Measured and modeled biomass growth in relation to photosynthesis acclimation of a bioenergy crop (Reed canary grass) under elevated temperature, CO2 enrichment and different water regimes

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

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Measured and modeled biomass growth in relation to photosynthesis acclimation of a bioenergy crop (Reed canary grass) under elevated temperature, CO2 enrichment and different water regimes Zhen-Ming Ge a,b,*, Xiao Zhou c, Seppo Kelloma¨ki b, Heli Peltola b, Christina Biasi d, Narasinha Shurpali d, Pertti J. Martikainen d, Kai-Yun Wang b a

State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 200062 Shanghai, China School of Forest Sciences, University of Eastern Finland, Joensuu Campus, Yliopistokatu 7, P.O. Box 111, FIN-80101 Joensuu, Finland c Shanghai Research Center for Transport, Port and Shipping Development, 200025 Shanghai, China d Department of Environmental Science, University of Eastern Finland, P.O. Box 1627, FIN-70211 Kuopio, Finland b

article info

abstract

Article history:

The seasonal biomass growth and photosynthesis performance of a bioenergy crop, Reed

Received 24 August 2010

canary grass (Phalaris arundinacea L.) under elevated temperature (ambient þ 3.5  C), CO2

Received in revised form

enrichment (700 mmol mol1) and different water regimes, was examined. To quantify the

26 June 2012

contributions of acclimated photosynthesis to biomass growth under the environmental

Accepted 29 August 2012

treatments, a simplified model was parameterized to simulate the seasonal biomass

Available online 27 September 2012

accumulation of this bioenergy crop. As a result, we found that during the early growing periods, the photosynthesis, leaf development and above-ground biomass growth of the

Keywords:

plants were enhanced under elevated temperature conditions, due to higher temperature

Photosynthesis

sum for crop development compared to ambient temperature conditions. However,

Biomass

elevation of temperature resulted also in earlier senescence and lower total biomass of RCG

Simulation

at the final harvest, which effect was the most pronounced with low soil water table. As

Climate change

a comparison, CO2 enrichment increased significantly the leaf development, photosyn-

Water table level

thesis and total biomass growth over the whole growing season. Under the combined

Phalaris arundinacea L.

elevation of temperature and CO2, the acclimation of photosynthesis and total biomass of the plants at the final harvest was similar to those caused by elevated temperature alone. In general, high water table favored the photosynthesis and biomass growth of the plants. To conclude, the simplified model built for this bioenergy crop simulated well the dynamics of seasonal canopy photosynthesis and biomass growth, and with good accuracy. Meanwhile, the uncertainty of model was also discussed. ª 2012 Elsevier Ltd. All rights reserved.

* Corresponding author. School of Forest Sciences, University of Eastern Finland, Joensuu Campus, Yliopistokatu 7, P.O. Box 111, FIN-80101 Joensuu, Finland. Tel.: þ358 13 251 4441; fax: þ358 13 251 4444. E-mail address: [email protected] (Z.-M. Ge). 0961-9534/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biombioe.2012.08.019

252

1.

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Introduction

The drained cut-over peat mining sites on organic soils are frequently cultivated for bioenergy crops such as Reed canary grass (hereafter RCG, Phalaris arundinacea L.) in northern Europe [1]. An important question on these organic soils is how to optimize the biomass production of RCG and the carbon balance of sites simultaneously [2e4]. This is important challenge as on the drained peat mining sites organic soils have a high risk of significant soil carbon losses [5]. Climate change, however, is likely to have a large impact on carbon accumulation in the biomass of RCG on peatlands. In Finland, the mean annual temperature is expected to increase by 2e7  C with a concurrent elevation of CO2 by the end of the 21st century [6,7]. The changing climate may also affect soil water availability and the consequent carbon uptake and plant growth, and finally plant biomass. In fact, the drought episodes are expected to become more frequent and limit plant growth even in the central boreal zone [8]. Many studies have been conducted to understand the effects of temperature, CO2 and soil water availability on photosynthesis of C3 herbaceous crops (e.g., wheat Triticum spp. and rice Oryza spp.) in natural and agricultural ecosystems [9e13]. In some earlier studies, increased temperature has been found to reduce crop biomass by decreasing photosynthesis, which could be a result of earlier deactivation of photosynthetic enzyme [11,13]. However, it was also reported that temperature had no significant effects on the biomass growth of crops [14]. In general, CO2 enrichment is expected to substantially increase net photosynthetic CO2 uptake and water use efficiency, and decrease transpiration through reducing stomatal conductance [15]. On the other hand, the stomatal response of plants exposed to CO2 enrichment has been found to vary among species [16,17]. The combined elevation of temperature and CO2 will also affect carbon uptake (photosynthesis), reflecting possibly some offsetting acclimation responses [12,18]. Drought has substantial negative influences on many physiological processes of plants such as photosynthesis, stomatal behavior, chlorophyll fluorescence and metabolite accumulation (e.g., [19]). It has been shown that high soil water availability favored the high rate of CO2 fixation by photosynthesis of RCG in the abandoned peatland [1]. It has also been previously demonstrated that increasing drought episodes will inhibit many growth processes, and that CO2 enrichment will partially mitigate some of these adverse effects [20]. Most of previous studies have focused on the interim photosynthetic performance of plant to climate change (i.e. temperature and CO2 elevation), though a few follow the response along the whole growing periods (e.g., [21]). This is despite, the plant growth and biomass accumulation are usually the focuses of research regarding the bioenergy crop. Up to date, there are very few studies that have either dealt with interaction among climatic factors and soil water availability (e.g., [20,22,23]). Thus, there is limited understanding available of the predicted biomass growth (through modeling approach) based on the photosynthetic acclimation of the boreal bioenergy crop (RCG) under the conditions of climate change.

In the above context, the aim of this work was to examine the seasonal acclimation of photosynthesis and biomass growth of RCG under elevated temperature (ambient þ 3.5  C), CO2 enrichment (700 mmol mol1) and varying soil water regimes. For this purpose we conducted a factorial experiment with RCG microcosms taken from a cut-over peat site to greenhouses where the environmental conditions could be accurately controlled either separately or concurrently over whole growing season. More specifically, the objective of this study was (1) to understand the seasonal characteristics of measured photosynthesis performance and biomass growth of RCG, and (2) to model the seasonal biomass accumulation with acclimated photosynthesis of RCG under different temperature, CO2 enrichment and soil water regimes based on a simple biomass growth model parameterized for RCG.

