Effectofelevated[CO2]and nutrientmanagement on wetand dry season rice production in subtropicalIndia

Sushree Sgrik Stpthy,Dillip Kumr Swin,*,Surendrnth Psuplk, Prtp Bhnu Singh Bhdori

aAgriculturaland Food Engineering Department,Indian Institute of Technology Kharagpur,PO Box 721302,Kharagpur,India

bOrissa University of Agriculture and Technology,Bhubaneswar,Odisha,India

Effectofelevated[CO2]and nutrientmanagement on wetand dry season rice production in subtropicalIndia

Sushree Sagarika Satapathya,Dillip Kumar Swaina,*,Surendranath Pasupalakb, Pratap Bhanu Singh Bhadoriaa

aAgriculturaland Food Engineering Department,Indian Institute of Technology Kharagpur,PO Box 721302,Kharagpur,India

bOrissa University of Agriculture and Technology,Bhubaneswar,Odisha,India

A R T I C L E I N F O

Article history:

4 August 2015

Accepted 10 September 2015

Available online 14 October 2015

Climate change Nutrient management Elevated[CO2] Rice yield Soil fertility

The present experiment was conducted to evaluate the effect of elevated[CO2]with varying nutrient management on rice-rice production system.The experiment was conducted in the open field and inside open-top chambers(OTCs)of ambient[CO2](≈390μmol L-1)and elevated[CO2]environment(25%above ambient)during wet and dry seasons in 2011-2013 at Kharagpur,India.The nutrient management included recommended doses of N,P,and K as chemical fertilizer(CF),integration of chemical and organic sources,and application of increased(25%higher)doses of CF.The higher[CO2]levelin the OTC increased aboveground biomass but marginally decreased filled grains per panicle and grain yield of rice,compared to the ambient environment.However,crop rootbiomass was increased significantly under elevated[CO2].With respect to nutrient management,increasing the dose of CF increased grain yield significantly in both seasons.At the recommended dose ofnutrients,integrated nutrient management was comparable to CF in the wet season,but significantly inferior in the dry season,in its effect on growth and yield of rice.The[CO2]elevation in OTC led to a marginal increase in organic C and available P content of soil,but a decrease in available N content.It was concluded that increased doses of nutrients via integration of chemical and organic sources in the wet season and chemical sources alone in the dry season will minimize the adverse effect of future climate on rice production in subtropical India.

?2015 Crop Science Society of China and Institute of Crop Science,CAAS.Production and hosting by Elsevier B.V.This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1.Introduction

Climate change resulting fromincreasing atmospheric temperature due to increasing levels of greenhouse gases,mainly [CO2],and variation in rainfallhas direct and indirect effects on global food production[1].As CO2is an essential substrate for photosynthesis,increasing[CO2]willstrongly affect agricultural production and global food security[2,3].Increased[CO2] increases the rate of photosynthesis of C3crops at the cellular level through increased carboxylation and decreased oxygenation,both catalyzed by ribulose-1,5-bisphosphate carboxylase [2].An increase in photosynthetic rates ultimately increases the biomass production and yield of agriculturalcrops[4,5].Several studies have been conducted in recent years to characterize the effects of elevated[CO2]on rice growth and yield in open-field and controlled-environment chamber experiments[6,7].Theirresults have shown that increased[CO2]would increase rice yield,as rice is a C3species and generally responds positively to elevated[CO2]by increasing its carbon assimilation rates.In the absence of temperature rise,several studies have shown increased yields of food grains with increased[CO2][8-10]. However,despite this favorable effect,the combined increase in temperature and variation in rainfallwill markedly affect food grain production.Under climate change scenarios,rising temperature nullifies the positive effect of increased[CO2] concentration on grain yield of cereal crops[11-13].This effect is due to impaired pollination that leads to increased spikelet sterility at high temperatures.

The effect of high temperature on crop growth is expected to be region-specific,because of differing temperature sensitivity of crops in different regions.In tropical and subtropical latitudes,the increased temperature due to global warming will probably be near or above the optimum temperature range for the physiological activities of rice[14,15].Warming will thus impair rice growth and cause spikelet sterility leading to grain yield reduction[16].Higher air temperature also affects soil health:for example,warmer conditions enhance the decomposition of organic matter and increase the rates ofother chemicaland biologicalprocesses that affect inherent soil fertility[17]and thereby food production.

Rice is the second most important food crop in the world, grown on 145 million ha with an annual production of 730 million tons of grain[18].In India,rice is grown on 44 million ha,28%of the world rice area,contributing 22%of rice grain production[18].Rice in India is grown mainly during the wet season(June-November)as a rainfed crop receiving the monsoon rain.Besides the wet-season crop,rice is also grown during the dry season(January-May)with irrigation,a practice more common in eastern India in the subtropical climate.The rice production of both rainfed and irrigated ecosystems is highly vulnerable to climate change,and the productivity of rice cultivation in India has declined since the 1990s in comparison with the rate of population growth[19].

The food grain production of tropical and subtropical countries including India is likely to be severely affected under future climate scenarios,complicating the food security of the developing world.This forecast is due to the generally predicted deleterious effects on agriculture,particularly in tropical and subtropicalcountries[20-22].It is thus important to predict the effect of elevated[CO2]and temperature on growth and yield of rice and changes in soil fertility status, using controlled-environment experiments for development of suitable agro-adaptations to climate change.In the present study,we used open-top chamber(OTC)field experimental facility to characterize the effect of elevated[CO2]with varying nutrient management on rice growth,yield,and nutrient use efficiency and changes in soil chemical properties of rice-rice production systems in subtropical India.

2.Material and methods

2.1.Experimentalsite

Field experiments for characterizing the effect of elevated [CO2]on growth,yield,and nutrient use efficiency of rice crop and analysis of changes in soil chemical properties were performed during the wet season(June-November)and dry season(January-May)in 2011-2012 and 2012-2013 on the research farm of the Agricultural and Food Engineering Department,Indian Institute of Technology Kharagpur, Kharagpur(22°19′N(xiāo) latitude and 87°19′E longitude),India. Soil at the location is red lateritic with sandy loam texture, low in organic C and available N content,medium in available P,and low in available K content.The detailed physical and chemical characteristics of the soil of the experimental field are presented in Table 1.The climate of Kharagpur is humid and subtropical.The location receives an average annual rainfall of 1600 mm with an occurrence of 70-75%of the total rainfall in the wet season(June to November).The average maximum temperature ranges from 25.8°C in December/ January to 36.0°C in April/May.The average minimum temperature ranges from 13.3°C in December/January to 25.9°C in June.

