Effect of CO2 enrichment on growth and daily radiation use efficiency of wheat in relation to temperature and growth stage

Europ. J. Agronomy 19 (2003) 411 /425 www.elsevier.com/locate/eja

Effect of CO2 enrichment on growth and daily radiation use efficiency of wheat in relation to temperature and growth stage Remy Manderscheid a,*, Stefan Burkart a, Andreas Bramm b, HansJoachim Weigel a b

a Institute of Agroecology, Federal Agricultural Research Centre, Bundesallee 50, D-38116 Braunschweig, Germany Institute of Crop and Grassland Science, Federal Agricultural Research Centre, Bundesallee 50, D-38116 Braunschweig, Germany

Received 21 November 2001; received in revised form 5 September 2002; accepted 5 September 2002

Abstract The objectives of the present study were to examine (i) the effect of whole season CO2 enrichment on seasonal radiation absorption and radiation use efficiency of above ground biomass production (RUE1) of wheat, (ii) the relationship between daily radiation use efficiency and temperature, and (iii) the effect of CO2 enrichment on this relationship in the period before and during grain filling when plant growth is assumed to be source and sink limited, respectively. During two consecutive years wheat (Triticum aestivum L. cv. Minaret) was grown in open-top chambers at different plot sizes (1 and 3 m2) at ambient and elevated CO2 concentrations (ca.
/280 ppm above ambient) with sufficient water and nutrient supply and analysed for final biomass and grain yield. In the 2nd year also light absorption by the green canopy and above ground biomass production were measured during the whole season. Canopy CO2 exchange rates (CCER) were recorded on 50 days (2nd year) from stem elongation until canopy senescence with canopy chambers. CCER were used for the calculation of daily radiation use efficiency of the net CO2 flux (dRUE2) before and during grain filling. Daily net carbon assimilation was linearly related to absorbed photosynthetic active radiation. Mean seasonal RUE2, which was calculated from this relationship, was increased by CO2 enrichment. This corresponded to the findings for RUE1. Seasonal light absorption was unaffected by the CO2 treatment. Final biomass and grain yield were increased under CO2 elevation by B/11 and B/13% in the 1st and 2nd year, respectively. Regression analysis yielded a significant negative relationship between dRUE2 and temperature under ambient CO2 in the period before and during grain filling. CO2 enrichment mitigated this negative relationship in the period only before but not during grain filling. The present experimental findings support the theoretically expected decrease of RUE at ambient CO2 and the increase of the CO2 effect with temperature in the preanthesis phase. The results also indicate that the positive CO2 x temperature interaction on canopy assimilation disappears during grain filling, which might be responsible for the decrease of the CO2 effect on plant biomass between anthesis and grain maturity. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Development; Elevated carbon dioxide; Growth; Open-top chambers; Radiation use efficiency; Wheat

* Corresponding author. Tel.:
/49-531-596-2579; fax:
/49-531-596-2599. E-mail address: [email protected] (R. Manderscheid). 1161-0301/02/$ - see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 1 1 6 1 - 0 3 0 1 ( 0 2 ) 0 0 1 3 3 - 8

412

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

1. Introduction Potential effects of future atmospheric CO2 enrichment on crop growth are estimated e.g. by using canopy based models (Goudriaan et al., 1999), in which daily crop growth is calculated from the product of the photosynthetic active radiation absorbed by the green canopy (APAR) and the radiation use efficiency of dry matter production (RUE). RUE has been found to be stable for a plant species across different environments (Sinclair and Muchow, 1999). The photosynthesis versus PAR response curve of a single leaf may be defined by the upper assymptote and light saturated rate of net CO2 fixation, and the initial slope, which represents the quantum yield F. It is suggested that radiation saturation is uncommon or of short duration for wheat canopies in temperate environments and therefore F dominates the rate of canopy photosynthesis (Baker et al., 1988). The stability of RUE is explained by the constancy of the photosynthetic efficiency (F ) of the canopy and the close relation between crop respiration and crop photosynthesis (Hay, 1999). However, for C3 plants F decreases at ambient CO2 concentrations with increasing temperature due to an increase in the affinity of Rubisco for O2 relative to CO2 and the reduced solubility of CO2 compared with O2. Elevated CO2 concentrations compensate for the decreased CO2 affinity of Rubisco and the decreased CO2 solubility at high temperature. Thus, the temperature related decrease of F is mitigated by high CO2 concentrations (Baker et al., 1988; Long, 1991). Moreover, maintenance respiration of the crop also varies with temperature. Therefore, the temperature sensitivity of both F and maintenance respiration implies that RUE depends on temperature, as has been shown in a model derived by Haxeltine and Prentice (1996). In addition, these authors also demonstrated the temperature dependence of RUE to be modified by atmospheric CO2 concentration. Most recently, the sensitivity of RUE of wheat to biophysical parameters has been assessed and it has been found that RUE is mainly affected by the fraction of diffuse light and by temperature (Choudhury, 2000).

However, experimental evidence for a temperature dependence of RUE is still scarce. Kumar et al. (1996), who analysed the variability in RUE of castor beans in relation to climatic parameters, observed a negative relationship of RUE with temperature. There is strong experimental evidence that RUE of wheat depends on water vapour pressure deficit, radiation environment and crop nitrogen status (Hay, 1999; Sinclair and Muchow, 1999). Moreover, it is generally accepted that RUE declines after anthesis (Hay, 1999), but remains unclear whether this change is related to growth stage or temperature or sink size of the grains (Fischer, 1993; Miralles and Slafer, 1997). Wheat growth is not always source limited (Evans and Wardlaw, 1996). It is assumed that there is a feed-forward effect of source size on sink size in the early growth stages while at later stages there are feed-back effects of sink demand on the photosynthetic rate of the plant. Grain number is fixed at anthesis and is strongly related to the source activity before this stage (Fischer, 1985, 1993). After anthesis crop growth is mainly composed of grain growth which is determined principally by temperature (Sofield et al. 1974). Previous CO2 enrichment studies with wheat have shown large variations of, e.g. biomass and yield response to CO2 under optimum growing conditions (Bender et al., 1999; Dijkstra et al., 1999; Pinter et al., 1996). Since plant growth was neither limited by nutrient nor by water supply, the variation in CO2 response could be expected to be based on the interaction between genotype, climatic conditions and atmospheric CO2 concentration. Detailed studies on the effect of CO2 and temperature did not reveal a generally positive interaction on these variables (Batts et al., 1997). This is explained by the fact that final yield is determined by several processes which are potentially altered in different ways with different CO2 and temperature conditions (Morison and Lawlor, 1999). The CO2 enhancement factor of plant biomass was found to decline toward the end of the growing period (Fangmeier et al., 1996; Mulholland et al., 1997; Pinter et al., 1996). This corresponds to the finding that photosynthetic capacity was not affected before but