2.

Material and methods

2.1.

Plant material and growing conditions

The RCG sampling was conducted in the Linnansuo peatland (latitude 62 320 1200 N; longitude 30 250 4500 E) in Eastern Finland. The field has been cultivated since 2001 (i.e. the cultivation was seven years old at the time of sampling) by a peat & bioenergy production company (Vapo Energy Ltd.). The cultivation of RCG on peat soils generally follows a 10e15 year rotation cycle. The RCG variety cultivated in the Linnansuo peatland was ‘Palaton’ obtained from Seed Link Inc. (Canada) by the Finnish seed company (S.G. Nieminen Oy). The general RCG cultivation practice in the Fenno-Scandinavian region is to harvest the crops in the spring of the following year. After harvesting, the Linnansuo peatland is fertilized with nitrogen (N) 59.5 kg ha1, phosphorus (P) 14.0 kg ha1 and potassium (K) 45.5 kg ha1. Fertilizers are applied every year. In March 2009, the RCG-peat monoliths were transplanted into high density polyethylene containers with internal size of 80 cm L  60 cm W  40 cm D (large size selected to reduce stress on the root system, see Shurpali et al. [24]). The volume of peat bulk sample was almost equal to the size of the container, and the gaps between peat and container were tamped with the small peat pieces. In April 2009, 48 containers with microcosms were moved into a greenhouse at Mekrija¨rvi Research Station (latitude 62 460 1500 N, longitude 30 580 2100 E, belong to University of Eastern Finland), about 30 km from the Linnansuo peatland. The greenhouse consists of two main structural sections: (i) control and facility center and (ii) 16 growth chambers [25]. Each chamber is an independent research unit, around 16 m2 in size. Room height is 4 m and the internal volume is 64 m3. The 16 chamber units were divided into 4 climate treatments following a factorial design: (i) ambient temperature and CO2 concentration (around 370 mmol mol1) (CON), (ii) elevated temperature and ambient CO2 concentration (ET), (iii) CO2 enrichment (around 700 mmol mol1) and ambient temperature (EC), and (iv) elevated temperature and CO2 enrichment (ETC). During the period of RCG cultivation (2009e2010), the CON chambers were set to follow outside free air temperature and CO2 concentration, while the target mean temperature

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

was set at þ3.5  C above the outside ambient temperature in the ET and ETC chambers (see technical details and performance of the chamber system in detail, [25]). Three containers in each chamber were treated with three soil water table levels, i.e. high water table level (HW, 100% volumetric soil water content), normal water table level (NW, w50% as field measurement), and low water table level (LW, w30%). The wilting point of drained agriculture peatland is about 20e30% of volumetric soil water content in Finland [26]. The irrigation targets were regulated with the manual soil moisture sensors. In order to avoid edge effects the containers were rotated once a week. The growth characters (height, stem diameter, leaf length and leaf area) of RCG in four replicates of each climate treatment were relatively homogenous, as listed in Table 1.

2.2.

Measurements

2.2.1.

Layout of measurements

Over two growing seasons (2009e2010), the measurements of photosynthetic responses and biomass growth (detail see below) were made on six occasions during the growing season in 2010. These measurement periods are denoted by Roman numerals; Approximately, I: 30th Maye15th June, II: 16th Junee30th June, III: 1st Julye15th July, IV: 16th Julye1st August, V: 2nd Auguste15th August, VI: 16th Auguste15th

Table 1 e Mean (SE) of height, stem diameter, leaf length and leaf area (per shoot) in 4 replicates of each ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC), elevated temperature and CO2 (ETC) chamber and field data during fifth growth period (period V, see Section 2.2.1) averaged by all water table levels. The plant shoots grown in the sample basal area of 153.4 cm2 (14 cmdiameter) based on 4 sampling replicates were measured. One-way ANOVA analysis was used to test the significant differences at P £ 0.05 level. Treatment

CON-1 CON-2 CON-3 CON-4 P ET-1 ET-2 ET-3 ET-4 P EC-1 EC-2 EC-3 EC-4 P ETC-1 ETC-2 ETC-3 ETC-4 P

Stem height (cm)

Stem diameter (mm)

106.7 (10.1) 107.2 (10.1) 106.8 (10.1) 106.6 (10.3) 0.20 95.3 (9.2) 92.4 (9.2) 93.3 (9.2) 98.1 (9.2) 0.55 110.5 (10.3) 109.3 (10.5) 109.6 (10.5) 109.3 (10.7) 0.31 105.6 (10.3) 105.5 (10.2) 105.0 (10.3) 105.3 (10.3) 0.41

0.24 (0.01) 0.23 (0.01) 0.24 (0.01) 0.23 (0.01) 0.09 0.24 (0.01) 0.25 (0.01) 0.24 (0.01) 0.24 (0.01) 0.15 0.27 (0.01) 0.26 (0.01) 0.28 (0.01) 0.27 (0.01) 0.08 0.24 (0.01) 0.26 (0.01) 0.27 (0.01) 0.26 (0.01) 0.07

Leaf length (cm) 16.6 16.4 16.3 16.6 0.40 16.6 16.2 16.3 16.2 0.29 18.2 18.8 18.4 18.7 0.24 18.3 18.1 18.3 18.2 0.62

(1.7) (1.1) (1.1) (1.1) (1.3) (1.2) (1.7) (1.4) (1.1) (1.2) (1.3) (1.8) (1.1) (1.1) (1.2) (1.2)

Leaf area (cm2) 28.5 (2.7) 28.3 (2.8) 28.2 (2.5) 28.6 (2.4) 0.44 27.7 (1.3) 28.1 (1.9) 28.3 (1.9) 27.8 (2.3) 0.12 30.7 (1.9) 30.4 (1.9) 30.4 (1.7) 30.8 (1.0) 0.16 28.8 (1.7) 29.3 (2.4) 32.5 (3.7) 29.2 (2.8) 0.16

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September, roughly following the RCG development stages in the field [27] (from “before flag emergence” to “seed ripening and plant senescence”).

2.2.2.

