock except of the 28th July and the 2nd measuring time of the 29th July when fapar was measured at 2 p.m. and at noon (12 h), respectively. Soil cover did not have a significant effect on either variable. Results are given with standard error (n = 6). (*)p < 0.10; *p < 0.05; **p < 0.01; ***p < 0.001.

24-Aug

8 7

90

22-Jun

0 1-Jun

22-Jun

13-Jul

3-Aug

24-Aug

14-Sep

Fig. 5. Seasonal changes in green leaf area index of maize grown over 2 years (2007, 2008) under different levels of water (WET, DRY) and CO2 supply (AMB, FACE). Different treatments of soil cover used in 2008 did not have a significant effect. Results are given with standard error (n = 3 in 2007 and n = 6 in 2008). (*)p < 0.10; *p < 0.05; **p < 0.01; ***p < 0.001.

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

yield was even 1% lower under elevated than under ambient [CO2 ]. However, under dry conditions CO2 enrichment increased growth as supported by the significant interaction of CO2 and water supply for all growth variables except for stem dry weight. Grain yield was increased by 41% due to a positive CO2 effect on grain number and thousand seed weight. Soil cover had no significant effect on plant growth at final harvest.

3000

2007

above ground biomass (g m )

2500

2000

1500

3.6. Radiation absorption (AR) and radiation (RUE) and water use efficiency (WUE)

1000

DRY AMB DRY FACE WET AMB WET FACE

500

0 1-Jun

22-Jun

13-Jul

3-Aug

24-Aug

* *** n.s.

** * n.s.

14-Sep

3000

2500 above ground biomass (g m )

17

ANOVA results CO n.s. water n.s. CxW n.s.

n.s. n.s. n.s.

* *** **

2000

1500

1000

DRY AMB DRY FACE WET AMB WET FACE

500

2008 0 1-Jun

22-Jun

13-Jul

3-Aug

24-Aug

14-Sep

Fig. 6. Seasonal changes in above ground biomass production of maize grown over 2 years (2007, 2008) under different levels of water (WET, DRY) and CO2 supply (AMB, FACE). Different treatments of soil cover used in 2008 did not have a significant effect. Results are given with standard error (n = 3 in 2007 and n = 6 in 2008). *p < 0.05; **p < 0.01; ***p < 0.001.

In the first year, the slight reduction in water supply had a small effect on seasonal radiation absorption and a clear effect on water use efficiency (Table 4). Percentage CO2 effect on AR and resource use efficiencies was ≤1% when averaged over both watering levels. This was similar to the results of AR and RUE obtained under the wet conditions in 2008. The strong drought stress in 2008 significantly affected AR, RUE and WUE of total biomass and there was also a significant interaction with the CO2 supply. Under dry conditions CO2 enrichment increased WUE by 25% and RUE by 19%. The CO2 response of the WUE for grain yield was even greater and amounted to 42%. Soil cover did not have any effect on these variables. As described in Section 2 incident photosynthetic radiation over the season was 7% lower under the rain shelter than in the WET plots. This has to be considered when comparing values for AR obtained in the dry and wet treatments. Thus, the decrease of AR of 15% and 9% observed under the rain shelter under ambient and elevated [CO2 ], respectively, resulted both from a change of the absorptivity of the green canopy for light and reduced incident radiation. The later can be included by correcting the AR values with a number of 1.07 as has been done for the growth variables. With this correction, AR values of the DRY AMB and DRY FACE treatment amounted to 666 and 722 MJ m−2 , respectively. Based on these numbers, CO2 enrichment increased AR by 8% and the drought stress hardly decreased AR under FACE (−2%) but under ambient [CO2 ] (−9%). 4. Discussion