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

after anthesis (Mitchell et al., 1999) and that the CO2 related stimulation of net photosynthetic rate started to decline during grain filling (Dijkstra et al., 1999; Garcia et al., 1998). Thus, it seems that also changes in source /sink relationship contribute to the final CO2 effect on grain yield. At the canopy level CO2 enrichment was observed to increase leaf area index (Batts et al., 1998; Mulholland et al., 1997, 1998a). Seasonal radiation absorption by the green canopy was found to be either increased (Mulholland et al. 1998a; Batts et al., 1998) or unaffected (Pinter et al., 1996; Rudorff et al., 1996). It was concluded that the CO2 effect on crop growth was mainly based on an increase in RUE (Mulholland et al., 1998a; Pinter et al., 1996; Rudorff et al., 1996). In canopy based models the effect of CO2 elevation on crop growth is normally simulated as a multiplier of RUE (Goudriaan et al., 1999; Jamieson et al., 2000), but the theoretically expected interaction of temperature and CO2 concentration on F and thus on RUE has not yet been considered. Also effects of sink size on RUE during the grain filling period are not taken into account. Melkonian et al. (1998) in using this approach included an adjustment of RUE for variation in ambient vapour pressure deficit. In the present study growth and canopy net CO2 flux of wheat cultivated at ambient and elevated atmospheric CO2 concentrations were measured over two seasons. The objectives were (i) to determine the CO2 effect on APAR and RUE and (ii) to test whether daily RUE calculated from canopy net CO2 flux is related to temperature and how this relation is affected by atmospheric CO2 concentration in the period before and after grain filling, when crop growth is suggested to be either mainly source or sink limited, respectively.

2. Materials and methods 2.1. Plant growth conditions and CO2 fumigation In 1998, spring wheat (Triticum aestivum cv. Minaret) was grown in simulated field plots in large volume soil containers (1 m diameter, 0.45 m

413

depth) buried in the ground, while in 1999 the plants were sown on an experimental field site (26 m/60 m) of the Federal Agricultural Research Centre in Braunschweig, Germany, prior to installation of eight open top chambers (OTC) and the plot area per chamber was 3 m2. The OTCs were cylindrical (3.2 m diameter, 3.4 m height) and a more detailed description is given by Weigel et al. (1992). In both years, the boundaries of the canopies were formed by shading clothes, which were moved up with the height of the plant to minimize edge effects. The soil, which was used in both years, was a loamy sand (pH 6.5) with low organic matter content (1.5%). CO2 enrichment was carried out in OTC as described by Weigel et al. (1992). In both years plants were sown at a density of 350 seeds m 2 (9 cm row distance). Four of the eight OTCs used in each year were operated at high CO2 concentrations 24 h per day. CO2 enrichment was started after emergence (Table 1) and continued until grain maturity. CO2 concentration was measured in all four enriched chambers and in at least two of the four ambient CO2 chambers. Air samples from the chambers were taken continuously and analysed for atmospheric CO2 concentration once per hour by infrared gas analysis. Air temperature and relative humidity were measured psychometrically and light intensity was recorded with a LI-190 quantum sensor (LICOR, Lincoln, Nebraska, USA) in two chambers just above the canopy. Standard agronomic practice was followed in both years (Table 1) to prevent growth restriction by nutrient limitation and plant diseases. At the end of the growing season, a fungal infection occurred on the unchambered field plots, which could not be controlled. Consequently, data from the final harvest from these plots were omitted. The plots were irrigated approximately twice per week (2 /10 /25 mm) to keep total soil water content between 60 and 90% of field capacity, which was controlled by TDR sensors (P2Z, IMKO, Mikromodultechnik GmbH, Ettlingen, Germany).

414

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

Table 1 Timetable of crop management and plant growth stages (GS) according to Tottman and Broad (1987) (dae /days after emergence) 1998, OTC

1999, OTC

1999, ambient field

12 Mar 30 Mar (dae/0) 1 May (dae /32) 31 May (dae/62) 27 Jul (dae /120)

17 Mar 29 Mar (dae /0) 8 May (dae /40) 4 Jun (dae/67) 23 Jul (dae/116)

15 Mar 29 Mar (dae/0) 16 May (dae /48) 9 Jun (dae /72) 30 Jul (dae /124)

Harvests 1st 2nd 3rd 4th 5th Final

Aug

18 May 2 June 17 Jun 1 Jul 14 Jul Aug

18 May 2 June 17 Jun 10 Jul / /

CO2 fumigation start end

3 Apr 27 Jul

13 Apr 23 Jul

/ /

Fertilization (kg ha 1 ) 1st 2nd 3rd

40 N, 40 P2O5, 30 K2O, 24 Apr 100 N, 100 P2O5, 75 K2O, 5 May 60 N, 10 MgO, 12 May

100 P2O5, 70 K2O, 20 MgO, 12 Mar 90 N, 29 Apr 90 N, 21 May

100 P2O5, 70 K2O, 20 MgO, 12 Mar 90 N, 29 Apr 90 N, 21 May

Insecticides applications

Tamaron, 7 Apr Parathion, 21 Apr Perfekthion, 2 Jun

Tamaron, 9 Apr, 25 May, 1 Jul Ecombi, 21 June

Ripcord, 14 Jun

Fungicides applications

Opus Top, 30 Apr Dyrene, 2 June Matador, 2 June

Opus Top, 12 May Bayfidan, 21 Jun Matador, 1 Jul Dyrene, 1 Jul

Corbel, 14 Jun

Growth stages Sowing Emergence GS31 GS 65 GS 92

2.2. Analysis of canopy light interception, leaf area index and growth Analyses were done in the 2nd year in all OTCs and in four plots of 1.2 m /3 m of the ambient field area. Percentage of photosynthetic active radiation absorbed by the green canopy (% APAR) was measured approximately once per week using a line quantum sensor (transmission meter EMS 7, PP Systems, Herts, UK). The measurements 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). % APAR was calculated using the following equation: % APAR  (J0 Jr Jc )=J0