Measurements of gas exchange

The gas exchange measurements on the RCG leaves were restricted to the time period between 0800 and 1100 h on sunny and generally cloud-free days, to minimize diurnal effects on photosynthesis. The light-saturated net photosynthetic rates (Psat, mmol m2 s1) of intact, second fully expanded leaves of RCG were measured under 1500 mmol m2 s1 photosynthetic photon flux densities (PPFD), using infrared gas analyzers built into a 2  3 cm standard leaf chamber in a portable Li-6400 infrared gasexchange system (Li-6400, Li-cor Inc., Nebraska, USA). The CO2 source for the measurements was a computer-controlled CO2 mixing system supplied with the Li-6400, and the CO2 concentration in leaf chamber was kept at 370  1 mmol mol1 and 700  2 mmol mol1 under ambient and elevated CO2 conditions, respectively. The CO2 supply was controlled as less than 0.1 mmol mol1 variation in 5 s. During all measurement processes, the temperature inside the leaf chamber was kept at 20  1  C. VPD was kept 1.0  0.1 kPa and relative humidity of the air in the leaf chamber was set above 60%. Leaves were equilibrated at saturating PPFD before initiation of the light response. Sufficient time was allowed for the saturated PPFD to stabilize and the concentration of CO2 inside the leaf chamber to mix totally before logging the measurements (typically requiring 20 min or less). As stomatal movements are very dynamic due to the complex regulation by multiple factors, only light-saturated stomatal conductance ( gsat, mol m2 s1), which is usually correlated with the average daily mean conductance, was measured.

2.2.3.

Measurement of growth parameters and biomass

RCG were harvested immediately after gas exchange measurement using a ring with 14 cm diameter (around 154 cm2) down to the soil surface, to identify the harvest area. From each treatment, total plants were taken to determine leaf length (LL, cm) and leaf area (LA, cm2). The number of shoots in each sample plot was recorded. The leaf area of the fully expanded leaves was determined by using a leaf area meter (Li-3100, Li-cor Inc., Nebraska, USA). After harvesting the aboveground part, a soil core (14 cm diameter) was additionally taken for determining the belowground root biomass. The soil core was sampled to a depth of 35 cm, thus, up to the maximum rooting depth of the plants [24]. In the laboratory conditions, the harvested roots were carefully washed over a 0.2 mm sieve. However, only living roots were sampled. The roots were also separated into coarse (diameter > 2 mm) and fine roots, respectively. The increment of root biomass was calculated based on the initial root biomass at the beginning of the growing season. Harvested leaves, stems and roots were dried in a forcedair oven at 70  C for at least 72 h to determine dry mass. Leaf development and organ dry mass were calculated as an average at shoot level. As the seed production of RCG is slightly unreliable (because of seed shattering and occasionally poor panicle production) we did not take seed biomass into account [28].

254

2.2.4.

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

Statistical analysis of measurements

Statistical analyses were carried out using the SPSS (Chicago, IL) software package (Version 16.0). Physiological parameters (i.e. Psat and gsat), growth and biomass characters (i.e. LA, LL, and organ biomass) were tested for the various treatment effects (CO2, temperature and soil water table level) and their interactions using three-way ANOVA. The results for different measurement periods (Periods IeVI) were analyzed separately. Differences between treatments are identified at P  0.05. Furthermore, mean differences among the four climate chambers (CON, ET, EC and ETC chambers) and among the three different soil water table levels (HW, NW and LW) in each climatic chamber were also tested using Tukey’s HSD test.

2.3.

The model

2.3.1.

Outlines for modeling

A simplified biomass growth model was constructed based on known principles of photosynthesis, autotrophic respiration, and growth increment and biomass partitioning. Plant photosynthesis is calculated by scaling leaf level Farquhar’s biochemical model [29,30] up to canopy-level implemented through a sunlit and shaded leaves separation algorithm [31,32]. The allometric carbon partitioning is identified [33], and the seasonal carbon loss of root respiration is taken into account [34]. In this model, seasonal acclimation of the photosynthetic parameters of RCG, as well as seasonal dynamics of the carbon allocation in plant, under elevated temperature, CO2 enrichment and varying soil water table regimes are highlighted [30,32,33]. The rate of leaf-level net photosynthesis (Pn) is limited by the processes shown in Eqs. (1)e(4) [29]: the Rubisco (ribulose1,5-bisphosphate carboxylase/oxygenase) limited rate of photosynthesis (Pc) and the RuBP (ribulose-1,5-bisphosphate) regeneration-limited rate of photosynthesis (Pj), considering the regulation by gs (stomatal conductance) and Ci (intercellular CO2 concentration). In addition, gs is assumed to be controlled by the net radiation on canopy (Ra), air temperature (Ta), vapor pressure deficit (Da), atmospheric CO2 (Ca) and soil water content (qs). Besides the Farquhar’s equations, the two core photosynthetic parameters of the maximum rate of Rubisco activity (Vcmax) and the maximum rate of electron transport (Jmax) are also related to the phase of maturity based on the daily temperature sum (TS, degree days), using the quadratic functions in Eq. (6).
 Pn ¼ min Pc ; Pj

(1)

 Pc ¼ Vcmax

 Ci  G  Rd Ci þ Kc ð1 þ O=Ko Þ

(2)

  Ci  G Pj ¼ f ðJmax Þ   Rd 4 Ci þ 8 G

(3)

Ci ¼ Ca  Pn =gs

(4)


 gs ¼ max gs:max f ðRa Þf ðTa Þf ðDa Þf ðCa Þf ðqs Þ; gs:min

(5)

Vcmax ; Jmax ¼ f ðDHa ; DHd ; DS; c; TSÞ

(6)

TS ¼

X

ðTd  5Þ

(7)

where Rd is the day-respiration rate, G* is the CO2 compensation point in the absence of dark respiration, Kc and Ko are the Michaelis constants for CO2 and O2, respectively, O is the oxygen concentration, DHa is the enthalpy of activation, DHd is the enthalpy of deactivation, DS is the entropy, c is a parameter, and Td is the daily average temperature. An integrated sunlit/shaded algorithm is used to consider the canopy-level carbon uptake (Pnc) with the area fraction of sunlit (LAsun) and shaded leaves (LAsh) in Eq. (8). To relate photosynthesis to the nitrogen concentration of leaf (NL) within canopy layers, we assumed Vcmax, Jmax and Rd in the models to be linear functions of NL in Eq. (9) [31,35]. The dynamics of light regime within canopy layers is estimated based on [31]. Pnc ¼ LAsun Pn:sun þ LAsh Pn:sh