treatment except for one harvest in early August after a hot summer period as described in the previous paragraph. At this date a slightly significant CO2 effect (p = 0.09) on biomass was detected. The reduction of water supply decreased total biomass production significantly as from the beginning of August. Moreover, there was a persistent significant effect of elevated [CO2 ] on total crop biomass from this date. 3.5. Final biomass and grain yield data Final dry weights of the total plant and of individual plant fractions are listed in Table 3. In 2007, water supply significantly affected only the biomass of total and green leaves and the grain number, which were decreased in the DRY treatment by up to 10% as compared to the WET treatment. All other growth parameters were unaffected by water supply and total biomass and grain yield of the WET and DRY treatment were quite similar. In the first year, CO2 enrichment did not significantly affect the dry weights of stem, leaves or grain yield. There was only a significant CO2 effect on the biomass of dead leaves, which reoccurred in 2008 and fits to the CO2 related decrease in leaf area index under wet conditions in 2008 (Fig. 5). In 2008, all growth variables except of stem dry weight were significantly affected by the reduction in water supply. Under ambient [CO2 ] drought stress decreased total above ground biomass and grain yield by 24% and 36%, respectively. Similar to the findings in 2007, there was no CO2 effect under wet conditions on dry weights of total biomass, leaves, stems or grains. For example total biomass was the same under both CO2 levels and grain

The objective of the present study was to investigate the effect of free air CO2 enrichment on the growth of maize under sufficient and restricted water supply. The FACE system was operated successfully and increased [CO2 ] by 170 ␮l l−1 as compared to ambient [CO2 ] control treatment. A sufficient water supply treatment was guaranteed by the application of drip irrigation. In contrast, drought stress could not be established in the first but in the second experimental season. In the first year, precipitation during summer was doubled as compared to the long term mean of the field site and the rain exclusion system used was too inefficient to produce a substantial decrease in SWC during summer. However, in the second year using a newly designed rain shelter precipitation in July and August could be decreased by 40%. Seasonal rainfall from June until September in 2008 was similar to the long term mean, and for this time period the area under the rain shelter received 30% less precipitation, which roughly corresponds to the changes predicted until the end of this century (Meehl et al., 2007). The operation of the rain shelter did not substantially affect the CO2 enrichment and the climatic conditions within the canopy except of the incident radiation, which was reduced on averaged by ca. 7% as compared to the field plots without rain shelter. Thus, before comparing the water effect on growth data from WET and DRY plots they should be adjusted for the difference in incident radiation (Erbs et al., 2011). Under optimum water and nutrient supply total biomass production depends linearly on incident radiation. As plants under the rain shelter received 7% less incident radiation, growth data of the dry plots have been adjusted with a factor of 1.07. If water becomes limited, the effect of

18

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

Table 3 Effect of different water (WET, DRY) and CO2 (AMB, FACE) supply on growth and yield variables of maize at final harvest in 2007 and 2008. In 2008, the effect of different soil covers was also analysed and included in the ANOVA. However, the effect of soil cover and the interactions were always non significant. Variable

Year

DRY

WET

ANOVA

AMB

FACE

%a

AMB

FACE

2007 2008

2139 ± 53 1722 ± 51

2154 ± 58 2131 ± 78

1 24

2138 ± 17 2248 ± 28

2184 ± 52 2248 ± 38

2 0

Stem DW (g m−2 )

2007 2008

613 ± 21 589 ± 28

611 ± 20 643 ± 18

0 9

576 ± 8 622 ± 10

607 ± 36 632 ± 10

Green leaves DW (g m−2 )

2007 2008

143 ± 10 14 ± 3

145 ± 6 39 ± 10

1 111

158 ± 4 118 ± 6

161 ± 4 99 ± 8

2007 2008

80 ± 3 190 ± 5

91 ± 4 198 ± 6

14 4

75 ± 2 118 ± 3

102 ± 9 138 ± 11

2007 2008

88 ± 3 60 ± 2

79 ± 2 70 ± 5

−10 17

86 ± 2 83 ± 2

87 ± 5 82 ± 4

2007 2008

311 ± 11 264 ± 5

315 ± 9 298 ± 9

1 13

319 ± 3 320 ± 5

2007 2008

198 ± 5 140 ± 5

197 ± 7 167 ± 6

0 19

201 ± 2 181 ± 3

−2

Total DW (g m

)

Dead leaves DW (g m−2 ) Husk leaves DW (g m−2 ) Total leaf DW (g m−2 ) −2

Rachis DW (g m

)

Grain number (m−2 )

2007 2008

1000 seed Weight (g) Grain yield (g m−2 ) Harvest index

4058 ± 136 3096 ± 144

3940 ± 157 3860 ± 158

−3 25

4208 ± 125 4095 ± 53

n.s.

n.s. **

5 2

n.s. (* )

n.s. n.s.

n.s. n.s.