(1)

Several destructive harvests were carried out starting before anthesis (Table 1). Plant samples were always taken out of the canopy (/20 cm distance from the edge). The harvested areas

consisted of a row section of 30 cm length (1st / 5th harvest in OTCs), of 3 /50 cm length (final harvest) and of 2/50 cm length (1st/4th harvest in ambient field plots), respectively. After separation of the green and non-green leaves and stems the projected area of the green leaves and stems were measured with a leaf area meter (model LI3100 from LICOR) and used to calculate green leaf area index (GLAI). In 1998 a row section of 1.0 m length was harvested and used for analysis of final biomass and grain yield. Total above ground dry weights were determined after drying at 95 8C for 24 h. At maturity grain yield, ear number, grain number and mean kernel weight were determined after drying and threshing each individual ear. 2.3. Canopy net CO2 flux measurements The canopy CO2 exchange rate per unit ground area was measured using an open system consist-

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

ing of four transportable canopy chambers (1.7 m height, 1.0 m diameter) and a monitoring unit (Burkart et al., 2000). Air was blown into the chamber at the top of the system and leaves the chamber through three outlet tubes at the bottom. The air volume flow rate was measured by plate anemometers (Thies, Go¨ttingen, Germany) and kept between ca. 2 and 4 m3 min 1. The boundary layer resistances of the leaves were minimized by a stirring fan. Canopy CO2-uptake was measured as differences in CO2 molar fractions between the reference gas sample taken at the air inlet and the measuring gas sample taken from outlet tubes by an infra-red gas analyzer (Binos 100 4P, Rosemount, Hanau, Germany). In addition, absolute molar fraction of CO2 was determined every hour with the same IRGA. Air temperature above the canopy was measured by a shielded and ventilated NTCthermistor (PT100), and photosynthetic active photon flux density was registrated by a line quantum sensor (sample sensor of the transmission meter EMS 7, PP Systems, Herts, UK), which previously had been calibrated with the quantum sensor LI-190 from LICOR used for measurement of indicident radiation in the OTC. CO2 and climate data of each canopy chamber were recorded one or two times per hour and averaged over 5/10 min. The canopy chambers were rotated between different plots weekly to minimize chamber effects on the plants. Canopy CO2-exchange rate (CCER, mmol m 2 1 s ) was calculated as follows CCER

DCO2 × F Vm × A

(2)

where DCO2 is the molar fraction difference of CO2 (mmol mol1), measured with IRGA, F is the volume flow rate (m3 s 1), A is the ground area (0.79 m2). Vm is the molar volume of air: Vm 

(T
273:16) × R P

(3)

where T is the temperature (K), R is the gas constant (8.314 J mol 1 K 1) and P is the air pressure (1.013 /105 Pa).

415

Canopy gas exchange was measured in OTCs with ambient and elevated atmospheric CO2 concentrations on ca. 50 days in 1999 from stem elongation until end of grain filling (44 B/dae B/ 109). 2.4. Calculation of seasonal and daily radiation use efficiency Seasonal RUE of above ground biomass production (RUE1, g dry weight mol1 photons) was calculated as the slope of the relation between accumulated biomass and accumulated photosynthetic active radiation absorbed by the green canopy (APAR). APAR was calculated from incident photosynthetic active radiation measured in the OTC and the % APAR readings. Seasonal RUE of the canopy net CO2 flux (RUE2) was calculated using the data from all days of canopy gas exchange measurements. RUE2 measured in mol CO2 per mol photons was converted to dry weight by taking into account the carbon content of the above ground biomass. Carbon content of above ground biomass was measured from plants sampled in 1999 at the first node stage and two weeks before grain maturity, respectively, using the Carbon Determinator IR12 (LECO Corporation, Michigan, USA). A mean carbon percentage of 39.5% was used for both CO2 treatments, as carbon content measured at the first (39.2%) and second date (39.8%) did not show a significant CO2 effect. Daily RUE (dRUE2) was calculated as the integral of the net daily canopy CO2 flux (0 /24 h) divided by the absorbed radiation. This was estimated from the incident photosynthetic active radiation measured in the canopy chamber and the % APAR readings for this particular day and OTC. dRUE2 was calculated from all measuring days except of the period of canopy senescence (dae /94). 2.5. Statistical analysis The effects of CO2 enrichment on growth variables and yield components were tested by analysis of variance (ANOVA). Multiple range test (LSD) was used to establish significant differ-

416

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

ences between treatment means. Year or harvest date was included as an additional independent variable when appropriate. The different kinds of radiation use efficiency (see above) were calculated by linear regression analysis and treatment effects were detected by comparing the confidence interval of the slopes. Linear regression analysis was also used to detect a significant relationship between dRUE2 and temperature, and the influences of growth phase and atmospheric CO2 concentration on the slopes of this relationship were examined by comparing the confidence interval.