(8)

Vcmax:i ; Jmax:i ; Rd:i ¼ c1 ðNL  c2 Þ

(9)

where Pn.sun and Pn.sh are photosynthesis separately accounted for the contribution of sunlit and shaded leaf fractions, respectively, i is the layer, and c1 and c2 are regressed parameters. Seasonal root respiration (Rroot) in this model is identified as a ratio of net photosynthesis under varying soil water conditions during different growth stages [34]. Regarding seasonal day matter (B) partitioning between above (leaf and stem) and below (root) parts of RCG, the carbon allocation in plant is firstly calculated during the development stages expressed as the quadratic functions of TS for aboveand below-ground fractions in Eqs. (11) and (12) [33]. Then, the carbon-biomass conversion factors [33] for plant organs are used to determine the seasonal accumulation of aboveground biomass (Babove) and increment of below-ground biomass (Bbelow). B ¼ Babove þ Bbelow

(10)

Babove ¼ ðPnc  Rroot Þvc:a Cini:a f ðTSÞ

(11)

Bbelow ¼ ðPnc  Rroot Þvc:b Cini:b f ðTSÞ

(12)

where vc.a and vc.b are the carbon-biomass conversion factors for above- and below-ground organs, respectively, and Cini.a and Cini.b are the initial rates of carbon allocation for aboveand below-ground organs, respectively.

2.3.2. Model parameterization and testing of model performance The model was parameterized based on measured RCG (or other herbaceous crops) data and other data reported in the literature. More specifically: (1) We parameterized the photosynthesis equations from the measured data set of RCG focusing on the seasonal acclimation of photosynthetic parameters to environmental treatments and phase of maturity (quantified as temperature sum) [30], as well as the distribution of nitrogen in canopy under elevated temperature, CO2 enrichment and varying soil water regimes and [32]; (2) Data from the literature for the ratio (ranging 10e20%) of

255

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3.1. Measured gas exchange, leaf development and biomass accumulation of RCG

(P < 0.05) all gas exchange parameters. Over all the periods, statistically significant (P < 0.05) interaction was found for CO2  T  W in regard to Psat. For gsat, significant interactions between CO2  W and CO2  T  W interactions across the various measurement periods were detected (Table 2). The values of Psat were lower at the beginning of growing periods, showing a peak at the end of June (under elevated temperature) or in the middle of July (under ambient temperature), and thereafter decreased during the latter part of the growing period. During the first growing periods (period IeIII), Psat tended to be higher in the ET chambers (on average 17% higher, P < 0.05) than in the CON chambers regardless of water levels (Fig. 1, Table 3). However, during periods IVeVI, Psat was, on average, 13% lower in the ET chambers than that in the CON chambers. CO2 enrichment (EC and ETC) increased Psat, on average, by 33% (P < 0.05) compared to ambient CO2 (CON and ET) through all the growing periods (Fig. 1), regardless of temperature treatments and water levels. Psat in the ETC chambers was, on average, 41% higher compared to the CON chambers during periods IeIII, but the increase was much smaller (on average 18% higher) during the periods IVeVI (Fig. 1, Table 3). Over all growing periods and soil water table levels, the values of gsat were, on average, 35% lower (P < 0.05) under CO2 enrichment compared to ambient CO2 (Fig. 1). However, it was not significantly affected by temperature elevation during the growing periods. Over all water table levels, gsat was under elevated temperature (ET and ETC), on average, 17% higher (P < 0.05) compared to ambient temperature (CON and EC) conditions, during growing periods IeIII. During the latter periods (IVeVI), gsat was, on average, 18% lower (Fig. 1). Irrespective of growing periods and climatic treatments, Psat and gsat were statistically significantly (P < 0.05) higher in HW and NW (on average 24% and 27% higher) compared to LW of RCG (Fig. 1, Table 3).

3.1.1.

3.1.2.

root respiration to photosynthesis in response to soil water conditions during different growth stages (jointing, anthesis and grain-filling) [34], was used to approximate the seasonal carbon loss of root respiration; (3) The parameters used in the calculation of carbon allocation were fitted using the reported data for RCG in [33]; (4) The carbon content of leaves, stems and roots of RCG used were 44  0.19, 46  0.81 and 47  2.46%, respectively, regardless of growing periods and environmental treatments [33]. Therefore, the mean constant values were used as carbon-biomass conversion factors for calculating the dry matter accumulation in the plant organs. The model requires climatic and environmental variables as inputs, which were recorded based on the sensor set installed in the chamber system [25]. The driving variables of solar radiation, air temperature, air humidity, atmospheric CO2 concentration, and soil water content were averaged hourly and daily for different sub-models for the growing period from 1st April to 30th September 2010. In order to determine the accuracy of the simulations, the relative biases and the root mean square errors (RMSEs) were calculated. bias ¼ 100 

 P
bi n yi  y P bi =n y

(13)

qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi 2 P
bi =ðn  1Þ yi  y P RMSEs ¼ 100  bi =n y

(14)

^i are the where n is the number of observations, and yi and y measured and modeled values.

3.

Results

Gas exchange

Different effects of CO2 levels were significant (P < 0.05) for the light-saturated net photosynthesis (Psat) and light-saturated stomatal conductance ( gsat) regardless of water levels and growing periods (Table 2). However, differences between temperature regimes were not significant for all the above parameters. Growing periods affected also significantly

Leaf development

For leaf area (LA), significant differences existed between CO2 enrichment and soil water table levels. For specific leaf area (SLA), significant (P < 0.05) differences were observed among temperature, CO2 enrichment and soil water table level regimes. No significant interactions for them were found for the leaf growth, however (Table 2).

