Crop growth responses to free air CO2 enrichment and nitrogen fertilization: Rotating barley, ryegrass, sugar beet and wheat

Europ. J. Agronomy 43 (2012) 97–107

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Crop growth responses to free air CO2 enrichment and nitrogen fertilization: Rotating barley, ryegrass, sugar beet and wheat Hans-Joachim Weigel, Remy Manderscheid ∗ Institute of Biodiversity, Johann Heinrich von Thuenen-Institute (vTI), 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 14 November 2011 Received in revised form 13 April 2012 Accepted 25 May 2012 Keywords: Barley Elevated CO2 FACE Nitrogen Ryegrass Sugar beet Wheat Yield

a b s t r a c t Model based projections of overall climate change effects on future crop yields strongly depend on the integration of the direct CO2 fertilization effect. For European crops little information from field experimentation with elevated CO2 levels ([eCO2 ]) exists, which may be used for model validation purposes. Over six years an arable crop rotation with winter barley, ryegrass, sugar beet and winter wheat was exposed to ambient and elevated CO2 levels (550 ppm) using a FACE facility under adequate nitrogen (N100) and 50% of adequate N fertilization (N50). Total plant N concentrations of all crops were lower between −4.9% and −17% under [eCO2 ] compared to ambient CO2 . Green leaf area index (GLAI) of sugar beet and ryegrass late in the growing season was reduced by [eCO2 ], while it slightly increased or remained unchanged for the cereals at anthesis. However, the results of total plant N and GLAI were statistically significant only for wheat and ryegrass. Final above-ground biomass and yield of all crop species significantly increased under [eCO2 ]. Averaged across both growth seasons and N supply levels the stimulation of total above ground biomass by [eCO2 ] amounted to +14% (barley), +11.9% (wheat), +10.6% (sugar beet) and +9.9% (ryegrass). On average, cereal grain yield and storage root yield were enhanced by +12.5% (barley), +12.7% (wheat) and +12.1% (sugar beet). There were no significant effects of [eCO2 ] on N yield. Contrary to expectations, [eCO2 ] effects on the plant growth variables were independent from the N supply level. Overall, growth and yield stimulations of the different crop species by [eCO2 ] under FACE conditions were smaller than observed in many previous enclosure studies. The losses observed for plant N concentrations point to possible future problems with animal forage quality if atmospheric CO2 levels continue to increase. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The change of the global atmospheric CO2 concentration ([CO2 ]) is the most prominent example of global climate change. The current growth of [CO2 ] will likely continue in the next decades and may bring [CO2 ] near to 550 ppm by 2050 and 730–1000 ppm by 2100 (Meehl et al., 2007), if no strong mitigation strategies are enforced. Photosynthetic processes and consequently plant growth of C3 plant species are known to be positively affected by elevated [CO2 ] (Cure and Acock, 1986; Kimball et al., 1993, 2002; Long et al., 2005) which mostly goes along with modified water and nutrient turnover. For C4 crops beneficial growth effects of elevated [CO2 ] seem to result solely from an improved water economy of the plants (Manderscheid et al., 2012; Leakey, 2009). Thus, the “CO2

∗ Corresponding author. Tel.: +49 531 5962579; fax: +49 531 5962599. E-mail addresses: [email protected] (H.-J. Weigel), [email protected] (R. Manderscheid). 1161-0301/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.eja.2012.05.011

fertilization effect” could be beneficial for future food production and this could modify potential negative consequences of changes of other climate change variables (e.g. temperature increase, more drought events, increase of tropospheric ozone) for global food supply (Parry et al., 2005; Gornall et al., 2010). Attempts to assess the full impact of the various interacting variables of climate change on food production and, based on this, to develop adaptation measures to climate change, have to understand to what extent crop plants respond to the rapidly changing CO2 concentration. The effects of elevated [CO2 ] on growth and yield of crop plants have been extensively studied during the last 30 years using different CO2 exposure methods including, inter alia, indoor growth chambers, greenhouses, field tunnels and closed or open-top field chambers (Ainsworth and McGrath, 2010). These exposure systems suffer from several limitations, e.g. changes in microclimatic conditions, limited pot size, edge effects, etc., which may prevent realistic estimates of the CO2 effect (Van Oijen et al., 1999). More recently, free air CO2 enrichment (FACE) techniques have been developed

98

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

and applied (McLeod and Long, 1999; Hendrey and Miglietta, 2006). The FACE technology leaves the natural environment of a crop plot nearly fully unperturbed and is currently regarded as the most realistic CO2 exposure system. Biomass and yield enhancements of crops by elevated [CO2 ] obtained under non-FACE conditions typically range between +20% to +30% at CO2 concentrations which are ca. +200 to +300 ppm above ambient air. Based on a compilation of published crop response results to elevated [CO2 ] from enclosure studies Ainsworth and McGrath (2010) calculated yield enhancements of the globally important crops wheat, soybean and rice of up to ca. +30% at a CO2 concentration of 550 ppm. Other estimates of elevated [CO2 ] effects on crop yields obtained from studies using enrichment techniques other than FACE range between +28% and +35% (Amthor, 2001; Jablonski et al., 2002). Arguments have been raised that such positive growth and yield responses of crops to elevated [CO2 ] may be lower under real field conditions than deduced from previous information obtained under idealized growth conditions (Long et al., 2005, 2006). Indeed, averaged across FACE (550 ppm) studies conducted during the last 15 years crop yields (wheat, rice, soybean, potato) were only enhanced by +13% to +17% (Kimball et al., 2002; Long et al., 2006) as compared to current CO2 levels. Results of crop modeling and of projections of future global food production under climate change very much depend on the integration of the CO2 fertilization effect (Parry et al., 2005; IPCC, 2007; Lobell et al., 2008; Lobell and Burke, 2010), and this has also been demonstrated for European growth conditions (Alexandrov et al., 2002). If such projections are based on results from idealized CO2 exposure systems, where large growth enhancements have been observed, true field level responses to elevated [CO2 ] may be overestimated with strong implication for the model outputs. However, according to Tubiello et al. (2007) yield rises owing to the CO2 fertilization effect are more or less consistent across a range of different experimental approaches. Similarly, Ziska and Bunce (2007) argue that the size of the relative yield stimulations in response to future CO2 concentration is similar for enclosure and FACE studies. The above debate remains elusive due to the very limited number of relevant FACE studies with arable crop species in comparison to many enclosure studies (Amthor, 2001). Interestingly, there is only one true experimental comparison of these enrichment technologies (Kimball et al., 1997). FACE experiments with globally important staple crops (wheat, rice, soybean) were carried out in China, Japan and the USA (Kim et al., 2003; Kimball et al., 2002; Long et al., 2005; Ma et al., 2007). In Europe existing studies of high [CO2 ] effects on arable C3 crop growth and yield are still nearly exclusively based on chamber studies (e.g. open-top chambers) or controlled environment approaches, respectively. Many of these studies have addressed wheat (e.g. Mitchell et al., 1993; Wolf, 1996; Batts et al., 1997; Mulholland et al., 1997; Bender et al., 1999) and potato (e.g. Schapendonk et al., 2000; Finnan et al., 2002; Perrson et al., 2003). Less information is available for barley (Weigel et al., 1994; Fangmeier et al., 2000; Martin-Olmedo et al., 2002) or sugar beet (Demmers-Derk et al., 1996, 1998). Until now FACE experiments with arable crops in Europe have been carried out in a study with potato (Bindi et al., 2006; Miglietta et al., 1998) and two small scale studies (mini-FACE) with oilseed rape and wheat (Franzaring et al., 2008; Högy et al., 2009). Moreover, this limited number of FACE studies dealt with the single effects of elevated [CO2 ] only and did not consider interactions with other climate change or agricultural management variables. As nitrogen (N) is the key nutrient with the highest agronomic and environmental relevance for crop growth in Europe and elsewhere (Spiertz, 2010), it is of interest to address the potential interactions of this nutrient with climate change. Under the