3. Results 3.1. CO2 concentration and climatic conditions during the growing season The 24-h seasonal mean of the atmospheric CO2 concentrations in the control and CO2 enriched OTCs amounted to 381 and 671 ppm in 1998, and to 408 and 684 ppm in 1999, respectively. Temperature increased steadily from plant emergence to maturity (Fig. 1). The mean temperature observed for the 30 days interval before anthesis was ca. 2 8C lower than the respective number after anthesis (Table 2). This long-term difference was superimposed by short-term temperature fluctuations of up to 108 C within a few days (Fig. 1). The two vegetation periods were similar regarding the seasonal variation in temperature, but radiation was higher in 1999 than in 1998 (Table 2). Inside the OTCs radiation was 20/ 30% lower and temperature by up to 18C higher as compared to the ambient field plots (Table 2). 3.2. Seasonal course of green leaf area index, above ground biomass production and yield Seasonal course of GLAI is shown in Fig. 2. Two-way ANOVA for the data from the different harvests and CO2 treatments yielded a significant CO2 effect (P /0.01). CO2 enrichment increased GLAI in the time period from canopy closure until the start of canopy senescence, i.e. harvest number 2 /4 (Fig. 2). The relative CO2 effect on GLAI

averaged over this interval amounted to 35%. However, there was no significant CO2 effect on seasonal APAR which could be explained by the fact that GLAI of the ambient CO2 treatment was already quite high ( /3). Plant development was accelerated (Table 1) and the initial increase in GLAI was much steeper in OTCs as compared to ambient field plots (Fig. 2). This can be attributed to the increase in air temperature in the OTCs (Table 2). Accumulation of above ground biomass was almost linearly related to APAR (Fig. 3) and the resulting slope, i.e. RUE1, was significantly increased by CO2 enrichment (Table 3). Calculated RUE1 of the non-chambered plots was significantly lower than the number observed inside OTCs at ambient CO2 (Table 3). The positive CO2 response of RUE1 implies a constant relative CO2 effect on plant growth during the vegetation period. However, a comparison of the growth data of the individual harvests showed that the stimulation in biomass amounted to ca. 50% at 3rd and 4th harvest, but only to 12% at grain maturity (Table 4). While biomass yield was almost identical between years, grain yield showed a slightly significant interannual difference, which was related to a lower grain weight in 1998 than in 1999 (Table 4). CO2 elevation increased ear number and grain number since grain number per ear was unaffected. The resulting stimulation of grain yield amounted to 5 and 12% in the 1st and 2nd year, respectively, however, this was not significant. The low CO2 response in 1998 was related to a decrease in mean grain weight, but the standard deviation for this value was unusually high. 3.3. Canopy net CO2 flux There was a linear relationship between the daily net canopy CO2 flux and the amount of APAR (Fig. 4). Variation in APAR accounted for /70% of the variation in daily net carbon fixation. The 95% confidence interval of the intercept obtained by regression analysis of the data indicated the intercept not to be significantly different from zero. Thus, the slopes forced

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

417

Fig. 1. Seasonal course of air temperature in OTCs in 1998 (dashed line) and 1999 (full line).

through zero of the relationship between canopy net CO2 fixation and APAR were calculated. The slopes can be taken as an integral measure of radiation use efficiency of net carbon production of the canopy including above and below ground dry matter production (RUE2) averaged over the main growth period from stem elongation until flag leaf senescence. Based on the confidence interval there was a significant CO2-related increase in RUE2 in 1999. RUE2 values on a dry weight basis were 23% higher both under ambient and elevated CO2 than RUE1 values obtained from destructive harvests (Table 3). Thus, it can be concluded that 81% of the total canopy net CO2 fixation was partitioned to above ground plant parts and the remaining 19% to the roots. Canopy CO2 exchange data were selected from those days when GLAI /3 and the canopy absorbed ]/75% of the incident PAR. These

data were divided into the period before start of grain filling (44 B/daeB/72) and during grain filling (74 B/dae B/95). Daily RUE2 (dRUE2) was calculated for these different periods and CO2 treatment levels. Multiple regression analysis of the data before grain filling with dRUE2 as dependent variable and climatic conditions as independent variables (temperature, incident PAR and VPD) yielded no significant relationships under elevated CO2. However, under ambient CO2 the strongest relationship was detected between dRUE2 and temperature and incident PAR explained only a minor part of the variation of dRUE2. As temperature and radiation are coupled in the field, it is difficult to separate the effect of these two factors. Fig. 5 shows the observed relationship between dRUE2 and temperature for ambient CO2 plants during the period before grain filling at low (13 /18 mol m2 day1) and high incident photosynthetic active radiation

Table 2 Mean air temperature (8C) and mean incident photosynthetic active radiation (PAR, mol photon m 2 d 1) in open-top chambers (OTC) in 1998 and 1999, and at field plots in 1999 during 30 days before and after anthesis, respectively Days after anthesis

/29 to 0 1 /30

Temperature

PAR

OTC 98

OTC 99

field 99

OTC 98

OTC 99

Field 99

16.0 18.2

15.8 17.4

14.9 16.3

23.7 21.0

26.9 29.9

38.3 40.7

418

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

Fig. 2. Seasonal course of green leaf area index of wheat plants grown in 1999 at ambient field plots (field) and in OTCs under ambient (amb) and elevated (elev) atmospheric CO2 concentrations. Values represent means9/standard deviation (n/4).

(21 /37 mol m 2 day1). There was a significant relationship between dRUE2 and temperature especially for the ‘low light’ class, where both the amount and variation of incident radiation was small, and the findings indicate a decrease of dRUE2 with increasing temperature. The relationship between dRUE2 and temperature for both CO2 treatment levels is shown in Fig. 6 and the results of the regression analysis are summarized in Table 5. The findings for the period

before start of grain filling demonstrated a significant negative relationship between dRUE2 and temperature under ambient CO2, since the upper limit of 95% CI of the slope was lower than zero (Table 5). In addition, the results obtained during grain filling were similar to those obtained before grain filling. CO2 enrichment affected the dRUE2 / temperature relationship significantly in the period until anthesis. Thus, the data indicate that dRUE2 is negatively related to temperature under ambient

Fig. 3. Relationship between total above ground biomass and accumulated absorbed photosynthetic active radiation (APAR) of wheat canopies grown 1999 in OTCs at ambient (amb) and elevated (elev) atmospheric CO2 concentrations and in unchambered field plots (field). Values represent means9/standard deviation (n/4).