Table 2 e Main and interactive effects (F values) between temperature, CO2, water table level and growing periods on the parameters of gas exchange, leaf development and biomass growth. Symbols used in the three-way ANOVA. Significance values: *P < 0.05; ns non-significant differences. Factors

Period (P) Temperature (T ) CO2 (C ) Water level (W ) TC TW CW TCW

Gas exchange

Leaf development

Biomass growth

Psat

gsat

LA

SLA

Leaf

Stem

Above-ground

11.4* 0.1 ns 33.3* 10.7* 0.1 ns 0.2 ns 0.2 ns 0.3 ns

11.17* 0.160 ns 27.83* 7.20* 0.18 ns 2.16 ns 8.43* 3.64*

94.9* 1.6 ns 15.4* 12.3* 0.4 ns 0.2 ns 0.0 ns 0.0 ns

87.9* 107.0* 42.1* 38.9* 0.4 ns 3.3 ns 0.9 ns 1.2 ns

103.3* 12.3* 36.7* 19.3 ns 0.8 ns 1.3 ns 0.1 ns 0.3 ns

324.2* 4.1* 22.3* 27.2* 0.0 ns 1.0 ns 0.0 ns 0.0 ns

243* 7.4* 30.2* 26.6* 0.2 ns 1.2 ns 0.0 ns 1.1 ns

Coarse root

Fine root

Below-ground

221* 3.8 ns 20.2* 7.9* 4.6 ns 0.1 ns 0.2 ns 0.1 ns

267* 4.2 ns 24.5 * 12.6 * 3.3 ns 0.1 ns 0.1 ns 0.1 ns

263* 4.3 ns 24.3* 11.6* 3.4 ns 0.1 ns 0.1 ns 0.1 ns

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P

( µ mol m s )

30 25

HW

NW

LW

ET

CON

EC

ETC

20 15 10 5

g

(mol m s )

0 0.3 0.2 0.1 60

25 HW

SLA (cm g )

NW

LW 20

40

15

30 10

20 10

5

0

0

LL (cm )

LA (cm )

50

300 200 100 0 I

II

III

IV

V

VI

II

I

III

IV

V

VI

II

I

III

IV

V

VI

II

I

III

IV

V

VI

Periods

Fig. 1 e Mean (SE) light-saturated net photosynthetic rates (Psat), light-saturated stomatal conductance ( gsat), leaf area per shoot (LA, bars), leaf length (LL, lines) and specific leaf area (SLA) of RCG in the ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC) and elevated temperature and CO2 (ETC) chambers combined with high (HW), normal (NW) and low (LW) water table level during the growing periods (IeVI, see Section 2.2.1), based on 4 replicates in each chamber.

Leaf Biomass (g)

0.6 HW

NW

I

II

EC

ET

CON

LW

ETC

0.4

0.2

Above-ground Biomass (g) Stem Biomass (g)

1.6 1.2 0.8 0.4 1.6 1.2 0.8 0.4 0 III

IV

V

VI

I

II

III

IV

V

VI

I

II

III

IV

V

VI

I

II

III

IV

V

VI

Periods

Fig. 2 e Mean (SE) leaf, stem and aboveground biomass (per shoot) of RCG in the ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC) and elevated temperature and CO2 (ETC) chambers combined with high (HW), normal (NW) and low (LW) water table level during the growing periods (IeVI, see Section 2.2.1), based on 4 replicates in each chamber.

257

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Table 3 e Statistical analysis (Tukey’s HSD test) of photosynthetic and leaf development parameters in four climatic treatments in the elevated temperature (ET), CO2 enrichment (EC), and elevated temperature and CO2 (ETC) chambers compared to ambient climate (CON) chambers during the six growing periods (IeVI, see Section 2.2.1). Significant increases and decreases at P £ 0.05 level is shown as [ and Y, respectively. The differences between water table levels were tested by comparing the normal water table level (NW) and low water table level (LW) with high water table level (HW). Significant increases and decreases at P £ 0.05 level is shown as (D) and (L), respectively. Non-significant differences are shown as ns. Blank grid means control blank. Parameters Treatment

I

II

HW NW Psat

gsat

LA

SLA

CON ET EC ETC CON ET EC ETC CON ET EC ETC CON ET EC ETC

[ [ [ [ ns ns [ [ [ ns ns Y

(ns) [(ns) [(ns) [() (ns) [(ns) ns(ns) ns(ns) (ns) [(ns) [(ns) [(ns) (ns) ns(ns) ns(ns) Y(ns)

LW HW NW () ns() [() [() () [() ns(ns) ns() (ns) [(ns) [(ns) ns(ns) (ns) Y() ns(ns) Y(ns)

[ [ [ [ Y ns [ [ [ ns ns Y

(ns) ns() [(ns) [() (ns) [() Y(ns) Y() (ns) [(ns) [(ns) [(ns) (ns) ns(ns) ns(ns) Y(ns)

III

IV

LW HW NW

LW HW NW

() ns() [() [() () [() Y(ns) Y() (ns) [(ns) [(ns) [(ns) (ns) Y() ns(ns) Y(ns)

ns [ [ ns Y Y ns [ [ Y ns Y

(ns) ns() [(ns) [(ns) (ns) ns(ns) Y(ns) Y(ns) (ns) ns(ns) [(ns) [(ns) (ns) Y(ns) Y(ns) Y(ns)

() ns() [() [() () ns() Y(ns) Y() (ns) ns() [(ns) [() (ns) Y() Y() Y()

ns [ [ ns Y Y ns ns ns ns ns Y

() ns() [(ns) ns() (ns) ns(ns) Y(ns) Y(ns) (ns) ns(ns) ns(ns) ns(ns) (ns) ns(ns) ns(ns) Y(ns)

V LW HW NW () ns() [() ns() () ns() Y() Y() (ns) ns() ns(ns) ns() (ns) Y() Y(ns) Y()

ns [ [ Y Y Y ns ns ns ns ns Y

(ns) ns() [() ns(ns) (ns) Y(ns) Y(ns) Y(ns) (ns) ns(ns) ns(ns) ns(ns) (ns) ns(ns) Y(ns) Y(ns)

VI LW HW NW () ns() [() ns() () Y() Y() Y() () ns() ns() ns() () Y() ns(ns) Y()

ns [ ns Y Y Y ns ns ns ns ns Y

(ns) ns(ns) ns ns ns(ns) (ns) Y(ns) Y(ns) Y(ns) (ns) Y(ns) ns(ns) ns(ns) (ns) ns(ns) Y(ns) Y(ns)