2.2.Experimentaldetails

The field experiments were performed in the open field and in OTCs.OTCs,made of polycarbonate sheets having a minimum of 80%light transmittance,are the most widely used and precise experimental method for exposing field grown plants to elevated[CO2]and other atmospheric gases.An experiment varying[CO2]environment and nutrient management was conducted during the wet and dry seasons of 2011-2012 and 2012-2013.Following are the treatment details of the[CO2]environmental design and nutrient management.

Factor 1:[CO2]environmental(E)design(3 levels)

E1-Open field,

E2-OTC with ambient[CO2]level([CO2]≈390μmol L-1) (ambient),and

E3-OTC with[CO2]level 25%higher than the ambient ([CO2]≈490μmol L-1)(elevated[CO2])

The desired[CO2]level in OTC was maintained with a computer-based data acquisition system,as explained later in the instrumentation section.

Factor 2:nutrient(N)management(5 levels)

N1-Chemical fertilizer(CF)at 100%recommendation of

N,P,and K via soil application:CF100

N2-Integrated nutrient management of CF at 50%recom

mendation of N,P,and K with organic fertilizer(OF)at 50%

N recommendation:CF50+OF50

N3-Integrated nutrient management of CF and OF with

conservation technology(CT):CF50+OF50+CT

N4-CF100 via soil application(SA)of full P and K and 85%

N and foliage application(FA)of remaining 15%N:

SA85+FA15

N5-CF at 125%recommendation of N,P and K through soil

application:CF125

The recommended CF100 dose of nutrients as N:P2O5:K2O was 120:50:60 kg ha-1for both wet and dry seasons.The OF sources were farmyard manure(FYM),sesbania as in-situ green manuring,and Azotobacter.Sesbania seed at 30 kg perhectare was sown 45 days before initial land preparation for rice transplanting and incorporated at the time of land preparation.FYM at 5 t ha-1was applied 15 days before rice transplanting and Azotobacter,a microbial fertilizer,was applied at 10 kg ha-1.The approximate N addition from sesbania,FYM,and Azotobacter as sources of OF was 30,25, and 5 kg ha-1,respectively,to meet 50%of the N recommendation of rice in each season.The P and K requirements of CF were applied in full as basal applications at the time of transplanting,as single superphosphate(16%P2O5)and muriate of potash(60%K2O),respectively.The N requirement of CF was applied as urea(46%N)in four equal splits at planting,active tillering,panicle initiation,and flowering stage of the cultivar.For the treatment with foliage application of N,spraying was performed three times in equal doses one week before and after panicle initiation and one week before heading with a 3%urea solution.In CT,during the harvest of the previous season's rice,stubbles were left with 8 cm above the ground surface and were later incorporated in the soil by normal tillage operations,and the soil was left loose and friable.After the tillage operation,the land was flooded with water to make the soilsofter for transplanting of rice seedling.Rice seedlings were transplanted under non-puddled conditions without disturbing the soil structure in this treatment.In the remaining treatments,conventional puddling was performed for transplanting of rice seedlings.

Table 1–Physical and chemical properties of experimental soil at 0–20 cm depth.

These five nutrient management treatments were applied in two replications in three environments:open field,and ambient and elevated[CO2]in the OTC.These 15 treatment combinations(three[environment]×five[nutrient management])were laid out in a randomized complete block design. The plot size for each treatment was 1.8 m×1.0 m in the OTCs.The land in the open field and OTCs was prepared by puddling for all treatments,except in the treatment with CT, where normalplowing was performed and thereafter the field was flooded with irrigation water for rice transplanting. Rice seedlings 25 days old were transplanted at 2-3 seedlings per hill at a spacing of 20 cm×15 cm.The transplanting dates were July 27 in 2011 and July 15 in 2012 for the wet season and January 31 in 2012 and January 30 in 2013 for the dry season.The cultivars were“Swarna sub1”(140-145 days)in the wet season and“Lalat”(120-125 days)in the dry season.

2.3.Instrumentation

Carbon dioxide monitors and temperature and relative humidity sensors were used to record[CO2]concentration, temperature,and relative humidity in the open field and OTCs.Release of CO2to the OTC was controlled by computer based SCADA(supervisory control and data acquisition) software.SCADA regulated the flow of CO2according to the set value for the OTC.Data loggers were used to record the mean[CO2]concentration as process values for all chambers at 1-min intervals.When the process value was lower than the set value,command passed from the system software to the switching-mode power supply for opening of a relay module to regulate the opening of a solenoid valve for releasing CO2into the OTC.When the process value reached the set value,the relay module and solenoid valve were closed to stop the release of CO2.[CO2]in the open field was about 390μmol L-1.Accordingly,the[CO2]of the OTC with elevated [CO2]was maintained at 25%higher than in the open field,or about 490μmol L-1,by the SCADA.

2.4.Plant sampling and observations

Observations were collected for crop growth parameters at periodic intervals and for yield attributes and yield at crop maturity.

2.4.1.Crop growth

Plant samples were collected from transplanting to harvest at 20-day intervals.For this purpose,nondestructive observations of tiller numbers of 20 hills of a plot were recorded,and the average tiller number of representative hill was established[23].From these 20 hills,two hills with average tiller number were considered as sample hills. Samples from these hills were cleaned and washed in water to remove surface contamination and were separated into stems,leaves,and panicles and placed in paper packets for oven-drying at 70°C to constant weight.The sum of the dry biomass of plant parts was taken as the aboveground biomass production.Leaf weight,stem weight,panicle weight,aboveground biomass,leaf area,and tiller production were recorded. For computing leaf area index(LAI),the leaf area per plant was measured using leaf area meter(Licor LI-3000A)and the LAI was computed following the procedure of[24].

2.4.2.Yield attributes and harvest yield

At the harvest of the rice crop,observations on yield attributes and grain and straw yield were recorded from a 60×60 cm area marked at the center of each plot from which plant sampling had not been performed earlier.The yield attribute total panicle number in this area was measured and average panicle number per m2was determined.From this area,two representative hills were selected and panicles and grains of these hills were separated to determine filled grains per panicle and 1000-grain weight.Grains of all hills of the marked area were separated from straw,and grain and straw weight were recorded for each plot.

2.4.3.Nitrogen uptake and nitrogen use efficiency

The dried leaf,stem and grain samples collected at crop maturity were analyzed for N content following standard protocols[25].From the N contents of the plant parts,the N uptake by plant organs was computed.The total N uptake by rice was the sum of the N uptake by stems,leaves,and grains. The N harvest index(NHI),physiological N use efficiency(PE), and grain N use efficiency(NUEg)were calculated[26,27].