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

419

Table 3 Seasonal RUE of above ground biomass production (RUE1, given in g dry weight per mol photons) calculated from the data shown in Fig. 3, and RUE of canopy net CO2 flux calculated from Fig. 4 (RUE2, g d.w. mol 1 photons; mol carbon was converted to dry weight using a carbon percentage of dry matter of 39.5%, CI /Confidence Interval) Treatment

RUE2

RUE1

Ambient CO2 High CO2 Field

Mean

95% CI

r2

Mean

95% CI

0.949 1.25 0.721

0.818 /1.08 1.12 /1.38 0.686 /0.755

0.930 0.955 0.998

1.17 1.54 /

1.10 /1.24 1.48 /1.60 /

CO2 and that this negative relationship is mitigated by CO2 enrichment. However, during grain filling the dRUE2 /temperature relationship detected under high CO2 approached the finding of the ambient CO2 treatment. Moreover, the slopes found under high CO2 for the first and second measuring period seemed to be different, however, this was only significant using 90% CI.

4. Discussion Given a ratio of two moles photons per MJ solar radiation (Slomka, 1989), the seasonal RUE of above ground biomass production of wheat observed in the present study at the ambient field plots of 0.72 g mol1 photons amounted to 1.44 g MJ 1 which corresponds to the potential RUE of 1.4 g MJ 1 solar radiation summarized by Sinclair

and Muchow (1999). However, the value obtained within OTCs at ambient CO2 was 32% higher as compared to the field. This is in agreement with several other OTC studies, where RUE was observed to be higher in the chambers as compared to ambient field conditions (Mulholland et al., 1998a; Rudorff et al., 1996; Unsworth et al., 1984). One reason for this difference seems to be the increase in the proportion of diffuse radiation resulting from the chamber foliage (Sinclair and Muchow, 1999). The enclosure method used in the present study to measure canopy net carbon flux included net CO2 exchange of the canopy and gross carbon transfer into the rhizosphere. CO2 fluxes derived from root respiration and soil microbial respiration were assumed to be excluded due to the slight overpressure in the canopy chamber (Nakayama and Kimball, 1988). Thus, radiation use efficiency

Table 4 P -values of the two-way ANOVA for the effects of year and CO2 (ambient/elevated) on growth variables of wheat at maturity, and the mean values (9/standard deviation (n/4)) for the different treatments and years Variable

P -value

1998

Year CO2 y*C Amb. CO2 2

Biomass (g m ) Ear number (m 2) Grain number per ear Mean grain weight (mg) Grain yield (g m 2) Harvest index (*)

P B/0.10. * P B/0.05. ** P B/0.01. *** P B/0.001.

/ ** *** / (*)

***

(*)

* / / /

/ / / (*)

/ /

18009/100 7009/70 34.69/1.0 34.59/1.6 8359/54 0.4589/0.011

1999 High CO2

% Effect

Amb. CO2

High CO2

% Effect

19899/238 8179/86 34.59/0.6 31.19/2.9 8759/124 0.4329/0.029

10.5 16.7 /0.3 /10.1 4.8 /5.8

18429/209 5889/68 44.99/1.8 34.49/1.8 9019/80 0.4909/0.015

20689/250 6599/71 44.19/1.9 34.89/1.6 10149/125 0.4909/0.007

12.2 12.0 /1.8 1.4 12.5 0.0

420

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

Fig. 4. Relationship between daily net canopy CO2 exchange rate (CCER) and the daily amount of absorbed photosynthetic active radiation (APAR) of wheat grown at ambient (amb) and elevated (elev) CO2 in 1999. Linear regression lines were fitted to the data; ambient CO2, y /0.0385x , r2 /0.73, 95% CI: 0.0362 /0.0408; elevated CO2, y/0.0506x , r2 /0.88, 95% CI: 0.0486 /0.0526.

calculated from daily net canopy CO2 fluxes (RUE2) should be higher than RUE1 which is based on above ground biomass only. Cereal species translocate about 20 /30% of assimilated carbon to the soil (Kuzyakov, 2001). According to Swinnen et al. (1994) carbon transfer to the rhizosphere amounts to ca. 22% of the total net assimilation averaged over the time period from stem elongation until grain maturity. This number

is quite similar to the difference of 23% between RUE2 and RUE1 found in the present study for both CO2 treatments in 1999. CO2 enrichment enhanced leaf area index which corresponds to previous findings (Batts et al., 1998; Mulholland et al., 1997, 1998a). However, this did not result in a significant increase in radiation absorption over the whole season, since the greatest stimulation occurred when the canopy

Fig. 5. Relationship between dRUE2 and air temperature for wheat canopies grown at ambient CO2 and for the period before start of grain filling in 1999 at low ( B/20 mol m 2 day 1) and high ( /20 mol m 2 day1) incident PAR. The results of the linear regression analysis are: low PAR, y /0.109/0.0036x , r2 /0.81; high PAR, y/0.077/0.0020x , r2 /0.60.

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

421

Fig. 6. Relationship between dRUE2 and air temperature for wheat canopies grown in 1999 under ambient (amb) and elevated (elev) CO2 for the period before (A) and after start of grain filling (B).

already had reached complete soil cover i.e. when changes in leaf area index do not result in detectable changes in canopy light absorption. This is consistent with findings from studies of Pinter et al. (1996) and Rudorff et al. (1996), but contrasts with reports where canopy light absorption was found to be increased by high CO2 (Mulholland et al. 1998a; Batts et al., 1998). Although, in these studies leaf area index of the ambient CO2 treatment was quite low. In the present study, above ground biomass was increased during the vegetation period up to ca. 50% due to CO2 fumigation, but this effect diminished until maturity as has been observed in previous experiments (Fangmeier et al., 1996; Mulholland et al., 1997; Pinter et al., 1996). At final harvest a slight but insignificant stimulation of ca. 10% in final biomass and grain yield was

detectable, which is at the lower range of CO2 responses previously found for the wheat cultivar ‘Minaret’ in an European multi-site CO2 enrichment experiment (Bender et al., 1999; Fangmeier et al., 1996; Mulholland et al., 1997, 1998a). The CO2-related increase in plant growth found in the present study was based on a stimulation of RUE as was also observed by others (Mulholland et al., 1998a; Pinter et al., 1996; Rudorff et al., 1996), while seasonal light absorption was not influenced. The difference in the magnitude of relative CO2 effect on RUE and final biomass or grain yield could be attributed to the decline of the CO2 enhancement factor for biomass towards maturity. The main objective of the present study was to test whether daily radiation use efficiency calculated from canopy gas exchange measurements (dRUE2) is related to temperature as has been

Table 5 Results of the regression analysis of the relationship between dRUE2 (mol mol 1) and temperature (8C) of wheat in 1999 under two CO2 treatment levels (ambient, elevated) and for different periods (before start of grain filling (A), after start of grain filling (B)) CO2

Period

Range

Slope

Amb. Elev. Amb. Elev.