LW (ns) ns() ns() ns() () Y() Y() Y() () Y() ns() ns() () ns() ns() Y()

Table 4 e Statistical analysis (Tukey’s HSD test) of biomass in four climatic treatments in the elevated temperature (ET), CO2 enrichment (EC), and elevated temperature and CO2 (ETC) chambers compared to ambient climate (CON) chambers during the six growing periods (IeVI, see Section 2.2.1). Significant increases and decreases at P £ 0.05 level is shown as [ and Y, respectively. The differences between water table levels were tested by comparing normal water table level (NW) and low water table level (LW) to high water table level (HW). Significant increases and decreases at p £ 0.05 level is shown as (D) and (L), respectively. Non-significant differences are shown as ns. Blank grid means control blank. Parameters

Treatment

I HW NW

Leaf biomass

Stem biomass

Above-ground biomass

Coarse root biomass

Fine root biomass

Below-ground biomass

CON ET EC ETC CON ET EC ETC CON ET EC ETC CON ET EC ETC CON ET EC ETC CON ET EC ETC

[ ns [ [ ns [ [ ns [ ns ns ns [ [ [ [ ns [

(ns) [(ns) ns(ns) [(ns) (ns) [(ns) ns(ns) [(ns) (ns) [(ns) ns(ns) [(ns) (ns) ns(ns) ns(ns) ns(ns) (ns) [(ns) [(ns) [(þ) (ns) [(ns) ns(ns) [(ns)

II LW HW NW (ns) [(ns) ns(ns) [(ns) (ns) ns() ns() ns() (ns) ns() ns() [() () ns(ns) ns(ns) ns(ns) (ns) ns(ns) Y() ns(ns) () [(ns) ns(ns) [(ns)

[ [ [ [ [ [ [ [ [ ns [ [ [ [ [ [ [ [

(ns) [(ns) ns(ns) [(ns) (ns) [(ns) ns() [() (ns) [(ns) [(ns) [(ns) (ns) ns(ns) ns(ns) [(þ) (þ) [(ns) Y() [(ns) (ns) [(ns) ns(ns) [(þ)

III

IV

LW HW NW

LW HW NW

(ns) [() [(ns) [() () [() ns() ns() () [() [() [() (ns) ns(ns) ns(ns) ns() () [() [() [() (ns) [(ns) [(ns) [()

[ [ [ [ [ [ [ [ [ ns ns [ [ [ [ [ [ [

(ns) [(ns) [(ns) [(ns) (ns) [(ns) [(ns) [(ns) (ns) [(ns) [(ns) [(ns) (þ) ns(ns) ns(ns) ns(ns) (þ) [() [(þ) [(þ) (þ) [(ns) [(ns) [(ns)

() ns() [() [() () [() [() [() () [() [() [() () [(ns) [(ns) [(ns) () [() [() [() () [() [(ns) [(ns)

ns [ [ [ [ [ ns [ [ ns [ ns Y [ [ ns [ [

(ns) ns(ns) [(ns) [(ns) (ns) ns(ns) [(ns) [(ns) (ns) ns(ns) [(ns) [(ns) (ns) ns(ns) [(ns) [(ns) () [(þ) [(ns) [(þ) (ns) ns(ns) [(ns) [(ns)

V LW HW NW () ns() [() [() () ns() [() [() () ns() [() [() (ns) ns(ns) ns() ns() () [() [() [() (ns) ns(ns) [() [()

ns [ [ ns ns ns ns [ [ ns [ ns ns [ [ Y [ [

(ns) ns(ns) [(ns) ns(ns) (ns) ns(ns) ns(ns) ns(ns) (ns) ns(ns) [(ns) [(ns) (þ) Y(þ) [(þ) ns() (þ) ns(þ) [(þ) ns(ns) (þ) Y(þ) [(þ) [()

VI LW HW NW

LW

() Y() [() ns() () Y() [() ns() () Y() [() [() () Y() [(ns) ns() () Y() [() ns() () Y() [(ns) Y()

() Y() [() ns() () Y() [() ns() () Y() [() ns() () Y() [() ns() () Y() [() Y() () Y() [() Y()

ns [ ns ns ns ns ns [ [ ns [ ns Y [ [ Y [ [

(ns) Y() [(ns) ns(ns) (ns) ns(ns) ns(ns) ns(ns) (ns) ns(ns) [(ns) ns(ns) (ns) Y(ns) [(ns) ns(þ) (ns) Y(þ) [(ns) [(þ) (ns) Y(ns) [(ns) [(þ)

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LA and leaf length (LL) increased rapidly and reached its peak during period IV regardless of climatic treatments and water levels (Fig. 1). Across the whole growing period and water table levels, CO2 enrichment significantly (P < 0.05) increased LA and LL (15% and 31% higher) compared to that under ambient CO2, regardless of temperature treatments (Table 3). The maximum value of LA and LL were, on average, 3% lower, 9% higher and 3% higher in the ET, EC and ETC chambers, respectively, compared to the CON chambers (Fig. 1). Along with the growing period, SLA showed a continual downward trend, regardless of climatic treatments and water table levels. Under elevated temperature, SLA dropped, however, much more slowly (P < 0.05) compared to that under the ambient temperature (Fig. 1, Table 3). SLA was not significantly modified under CO2 enrichment. For periods VI and V, the RCG subjected to LW produced significantly (P < 0.05) smaller leaves and SLA compared with the well-watered plants, regardless of climatic treatments (Fig. 1, Table 3).

3.1.3.