2.5.Soil chemical analysis

Soil samples from a depth of 0-20 cm were collected from each plot after harvest.The samples were collected fromthree randomly selected spots in each plot and were thoroughly mixed to prepare a homogeneous sample.The samples were dried under shade,ground with mortar and pestle,and passed through a 2 mm sieve for analysis of chemicalproperties.Soil samples were analyzed for organic carbon content by the Walkley and Black method[25],available N by the alkaline KMnO4method[28],available P by the NH4F-extraction method[25],and available K by the NH4OAc-extraction method[25].

2.6.Statistical analysis

The crop observations of the two years field experiments were averaged for both wet and dry seasons and subjected to statistical analysis following standard procedure[29].Analysis of variance of the data was calculated and the significance of the factors(environment and nutrient management)was tested at P=0.05.Least significant differences(at P=0.05) among treatment means were calculated for evaluation of treatment effects.

3.Results

The performances of the rice production system under different environments with varying nutrient management as recorded through crop growth,yield,and nutrient use efficiency in the wet and dry seasons separately and the changes in soil chemical properties after harvest of each crop season in the field experimentation are presented as follows.

3.1.Wet season

3.1.1.Environmentalparameters

Variation in key environmentalparameters([CO2]content and temperature)inside OTCs and outside(open field),was recorded at 1-min intervals during the crop growing period in the wet seasons of 2011 and 2012.As averaged over the crop growing period,the[CO2]values were 390,402,and 491μmol L-1in the open field,ambient OTC,and elevated [CO2]OTC,respectively during the year 2011.The[CO2]values of the corresponding environments during 2012 were 384,401, and 501μmol L-1.The average daily air temperatures in the open field were 28.4°C during 2011 and 29.5°C during 2012. The average air temperatures of ambient and elevated[CO2] environments in the OTC were 29.4°C and 30.3°C,respectively,in 2011 and 31.3°C and 32.0°C in 2012.As averaged over the crop growing period,an increased[CO2]content of 92μmol L-1with a corresponding rise in temperature of 0.8°C was recorded in the OTC with elevated[CO2],compared to the ambient OTC.

3.1.2.Growth

The growth parameters recorded,such as maximum tiller production at panicle initiation stage,leaf area and root weight at flowering,and aboveground biomass at maturity are given in Table 2.The crop grown in the open-field environment produced the most tillers(349 per m2),LAI(5.2),root weight(861 kg ha-1),and aboveground biomass at flowering (8985 kg ha-1),and harvest(12,267 kg ha-1)followed by theelevated[CO2]and ambient environments in the OTC.The ambient and elevated[CO2]environments in the OTC gave comparable tiller and aboveground biomass production values,but these were significantly lower than the open field values.The increasing[CO2]in OTC increased the root weight significantly.Among the nutrient management treatments, CF125 showed significantly higher tiller production than the other treatments.The treatments with the recommended dose of nutrients,CF100,CF50+OF50,CF50+OF50+CT,and SA85+FA15,had comparable tiller production.Treatment CF125 gave the highest aboveground biomass(11,503 kg ha-1) and root biomass(762 kg ha-1),which were comparable with those of CF100,but significantly higher than those of the other nutrient management treatments.The recommended dose of nutrients through integrated sources(CF50+OF50 and CF50+OF50+CT)gave significantly lower aboveground biomass and root biomass than only CF(CF100).LAI was not influenced by the varying environments and nutrient management.

Table 2–Tiller production,leaf area index(LAI),root biomass at flowering,and aboveground biomass of rice grown with different nutrient management and environments in the open field and inside OTC as ambient and elevated[CO2]during the wet season at Kharagpur,India.

3.1.3.Yield attributes and yield

The rice crop grown in the open-field environment produced significantly higher number of panicles per m2,filled grain percentage,harvest index,1000-grain weight,grain yield,andstraw yield than that grown in the OTC environment(Table 3). Increasing[CO2]in the OTC increased panicle number by 6%, but decreased filled grain number per panicle by 5%and grain yield by 6%.However,the elevated[CO2]and ambient environments in the OTC had comparable effects on yield attributes and grain and straw yield of rice.The effect of nutrient management was not significant for panicle number, filled grain percentage,or 1000-grain weight of rice.Increasing levels of nutrients via CF(CF125)resulted in a significant increase in grain and straw yield of rice as compared to the normal recommendation as CF100 and the other nutrient management regimes.The recommended doses of integrated nutrient management treatments(CF50+OF50 and CF50+OF50+CT)were comparable to CF100 with respect to grain yield production,but gave significantly lower straw yield.The interaction effect of environment and nutrient management was not significant for the yield attributes and yield.The interaction effect of year,environment,and nutrient management was not significant for grain yield(Table 4).

Table 3–Yield attributes,strawyield,N uptake,and N use efficiency for grain production(NUEg)of rice grown with different nutrient managements and environments in the open field and inside OTCs as ambient and elevated[CO2]during the wet season at Kharagpur,India.

3.1.4.Nitrogen uptake and use efficiency

The crop grown under open field had significantly higher grain yield and total N uptake than that in the OTC environment(Table 3).In OTC,the[CO2]elevation resulted in lower grain N uptake,but the values were not significantly different.Among the nutrient management treatments,the treatment with an increased nutrient dose(CF125)resulted in significantly higher grain Nuptake than the treatments with a recommended dose,CF(CF100)and the combinations of CF and OF(CF50+OF50 and CF50+OF50+CT).Increasing[CO2] in OTC and varying nutrient management had no significant influence on total N uptake of rice.A significantly higher NUEg was noted in the open field than in the ambient environment or elevated[CO2]in OTC.The increasing[CO2] in OTC resulted in a nonsignificant lower NUEg compared to that of the ambient environment(Table 3).The varying nutrient management had no significant influence on NHI, PE,and NUEg.

Table 4–Grain yield(kg ha-1)of rice grown with different nutrient managements and environments in the open field and inside OTC as ambient and elevated[CO2]during the wet season in 2011 and 2012 at Kharagpur,India.

3.2.Dry season

3.2.1.Environmental parameters

Averaged over the crop growing period,the[CO2]values were 389,397,and 496μmol L-1in the open field,ambient OTC,and elevated[CO2]OTC environment,respectively,during 2012. During 2013,[CO2]values for the corresponding environments were 388,397,and 499μmol L-1.The average daily air temperatures during crop growing period for open field, ambient OTC,and elevated[CO2]OTC were 27.7,28.7,and 29.7°C,respectively,in 2012 and 28.4,29.4,and 30.2°Cin 2013. Averaged over the crop growing period,an increased[CO2] content of 101μmol L-1with a corresponding rise in temperature of 0.9°C was observed in the OTC with elevated[CO2]as compared to the ambient environment.