A A B B

12 /228C 12 /228C 16 /228C 15 /228C

/0.0028 /0.0007 /0.0018 /0.0023

(/0.0037, (/0.0017, (/0.0039, (/0.0032,

/0.0019) 0.0002) 0.0004) /0.0014)

Intercept

n

r2

0.094 (0.078, 0.110) 0.0705 (0.054, 0.087) 0.070 (0.030, 0.109) 0.090 (0.074, 0.106)

20 17 10 16

0.70 0.15 0.31 0.70

Slopes and intercepts are given with 95% confidence interval in parentheses, n/number of observation, range/range in daily mean temperature.

422

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

shown by theoretical analysis (Choudhury, 2000; Haxeltine and Prentice, 1996). In order to unravel this relationship additional growth factors which also might influence RUE were controlled or analysed separately. RUE is related to the lightsaturated CO2 assimilation rate for individual leaves which in turn depends on the nitrogen supply to the crop (Sinclair and Muchow, 1999). In the present case analysis of the nitrogen content of the plants at anthesis proved that the crop did no suffer from nitrogen deficiency (data not shown). Consequently, it can be assumed that at least for the period before start of grain filling light-saturated CO2 assimilation rates for individual leaves should have not varied due to nitrogen limitation. Possible effects of crop growth stage and changes in source /sink relations, respectively, on RUE were considered by analysing RUE separately for the period before and after start of grain filling, when growth is assumed to be either source or sink limited (Evans and Wardlaw, 1996). As light response curve of canopy photosynthesis becomes non /linear at very high irradiance levels and low GLAI (Sinclair, 1994), in the present study only gas exchange data from canopies with GLAI /3 were used. Another problem can arise from the carbon transfer to the rhizosphere which is included in the gas exchange measurements. However, dry matter allocated to the root is a great proportion of total assimilates produced at early growth stages but a small proportion during the later growth stages (Swinnen et al., 1994), when canopy gas exchange measurements were performed. Consequently, it can be supposed that variations in dRUE2 detected in the present study are due mainly to changes in radiation, temperature and atmospheric CO2 concentration. Although temperature and radiation are coupled in the field, the comparison of the dRUE2 /temperature relationship for cloudy and sunny days in 1999 supported the theoretical expectation that RUE under ambient CO2 concentration is more dominated by temperature than by incident radiation (Choudhury, 2000). Our results also showed a significant difference in the dRUE2 /temperature relationship between the two CO2 treatments indicating a CO2 /temperature interaction on dRUE2 as has

been theoretically expected (Haxeltine and Prentice, 1996). As the negative relation between dRUE2 and temperature is based on the increase in dark respiration and photorespiration with increasing temperature, the mitigation of this negative relationship under elevated CO2 concentrations may be due to the suppression of photorespiration, while dark respiration does not seem to be directly affected (Amthor, 1997). Under ambient CO2 the response of dRUE2 to temperature was not affected by the growth stage. However, under elevated CO2 the findings for the two developmental stages were slightly different, since during grain filling dRUE2 showed a relationship to temperature which was similar to the findings obtained under ambient CO2. Thus, our results indicate a strong CO2 /temperature interaction on plant growth before anthesis but not during grain filling. Although the dRUE2 /temperature relationship analysed for different PAR conditions indicates that PAR does not substantially modify this relation it cannot be excluded that part of this is a positive CO2 x PAR interaction which is also theoretically expected. The decrease of the CO2 effect on dRUE2 after anthesis is consistent with the response of canopy CO2 exchange to elevated CO2 levels observed by Dijkstra et al. (1999), the decrease of the CO2 effect on net photosynthetic rate at the leaf level (Mitchell et al., 1999; Garcia et al., 1998) and the decline of the CO2 enhancement factor of above ground biomass observed in the present and in previous experiments (Fangmeier et al., 1996; Mulholland et al., 1997; Pinter et al., 1996). During preanthesis plant growth is supposed to be mainly source limited and crop growth rate during the last weeks before anthesis is known to determine final grain number (Fischer, 1985, 1993). In the postanthesis period nearly all the assimilated carbon is used for grain growth, which is determined by two temperature dependent processes, namely the grain filling rate and grain filling duration (Sofield et al., 1974). Both processes seem to be unaffected by atmospheric CO2 concentration (Wheeler et al., 1996; Mulholland et al., 1998b). Consequently, CO2 elevation influences grain yield primarily by enhancing grain number as observed here and in previous studies