various environmental factors that determine the response of crop biomass and yield formation to elevated [CO2 ] N availability can have a large effect. A number of studies have shown CO2 × N interactions (Stitt and Krapp, 1999; Kimball et al., 2002) and a common presumption assumes that N deficiency acts as a growth inhibitory factor which may decrease the relative response to elevated [CO2 ] (Ainsworth and Long, 2005). In general, studies across a range of ecosystem types addressing biomass accrual under elevated CO2 and variable N supply levels show inconsistent results (Reich et al., 2006). According to Ziska and Bunce (2007) there is now sufficient evidence that crop yield stimulation by elevated CO2 is dependent on N availability. For example, this has been shown for wheat (Wolf, 1996) and barley (Kleemola et al., 1994) in chamber studies. However, some recent studies with rice that examined crop responses under FACE conditions and low N availability reported similar yield stimulation by elevated [CO2 ] as under sufficient N supply (Kim et al., 2003; Liu et al., 2008; Yang et al., 2009). There are still uncertainties whether this holds true also for other crop species under field conditions. The understanding and assessment of crop yield at elevated [CO2 ] under N restriction is important since areas with limited N resources are still common in some parts of the world and a low N input scenario is one option of future sustainable agricultural management. According to Jaggard et al. (2010) it may be debated if future atmospheric CO2 levels may help to limit negative yield effects if future N fertilizer use should be restricted due to either environmental or financial reasons. Moreover, the CO2 × N interaction is particularly relevant with respect to future yield quality of crops, e.g. as significant decreases of N and crude protein concentration in leaf and grain tissue have been observed under elevated [CO2 ] (Weigel and Manderscheid, 2005; Taub et al., 2008; Wieser et al., 2008). Overall, considering the need for a better forecasting of crop yields under climate change conditions there is still a lack of relevant field experiments which address the question of the magnitude of crop responses to increasing atmospheric CO2 concentration and the uncertainties connected to its interaction with other factors (Tubiello and Ewert, 2002). A FACE experiment was therefore carried out in Braunschweig, Germany to investigate the effects of elevated CO2 , singly and in combination with N supply on arable crops (Weigel and Dämmgen, 2000; Weigel et al., 2006). It is the only FACE experiment in Europe which, in order to follow real agricultural conditions as closely as possible, was applied to a crop rotation under true farm conditions. For barley and sugar beet an analysis of the seasonal growth dynamics in response to the CO2 and N treatments during this experiments has been given by Manderscheid et al. (2009, 2010). The objective of the present paper is to summarize the responses of key agronomic variables of barley, ryegrass, sugar beet and wheat to the elevated [CO2 ] and N supply treatments during the total rotation period of six years. We focus on tissue N concentration and N yield at the end of the respective growing seasons and on the responses of final biomass and yield of all crop species.

2. Materials and methods 2.1. Study site, crops and crop management The experiments were conducted on a 22 ha field at the Johann Heinrich von Thuenen-Institute, Federal Research Institute for Rural Areas, Forestry and Fisheries (formerly Federal Agricultural Research Centre, FAL), Braunschweig, South-East Lower Saxony, Germany (528180N, 108260E, 79 m a.s.l.). The soil at this site is a luvisol of a loamy sand texture in the plough horizon with 0.4 m

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

99

Table 1 Agricultural management and treatment details during the FACE experiment in Braunschweig. Management

2001

2001/2002

2002/2003

2004

2004/2005

Barley

Ryegrass

Sugar beet

Wheat

Barley

Ryegrass

Sugar beet

Wheat

24.09.99 280 01.10.99 4 262/105

28.07.00 40 kg ha−1 02.08.00 2 197/99

10.04.01 11 30.04.01 2 126/63

06.11.01 360 05.12.01 5 251/114

27.09.02 270 04.10.02 5 179/105

21.08.03 40 kg ha−1 27.08.03 1 72/36

14.04.04 11 26.04.04 3 156/78

26.10.04 360 16.11.04 5 168/84

Herbicide application

Date No. m−2 Date No. N100/N50 [kg ha−1 ] Date

13.10.99

24.08.00

02.04.02

01.11.02

18.09.03

03.05.04 19.05.04

26.04.05

Fungicide application

Date

11.04.00

–

14.05.01 21.05.01 30.05.01 09.08.01

08.05.02

12.05.03

–

08.06.05

Irrigation Final harvest 1st CO2 -enrichment Last CO2 -enrichment Total CO2 -enrichment Mean daytime [CO2 ] (ambient/elevated)

No./mm Date Date Date Days [␮mol mol−1 ]