3.2.2.Growth

The growth parameters recorded,such as maximum tiller production at panicle initiation stage,leaf area and root weight at flowering,and aboveground biomass at maturity, are given in Table 5.The crop grown in the elevated[CO2] environment had the most tillers(295 per m2)and the highest LAI(4.5).Aboveground biomass at flowering(8553 kg ha-1) and at harvest(11,626 kg ha-1)was followed by those in the ambient environment in OTCs and open field.However for all these growth parameters,the ambient and elevated [CO2]environments were comparable,whereas root weight was significantly increased under elevated[CO2]environment compared to the ambient environment.Among the nutrient management treatments,CF125 and CF100 were comparable and significantly superior to the recommended dose of integrated nutrient management(CF50+OF50, CF50+OF50+CT)in increasing these growth parameters of rice.

3.2.3.Yield attributes and yield

The crop grown in the open-field environment had significantly lower number of panicles per m2,filled grain percentage,1000-grain weight,harvest index,grain yield,and strawyield than those in the OTC environment(Table 6).Increasing [CO2]in OTC marginally decreased yield attributes and grain and straw yield of rice.The effect of nutrient management was significant for filled grains per panicle and grain yield production.Increasing the level of nutrients through CF (CF125)led to a significant increase in filled grain number and grain yield.The recommended dose of nutrients as CF100 and SA85+FA15 gave comparable grain yields,significantly greater than those under integrated nutrient management (CF50+OF50 and CF50+OF50+CT).The interaction effect of environment and nutrient management was not significant for the yield attributes and yield.The interaction effect of year,environment,and nutrient management was not significant for grain yield(Table 7).

Table 5–Tiller production,leaf area index(LAI),root biomass at flowering,and aboveground biomass of rice grown with different nutrient management and environments as open field and inside OTC as ambient and elevated[CO2]during the dry season at Kharagpur,India.

3.2.4.Nitrogen uptake and use efficiency

The crop grown in the open field had significantly lower grain and total N uptake than that in the OTC environment.In the OTC,the elevated[CO2]and ambient environments gave comparable N uptake(Table 6).The increasing nutrient dose(CF125)did not increase the grain and total N uptake significantly compared to CF100.Among the recommended

Table 6–Yield attributes,strawyield,N uptake,and N use efficiency for grain production(NUEg)of rice grown with different nutrient management and environments in open field and inside OTC with ambient and elevated[CO2]during the dry season at Kharagpur,India.

Table 7–Grain yield(kg ha-1)of rice grown with different nutrient management and environments in open field and inside OTC with ambient and elevated[CO2]during the dry season in 2012 and 2013 at Kharagpur,India.

CF,chemicalfertilizer;OF,organic fertilizer;CT,conservation technology;SA,soilapplication of CF as N and full P and K;FA,Foliage application of CF as N.The values represent percentage of nutrient application through respective sources,especially N,P and K in CF and Nin OF,SA,and FA.SEm,standard error of mean;LSD,least significant difference;NS,not significant. nutrient management treatments,CF100 and SA85+FA15 were comparable and both gave significantly higher grain and total N uptake than the integrated nutrient management treatments(CF50+OF50 and CF50+OF50+CT).The varying environments and nutrient management had no significant influence on NHI,PE,and NUEg.

3.3.Soilchemicalproperties

Changes in chemical properties of soil under varying environments due to application of chemical and organic fertilizer sources,analyzed at harvest of wet and dry season crops in both years,are shown in Figs.1 and 2, respectively.

3.3.1.Organic carbon

In the wet seasons,higher organic carbon was observed with integrated nutrients than with CF alone.The effect of environmental variation on soil organic carbon content was not significant.However,the organic carbon content was marginally increased under elevated[CO2]compared to the ambient environment in the OTC.The organic carbon contentof soilanalyzed after harvest of the dry season crop followed a pattern similar to that of the wet season.

Fig.1–Organic carbon and available N,P,and K contents of soil at harvest of rice grown with different nutrient management and environments in open field and inside OTC with ambient and elevated[CO2]during the wet season of 2011 and 2012 at Kharagpur,India.

Fig.2–Organic carbon and available N,P,and K contents of soil at harvest of rice grown with different nutrient management and environments in open field and inside OTC with ambient and elevated[CO2]during the dry season of 2012 and 2013 at Kharagpur,India.

3.3.2.Available nitrogen

The elevated[CO2]gave lower available N content than the ambient environment in the OTC during both wet and dry seasons.The available N contents under the treatments CF50+OF50,CF50+OF50+CT,and SA85+FA15 were significantly lower than that under the treatment with a higher nutrient dose(CF125)in the first wet season.However in the second wet season,all the nutrient management treatments gave comparable available N content.Similarly in the dry season,the available Ncontents under nutrient management treatments of chemical or integrated sources with similar N dose were not significantly different.

3.3.3.Available phosphorus

Among the environments,the open field showed the highest available P in all the wet and dry seasons.It was not significantly different from that under elevated[CO2],but significantly higher than that under the ambient environment in the OTC.As compared to the ambient environment, elevated[CO2]in the OTC increased the soil available P content by 8%and 16%in the first and second wet seasons and by 26%and 18%in the first and second dry seasons, respectively.The effect of varying nutrient management on soilavailable P content was not significant in either the wet or dry season of either year.

3.3.4.Available potassium

In general,the open field gave lower available K content than the OTC environment.In the OTC,the elevated[CO2]and ambient environments gave comparable available K content. The available K content was not influenced by varying nutrient management in the wet or dry seasons.

4.Discussion

4.1.Effect of elevated[CO2]with nutrient management on rice crop performance

In our experiment,the aboveground biomass at harvest of the crop grown under elevated[CO2](≈490μmol L-1)increased by 10%in the wet season and 6%in dry season compared to that under ambient[CO2](≈390μmol L-1)in the OTC.The increase in aboveground biomass under elevated[CO2]was due to increasing LAI and tiller production in both seasons.The increased biomass accumulation due to[CO2]elevation was at a maximum at the initial period of crop growth,declining as the crop progressed towards maturity.The aboveground biomass was increased by up to 13%at active tillering,7%at panicle initiation and 9%at flowering of the crop under[CO2] elevation during the wet season.The increase in biomass during the dry season was up to 23%at active tillering,18%at panicle initiation,and 11%at flowering of the crop.The observed higher response of biomass to elevated[CO2]early in the growing season may have been due to higher N uptake with greater root development under elevated[CO2]environment[30].A higher increase in aboveground biomass due to [CO2]enrichment during the early than during the later growth period has been reported[31].Some studies have concluded that the positive effect of elevated[CO2]on plant biomass declined from tillering towards maturity[7,32,42].De Costa et al.[33]reported that rice plants grown under elevated [CO2](570μmol L-1)accumulated biomass faster than thosegrown under ambient[CO2]environment during the vegetative and grain-filling stages.Increased biomass under elevated[CO2]is due to increased rate of photosynthesis and net assimilation capacity by promotion of carboxylation and inhibition of oxygenation of ribulose-1,5-bisphosphate carboxylase[2].Similar findings have been reported by many researchers[34-36].