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

(Mulholland et al., 1997, 1998a; Wheeler et al., 1996). The comparison of the relationship between dRUE2 and temperature before and after anthesis gives a rough indication of the degree of source / sink limitation of grain growth during grain filling. The relationships found for the two periods under ambient CO2 were similar but those found under CO2 enrichment were slightly different. This points to a sink limitation of crop growth under high CO2 during the grain filling period. In our study air temperature averaged over 4 weeks before anthesis was ca. 2 8C lower than during the respective time period after anthesis. Given the positive CO2 /temperature interaction on net photosynthesis a greater CO2 related stimulation of carbon assimilation due to higher temperatures should be expected during grain filling than before anthesis. This could be the reason for the imbalance of the source /sink activities during grain filling under high CO2. The strong CO2 response of above ground biomass observed near anthesis and the subsequent decline of the CO2 enhancement factor until maturity could be explained by an initial increase in stem growth as observed in several studies (e.g. Fangmeier et al., 1996; Mulholland et al., 1998a; Pinter et al., 1996), which functions as a temporary storage buffer for assimilates and which can subsequently be used for grain growth. Based on the considerations outlined above the benefits of additional CO2 in the atmosphere for crop yield can better be exploited by readjusting the balance between source and sink activity during grain filling. Since the different temperature conditions result in a greater stimulation of potential source activity during grain filling than during the critical period determining grain number before anthesis, the source activity for the first period has to be increased. One possible solution might be to elongate the critical time period from terminal spikelet to heading, which has been demonstrated to raise the grain number of wheat (Miralles et al., 2000) and thus the sink activity during grain filling. In conclusion, the findings of the present study confirm the theoretical expected decrease of RUE with temperature, when crop growth depends on

423

source activity. Moreover, the results question the use of a constant multiplier of RUE to model effects of increased atmospheric CO2 concentrations on crop growth (Goudriaan et al., 1999; Jamieson et al., 2000). Rather, our findings suggest to include a temperature dependence of RUE which is modified by atmospheric CO2 concentration as has been applied by Haxeltine and Prentice (1996). In addition, it can be concluded that for understanding the effect of high CO2 on crop growth not only the interaction between atmospheric CO2 concentrations and weather conditions has to be taken into account but also the influence of the developmental stage of the plant.

Acknowledgements We are grateful to Peter Braunisch, Martina Heuer, Anke Mundt, Britta Mu¨ller, Peter Seehawer, Ralf-Dietrich Staudte and Wilfried Woyde for technical support, and we thank Frank Ewert, Rowan Mitchell and Daniel Rodriguez for helpful discussion. This research is part of the IMPETUSproject funded by the EC (ENV4-CT97-0496).

References Amthor, J.S., 1997. Plant respiratory responses to elevated carbon dioxide partial pressure. In: Allen, L.H., Jr., Kirkham, M.B., Olszyk, D.M., Whitman, C.E. (Eds.), Advances in Carbon Dioxide Effects Research. ASA Special Publication Number 61, Madison, WI. Baker, N.R., Long, S.P., Ort, D.R., 1988. Photosynthesis and temperature, with particular reference to effects on quantum yield. In: Long, S.P., Woodward, F.I. (Eds.), Plants and Temperature. Society for Experimental Biology, Cambridge. Batts, G.R., Morison, J.I.L., Ellis, R.H., Hadley, P., Wheeler, T.R., 1997. Effects of CO2 and temperature on growth and yield of crops of winter wheat over four seasons. Eur. J. Agron. 7, 43 /52. Batts, G.R., Ellis, R.H., Morison, J.I.L., Hadley, P., 1998. Canopy development and tillering of field-grown crops of two contrasting cultivars of winter wheat (Triticum aestivum L.) in response to CO2 and temperature. Ann. Appl. Biol. 133, 101 /109. Bender, J., Hertstein, U., Black, C.R., 1999. Growth and yield responses of spring wheat to increasing carbon dioxide,

424

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425

ozone and physiological stresses: a statistical analysis of ‘ESPACE-wheat’ results. Eur. J. Agron. 10, 185 /195. Burkart, S., Manderscheid, R., Weigel, H.J., 2000. Interacting effects on photosynthetic photon flux density and temperature on canopy photosynthesis of spring wheat under different CO2-concentrations. J. Plant Physiol. 157, 31 /39. Choudhury, B.J., 2000. A sensitivity analysis of the radiation use efficiency for gross photosynthesis and net carbon accumulation by wheat. Agric. For. Meteorol. 101, 217 / 234. Dijkstra, P., Schapendonk, A.H.M.C., Groenwold, K., Jansen, M., Van de Geijn, S.C., 1999. Seasonal changes in the response of winter wheat to elevated atmospheric CO2 concentration grown in open-top chambers and field tracking enclosures. Glob. Change Biol. 5 (5), 563 /576. Evans, L.T., Wardlaw, I.F., 1996. Wheat. In: Zamski, E., Schaffer, A.A. (Eds.), Photoassimilate Distribution in Plants and Crops: Source /Sink Relationships. Marcel Dekker, New York. Fangmeier, A., Gru¨ters, U., Hertstein, U., Sandhage-Hofmann, A., Vermehren, B., Ja¨ger, H.J., 1996. Effects of elevated CO2, nitrogen supply and tropospheric ozone on spring wheat. 1. Growth and yield. Environ. Pollut. 91, 381 /390. Fischer, R.A., 1985. Number of kernels in wheat crops and the influence of solar radiation and temperature. J. Agric. Sci. Camb. 105, 447 /461. Fischer, R.A., 1993. Irrigated spring wheat and timing and amount of nitrogen fertilizer. 2. Physiology of grain yield response. Field Crops Res. 33, 57 /80. Garcia, R.L., Long, S.P., Wall, G.W., Osborne, C.P., Kimball, B.A., Nie, G.Y., Pinter, P.J., Lamorte, R.L., Wechsung, F., 1998. Photosynthesis and conductance of spring-wheat leaves: field response to continuous free-air atmospheric CO2 enrichment. Plant Cell Environ. 21, 659 /669. Goudriaan, J., Shugart, H.H., Bugmann, H., Cramer, W., Bondeau, A., Gardner, R.H., Hunt, L.A., Lauenroth, W.K., Landsberg, J.J., Linder, S., Noble, I.R., Parton, W.J., Pitelka, L.F., Stafford, S.M., Sutherst, R.W., Valentin, C., Woodward, F.I., 1999. Use of models in global change studies. In: Walker, B., Steffen, W., Canadell, J., Ingram, J. (Eds.), The Terrestrial Biosphere and Global Change. Cambridge University Press, Cambridge, UK. Haxeltine, A., Prentice, I.C., 1996. A general model for the light-use efficiency of primary production. Funct. Ecol. 10, 551 /561. Hay, R.K.M., 1999. Physiological control of growth and yield in wheat: analysis and synthesis. In: Smith, D.L., Hamel, C. (Eds.), Crop Yield. Physiology and Processes. SpringerVerlag, Berlin. Jamieson, P.D., Berntsen, J., Ewert, F., Kimball, B.A., Olesen, J.E., Pinter, P.J., Porter, J.R., Semenov, M.A., 2000. Modelling CO2 effects on wheat with varying nitrogen supplies. Agric. Ecosyst. Environ. 82, 27 /37. Kumar, P.V., Srivastava, N.N., Victor, U.S., Rao, D.G., Rao, A.V.M.S., Ramakrishna, Y.S., Rao, B.V.R., 1996. Radiation and water use efficiencies of rainfed castor beans