Biomass accumulation

For biomass growth of RCG, different effects of temperatures, CO2 and water levels were significant (P < 0.05) through the whole growing period, except the response of below-ground biomass to temperature (Table 2). No significant interactions were identified in any biomass accumulation. Regardless of climatic treatments and water table levels, the above-ground biomass (both leaf and stem) showed a clear increase from period I to period V. While the decrease in leaf biomass started from the period IV in the elevated temperature chambers (Fig. 2). At the final harvest period (period VI), irrespective of water levels, the above-ground biomass was, on average, 12% lower in the ET chambers compared to the

CON chamber, with 14% and 11% lower in leaf and stem biomass, respectively. While in the EC and ETC chambers, the values of leaf and stem biomass were, on average, 12% (16% and 10% higher in leaf and stem biomass, respectively) and 6% (9% and 5% higher in leaf and stem biomass, respectively) higher than that in the CON chambers (Fig. 2, Table 4). Through the growing season, the increment of fine root biomass was significantly (P < 0.05) higher than that of coarse root biomass over different climatic treatments and soil water table levels. At the end of measurement period, the increment of total root biomass was, on average, 10% lower in the ET chambers than that in the CON chambers, irrespective of water levels (Fig. 3). In the EC chamber, the increment of root biomass increased on average by 24% compared to the CON chamber. However, little difference (on average 3% higher) of the increment was found in the ETC chambers compared to in the CON chambers (Fig. 3). The above-ground biomass was significantly (P < 0.05) lower in LW than that in HW and NW, through all growing periods and climatic treatments (Fig. 2, Table 4). At the end of measurement period, the above-ground biomass was, on average, 19% lower (P < 0.05) in LW compared to HW and NW. On average, the increment of below-ground biomass responded to the different water levels significantly (P < 0.05) regardless of climatic treatments and growing periods (Table 4). In LW, the increment of total root biomass was, on average, 24% and 28% lower (P < 0.05) than that in HW and NW at the end of measurement period, respectively (Fig. 3, Table 4).

3.2.

RCG model performance

The modeled seasonal canopy net photosynthesis (Pnc), above-ground biomass (Babove) and increment of below-

Coarse Root

HW

NW

I

II

EC

ET

CON

LW

ETC

0.3 0.2 0.1 1.6

Fine Root

1.2 0.8 0.4 1.6

Total Root

Average increment of shoot Biomass (g)

0.4

1.2 0.8 0.4 0

III

IV

V

VI

I

II

III

IV

V

VI

I

II

III

IV

V

VI

I

II

III

IV

V

VI

Periods

Fig. 3 e Mean (SE) increment of coarse, fine root and below-ground biomass (per shoot) of RCG in the ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC) and elevated temperature and CO2 (ETC) chambers combined with high (HW), normal (NW) and low (LW) water table level during the growing periods (IeVI, see Section 2.2.1), based on 4 replicates in each chamber.

259

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

ground biomass (Bbelow) of RCG are presented in Fig. 4. As simulated, the values of Pnc in the elevated temperature chambers were higher than that in the ambient temperature chambers till mid-July, thereafter, Pnc declined rapidly towards the end of the growing season. CO2 enrichment increased Pnc across the growing season, compared to ambient CO2. The model realistically simulated the seasonal biomass growth of RCG under each climatic treatments and water levels (Fig. 4, Table 5). For Babove and Bbelow, correlation coefficients (1:1 regression) between modeled and measured biomass growth were ranged from 0.93 to 0.97 and from 0.88 to 0.95, respectively, regardless of climatic treatments and water levels. The modeled maximum Bbelow at the later growing period was slightly higher than the measured values, and the measured lower Bbelow in HW compared to NW was not expressed by the model.

Table 5 e Relative bias, RMSEs and correlation coefficients (R2) between modeled and measured biomass growth through six growing periods (n [ 6) in the ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC) and elevated temperature and CO2 (ETC) chambers combined with high (HW), normal (NW) and low (LW) water table level. Climatic Water treatment level CON

ET

EC

ETC

4.

Discussion

4.1.

Effects of climatic factors over water table levels

2

Bias

RMSEs

R

Bias

RMSEs

R2

1.32 0.63 2.64 3.94 2.37 2.30 3.71 3.65 2.96 1.20 2.52 1.07

0.27 0.26 0.19 0.31 0.20 0.32 0.22 0.24 0.22 0.07 0.15 0.09

0.96 0.97 0.94 0.93 0.94 0.94 0.94 0.94 0.94 0.96 0.94 0.95

4.20 0.85 0.33 3.78 1.93 2.02 3.68 1.86 0.77 6.53 4.24 5.73

0.58 0.21 0.36 0.56 0.27 0.28 0.46 0.31 0.37 1.07 0.52 0.67

0.90 0.94 0.95 0.91 0.93 0.92 0.91 0.93 0.94 0.88 0.90 0.89

the photosynthesis declined earlier under the elevated temperature (from period IV), accompanied by a lower leaf area during the later growing season. Therefore, less time for carbon fixation before seed set resulted in a lower biomass at the end of growing season. As presented previously, the temperature elevation accelerated the ontogenetic development and caused earlier growth senescence resulting from the faster accumulation of thermal time for

We found that elevated temperature stimulated the leaf development, light-saturated photosynthesis and aboveground biomass growth during the early growing season. It was probably because that the developmental stages of RCG are triggered by thermal temperature [27]. Even quite a small increase in temperature could also have considerable cumulative effects on the development of leaves. However,

(g) Shoot average P ( µ mol d )

HW NW LW HW NW LW HW NW LW HW NW LW

Bbelow

Babove

1.2 0.9

HW NW LW

CON

ET

EC

ETC

0.6 0.3 1.6

(g) Shoot average B

1.2 0.8 0.4 1.6

Shoot average B

1.2 0.8 0.4 0

st st 1st Apr. 1st May 1st Jun. 1st Jul. 1st Aug. 1st Sep. 1st Apr. 1st May 1st Jun. 1st Jul. 1st Aug. 1st Sep. 1st Apr. 1 May 1st Jun. 1st Jul. 1st Aug. 1 Sep. 1st Apr. 1st May 1st Jun. 1st Jul. 1st Aug. 1st Sep. 30th Sep.

Date

Fig. 4 e Modeled (lines) canopy net photosynthesis (Pnc, per shoot) and biomass growth against measured (scatters) aboveground biomass (Babove, per shoot) and increment of below-ground biomass (Bbelow, per shoot) of RCG in the ambient climate (CON), elevated temperature (ET), CO2 enrichment (EC) and elevated temperature and CO2 (ETC) chambers combined with high (HW), normal (NW) and low (LW) water table level. The measured biomass data are the same presented in Figs. 2 and 3. The arrows indicated that Pnc began to be lower in the ET and ETC chambers than that in the CON and EC chambers, respectively.