The rice root system is a vital organ for water and nutrient acquisition,and root number and activity affect the growth of aerial parts and economic yield.The consensus is that photosynthesis and C allocation to plant roots increase as atmospheric[CO2]rises,leading to an increase in root weight [37].Our results indicated increasing root weight with elevated[CO2]in the OTC experiment.The increase in root weight of the crop grown under elevated[CO2](≈490μmol L-1) was 15-16%in wet seasons and 36-48%in dry seasons as compared to the ambient[CO2](≈390μmol L-1)in the OTC. Kimball et al.[5]reported an increase of 47%in root biomass in response to elevated[CO2]under sufficient mineral nutrition and water condition.Other researchers have also reported increasing root weight under elevated[CO2][38].

Rice yield is determined by panicle number per unit area, filled grains per panicle,filled grain percentage,and individual grain weight.The productive tiller number as panicle number appears after tiller degeneration during the reproductive stage.In general,growth and yield of rice are expected to increase with[CO2]elevation,but high temperature has a negative effect.In our experiment,the elevated[CO2] decreased filled grain number per panicle by 5%to 6%in the wet season and 2%in the dry season,though they were not significantly different.In contrast,the 1000-grain weight of rice grain was decreased markedly under elevated[CO2] compared to that under the ambient environment in the OTC during the wet season.

The increasing frequency and intensity of high temperature(＞33°C)pose a serious threat to agricultural production, especially in cereals such as rice[39].The threat is highest when high temperatures coincide with anthesis[40]and the grain-filling period[41].The average day time temperatures of 28.1 to 30.4°C in the wet season and 33.7 to 34.3°C in the dry season in the elevated[CO2]environment,in contrast to the corresponding ambient temperatures of 27.3 to 29.6°C in the wet and 32.6 to 33.5°C in the dry season during the grain filling phase,resulted in poor grain filling rate and reduced grain yield during the wet as well as the dry season,though they were not significantly different.Researchers have reported that elevated[CO2]alone increased yields mainly because of the more tiller productions[8,42].High temperature induced spikelet sterility[43,44],thereby reducing grain yield.The rising temperature nullifies the positive effect of increased[CO2]concentration on grain yield.There are a variety of rice responses to increasing temperature that limit the yield response to increased[CO2].Even just a 1°C increase in temperature could result in a large yield decrease,owing to the lower number of grains being formed[45].Matsui and Omasa[46]reported that high temperature at anthesis inhibits swelling of the pollen grains and induces spikelet sterility,thereby decreasing rice yield.

Nitrogen fertilizer is an essential plant nutrient and key input for increasing crop growth and yield[47,48].The higher nutrient application(CF125)increased the aboveground biomass by 4-12%and grain yield by 9-18%as compared to a recommended dose(CF100).This response was due to increases in tiller production,LAI,and yield attributes (panicles per m2,filled grains per panicle)with an increasing nutrient dose in both seasons.Higher nutrient application in tropical rice soil could enhance dry matter accumulation and distribution under elevated[CO2][32].Photosynthetic rates increased at high[CO2]and high nitrogen,possibly leading to better translocation of source to sink,hence enhanced grain yield of rice[49].The treatments with similar N application level through CF(CF100 and SA85+FA15)and though integrated nutrients(CF50+OF50 and CF50+OF50+CT) gave comparable grain yields during the wet season.This response was due to comparable growth(biomass,LAI,and tiller production),yield attributes(panicle number,filled grain number,and grain weight)and yield among these nutrient management treatments.In contrast,in the dry season,the treatments with CF alone gave significantly higher grain yield production than the integrated nutrient management treatments.Temperature,as a main regulator of microbial processes,affects the rate of organic matter mineralization in integrated nutrient management[50].Increasing the temperature can increase organic matter solubility[51]and affect the activity of extracellular enzymes that convert large organic matter molecules to forms that can be assimilated by microbial biomass[52].In our experiment,the air temperatures at the time of organic fertilizer application were 29.9°C and 19.3°C in the wet and dry seasons,respectively.The lower air temperature at the time of organic fertilizer application in the dry season may have reduced the mineralization process,thereby lowering the availability of nutrients to crops in the vegetative stages and reducing the biomass and yield under integrated nutrient management.In the wet season,the grain yield in 2011 was lower than that in 2012. Temperature and solar radiation are the main climatic factors affecting rice growth and yield.The higher maximum air temperature during the grain filling period in 2011 possibly resulted in higher spikelet sterility,leading to a lower number of filled grains and lower yield than in 2012.Solar radiation activates the photosystem so that the light reaction of photosynthesis starts and electrons generated by photolysis of water move to produce energy carriers such as NADPH and ATP for biomass accumulation and grain yield formation. There was a negative relationship between grain yield and temperature and a positive relationship between grain yield and radiation.The difference in grain yield between open field and ambient was higher in the wet season than in the dry season.The lower grain yield in the ambient environment during the wet season was due to lower solar radiation during the grain-filling phase.

Total crop N uptake in elevated[CO2]was marginally, though not significantly,higher than in the ambient environment.An OTC study[34]and a Free Air Carbon dioxide Enrichment(ACE)study[32]found that the total amount of N uptake was similar for elevated and ambient[CO2]crops by the end of the experiments(at flowering or at maturity).FACE experiments performed in China and Japan found that elevated[CO2]decreased the N concentration and increased the N absorption by rice plants at normal and high levels of Napplication[53,54].Both effects result from a dilution effect caused by enhanced accumulation of carbohydrates[55]. In general,the NHI,PE,and NUEg were not significantly influenced by the change in environment and nutrient management.