5/107 26.06.00 04.10.99 19.06.00 260 373/549

2/44 12.10.00 05.08.00 13.10.00 69 373/550

5/107 27.09.01 14.05.01 25.09.01 134 371/550

3/60 31.07.02 22.01.02 23.07.02 182 377/548

5/77 25.06.03 10.10.02 23.06.03 258 378/547

– 22.10.03 01.09.03 22.10.03 51 380/550

27.07.04 02.09.04 4/84 30.09.04 14.05.04 30.09.04 139 377/549

Sowing Sowing density Emergence N-fertilization

Units

1999/2000

depth (69% sand, 24% silt, and 7% clay). It has a low to intermediate fertility, a comparatively shallow rooting zone, an average pH of 6.5 and a mean organic matter content of 1.4%. Field capacity and permanent wilting point are at volumetric soil water contents of 23% and 5%, respectively. A winter grain crop, followed by a cover crop, a (spring sown) row crop and a winter grain crop again comprise a typical crop rotation in northern Germany. The FACE experiment was therefore applied to a rotation consisting of winter barley (Hordeum vulgare) → a ryegrass mixture (Lolium multiflorum Lam.) as a cover crop → sugar beet (Beta vulgaris) → winter wheat (Triticum aestivum). The rotation cycle was repeated once resulting in a total duration of the CO2 exposure experiments of six years (1999–2005). Cultivars chosen for barley (cv. Theresa), sugar beet (cv. 1st cycle Wiebke, 2nd cycle Impuls) and wheat (cv. Batis) were among the most frequently cultivated varieties in Germany. Agricultural management measures of the total 22 ha field and the FACE plots, respectively, were carried out according to local farm practices and included plough tillage, mineral fertilization and pesticide applications. Fertilisers during the growing season were added based on soil analysis in springtime. Table 1 lists the key management measures during the different growing periods of the crop species. While the management measures for barley and sugar beet are described in detail elsewhere (Manderscheid et al., 2009, 2010), the cultivation of wheat and ryegrass is briefly summarized as follows (see also Table 1). Winter wheat was sown at late October (2001) or early November (2004) in east-west rows spaced 0.12 m with a seeding density of 360 plants m−2 . Mineral nitrogen was added five times from March until June as urea ammonium nitrate or as calcium ammonium nitrate. A mixture of three cultivars of Westerwolds ryegrass (Lolium multiflorum, cvs. (each 33%) Lirasand, Lifloria and Litoro) was sown (40 kg ha−1 ) in July (2000) or August (2003) after the final harvest of winter barley. Nitrogen fertilizer was applied as liquid slurry one week before sowing in 2000 and additionally in both years as liquid urea ammonium nitrate shortly after sowing. For all experiments, mineral nutrients were added according to local fertilizing practices and based on analysis of soil nutrient contents (K, Mg, N, P, S) determined in early springtime. A linear irrigation system to keep the soil water content above 50% plant available water content (PAWC) was used to irrigate the field in order to avoid interacting effects with drought stress in the

7/121 27.07.05 12.01.05 20.07.05 189 378/549

different treatments (Burkart et al., 2011; see Table 1). Climate data (air temperature, global radiation, and precipitation) measured at 2 m height at a distance of ca. 300 m from the FACE site were provided by the German Weather Service. 2.2. The FACE experiment A circular free-air CO2 enrichment (FACE) system of the Brookhaven National Laboratory design (Lewin et al., 1992; Hendrey and Miglietta, 2006) with experimental rings of 20 m in diameter was operated for the experiments. Treatments included two rings operated with blowers at ambient air CO2 concentration (=ambient) and two rings equipped with blowers and air enriched with CO2 (=elevated). The target CO2 concentration in the plots was set to 550 mmol mol−1 during daylight hours. At wind speeds >6 m s−1 or air temperatures <5 ◦ C, when plant metabolism is low and photosynthesis does hardly respond to CO2 enrichment (Long et al., 2005) CO2 fumigation was not carried out. CO2 treatments started shortly after emergence of the crops (Table 1). The FACE rings were placed exactly at the same position in each growing season. Interactive effects between elevated CO2 concentration and nitrogen (N) supply were studied by dividing each ring into two semicircles and restricting the adequate N fertilization (=N100) to 50% (=N50) in half of the rings. Total amounts of N fertilization in the different treatments are shown in Table 1. 2.3. Crop growth measurements and N determination Crop biomass and yield was analyzed at maturity (cereals) or at the end of the vegetation period (ryegrass and sugar beet; see Table 1). Total above ground biomass was harvested within each half of a ring from a ground area of 1.2 m2 (ryegrass), 2–4 m2 (barley, wheat) and 10 m2 (sugar beet). The major fraction (70–90%) of the plant sample was dried at 105 ◦ C and the dry weight was determined. A smaller fraction (10–30%) was used for the dry weight measurement of different plant components including yield components (dry weights of grains of cereals and of storage root of sugar beet). Prior to that the area of the green leaves was quantified with a leaf area meter (LI-3100, LICOR) and used to calculate the green leaf area index. In the case of cereals leaf area index was measured at an additional sampling date at anthesis, when plant samples were taken from a ground area of 0.5–1 m2 . The plant material was milled

1999

2000

2002

2003

2004

Apr

Jun

Feb

Oct

Dec

Aug

Apr

Jun

Feb

Oct

Dec

Aug

Apr

Jun

Feb

Oct

Dec

Aug

Apr

2001

Jun

Feb

Oct

-5 Dec

0 Aug

0

Apr

40

Jun

5

Feb

80

Oct

10

Dec

120

Aug

15

Apr

160

Jun

20

Feb

200

Oct

25

Dec

240

Temperature [°C]

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

Preciptation [mm] / Global radiation [KJ cm-2]

100

2005

Month / Year Fig. 1. Monthly sums of global radiation (dotted line) and precipitation (grey bars) and monthly mean values of air temperature (solid line) at the Braunschweig FACE site between 1999 and 2005.