260

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

RCG [33]. The changes in leaf size and overall leaf area duration can have major impacts on total canopy photosynthesis and biomass accumulation (even below-ground). This thermal effect has also been found for other fastgrowing plant species [36]. In this study, CO2 enrichment stimulated the photosynthesis, which was in agreement with the previous studies [10e12]. The probable reason for this was that Rubisco in chloroplast is not CO2-saturated at the current atmosphere CO2 concentration status. Although O2 competes for place in Rubisco with CO2, Rubisco after all favors CO2. Despite the fact that CO2 may reduce gsat by up to about 33% of ambient CO2 values, stomatal apertures are capable of supplying sufficient CO2 to mesophyll cells (e.g., [37]). The CO2 enrichment also increases water use efficiency by decreasing water consumption due to a decline in stomatal conductance [38], by enhancing CO2 fixation, or by the interaction of both [10,39]. Increased biomass growth was also related to expanded leaf area under CO2 elevation, which agreed with [40e42]. In our study, the CO2 enrichment increased below-ground biomass growth. As presented by Pe´rez et al. [43], to alleviate the pressure of carbohydrate accumulation in the leaves and shoots under CO2 enrichment the plants may transport more carbon to the root pools. Additionally, CO2 enrichment increases both carbon partitioning to the rapidly cycling carbon pools (belowground) and root turnover due to increased demand for below-ground resources [44]. During the early growing periods, the light-saturated photosynthesis was highest in the ETC chambers. However, the rate of carbon uptake in ETC was lower compared to EC during the later periods. At the end of growing season, ETC did not significantly enhance the biomass growth compared to CON. This was in agreement with earlier work [14], in which it was demonstrated that high temperatures reduce the stimulatory effect of CO2 enrichment on the production of crop if both continue to increase, probably due to the accelerated senescence and increased autotrophic respiration under warmer environment.

4.2. Effects of soil water table levels over climatic treatments Lower leaf area and biomass growth were found in droughtstressed plants, which were in agreement with previous studies [45,46]. This was related to decreased photosynthesis compared to the well-watered plants due to limited stomatal behavior. In our previous study [32], we found that the chlorophyll fluorescence of RCG in LW was reduced significantly, probably indicating a deactivation or metabolic impairment in photosynthesis center. The decrease in SLA in LW may also be related to the fact that drought stress also affects leaf expansion earlier than photosynthesis [47], and the reduction of SLA is assumed to be a way to adapt to drought conditions [48]. The soil water table level effects have also recently been observed in eddy covariance data in the field experiments for RCG in Linnansuo peatland [1], i.e. high soil moisture and low evaporation favored CO2 uptake, but low soil moisture and high atmospheric stress severely restricted photosynthetic activity.

4.3. levels

Synergetic effects of climatic treatments and water

This study showed that the temperature, CO2 enrichment and soil water table level regimes modified the physiological responses and biomass growth of RCG. However, the statistical differences on interactive effects on biomass growth were not significant. Regarding the measured values, elevated temperature further decreased the plant growth in LW. Especially at late growing periods, ET produced the lowest biomass growth in LW. On the other hand, CO2 enrichment decreased stomatal conductance of RCG in LW, indicating that plants were prevented from excessive water loss, as presented by Aranjuelo et al. [37]. Our results also revealed that CO2 enrichment together with ambient temperature and high water availability resulted in the highest total biomass growth.

4.4. Evaluation of RCG model performance against measurements In line with the measured seasonal dynamics of the lightsaturated photosynthesis of RCG, the modeled canopy photosynthesis was also higher in the elevated temperature chambers during the early growing period with a rapid decline towards the end of summer, compared to ambient temperature. The model performance was based on specific parameterization of the key photosynthetic parameters in response to seasonal leaf nitrogen within canopy layers [32] and temperature sum [30], which was various in the ambient and elevated temperature chambers. Based on the quadratic algorithm, the higher temperature sum during the early period increased the photosynthetic parameters in the elevated temperature chambers. However, the subsequent much higher thermal accumulation reduced the values of parameters more than that in the ambient chambers. In addition, the photosynthesis of RCG under the CO2 enrichment and varying water conditions was reasonably well simulated by our model with the acclimation of the photosynthetic parameters [30]. Furthermore, the seasonal pattern of carbon allocation to different organs of RCG was calibrated for the model [33], resulting in a relatively high correlation between the modeled seasonal biomass growth and measured values. But, the model slightly overestimated the below-ground biomass growth, and it did not express a slightly lower increment of below-ground biomass in HW compared to NW, as measured. One of the probable reasons was the lack of data on the root mortality. Therefore, less dry matter is partitioned to the root system when soil water is excessively provided, as presented by Adiku et al. [49].

5.

Conclusions

Through this study, we found that elevated temperature and water shortage had affected strongly negatively the biomass accumulation of RCG, due to thermal effects and resource limitation in regard to the impacts on photosynthesis performance. The CO2 enrichment positively enhanced the carbon uptake and growth of bioenergy crop. This stimulation might be attributed to higher leaf area and “CO2-fertilzation” effect.

b i o m a s s a n d b i o e n e r g y 4 6 ( 2 0 1 2 ) 2 5 1 e2 6 2

However, the stimulatory effect of CO2 enrichment on the biomass growth of RCG was offset by temperatures elevation. To mitigate the adverse impact of higher temperature, with enough high soil moisture on the drained peatlands, RCG could be expected to be capable to adapt relatively well to the expected climate change. Moreover, different cultivars would be tested in order to identify those with characteristics that would adapt to climate change. Regarding the model, there must be some uncertainties and scarcities because of the potential absence of comprehensive experimental setup and parameterization on the complex processes of plant physiology and growth. Nevertheless, the current model for RCG biomass growth could be much improved for field management and adaptive strategy to climate change, if more information were available.

Acknowledgments This work was funded through the National Program on Key Basic Research Project of China (No. 2010CB951204), the Finland Distinguished Professor Programme (FiDiPro) of the Academy of Finland (No. 127299-A5060-06) and the National Natural Science Foundation of China (No. 41201091). The controlled environment chamber system was covered by the European Regional Development Fund (ERDF) granted by the State Provincial Office of Eastern Finland. Matti Lemettinen, Alpo Hassinen and Risto Ikonen, at Mekrija¨rvi Research Station, are thanked for technical assistance. Dr. David Gritten is greatly thanked for revising the language of this paper.

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