4.2.Effect of elevated[CO2]with nutrient management on soil chemicalproperties

In our experiment,soil organic carbon under elevated[CO2] was marginally higher than that in the ambient environment during both the seasons.Further,the treatment with integrated nutrient management gave marginally higher organic carbon content than the treatments with CF alone.Studies have reported increasing soil organic carbon content with [CO2]elevation[56]and integration of organic and inorganic sources of nutrients[57,58]in tropical and subtropical climates.Elevated[CO2]can increase soil organic C content mainly by increasing production and allocation of photosynthate to the rhizosphere and thus increasing C input into the soil[59].Some studies found that elevated[CO2]concentration tended to increase plant photosynthesis rate and biomass accumulation and in turn increased rhizodeposition and influenced rhizospheric C dynamics[30].Studies have shown that balanced application of chemical fertilizers or organic manure plus chemical fertilizers can increase soil organic carbon(SOC)and maintain soil productivity[60].In our experiment,incorporation of green manure and application of FYM supplied additional C in soil,with the integrated nutrient management resulting in higher SOC than with only CF.The low organic carbon content in soil observed under CF treatments was due mostly to rapid mineralization and absence of formation of organo-mineral complexes[24]. There was a consistent decrease in soil available N in the elevated[CO2]environment as compared to the ambient environment.The increased C input under elevated[CO2] caused an increase in soil microbial use of N[56],possibly decreasing the available N.Studies have shown that temperature elevation promotes soil microbial activity,whereas [CO2]elevation enhances microbial N-utilization rate in soil [61].Moreover,the availability of additional photosynthate enables most plants to grow faster under elevated[CO2]with higher dry matter production[62,55]and increased uptake of nutrients from soil,resulting in depletion of nutrients in soils with location exchange capacity such as ours,a red lateritic soil that needs a continued supply of external nutrients for maintenance of high production.

Soilavailable P increased consistently in the elevated[CO2] environment compared to the ambient environment in both seasons.There are mechanisms by which increased[CO2] leads to increased soil P mineralization and thereby its availability.In a rice/wheat FACE experiment in China [63,64],higher root biomass and exudates under elevated [CO2]enhanced the availability of soil P.P is linked by ester bonds to soil organic matter,and may be made available by the action of phosphatase secreted by roots,mycorrhizae, and bacteria.Exudation of acid phosphatase enzyme by roots may constitute a very small portion of the total C lost to the root,but that part is extremely important for releasing P from phosphate esters in soil organic matter for plant use, particularly in P-limited environments[65,66].In the present study,increased root biomass of 15%and 48%in the wet and dry seasons,respectively,in the elevated[CO2]environment may have increased phosphatase activity in the rhizosphere and thereby soil extractable P.The available K content of soil was not influenced significantly by[CO2]elevation.

5.Conclusions

We studied the effect of elevated[CO2]on growth and yield of promising cultivars grown during wet and dry seasons in subtropical India.Growth parameters of rice were favored,but grain yield was adversely affected by increased[CO2]level (25%higher than ambient)in an OTC experiment,though they were statistically not significantly different in the wet and dry seasons.Compared to CF alone with recommended doses of nutrients,the effects of integrated nutrient management on growth and yield of rice were not significantly different during wet season,but significantly lower during the dry season. Further increasing nutrient dose(by 25%)via CF increased the rice grain yield significantly in both seasons.[CO2]elevation in the OTC led to marginal increases in organic carbon and available P content of soil,but decreased available N content at harvest of both wet and dry season crops.This result suggests that rising[CO2]level(97μmol L-1)and air temperature(0.85°C)will have no strong influence on growth and yield of rice crop and changes in soil fertility in both wet and dry seasons in subtropical India.However,the trend of marginal decreases in crop yield and soil available N content may become alarming if suitable adaptations are not introduced.Higher nutrient doses by integration of organic and chemical sources in the wet season and chemical sources alone in the dry season should be applied to meet the crop N requirement for increasing rice production in subtropical India under climate change scenarios.

Acknowledgments

National Agricultural Innovation Project,Indian Council of Agricultural Research New Delhiis gratefully acknowledged for providing a financial grant(NAIP/COMP-4/C-30023/2008-09, Dated 06-01-2009)for execution of the research project.

R E F E R E N C E S

[1]Y.Kang,S.Khan,X.Ma,Climate change impacts on crop yield,crop water productivity and food security-a review, Prog.Nat.Sci.19(2009)665-1674.

[2]S.P.Long,E.A.Ainsworth,A.D.B.Leakey,J.N?sberger,D.R.Ort, Food for thought:lower-than-expected crop yield stimulation with rising CO2concentrations,Science 312(2006)1918-1921.

[3]E.A.Ainsworth,Rice production in a changing climate:a meta-analysis of responses to elevated carbon dioxide and elevated ozone concentrations,Glob.Chang.Biol.14(2008) 1642-1650.

[4]L.M.Jablonski,X.Wang,P.S.Curtis,Plant reproduction under elevated CO2conditions:a meta-analysis of reports on 79 crop and wild species,New Phytol.156(2002)9-26.

[5]B.A.Kimball,K.Kobayashi,M.Bindi,Responses of agricultural crops to free-air CO2enrichment,Adv.Agron.77 (2002)293-386.

[6]L.X.Yang,J.Y.Huang,H.J.Yang,G.C.Dong,G.Liu,J.G.Zhu, Y.L.Wang,Seasonal changes in the effects of free-air CO2enrichment(FACE)on dry matter production and distribution of rice(Oryza sativa L.),Field Crops Res.98(2006)12-19.

[7]H.Sasaki,T.Hara,S.Ito,N.Uehara,H.Y.Kim,M.Lieffering,M. Okada,K.Kobayashi,Effect of free-air CO2enrichment on the storage ofcarbohydrate fixed at differentstages in rice(Oryza sativa L.),Field Crops Res.100(2007)24-31.

[8]J.T.Baker,L.H.Allen Jr.,K.J.Boote,N.B.Pickering,Assessment of rice response to global climate change:CO2and temperature,in:G.W.Koch,H.A.Mooney(Eds.),Carbon Dioxide and Terrestrial Ecosystems,Academic Press,San Diego,USA 1996,pp.265-282.

[9]M.A.Razzaque,M.M.Haque,Q.A.Khaliq,A.R.M.Soliman,A. Hamid,Effects of CO2and nitrogen levels on yield and yield attributes of rice cultivars,Bangl.J.Agric.Res.36(2011) 213-221.

[10]P.Madan,S.V.K.Jagadish,P.Q.Craufurd,M.Fitzgerald,T. Lafarge,T.R.Wheeler,Effect of elevated CO2and high temperature on seed-set and grain quality of rice,J.Exp.Bot. 63(2012)3843-3852.

[11]P.Krishnan,D.K.Swain,B.C.Bhaskar,S.K.Nayak,R.N.Dash, Impact of elevated CO2and temperature on rice yield and methods of adaptations as evaluated by crop simulation studies,Agric.Ecosyst.Environ.122(2007)233-242.