2 −16

n.s. n.s.

*

n.s.

***

*

35 17

*

n.s.

*

***

n.s. n.s.

1 −1

n.s. n.s.

349 ± 16 319 ± 9

9 0

n.s. n.s.

196 ± 3 180 ± 10

2 −1

n.s. n.s.

4164 ± 130 3978 ± 46

−1 −3

n.s. n.s.

4 13

247 ± 4 275 ± 3

247 ± 2 281 ± 2

2007 2008

1004 ± 18 729 ± 45

1017 ± 38 1024 ± 54

1 41

1038 ± 21 1125 ± 13

1029 ± 25 1117 ± 15

0.49 ± 0.01 0.50 ± 0.00

1 14

C×W

***

258 ± 3 265 ± 5

0.47 ± 0.01 0.48 ± 0.01

W

n.s.

248 ± 8 235 ± 5

0.47 ± 0.00 0.42 ± 0.02

CO2 *

2007 2008

2007 2008

%a

0 2 −1 −1

0.47 ± 0.00 0.50 ± 0.01

−3 −1

n.s. ***

n.s. n.s.

*

n.s.

***

*

n.s.

n.s. (* )

*** **

n.s.

***

**

n.s.

n.s.

n.s.

**

***

*

n.s.

n.s.

n.s.

*

***

**

n.s. n.s.

n.s.

n.s.

***

*

a Percentage CO2 effect. (* )p < 0.10. * p < 0.05. ** p < 0.01. *** p < 0.001.

Table 4 Effect of different soil cover (SC: BARE, MULCH), water (WET, DRY) and CO2 (AMB, FACE) supply on accumulated seasonal radiation absorbed by the green canopy (AR), radiation use efficiency (RUE) and water use efficiency of total biomass (WUEb ) and grain yield (WUEy ) of maize in 2007 and 2008. Soil cover was varied only in 2008. Values represent means + standard error (n = 3). SC

2007 BARE

H2 O

WET DRY

AR (MJ m−2 )

%a

AMB

FACE

695 ± 17 683 ± 25

698 ± 9 696 ± 6

0 2

RUE (g MJ−1 )

%a

AMB

FACE

2.88 ± 0.16 2.88 ± 0.09

2.91 ± 0.22 2.81 ± 0.22

1 −2

WUEb (g kg−1 )

%a

AMB

FACE

6.68 ± 0.11 7.73 ± 0.32

6.69 ± 0.15 7.78 ± 0.08

0 1

WUEy (g kg−1 )

%a

AMB

FACE

3.24 ± 0.06 3.63 ± 0.12

3.15 ± 0.17 3.68 ± 0.10

−3 1

ANOVA CO2 H2 O C×H 2008 BARE MULCH

WET DRY WET DRY

734 ± 5 622 ± 15 730 ± 9 620 ± 15

n.s. (* ) n.s. 738 ± 7 675 ± 15 730 ± 2 671 ± 26

n.s. n.s. n.s. 1 9 0 8

3.11 ± 0.06 2.46 ± 0.11 3.01 ± 0.03 2.56 ± 0.22

3.09 ± 0.23 3.00 ± 0.29 3.03 ± 0.24 2.97 ± 0.27

0 22 1 16

7.65 ± 0.01 8.08 ± 0.19 7.54 ± 0.16 8.03 ± 0.29

n.s.

n.s.

***

**

n.s.

n.s.