to a fine powder (1 mm) and the N content of the total plant was determined using the Leco TruSpec CNS element analyzer. Nitrogen use efficiency was calculated as the reciprocal value of the nitrogen content of the total plant. 2.4. Statistical analysis For crop analysis each ring was divided into four quarters from which samples were taken. Average values of the variable calculated from the two sampling areas of each ring half were used in the statistical analysis. Data of each crop species and year were analyzed as a completely randomized design with ambient (n = 2) and elevated CO2 (n = 2) treatments each split for N (n = 8) with the R statistical software package (Version 2.0.0, R Development Core Team 2004). In general, experimental year was treated as a fixed effect. In the first field experiment with sugar beet one blower and one FACE ring was infected by rhizomania and statistical analysis was not possible as described recently (Manderscheid et al., 2010). 3. Results 3.1. Environmental conditions and FACE performance during the crop rotation Monthly mean values of key climatic variables during the 6-years experiment are shown in Fig. 1. Average temperatures (◦ C) during the main growing periods were 12.2/12.0 for barley (March–June 2000/2003), 14.6/13.8 for ryegrass (August–October 2000/2003), 14.6/14.6 for sugar beet (April–September 2001/2004) and 14.4./14.5 for wheat (April–July 2002/2005). Overall, the growing seasons of wheat and sugar beet were

characterized by warmer conditions as compared to the barley seasons (Fig. 1). Operational times of the CO2 enrichment and average CO2 concentration values in the rings are also shown in Table 1. For all crops tested the average 1-min CO2 concentration in the FACE plots was within ±10% of the target concentration of 550 ppm for > 97% of the operational time. Compared to the maximum possible CO2 fumigation times during this period (i.e. daylight hours) CO2 fumigation was interrupted for 27–38% for the cereals and only 1–2% for sugar beet. While for the cereals this was almost exclusively due to the low temperature cut-off (i.e. <5 ◦ C) during the winter season, for sugar beet it was due to both low temperature regimes and high wind speeds. 3.2. N concentration in above ground biomass A statistically significant and consistent reduction of the N concentration in the above ground biomass of all crop species was observed under the N50 treatment (Table 2). Across both CO2 levels and growing seasons the percent reduction ranged between a minimum value of ca. −15% (sugar beet) to a maximum reduction of −26% (ryegrass). With one exception (sugar beet) elevated CO2 reduced above ground biomass N concentration of all crops in all years and N supply levels, the reduction ranging from −2.9% to a maximum of −19.8% compared to ambient CO2 . However, this reduction was statistically significant only for ryegrass and wheat. Due to a slightly positive CO2 effect on plant N concentration in the 2004 growing under low N supply for sugar beet a CO2 × N interaction was observed. For all other crop species the reduction of the N concentration due to elevated CO2 was in a similar range between both N treatments.

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

101

Table 2 Nitrogen content in above ground biomass (% dry matter) of crop species grown in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons; results are for the final harvest (cereals: grain maturity; sugar beet: late September, grass: late October). Means + standard error (n = 2) are shown. 2001

2002

2003

2004

2005

CO2

N

Barley

2000 Grass

Sugar beeta

Wheat

Barley

Grass

Sugar beet

Wheat

Ambient

100 50 100 50 100 50

1.72 + 0.08 1.43 + 0.04 1.38 + 0.02 1.15 + 0.02 −19.8 −19.6

2.65 + 0.04 1.97 + 0.19 2.20 + 0.04 1.63 + 0.03 −17.0 −17.3

1.15 0.95 1.04 0.88 −9.6 −7.4

1.38 + 0.01 1.14 + 0.07 1.34 + 0.11 1.03 + 0.01 −2.9 −9.6

1.52 + 0.11 1.24 + 0.02 1.30 + 0.04 1.09 + 0.00 −14.5 −12.1

2.09 + 0.01 1.55 + 0.10 1.97 + 0.19 1.43 + 0.01 −5.7 −7.7

1.02 + 0.08 0.81 + 0.07 0.89 + 0.01 0.83 + 0.00 −12.7 +2.5

1.57 + 0.02 1.18 + 0.02 1.32 + 0.04 1.06 + 0.02 −15.9 −10.7

Elevated % CO2 effect

ANOVA

Barley

Grass

Sugar beeta

Wheat

CO2 CO2 × year N C×N N × year C×N×Y

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

Only one plot per treatment in 2001. n.s., not significant. * P < 0.05. ** P < 0.01. *** P < 0.001.

3.3. Leaf area index Green leaf area index (GLAI) of all crop species was significantly reduced under the low N treatment (N50) (Table 3). Averaged across both CO2 levels and growing seasons GLAI reduction ranged from ca. −25% (wheat) to −41% (ryegrass) as compared to adequate N supply. GLAI responses under elevated CO2 differed between crop species. For barley and wheat no statistically significant CO2 effect was observed, while GLAI was significantly decreased for ryegrass under both N levels and for sugar beet only under the N100 treatment as indicated by a significant CO2 × N interaction. 3.4. Total above ground biomass and yield While the control (N100; ambient CO2 ) biomass production of sugar beet was very similar in the two growing seasons, there were large year-by-year differences in biomass production for the cereals

and ryegrass (Table 4). With the exception of ryegrass in the 1st season plants grown under reduced N supply had produced significantly less biomass than under adequate N supply. For example, averaged across both CO2 treatment levels and growing seasons the reduction amounted to −17% for barley and −14% for sugar beet. The relative N effects were quite similar between ambient and elevated CO2 except for wheat and sugar beet in the 2nd growing season. CO2 enrichment resulted in significantly increased final biomass production for all crop species in the rotation. Across both growing seasons the relative growth enhancement by elevated CO2 was in a similar range between the two N supply levels for barley and ryegrass. With the exception of sugar beet and wheat under the N50 treatment in the 2nd growing season the relative growth enhancement by CO2 were quite similar between both N supply levels. For wheat in both growing seasons the relative biomass enhancement by elevated [CO2 ] was lower under the low N supply and a significant CO2 × N interaction was observed. Across both

Table 3 Green leaf area index (m−2 m−2 ) of crop species grown in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons; results are for the stage at anthesis (cereals), for late September (sugar beet) and late October (grass). Means + standard error (n = 2) are shown. CO2

Ambient Elevated % CO2 effect

ANOVA CO2 CO2 × year N C×N N × year C×N×Y a

N

100 50 100 50 100 50

2000

2001

2002

2003

2004

2005

Barley

Grass

Sugar beeta

Wheat

Barley

Grass

Sugar beet

Wheat

4.77 + 0.22 3.42 + 0.55 5.17 + 0.60 3.57 + 0.31 8.4 4.4

5.19 + 0.25 3.59 + 0.04 4.38 + 0.71 2.66 + 0.05 −15.6 −25.9

3.36 2.40 2.76 1.49 −17.9 −37.9

2.60 + 0.12 2.46 + 0.11 2.95 + 0.36 2.72 + 0.32 13.5 10.6

3.53 + 0.44 2.20 + 0.20 3.03 + 0.03 2.15 + 0.18 −14.2 −2.3

4.84 + 0.12 2.46 + 0.05 4.08 + 0.57 2.26 + 0.11 −15.7 −8.1

3.10 + 0.40 1.54 + 0.31 2.39 + 0.19 1.62 + 0.07 −22.9 5.2

3.49 + 0.24 1.99 + 0.14 3.52 + 0.36 1.96 + 0.01 0.9 −1.5

Barley

Grass

Sugar beeta

Wheat

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.