[12]Y.Masutomi,K.Takahashi,H.Harasawa,Y.Matsuoka, Impact assessment of climate change on rice production in Asia in comprehensive consideration of process/parameter uncertainty in general circulation models,Agric.Ecosyst. Environ.131(2009)281-291.

[13]A.R.Mohammed,L.Tarpley,High night time temperatures affect rice productivity through altered pollen germination and spikelet fertility,Agric.For.Meteorol.149(2009)999-1008.

[14]K.P.Hogan,A.P.Smith,L.H.Ziska,Potential effects of elevated CO2and changes in temperature on tropical plants, Plant Cell Environ.14(1991)763-778.

[15]J.T.Baker,L.H.Allen Jr.,K.J.Boote,Temperature effects on rice at elevated CO2concentration,J.Exp.Bot.43(1992)959-964.

[16]T.Satake,S.Yoshida,High temperature-induced sterility in indica rices at flowering,Jpn.J.Crop Sci.47(1978)6-17.

[17]R.Lal,Soilcarbon sequestration in China through agricultural intensification,and restoration of degraded and desertified ecosystems,Land Degrad.Dev.13(2002)469-478.

[18]FAO(Food and Agriculture Organization of the United Nations),Electronic online database,Online at http://faostat. fao.org/site/567/desktopdefault.aspx#ancor.

[19]Md.F.Ahmad,S.Haseen,The performance of India's food grains production:a pre and post reform assessment,Int.J. Sci.Res.Publ.2(2012)1-15.

[20]M.L.Parry,C.Rosenzweig,A.Iglesias,M.Livermore,G.Fisher, Assessing the effects of climate change on global food production under socio-economic scenarios,Glob.Environ. Chang.14(2004)53-67.

[21]M.Sanderson,J.Intsiful,J.Lowe,V.Pope,F.Smith,R.Jones, Effects of Climate Change in the Developing Countries,Met Office Hadley-Centre report,UK,2006.

[22]N.Stern,The Economics of Climate Change-The Stern Review,Cambridge University Press,London,2006.

[23]T.M.Thyagarajan,R.Sivasamy,M.N.Budhar,Procedure for collecting plant samples at different growth stages of transplanted rice crop,in:T.M.Thiyagarajan,H.F.M.Ten Berge,M.C.S.Wopereis(Eds.),Nitrogen Management Studies in Irrigated Rice,International Rice Research Institute,Los Banos,Philippines 1995,pp.99-102.

[24]T.Yoshida,B.C.Padre Jr.,Effect of organic matter application and water regimes on the transformation of fertilizer nitrogen in a Philippine soil,J.Soil Sci.Plant Nutr.21(1975) 281-292.

[25]M.L.Jackson,Soil Chemical Analysis,Prentice Hall of India, Pvt.Ltd,New Delhi,1973.

[26]R.H.Moll,E.J.Kamprath,W.A.Jackson,Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization,Agron.J.74(1982)562-564.

[27]D.K.Swain,B.C.Bhaskar,P.Krishman,K.S.Rao,S.K.Nayak, R.N.Dash,Variation in yield,Nuptake and N use efficiency of medium and late duration rice varieties,J.Agric.Sci.144 (2006)69-83.

[28]B.V.Subbaiah,G.L.Asija,A rapid procedure for estimation of available nitrogen in soil,Curr.Sci.25(1956)259-260.

[29]K.A.Gomez,A.A.Gomez,Statistical Procedures for Agricultural Research,2nd edition,John Wiley and Sons,UK, 1984 680.

[30]H.Y.Kim,M.Lieffering,S.Miura,K.Kobayashi,M.Okada, Growth and nitrogen uptake of CO2enriched rice under field conditions,New Phytol.150(2001)223-229.

[31]D.S.Jitla,G.S.Rogers,S.P.Seneweera,A.S.Basra,R.I. Oldfield,P.Jann,J.P.Conroy,Accelerated early growth of rice at elevated CO2,Is it related to developmentalchanges in the shootapex?Plant Physiol.11 (1997)15-22.

[32]H.Y.Kim,M.Lieffering,K.Kobayashi,M.Okada,M.W. Mitchell,M.Gumpertz,Effects offree-air CO2enrichment and nitrogen supply on the yield of temperate paddy rice crops, Field Crops Res.83(2003)261-270.

[33]W.A.J.M.De Costa,W.M.W.Weerakoon,H.M.L.K.Herath, K.S.P.Amaratunga,R.M.I.Abeywardena,Physiology of yield determination of rice under elevated carbon dioxide at high temperatures in a subhumid tropical climate,Field Crops Res. 96(2006)336-347.

[34]L.H.Ziska,P.A.Manalo,R.A.Ordon,Intraspecific variation in the response of rice(Oryza sativa L.)to increased CO2and temperature:growth and yield response of 17 cultivars,J.Exp. Bot.47(1996)1353-1359.

[35]K.S.Roy,P.Bhattacharyya,S.Neogi,K.S.Rao,T.K.Adhya, Combined effect of elevated CO2and temperature on dry matter production,net assimilation rate,C and N allocations in tropical rice(Oryza sativa L.),Field Crops Res.139(2012) 71-79.

[36]P.Bhattacharyya,K.S.Roy,P.K.Dash,S.Neogi,M.D.Shahid, A.K.Nayak,R.Raja,S.Karthikeyan,D.Balachandar,K.S.Rao, Effect of elevated carbon dioxide and temperature on phosphorus uptake in tropical flooded rice(Oryza sativa L.), Eur.J.Agron.53(2014)28-37.

[37]E.Pendall,S.Bridgham,P.J.Hanson,B.Hungate,D.W. Kicklighter,D.W.Johnson,B.E.Law,Y.Luo,J.P.Megonigal,M. Olsrud,M.G.Ryan,S.Wan,Below-ground process responses to elevated CO2and temperature:a discussion of observations,measurement methods,and models,New Phytol.162(2004)311-322.

[38]C.W.Zhu,W.G.Cheng,H.Sakai,S.Oikawa,R.C.Laza,Y.Usui, T.Hasegawa,Effects of elevated[CO2]on stem and root lodging among rice cultivars,Chin.Sci.Bull.58(2013) 1787-1794.

[39]R.Wassmann,S.V.K.Jagadish,S.Heur,A.Ismail,E.Redona,R. Serraj,R.K.Singh,G.Howell,H.Pathak,K.Sumfleth,Climate change affecting rice production:the physiologicaland agronomic basis for possible adaptation strategies,Adv. Agron.101(2009)59-122.

[40]Z.W.Rang,S.V.K.Jagadish,Q.M.Zhou,P.Q.Craufurd,S. Heuer,Effect of high temperature and water stress on pollen germination and spikelet fertility in rice,Environ.Exp.Bot.70 (2011)58-65.