8.35 ± 0.27 10.0 ± 0.67 8.33 ± 0.19 10.1 ± 0.76

9 24 10 25

3.82 ± 0.03 3.51 ± 0.21 3.78 ± 0.07 3.31 ± 0.35

4.12 ± 0.08 4.88 ± 0.37 4.17 ± 0.13 4.77 ± 0.49

ANOVA CO2 Water SC C×W C×S W×S C×W×S a Percentage CO2 effect. (* )p < 0.10. * p < 0.05. ** p < 0.01. *** p < 0.001.

*

(* )

*

*

***

**

**

n.s.

n.s.

n.s.

n.s. n.s.

***

*

*

**

n.s. n.s. n.s.

n.s. n.s. n.s.

n.s. n.s. n.s.

n.s. n.s. n.s.

8 39 10 44

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

radiation on growth ceases and the usage of the correction factor would result in an over-adjustment of plant growth data. In our experiment, plant growth under the rain shelters was more affected by SWC under AMB than FACE. Consequently, the application of the correction factor produced a greater overestimation for AMB than FACE data. Nevertheless, the effects of the change in light conditions are much smaller than the effects of changes in soil water on plant growth. In our field experiment, the CO2 enrichment increased SWC under both sufficient and restricted water supply. This CO2 response is similar to the results of maize studies done in the greenhouse (Samarakoon and Gifford, 1996) and in the field (Leakey et al., 2006; Markelz et al., 2011) but in contrast to the findings with sorghum (Conley et al., 2001). The soil water response is based on the decrease in transpiration rate under high [CO2 ] (Ghannoum et al., 2000). Concomitant measurements of plant transpiration rate in our experiment by means of stem sap flow sensors in 2007 indicated a decrease of plant water use of nearly 25% in the WET FACE plots as compared to the WET AMB plots (data unpublished). However, the CO2 effect on PAW was lower than one would expect from this number. This indicated that a large fraction of the remaining soil water resulting from the reduced transpiration was probably lost by augmented evaporation as demonstrated by Wilson et al. (1999) with a model approach. However, our attempt to minimize evaporative water loss by soil cover with a straw layer in the second growing season to test this assumption was not successful. The results were inconsistent. The reason for that might be that the straw layer did not only prevent evaporation from the upper soil layer, but also absorbed part of the rainfall which subsequently evaporates from the straw layer into the atmosphere. Nevertheless, it may be speculated that the water savings in the soil due to CO2 enrichment could be optimized by cover if rainfall is seldom and amounts are high or if the water is supplied by drip irrigation installed below the mulch layer. The smaller soil water depletion under FACE than under AMB has contributed to the maintenance of higher leaf turgor as indicated by RWC and the delay of leaf curling under drought during a hot weather period at the end of July in 2008. In the WET treatment PAW was always above 50% of the field capacity, which is the threshold below which growth of monocots is affected by soil water availability (Sadras and Milroy, 1996). Maize growth measured at final harvest was not increased by the CO2 enrichment in the WET treatment. This is in agreement with the results obtained in two FACE studies (Leakey et al., 2006; Markelz et al., 2011) and several studies done in enclosures (Bethenod et al., 2001; Kim et al., 2007; Rudorff et al., 1996; Samarakoon and Gifford, 1996). In addition, measurements of crop growth over the vegetation period yielded no CO2 effect under WET conditions except of the harvest data from the 5th August in 2008, when plants grown under FACE had a slightly significant higher total dry weight than plant from ambient plots. However, during the preceding days the weather was quite hot with a high atmospheric demand. It is known that the threshold below which leaf gas exchange is affected by PAW increases with atmospheric demand (Sadras and Milroy, 1996). Thus, the positive CO2 effect detected in early August in the WET plots does not contradict the findings from other harvests showing no CO2 response under WET. It rather indicates that over a short period at the end of July SWC content was not sufficient for the crop resulting in a decrease of photosynthesis of AMB plots but not of FACE plots due to the water saving effect of elevated [CO2 ]. In our FACE experiment leaf senescence was significantly influenced by elevated [CO2 ] under WET conditions. There was a higher dry weight of dead leaves at the end of both seasons in FACE plots than in AMB plots. This was also recognized by the LAI data at the end of September in 2008 when a slightly significant interaction of CO2 and water supply was detected due a decrease in