– –

**

Only one plot per treatment in 2001. n.s., not significant. (*) P < 0.10. * P < 0.05. ** P < 0.01. *** P < 0.001.

n.s.

102

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

Table 4 Total above ground biomass (g m−2 ) at final harvest (cereals: grain maturity; sugar beet: late September, grass: late October) of crop species grown in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons. Means + standard error (n = 2) are shown. CO2

Ambient Elevated % CO2 effect

N

2000

100 50 100 50 100 50

Barley

Grass

1679 + 24 1360 + 56 1815 + 2 1546 + 13 8.1 13.7

484 + 7 484 + 3 543 + 39 531 + 5 12.1 9.7

2001

2002

2003

Sugar beeta

Wheat

Barley

Grass

1277 + 33 1163 + 13 1456 + 50 1292 + 25 14.5 11.1

1216 + 55 983 + 126 1430 + 22 1173 + 19 17.6 19.3

325 + 12 222 + 1 343 + 27 245 + 17 5.5 10.4

2294 1919 2481 2036 8.2 6.1

2004

2005

Sugar beet

Wheat

2372 + 104 1971 + 23 2528 + 67 2388 + 70 6.6 21.2

1683 + 18 1410 + 67 1938 + 44 1422 + 31 15.2 4.4

ANOVA

Barley

Grass

Sugar beeta

CO2 CO2 × year N C×N N × year C×N×Y

***

*

*

**

n.s.

n.s.

–

n.s.

**

*

(*)

***

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

n.s.

n.s. – –

(*)

*

n.s.

Wheat

**

n.s.

a

Only one plot per treatment in 2001. n.s., not significant. (*) P < 0.10. * P < 0.05. ** P < 0.01. *** P < 0.001.

growing seasons and N treatments the growth stimulation by the CO2 elevation amounted to +14.7% for barley, +9.9% for ryegrass, +10.2% for sugar beet and 11.3% for wheat. Grain yield and beet root yield were affected by the CO2 and N treatment in a similar manner as above ground biomass (Table 5). N reduction significantly decreased grain yields of cereals between ca. −10% and −22% compared to adequate N supply. Beet root yield was reduced by the N reduction to a lower extent and this effect was not significant. Averaged across both N levels cereal plants grown under elevated CO2 had +8% and +17% (barley) and +13% and +10% (wheat) higher grain yields in the 1st and 2nd growing season, respectively, while for sugar beet the respective stimulation amounted to +12% and +14%. Thus, across both growing seasons marketable yields of barley, sugar beet and wheat were enhanced by elevated CO2 by +12.5%, +13% and +11.5%. Except for wheat there were no statistically significant CO2 × N interactions.

3.5. N yield and N use efficiency As expected N yield responded strongly and statistically significant to the reduction of N supply (Table 6) and was mostly reduced by 20–30% with high values up to >45% (ryegrass). On the other hand, there were no significant and consistent effects between crop species and years of the elevated CO2 treatment on N yield. For example, while in the 1st years N yields of barley, ryegrass and sugar beet tended to decrease due to the CO2 elevation, N yields of these crops remained unchanged or responded with an increase to CO2 in the 2nd years. Wheat N yield was affected positively in the 1st and negatively in the 2nd year. With one exception (sugar beet 2004; N50) the changes induced by elevated CO2 were in the range of ±10% as compared to ambient CO2 . While there was no CO2 × N interaction, a CO2 × growing season interaction was observed for wheat.

Table 5 Final grain and beet (storage root) yield (g m−2 ) of crop species grown in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons. Means + standard error (n = 2) are shown. CO2

N

Ambient

100 50 100 50 100 50

Elevated % CO2 effect

2000 Barley 952 + 11 784 + 49 1023 + 23 850 + 10 7.5 8.5

2001 Sugar beeta 1493 1323 1637 1506 9.6 13.8

2002 Wheat 570 + 6 474 + 11 659 + 20 594 + 22 15.6 11.7

2003 Barley 590 + 44 474 + 59 687 + 10 558 + 1 16.5 17.6

ANOVA

Barley

Sugar beeta

Wheat

CO2 CO2 × year N C×N N × year C×N×Y

**

**

**

n.s.

– n.s. n.s. – –

n.s.

a

**

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

Only one plot per treatment in 2001. n.s., not significant. * P < 0.05. ** P < 0.01. *** P < 0.001.

*** * **

n.s.

2004 Sugar beet 1565 + 6 1417 + 14 1689 + 45 1658 + 64 7.9 17.0

2005 Wheat 838 + 2 731 + 38 970 + 6 758 + 12 15.8 3.7

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

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Table 6 Nitrogen yield (g m−2 ) of crop species in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons; results are for the final harvest (cereals: grain maturity; sugar beet: late September, grass: late October). Means + standard error (n = 2) are shown. CO2

Ambient Elevated % CO2 effect

N

100 50 100 50 100 50

2000

2001

2002

2003

2004

2005

Barley

Grass

Sugar beeta

Wheat

Barley

Grass

Sugar beet

Wheat

28.8 + 0.9 19.4 + 1.4 25.1 + 0.3 17.8 + 0.1 −12.8 −8.7

12.8 + 0.3 9.52 + 0.9 11.9 + 0.6 8.63 + 0.3 −7.0 −9.3

26.5 18.3 25.7 17.8 −3.0 −2.7

17.6 + 0.3 13.2 + 0.6 19.4 + 0.9 13.3 + 0.3 +10.2 +0.8

18.4 + 0.4 12.2 + 1.8 18.5 + 0.3 12.8 + 0.2 +0.5 +4.9

6.76 + 0.2 3.46 + 0.2 6.83 + 1.2 3.50 + 0.2 +1.0 +1.2

24.3 + 2.9 15.9 + 1.6 22.6 + 0.9 19.7 + 0.7 −7.0 +23.9

26.4 + 0.5 16.7 + 1.0 25.5 + 0.1 15.6 + 0.6 −3.4 −6.6

ANOVA

Barley

Grassa

Sugar beeta

CO2 CO2 × year N C×N N × year C×N×Y

n.s. n.s.

n.s. n.s.

n.s. –

***

**

*

***

n.s.