[41]M.A.Fitzgerald,A.P.Resurreccion,Maintaining the yield of edible rice in a warming world,Funct.Plant Biol.36(2009) 1037-1045.

[42]K.Imai,D.F.Coleman,T.Yanagisawa,Increase of atmospheric partialpressure of carbon dioxide and growth and yield office(Oryza sativa L.),Jpn.J.Crop Sci.54(1985) 413-418.

[43]P.V.V.Prasad,K.J.Boote,L.H.Allen,J.E.Sheehy,J.M.G. Thomas,Species,ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress,Field Crops Res.95(2006)398-411.

[44]S.V.K.Jagadish,P.Q.Craufurd,T.R.Wheeler,High temperature stress and spikelet fertility in rice(Oryza sativa L.),J.Exp.Bot.58(2007)1627-1635.

[45]S.B.Peng,J.L.Huang,J.E.Sheehy,R.C.Laza,R.M.Visperas,X. Zhong,G.S.Centeno,G.S.Khush,K.G.Cassman,Rice yield decline with higher night temperature from globalwarming, Proc.Natl.Acad.Sci.U.S.A.101(2004)9971-9975.

[46]T.Matsui,K.Omasa,Rice(Oryza sativa L.)cultivars tolerant to high temperature at flowering:anther characteristics,Ann. Bot.89(2002)683-687.

[47]M.M.Alam,M.Hassanuzzaman,K.Nahar,Tiller dynamics of three irrigated rice varieties under varying phosphorus levels American-Eurasian,J.Agron.2(2009)89-94.

[48]S.Dastan,M.Siavoshi,D.Zakavi,M.A.Ghanbaria,R.Yadi, D.E.Ghorbannia,A.R.Nasiri,Application of nitrogen and silicon rates on morphological and chemical lodging related characteristics in rice(Oryza sativa L.)north of Iran,J.Agric. Sci.4(2012)1-12.

[49]P.Sarma-Natu,V.Pandurangam,M.C.Ghildiyal, Photosynthetic acclimation and productivity of mungbean cultivars under elevated CO2concentration,J.Agron.Crop Sci.190(2004)81-85.

[50]J.Lloyd,J.A.Taylor,On the temperature dependence of soil respiration,Funct.Ecol.8(1994)315-323.

[51]M.H.Chantigny,D.Curtin,M.H.Beare,L.G.Greenfield, Influence of temperature on water-extractable organic matter and ammonium production in mineralsoils,Soil Sci. Soc.Am.J.74(2010)517-524.

[52]S.D.Allison,M.D.Wallenstein,M.A.Bradford,Soil-carbon response to warming dependent on microbialphysiology, Nat.Geosci.3(2010)336-340.

[53]M.Lieffering,H.Y.Kim,K.Kobayashi,M.Okada,The impact of elevated CO2on the elemental concentrations of field-grown rice grains,Field Crops Res.88(2004)279-286.

[54]L.Yang,H.Liu,Y.Wang,J.Zhu,J.Huang,G.Liu,G.Dong,Y. Wang,Impact of elevated CO2concentration on inter-sub specific hybrid rice cultivar Liangyoupeijiu under fully open-air field conditions,Field Crops Res.112(2009)7-15.

[55]M.A.De Graaff,K.J.Van Groenigen,J.Six,B.Hungate,C.van Kessel,Interactions between plant growth and soil nutrient cycling under elevated CO2:a meta-analysis,Glob.Chang. Biol.12(2006)2077-2091.

[56]P.Bhattacharyya,K.S.Roy,S.Neogi,M.C.Manna,T.K.Adhya, K.S.Rao,A.K.Nayak,Influence of elevated carbon dioxide and temperature on belowground carbon allocation and enzyme activities in tropical flooded soil planted to rice, Environ.Monit.Assess.185(2013)8659-8671.

[57]R.L.Yadav,B.S.Dwivedi,K.Prasad,O.K.Tomar,N.J.Shurpali, P.S.Pandey,Yield trends,and changes in soil organic-C and available NPK in a long-term rice-wheat system under integrated use of manures and fertilizers,Field Crops Res.68 (2000)219-246.

[58]R.Dubey,R.S.Sharma,D.P.Dubey,Effect of organic,inorganic and integrated nutrient management on crop productivity, water productivity and soil properties under various rice-based cropping systems in Madhya Pradesh,India,Int.J. Curr.Microb.Appl.Sci.3(2014)381-389.

[59]Z.Xie,G.Cadisch,G.Edwards,E.M.Baggs,H.Blum,Carbon dynamics in a temperate grassland soilafter 9 years exposure to elevated CO2(Swiss FACE),Soil Biol.Biochem.37 (2005)1387-1395.

[60]W.Gong,X.Y.Yan,J.Y.Wang,T.X.Hu,Y.B.Gong,Long-term manuring and fertilization effects on soilorganic carbon pools under a wheat-maize cropping system in North China Plain,Plant Soil314(2009)67-76.

[61]S.J.Hu,J.S.Wu,K.O.Burkey,M.K.Firestone,Plant and microbial N acquisition under elevated atmospheric CO2in two mesocosm experiments with annual grasses,Glob. Chang.Biol.11(2005)213-223.

[62]E.A.Ainsworth,S.P.Long,What have we learned from 15 years of free air CO2enrichment(FACE)?A meta-analytic review ofthe responses ofphotosynthesis,canopy properties and plant production to rising CO2,New Phytol.165(2005) 351-372.

[63]Z.B.Xie,J.G.Zhu,Y.L.Zhang,H.L.Ma,G.Liu,Y.Han,Q.Zeng, Z.C.Cai,Responses of rice(Oryza sativa)growth and its C,N and P composition to FACE(free-air carbon dioxide enrichment)and N,P fertilization,Chin.J.Appl.Ecol.13(2002) 1223-1230(in Chinese with English abstract).

[64]H.L.Ma,J.G.Zhu,Z.B.Xie,G.Liu,Y.L.Zhang,Q.Zeng,Effects of free-air carbon dioxide enrichment on growth and uptake of nitrogen in winter wheat,Acta Agron.Sin.31(2005) 1634-1639(in Chinese with English abstract).

[65]Z.G.Cardon,Influence ofrhizodeposition under elevated CO2on plant nutrition and soil organic matter,Plant Soil187 (1996)277-288.

[66]D.J.Barrett,A.E.Richardson,R.M.Gifford,Elevated atmospheric CO2concentrations increase wheat root phosphatase activity when growth is limited by phosphorus, Aust.J.Plant Physiol.25(1998)87-93.

10 May 2015

in revised form

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