19

LAI in the FACE WET but not in the FACE DRY treatment. Such a CO2 response has also been recorded with maize under controlled environmental conditions (King and Greer, 1986) and in a previous FACE experiment with sorghum (Ottman et al., 2001). One possible reason for the accelerated senescence under CO2 enrichment could be the decrease in leaf transpiration which in turn increases leaf temperature (Triggs et al., 2004) resulting in an acceleration of plant development. The strong drought stress applied in 2008 caused a decline in LAI which was temporarily mitigated by CO2 enrichment as observed in a field experiment with sorghum (Ottman et al., 2001) and a greenhouse study with maize (Samarakoon and Gifford, 1996), but was not detectable under controlled environmental conditions (King and Greer, 1986). Moreover, in the present field study drought stress decreased crop growth and yield, however, this effect was diminished by CO2 enrichment as it was previously shown in one greenhouse study (Samarakoon and Gifford, 1996), but not in two others (King and Greer, 1986; Kang et al., 2002). Grain yield was more increased than biomass yield under FACE and the interaction of CO2 and water supply on yield and yield components was greater than previously observed for another C4 crop (Ottman et al., 2001). For example, the CO2 effect under restricted water supply on biomass and grain yield amounted to 24% and 41% in the current maize FACE experiment and to 15% and 20% in a previous sorghum FACE experiment (Ottman et al., 2001). Grain yield is particularly sensitive to water deficits during the early phase of plant reproduction (e.g. Otegui et al., 1995). In the experiment in 2008, PAW in the DRY AMB treatment reached the first minimum 3 days after anthesis. In addition, atmospheric demand was quite high during this period and the plants showed visible symptoms of drought stress. However, under DRY FACE PAW was much higher due to the water savings in the preceding period and symptoms of drought stress like leaf curling and leaf relative water content were much smaller than under DRY AMB. These findings indicate that crop growth was much more decreased by drought under AMB than under FACE treatment in the period which is most important for final grain number. This seems to be responsible for the finding that the CO2 effect was much stronger on grain yield than on total biomass. Soil water deficit decreases crop growth by reducing PAR absorption due to changes in green leaf area (Stone et al., 2001) and by reducing RUE due to effects on stomatal conductance (Sinclair and Muchow, 1999). It has been shown in field studies with maize that RUE is more affected by drought than PAR absorption (Earl and Davis, 2003; Stone et al., 2001). Similar findings were obtained in the present experiment, with both mechanisms contributing to the decrease in plant growth under drought in 2008. However, the interference of the rain shelter with incident radiation has to be taken into account. The rain shelter decreased incident PAR by ca. 7% over the season. If accumulated seasonal radiation absorption of the DRY plots is adjusted for this value, the effect of water deficit on this parameter adds up to −9% and −2% for the AMB and FACE plots, respectively. The effect on RUE amounted to −18% and −2% for the two CO2 treatments. Thus, in the present study water deficit influenced crop growth under ambient [CO2 ] primarily by decreasing RUE, while radiation absorption was less affected which corresponds to previous findings (Earl and Davis, 2003; Stone et al., 2001). The water savings under CO2 enrichment prevented the occurrence of drought stress effects on both RUE and radiation absorption. The effect of CO2 enrichment on RUE of maize has already been measured in a previous study but only under sufficient water supply when no CO2 effect on RUE was detected (Rudorff et al., 1996). There is strong evidence that elevated [CO2 ] does not directly stimulate C4 photosynthesis (Leakey, 2009), as confirmed by the growth data of the present FACE experiment with maize over