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

n.s. – –

n.s.

*

n.s.

Wheat n.s. *

*

n.s.

a

Only one plot per treatment in 2001. n.s., not significant. * P < 0.05. ** P < 0.01. *** P < 0.001.

N use efficiency (NUE) was highest in sugar beet with the great storage root and lowest in the leafy grass, while the cereals were positioned between them (Table 7). Low N supply increased NUE significantly and again the effect was greatest for the leafy grass and smallest for sugar beet. CO2 enrichment also increased NUE independent of nitrogen fertilization for three of the four crop species. However, in the case of sugar beet an interaction between nitrogen and CO2 supply was found in the 2nd year, when CO2 enrichment increased NUE only under adequate N supply. 4. Discussion The present study intended to produce new experimental data on how important European crop species may respond to future atmospheric CO2 levels under real agricultural field conditions and how this may be affected by N nutrition. While for wheat and

ryegrass FACE experiments have been carried out previously, for barley and sugar beet the present study was the first under free air CO2 enrichment conditions. As expected low N supply resulted in a consistent reduction in the above ground tissue N concentration in all species. Similarly, exposure of the plants to elevated [CO2 ] reduced the N concentration in the plants at harvest, albeit the extent of this reduction was very variable between the different crop species and the results were only significant for ryegrass and wheat. Overall, this result is in line with other information, which shows that, on average, tissue N concentrations of crop and non-crop species were reported to decrease by 10–15% by elevated [CO2 ], although there was considerable variability in the results of the individual studies (Cotrufo et al., 1998; Kimball et al., 2002; Ainsworth and Long, 2005; Weigel and Manderscheid, 2005; Taub et al., 2008). In the present study there was no unambiguous indication that the reduction of tissue

Table 7 Nitrogen use efficiency (g g−1 ) of crop species in a rotation after exposure to ambient and elevated (550 ppm) CO2 and different nitrogen supply (N100 = adequate N supply; N50 = 50% of N100) during two growing seasons; results are for the final harvest (cereals: grain maturity; sugar beet: late September, grass: late October). Means + standard error (n = 2) are shown. CO2

Ambient Elevated % CO2 effect

N

100 50 100 50 100 50

2000

2001

2002

2003

2004

2005

Barley

Grass

Sugar beeta

Wheat

Barley

Grass

Sugar beet

Wheat

58.3 + 2.7 70.1 + 1.8 72.5 + 1.1 86.6 + 1.6 +24.4 +23.5

37.8 + 0.5 51.3 + 4.9 45.5 + 0.8 61.5 + 1.2 +20.4 +19.9

87.0 105.3 96.7 114.2 +11.1 +8.5

72.4 + 0.6 88.2 + 5.1 75.4 + 6.1 97.1 + 0.5 +4.1 +10.1

66.1 + 4.6 80.5 + 1.5 77.2 + 2.3 91.7 + 0.2 +16.8 +13.9

48.0 + 0.3 64.7 + 4.3 51.1 + 4.8 69.9 + 0.3 +6.5 +8.0

98.5 + 7.5 125.0 + 11.2 112.0 + 1.4 121.2 + 0.5 +13.7 −3.0

63.8 + 0.6 84.5 + 1.1 75.9 + 2.1 94.7 + 1.6 +19.0 +12.0

ANOVA

Barley

Grass

Sugar beeta

Wheat

CO2 CO2 × year N C×N N × year C × N × year

**

*

**

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 Only one plot per treatment in 2001. n.s., not significant. (*) P < 0.10. * P < 0.05. ** P < 0.01. *** P < 0.001.

– –

n.s.

104

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N concentration was smaller under adequate than under reduced N supply levels of the plants. Several other studies (for review see Stitt and Krapp, 1999; Kimball et al., 2002) have shown large decreases in total leaf N under elevated CO2 conditions when plants were grown at low N supply, whereas there was only a small or no decrease at high N supply. On the other hand, as evidenced from the literature examination of Cotrufo et al. (1998) and Wand et al. (1999) with a range of C3 and C4 plants species mostly investigated in chamber experiments, the average leaf N concentration reduction by elevated [CO2 ] did not depend on the N regime of the growth substrate. Also for ryegrass Weigel and Manderscheid (2005) in compilation of own results obtained in- and outdoor chamber studies did not find a relation between tissue N concentration by elevated CO2 and N availability. Overall, the present results show that high CO2 levels and low N supply affect leaf N status to a similar extent, obviously by widening the carbon:nitrogen ratio in the plant tissue. From the perspective of animal forage quality the loss of N (which corresponds to crude protein) in the leaf material of all crop species due to the CO2 elevation observed in the present study may be considered as a serious negative consequence of a future high-CO2 world (DaMatta et al., 2010). Under application rates of N fertilizers, which may be regarded as optimal for maximum yield, the quality of the forage crops was reduced under elevated CO2 . Green leaf area index (GLAI) is the main determinant of light interception which in turn is closely related to biomass production. N supply along with water availability and climate are key factors which contribute to the variation of GLAI observed in the field. The understanding of potential effects of elevated [CO2 ] on GLAI has been regarded as important for crop production modeling purposes (Ewert, 2004) and high [CO2 ] effects on GLAI have been investigated repeatedly, however, with variable results. For example Kimball et al. (2002) in their review of FACE experiments with agricultural crops reported on moderate increases of LAI among C3 grasses (wheat, ryegrass, rice), while for potato LAI decreased under high [CO2 ]. Ainsworth and Long (2005) conclude from FACE studies with trees and crops that LAI does not change under elevated CO2 conditions. Along with the negative effect on leaf N concentration the present results clearly demonstrate a negative effect of reduced N supply on LAI of all crop species. On the other hand, the CO2 treatment resulted in highly variable responses between the different crop species and years. For example, ryegrass responded with a significant and consistent decrease of LAI across both N supply levels and growing seasons, while LAI of the cereals at anthesis was affected slightly positive or remained unchanged. In a recent FACE study with rice [CO2 ] elevation stimulated LAI early in the growing season while maximum LAI did not differ between the treatment (Kim et al., 2003). While FACE studies with wheat, ryegrass and rice have shown smaller enhancements of LAI under low N as compared to ample N supply (Kimball et al., 2002), the present results do not support this observation. In accordance with information obtained from other root crops, e.g. potatoes, sugar beet showed a tendency of reduced LAI at the end of the growing season, although the results were not significant. In several studies with potatoes LAI was found to be lower under elevated [CO2 ] at the phase of plant senescence (Hacour et al., 2002). Manderscheid et al. (2010) investigated the seasonal course of LAI of sugar beet under FACE conditions and showed that an increased fraction of senescent leaves under high CO2 levels – at least under ample N supply – contributed to the negative effects on LAI at the end of the growing season. Because of the economic importance observations on the effects of elevated [CO2 ] on crop biomass production, yield and N yield are of particular relevance. While in the present study N yields of the different crop species were hardly affected the extent of the above ground biomass and yield enhancements by elevated [CO2 ]