(Ricinus communis L.) in relation to different weather parameters. Agric. For. Meteorol. 81, 241 /253. Kuzyakov, Y.V., 2001. Tracer studies of carbon translocation by plants from the atmosphere into the soil (a review). Eurasian Soil Sci. 34, 28 /42. Long, S.P., 1991. Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations */has its importance been underestimated? Plant Cell Environ. 14, 729 /739. Melkonian, J., Riha, S.J., Wilks, D.S., 1998. Simulation of elevated CO2 effects on daily net canopy carbon assimilation and crop yield. Agric. Syst. 58, 87 /106. Miralles, D.J., Slafer, G.A., 1997. Radiation interception and radiation use efficiency of near-isogenic wheat lines with different height. Euphytica 97, 201 /208. Miralles, D.J., Richards, R.A., Slafer, G.A., 2000. Duration of the stem elongation period influences the number of fertile florets in wheat and barley. Aust. J. Plant Physiol. 27, 931 / 940. Mitchell, R.A.C., Black, C.R., Burkart, S., Burke, J.I., Donnelly, A., de Temmmerman, L., Fangmeier, A., Mulholland, B.J., Theobald, J.C., Van Oijen, M., 1999. Photosynthetic responses in spring wheat grown under elevated CO2 concentrations and stress conditions in the European, multiple-site experiment ‘ESPACE-wheat’. Eur. J. Agron. 10, 205 /214. Morison, J.I.L., Lawlor, D.W., 1999. Interactions between increasing CO2 concentration and temperature on plant growth. Plant Cell Environ. 22, 659 /682. Mulholland, B.J., Craigon, J., Black, C.R., Colls, J.J., Atherton, J., Landon, G., 1997. Effects of elevated carbon dioxide and ozone on the growth and yield of spring wheat (Triticum aestivum L.). J. Exp. Bot. 48, 113 /122. Mulholland, B.J., Craigon, J., Black, C.R., Colls, J.J., Atherton, J., Landon, G., 1998a. Growth, light interception and yield responses of spring wheat (Triticum aestivum L.) grown under elevated CO2 and O3 in open-top chambers. Glob. Change Biol. 4, 121 /130. Mulholland, B.J., Craigon, J., Black, C.R., Colls, J.J., Atherton, J., Landon, G., 1998b. Effects of elevated CO2 and O3 on the rate and duration of grain growth and harvest index in spring wheat (Triticum aestivum L.). Glob. Change Biol. 4, 627 /635. Nakayama, F.S., Kimball, B.A., 1988. Soil carbon dioxide distribution and flux within the open-top chamber. Agron. J. 80, 394 /398. Pinter, P.J., Kimball, B.A., Garcia, R.L., Wall, G.W., Hunsaker, D.J., Lamorte, R.L., 1996. Free-air CO2 enrichment: responses of cotton and wheat crops. In: Koch, G.W., Mooney, H.A. (Eds.), Carbon Dioxide and Terrestrial Ecosystems. Academic Press, San Diego. Rudorff, B.F.T., Mulchi, C.L., Daughtry, C.S.T., Lee, E.H., 1996. Growth, radiation use efficiency, and canopy reflectance of wheat and corn grown under elevated ozone and carbon dioxide atmospheres. Remote Sens. Environ. 55, 163 /173.

R. Manderscheid et al. / Europ. J. Agronomy 19 (2003) 411 /425 Sinclair, T.R., 1994. Limits to cop yield? In: Boote, K.J., Bennett, J.M., Sinclair, T.R., Paulsen, G.M. (Eds.), Physiology and Determination of Crop Yield. American Society of Agronomy, Madison, WI. Sinclair, T.R., Muchow, R.C., 1999. Radiation use efficiency. Agron. J. 65, 215 /265. Slomka, J., 1989. Photosynthetic photon inflow in relation to sunshine duration at Belsk. Publ. Inst. Geophys. Pol. Acad. Sci. 32, 85 /89. Sofield, I., Evans, L.T., Wardlaw, I.F., 1974. The effects of temperature and light on grain filling in wheat. R. Soc. N. Z. Bull. 12, 909 /915. Swinnen, J., Van Veen, J.A., Merckx, R., 1994. Rhizosphere carbon fluxes in field-grown spring wheat-model calculations based on C-14 partitioning after pulse- labelling. Soil Biol. Biochem. 26, 171 /182.

425

Tottman, D.R., Broad, H., 1987. The decimal code for the growth stages of cereals, with illustrations. Ann. Appl. Biol. 110, 441 /454. Unsworth, M.H., Lesser, V.M., Heagle, A.S., 1984. Radiation interception and the growth of soybeans exposed to ozone in open-top field chambers. J. Appl. Ecol. 21, 1059 /1079. Weigel, H.J., Mejer, G.J., Ja¨ger, H.J., 1992. Impact of climate change on agriculture */open-top chambers as a tool to investigate long-term effects of elevated CO2 levels on plants. J. Appl. Bot. 66, 135 /142. Wheeler, T.R., Hong, T.D., Ellis, R.H., Batts, G.R., Morison, J.I.L., Hadley, P., 1996. The duration and rate of grain growth, and harvest index, of wheat (Triticum aestivum L.) in response to temperature and CO2. J. Exp. Bot. 47, 623 / 630.