20

R. Manderscheid et al. / Europ. J. Agronomy 52 (2014) 11–21

two seasons. Maize will only benefit from elevated [CO2 ] when water supply is limited, because the CO2 effect on stomatal conductance results in soil water conservation and retardation of soil water depletion. Beside this CO2 effect on transpiration, increases in exploitation of soil water could also contribute to an increase of maize growth under limited water availability. However, there was no difference in water use in the DRY plots between the plants grown under AMB and FACE in our study. Moreover, in a FACE experiment with sorghum rooting depth was not enhanced by CO2 enrichment (Wall et al., 2001). Thus, the decrease in transpiration rate and the resulting increase in WUE might be the main mechanism for explaining the growth response of maize to CO2 enrichment under drought. In our experiment, WUE of total biomass and grain yield production included the water lost by both transpiration and evaporation. Evaporation can contribute up to one third of the total seasonal water use for a well watered maize crop (Liu et al., 2002). WUE was higher under DRY than WET conditions. This was also observed by others (Chun et al., 2011; Conley et al., 2001; Otegui et al., 1995) and ascribed to differences in evaporation (Otegui et al., 1995). CO2 enrichment did not affect WUE of maize in the first year. The reasons for this remain open. Probably as modelled by Wilson et al. (1999) the water conserved by decreased transpiration under FACE was lost by increased evaporation. In the second season, when evaporation in the DRY plots was small due to the low SWC, a significant interaction of CO2 and water supply was detected. The CO2 effect on WUE amounted to +10% and +25%, respectively, in the WET and DRY treatments. Again the smaller CO2 effect under WET might be due to a higher evaporation under FACE than AMB resulting from differences in SWC. Moreover, it could be assumed that in the DRY plots evaporation was quite small and thus, the CO2 induced decrease in transpiration became evident. In the sorghum FACE study WUE also increased by CO2 enrichment, while the effect was quite similar under sufficient and restricted water supply and amounted to 16% (Conley et al., 2001). WUE has been analysed in several CO2 enrichment studies done in greenhouses (Bethenod et al., 2001; Samarakoon and Gifford, 1996) and in controlled environment chambers, where evaporation was impeded by the plastic screen (Bethenod et al., 2001) or where daily water use was corrected for evaporation using weight loss from pots without plants (Samarakoon and Gifford, 1996). In these experiments the CO2 effect on WUE ranged from +23% (Bethenod et al., 2001) to +55% (Samarakoon and Gifford, 1996) depending on the CO2 enrichment level. If these values are recalculated for an increase in [CO2 ] of 170 ␮l l−1 as in our FACE study, the respective numbers are +13% (Bethenod et al., 2001), +23% (King and Greer, 1986) and +24% (Samarakoon and Gifford, 1996). In a more recent experiment done in sunlit growth chambers, the CO2 effect on WUE was highest under drought and amounted to +21% for a 170 ␮l l−1 increase in [CO2 ] (Chun et al., 2011). Thus, in most of these studies the CO2 effect on WUE was quantitatively similar to our findings in the field (+25%).

5. Conclusions The present FACE study with maize in which for the first time this crop was exposed to CO2 enrichment simultaneously under high and low water availability, clearly showed that rising [CO2 ] will benefit maize growth only under drought conditions. The drought stress treatment was successfully achieved in the second experimental season by combining the FACE technique with rain shelters. Maize growth benefited from CO2 enrichment under drought mainly due to higher RUE and WUE. The findings also indicate that maize needs approximately one quarter less water if [CO2 ] increases by 170 ␮l l−1 . This water saving effect by [CO2 ]