varied strongly between crops, years and N treatments. Excluding ryegrass, which was only shortly exposed to CO2 , and considering the standard agronomic N100 treatment only, the growth and yield stimulation of sugar beet (+6% to +9.6%) and wheat (+14.5% to +15.8%) were fairly consistent between the individual years, while for barley there was a larger difference between the years (+7.5% to +17.5%.) Averaged across growing seasons and N supply levels the growth and yield stimulation by elevated [CO2 ] only varied between +9.5% (biomass ryegrass) to +14.7% (biomass barley). These averaged ranges of biomass and yield responses to elevated [CO2 ] found in the present study are similar to the results described in several recent compilations of other FACE studies with various crop species (e.g. Kimball et al., 2002; Long et al., 2006; Ainsworth and McGrath, 2010), for which yield enhancements by elevated [CO2 ] between +13% and +17% have been found. For barley Manderscheid et al. (2009) in a detailed yield analysis of a FACE experiment attributed the higher relative CO2 response of this crop in the growing season 2003 as compared to 2000 to a water supply deficit early in the growing season and to higher temperatures shortly before anthesis during the 2nd year. In 2003 CO2 enrichment increased canopy growth already at stem elongation but not in 2000. This could have contributed to the different CO2 effect on nitrogen yield in the 1st (−11%) and 2nd year (+3%). During the 2nd growing season barley yields under the control treatment (ambient CO2 ; ample N supply) were also considerably lower than in the 1st year. With respect to grain yield of barley the enhancement by elevated [CO2 ] in our FACE study (ca. +8% to +17%) is clearly smaller than observed in previous CO2 enrichment studies with this crop, which have exclusively been carried out under enclosure conditions and mostly using potted plants at CO2 concentrations higher than 550 ppm (e.g. Weigel et al., 1994; Fangmeier et al., 2000; Martin-Olmedo et al., 2002). Calculated for a comparable CO2 enrichment concentration as in our FACE experiment these studies showed a mean grain yield stimulation of ca. +28% as compared to ambient [CO2 ] (ca. 370–380 ppm). Ryegrass was used as a cover crop in the present experiment and was exposed to CO2 late in the growing for only roughly two months. Biomass responses of the ryegrass swards to elevated CO2 ranged between ca. +6% and +12% depending on the year and the N fertilization treatment. This size of the CO2 effect is in line with results from the Swiss grassland FACE experiment (550 ppm CO2 ), where in the course of several years of experimentation, annual average biomass increases of Lolium spp. due to CO2 of ca. +8% were observed, although the yield responses varied between −11% and +32% depending on the years and N fertilizations (Lüscher et al., 2006). A yield increase of ca. +8% of grassland swards in New Zealand under FACE conditions (495 ppm) was observed by Newton et al. (2006). Higher yield increments (+17% to >+25%) under elevated CO2 have been observed in controlled environment and field chamber studies with CO2 concentrations higher than 550 ppm (Campbell et al., 2000; Nösberger et al., 2000). While in the studies with grass species cited above the size of the CO2 fertilization strongly depended on the availability of N in the soil, this was not observed in the present experiment. With the exception of the low N treatment in the 2nd growing season the biomass (+6.1% to +8.2%) and storage root growth (+7.9% to +13.8%) enhancement of sugar beet by elevated CO2 was quite consistent. There are no previous FACE experiments with sugar beet, so our results can only be compared to the few studies with this crop which were carried out in growth chambers or greenhouses (Wyse, 1980; Demmers-Derk et al., 1998; Wolf, 1988). For a comparable CO2 elevation storage root weight increased between +14% and +16% in these studies, which is only slightly higher than in our FACE experiment. As discussed by Manderscheid et al. (2010) this relatively small growth enhancements of the sugar beet storage root by elevated [CO2 ] may be related to a sink limitation which

H.-J. Weigel, R. Manderscheid / Europ. J. Agronomy 43 (2012) 97–107

may prevent a better exploitation of the higher CO2 supply. Low or even negative effects of elevated [CO2 ] on above-ground biomass production have also been observed with the other important root crop potato (e.g. Miglietta et al., 1998). The order of magnitude of the biomass and yield enhancement of wheat (+11% to +16%) by elevated [CO2 ] was similar to the results obtained with barley. Under the full N treatment there was hardly any difference in the relative CO2 response of biomass and yield of wheat between the different growing seasons. Kimball et al. (1995) showed similar consistent results in their FACE study with wheat when shoot biomass increased on average by +8.4% by elevated CO2 in a 2-year FACE study. On the other hand, Ma et al. (2007) in a Chinese wheat FACE (550 ppm) experiment observed a stronger stimulation of final above ground biomass of +26.8% under high (250 kg N ha−1 ) and +13.5% under low (125 kg ha−1 ) N supply. Biomass and grain yield of wheat (cv. “Ritmo”) cultivated over three consecutive growing seasons in a mini-FACE system (380 vs. 550 ppm CO2 ) in Germany (Högy et al., 2009) were enhanced by +11.8% and +10.4%, respectively, by elevated CO2 which also is in a very similar range as in the present study. Other European CO2 exposure studies with wheat under non-FACE conditions have resulted in variable results. For example, in the European multi-site open-top chamber experiment ESPACE wheat (Bender et al., 1999) with the spring wheat cultivar “Minaret” a CO2 elevation from ca. 375 ppm to 580–750 ppm resulted in an average yield enhancement of ca. +35% which is equivalent to ca. +11% per 100 ppm CO2 increase. However, there were large differences in the responses to elevated CO2 between the different European sites, as the yield increases ranged from +11% to +121%. In a four yield field tunnel experiment with winter wheat Batts et al. (1997) yield stimulation by elevated [CO2 ] varied considerably between the different growing seasons but was, on average, equivalent to +17% per 100 ppm CO2 increment. In a two year open-top chamber study in the field under unlimited water and nutrient supply biomass and yield of the spring wheat cultivar “Minaret” were enhanced by elevated CO2 (ca. 680 ppm) on average by +10.4% and +8.0%, respectively (Manderscheid and Weigel, 2007). Amthor (2001) in his compilation of 156 indoor and outdoor experiments with wheat including mostly chamber studies and only two FACE experiments reported that wheat growth increased on average by +31% when CO2 was raised from ca. 350 ppm to ca. 700 ppm. This stimulation is equivalent to ca. +8.8% per 100 ppm CO2 increment. Compared to these results the wheat grain yield stimulation observed in the present FACE study (adequate N supply only) is equivalent to ca. +9.3% per 100 ppm CO2 increment which is close to the numbers given by Amthor (2001).