elevation can mitigate negative effects on maize growth resulting from decreases in summer precipitation as predicted by climate change models for the future (Meehl et al., 2007). There will be an increasing demand for crop production in the future not least because of the additional usage to produce biofuels (Leakey, 2009). Our study confirms previous findings (Leakey, 2009) that growth of C4 crops will only benefit from the increase in [CO2 ] when water supply is limited. Thus, under sufficient water supply and rapidly increasing [CO2 ] C3 crops will have an increasingly better growth performance in the future as compared to C4 crops. In addition, WUE of C3 crops is also strongly increased by [CO2 ] elevation under drought stress. Assuming a linear response to CO2 enrichment the effect of a 170 ␮l l−1 increase in [CO2 ] on WUE of C3 crops was maximal 23% in a field study in the US (Hunsaker et al., 1996) and 26% in Germany (Manderscheid and Weigel, 2007). Consequently, the benefits of increasing [CO2 ] for crop growth under limited water supply seem not to be very different between C4 and C3 crops. However, the per se higher WUE of C4 as compared to C3 crops (Zwart and Bastiaanssen, 2004) might still promote the growth performance of C4 crops under conditions of restricted water supply. Acknowledgements This research was supported by the German Federal Ministry of Education and Research (BMBF) and was part of the project LandCaRe 2020. The FACE apparatus was engineered by Brookhaven National Laboratory and we are grateful to Keith Lewin and Dr. John Nagy for their support. We acknowledge the technical assistance and the work of the people contributing to the experiment: P. Braunisch, Dr. S. Burkardt, A. Kremling, R. Isaak, A. Mundt, E. Nozinski, E. Schummer, and R. Staudte. The Experimental Station of the Friedrich Loffler-Institute, Braunschweig is thanked for conducting the agricultural measures at the experimental area. References Ainsworth, E.A., Rogers, A., 2007. The response of photosynthesis and stomatal conductance to rising [CO2 ]: mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270. Bethenod, O., Ruget, F., Katerji, N., Combe, L., Renard, D., 2001. Impact of atmospheric CO2 concentration on water use efficiency of maize. Maydica 46 (2), 75–80. Bond, J.J., Willis, W.O., 1969. Soil water evaporation—surface residue rate and placement effects. Soil Sci. Soc. Am. Proc. 33, 445–448. Chun, J.A., Wang, Q., Timlin, D., Fleisher, D., Reddy, V.R., 2011. Effect of elevated carbon dioxide and water stress on gas exchange and water use efficiency in corn. Agric. For. Meteorol. 151, 378–384. Conley, M.M., Kimball, B.A., Brooks, T.J., Pinter, P.J., Hunsaker, D.J., Wall, G.W., Adam, N.R., Lamorte, R.L., Matthias, A.D., Thompson, T.L., Leavitt, S.W., Ottman, M.J., Cousins, A.B., Triggs, J.M., 2001. CO2 enrichment increases water-use efficiency in sorghum. New Phytol. 151 (2), 407–412. Cousins, A.B., Adam, N.R., Wall, G.W., Kimball, B.A., Pinter, P.J., Leavitt, S.W., Lamorte, R.L., Matthias, A.D., Ottman, M.J., Thompson, T.L., Webber, A.N., 2001. Reduced photorespiration and increased energy-use efficiency in young CO2 -enriched sorghum leaves. New Phytol. 150, 275–284. Driscoll, S.P., Prins, A., Olmos, E., Kunert, K.J., Foyer, C.H., 2006. Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves. J. Exp. Bot. 57, 81–390. Earl, H.J., Davis, R.F., 2003. Effect of drought stress on leaf and whole canopy radiation use efficiency and yield of maize. Agron. J. 95, 688–696. Easterling, W.E., Aggarwal, P.K., Batima, P., Brander, K.M., Erda, L., Howden, S.M., Kirilenko, A., Morton, J., Soussana, J.F., Schmidhuber, J., Tubiello, F.N., 2007. Food, fibre and forest products. In: Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.), Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp. 273–313. Erbs, M., Manderscheid, R., Weigel, H.J., 2011. A combined rain shelter and free-air CO2 enrichment system to study climate change impacts on plants in the field. MEE, doi:10.1111/j.2041-210X.2011.00143.x. FAOSTAT, 2009. Online at http://faostat.fao.org. Ghannoum, O., Von Caemmerer, S., Ziska, L.H., Conroy, J.P., 2000. The growth response of C4 plants to rising atmospheric CO2 partial pressure: a reassessment. Plant Cell Environ. 23, 931–942.

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