5. Conclusion Model predictions of European crop yields under future climate conditions are strongly influenced by direct effects of increasing atmospheric CO2 concentrations. In order to make more reliable predictions these models require data from CO2 enrichment experiments under true field conditions. The present FACE experiment carried out under conditions of a crop rotation over six years shows consistent negative CO2 effects on tissue N concentrations of all crop species tested which is of particular importance with respect to forage quality. Average biomass and yield enhancements by elevated CO2 concentrations between ca. +10% and +15% were observed, which are lower than in most previous chamber studies using the same crop species. Contrary to expectations there was no unambiguous evidence that N fertilization determines the extent of tissue N losses and biomass and yield stimulations by elevated CO2 . Overall, the results support the assumption (Ainsworth et al., 2008) that lower growth enhancements can be expected if crop

105

plants are exposed to elevated CO2 under FACE rather than chamber or enclosure conditions. Assuming no fundamental physiological differences per se in the CO2 response mechanisms between the different crop species the present data do not allow to explain the variability of the effect between years and N supply. Also, the data do not account for any indirect CO2 effects on the crops in the course of the six years rotation period which could have been mediated by cumulative responses of soil variables, e.g. due to CO2 induced changes in the plant root and rhizosphere environment (Anderson et al., 2011). Acknowledgements The FACE apparatus was engineered by Brookhaven National Laboratory and we are grateful to Dr. George Hendrey, Mr. Keith Lewin, and Dr. John Nagy for their support. Technical assistance by the staff of the Institute of Agroecology of the former Federal Agricultural Research Centre (FAL), by the Agrometeorological Research Station of the German Weather Service at Braunschweig and by the staff of the experimental station of the former FAL is gratefully acknowledged. We are also indebted to Dr. Cathleen Frühauf and Dr. Andreas Pacholski for managing the FACE apparatus. We also would like to thank the Federal Ministry of Food, Agriculture and Consumer Protection for financial support. References Ainsworth, E.A., Long, S.P., 2005. What have we learned from 15 years of free air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2 . New Phytology 165, 351–372. Ainsworth, E.A., Leakey, A.D.B, Ort, D.R., Long, S.P., 2008. FACE-ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2 ] impacts on crop yield and food supply. New Phytology 179, 5–9. Ainsworth, E.A., McGrath, J.M., 2010. Direct effects of rising atmospheric carbon dioxide and ozone on crop yields. In: Lobell, D., Burke, M. (Eds.), Climate Change and Food Security. Adapating Agriculture to a Warmer World. Advances in Global Change Research 37, 109–130. Alexandrov, V., Eitzinger, J., Cajic, V., Oberforster, M., 2002. Potential impact of climate change on selected agricultural crops in north-eastern Austria. Global Change Biology 8, 372–389. Amthor, J.S., 2001. Effects of atmospheric CO2 concentration on wheat yield: review of results from experiments using various approaches to control CO2 concentrations. Field Crops Research 73, 1–34. Anderson, T.H., Heinemeyer, O., Weigel, H.J., 2011. Changes in the fungal-to-bacterial respiratory ratio and microbial biomass in agriculturally managed soils under free-air CO2 enrichment (FACE)—a six-year survey of a field study. Soil Biology and Biochemistry 43, 895–904. 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. European Journal of Agronomy 7, 43–52. Bender, J., Hertstein, U., Black, C.R., 1999. Growth and yield responses of spring wheat to increasing carbon dioxide, ozone and physiological stresses: a statistical analysis of ‘ESPACE-Wheat’ results. European Journal of Agronomy 10, 185–195. Bindi, M., Migliett, F., Vaccari, F., Magliulo, E., Giuntola, E., 2006. Growth and quality responses of potato to elevated [CO2 ]. In: Nösberger, J., Long, S.P., Norby, R.J., Stitt, M., Hendrey, G.R., Blum, H. (Eds.), Managed Ecosystems and CO2 , vol. 187. Springer. Burkart, S., Manderscheid, R., Wittich, K.P., Löpmeier, F.J., Weigel, H.J., 2011. Elevated CO2 effects on canopy and soil water flux parameters measured using a large chamber in crops grown in free air CO2 -enrichment. Plant Biology 13, 258–269. Campbell, B.D., Stafford Smith, D.M., Ash, A.J., Fuhrer, J., Gifford, R.M., Hiernaux, P., Howden, S.M., Jones, M.B., Ludwig, J.A., Manderscheid, R., Morgan, J.A., Newton, P.C.D., Nösberger, J., Owensby, C.E., Soussana, J.F., Tuba, Z., ZuoZhong, C., 2000. A synthesis of recent global change research on pasture and rangeland production: reduced uncertainties and their management implications. Agriculture, Ecosystems and Environment 82, 39–55. Cotrufo, M.F., Ineson, P., Scott, A., 1998. Elevated CO2 reduces the nitrogen concentration of plant tissue. Global Change Biology 4, 43–54. Cure, J.D., Acock, B., 1986. Crop responses to carbon dioxide doubling: a literature survey. Agricultural and Forest Meteorology 38, 127–145. DaMatta, F.M., Grandis, A., Arenque, B.C., Buckeridge, M.S., 2010. Impacts of climate change on crop physiology and food quality. Food Research International 43, 1814–1823. Demmers-Derk, H., Mitchell, R.A.C., Mitchel, V.J., Driscoll, S.P., Gibbard, C., Lawlor, D.W., 1996. Sugar beet under climatic change: photosynthesis and production. Aspects of Applied Biology 45, 163–170.

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