Effect of elevated tropospheric ozone on methane and nitrous oxide emission from rice soil in north India

Agriculture, Ecosystems and Environment 144 (2011) 21–28

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Effect of elevated tropospheric ozone on methane and nitrous oxide emission from rice soil in north India A. Bhatia ∗ , A. Ghosh, V. Kumar, R. Tomer, S.D. Singh, H. Pathak Division of Environmental Sciences, Indian Agricultural Research Institute, New Delhi 110012, India

a r t i c l e

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Article history: Received 31 January 2011 Received in revised form 5 July 2011 Accepted 7 July 2011 Available online 20 September 2011 Keywords: Greenhouse gas emission Elevated ozone Charcoal filtration Rice yield Non-filtered air Global warming potential

a b s t r a c t Physiological changes in crop plants in response to the elevated tropospheric ozone (O3 ) may alter N and C cycles in soil. This may also affect the atmosphere–biosphere exchange of radiatively important greenhouse gases (GHGs), e.g. methane (CH4 ) and nitrous oxide (N2 O) from soil. A study was carried out during July to November of 2007 and 2008 in the experimental farm of Indian Agricultural Research Institute, New Delhi to assess the effects of elevated tropospheric ozone on methane and nitrous oxide emissions from rice (Oryza sativa L.) soil. Rice crop was grown in open top chambers (OTC) under elevated ozone (EO), non-filtered air (NF), charcoal filtered air (CF) and ambient air (AA). Seasonal mean concentrations of O3 were 4.3 ± 0.9, 26.2 ± 1.9, 59.1 ± 4.2 and 27.5 ± 2.3 ppb during year 2007 and 5.9 ± 1.1, 37.2 ± 2.5, 69.7 ± 3.9 and 39.2 ± 1.8 ppb during year 2008 for treatments CF, NF, EO and AA, respectively. Cumulative seasonal CH4 emission reduced by 29.7% and 40.4% under the elevated ozone (EO) compared to the nonfiltered air (NF), whereas the emission increased by 21.5% and 16.7% in the charcoal filtered air (CF) in 2007 and 2008, respectively. Cumulative seasonal emission of N2 O ranged from 47.8 mg m−2 in elevated ozone to 54.6 mg m−2 in charcoal filtered air in 2007 and from 46.4 to 62.1 mg m−2 in 2008. Elevated ozone reduced grain yield by 11.3% and 12.4% in 2007 and 2008, respectively. Global warming potential (GWP) per unit of rice yield was the least under elevated ozone levels. Dissolved organic C content of soil was lowest under the elevated ozone treatment. Decrease in availability of substrate i.e., dissolved organic C under elevated ozone resulted in a decline in GHG emissions. Filtration of ozone from ambient air increased grain yield and growth parameters of rice and emission of GHGs. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Since the industrial revolution anthropogenic activity has increased the concentration of tropospheric ozone (O3 ) (Vingarzan, 2004), which is an air pollutant and a greenhouse gas (GHG). Global mean values of tropospheric ozone have increased from an estimated pre-industrial level of 38 ppbV (US EPA, 1996) to about 60 ppbV during mid-summer with even greater local concentrations in nearly one-quarter of the earth’s surface (Morgan et al., 2006). Formation of ozone in the troposphere depends on solar energy level received at earth surface and higher concentrations

Abbreviations: O3 , ozone; CH4 , methane; N2 O, nitrous oxide; EO, elevated ozone; CF, charcoal filtered air; NF, non-filtered air; AA, ambient air; OTC, open-top chambers; GHG, greenhouse gas; DAT, days after transplanting; AOT40, accumulated exposure over a threshold of 40 ppbV; FID, flame ionization detector; ECD, electron capture detector; TTC, triphenyl tetrazolium chloride; GWP, global warming potential; ppb, parts per billion; DOC, dissolved organic carbon; SOC, soil organic carbon; NH4 + –N, ammonical nitrogen; NO3 − –N, nitrate nitrogen. ∗ Corresponding author. Tel.: +91 11 25841490; fax: +91 11 25841866. E-mail addresses: [email protected], [email protected] (A. Bhatia). 0167-8809/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2011.07.003

occur from May to September in the afternoon in the northern hemisphere (Stockwell et al., 1997). Elevated ozone is known to decrease net photosynthesis via oxidative damage to cell membranes, chloroplasts (Karberg et al., 2005) and consequently reduces dry matter production (Feng et al., 2007). Physiological changes in roots in response to elevated ozone can lead to significant alterations in below ground soil processes, nutrient cycling and microbial activities (Andersen, 2003). The ozone pollution is reported to have a substantial effect on agricultural production in North America, Western Europe (Wang et al., 2005) and Asia (Wahid, 2006). Cereals are highly sensitive and have shown decreased yields with increasing O3 levels. There may be tremendous losses of crop yields in India also due to rising O3 concentration in the troposphere (Rai and Agrawal, 2008; Singh et al., 2010). With increasing levels of tropospheric ozone there might be changes in the C and N cycles in soils (Islam et al., 2000; Larson et al., 2002) affecting emissions of GHGs such as methane (CH4 ) and nitrous oxide (N2 O). There is limited knowledge on the effect of tropospheric ozone levels on the emission of GHGs from rice (Oryza sativa L.) soils which are considered to be one of the major sources of GHGs. The objectives of the study were to (a) assess the impact of

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A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

Table 1 Mean seasonal O3 , SO2 and NO2 concentrations and AOT 40 (accumulated exposure over a threshold of 40 ppbV of ozone) values in different ozone treatments. Treatment

Seasonal mean O3 (ppb)

AOT 40 (ppmV h)

Seasonal mean SO2 (ppb)

Seasonal mean NO2 (ppb)

2007

2007

2008

2007

2007

3.54 ± 0.43 3.3 ± 0.2 0 14.1 ± 1.3

4.1 ± 0.32 3.8 ± 0.31 0 19.2 ± 1.8

17 18 2.5 19

Ambient air (AA) Non-filtered air (NF) Charcoal filtered air (CF) Elevated ozone (EO)

27.5 26.2 4.3 59.1

2008 ± ± ± ±

2.3 1.9 0.9 4.2

39.2 37.2 5.9 69.7

± ± ± ±

1.8 2.5 1.1 3.9

± ± ± ±

2008 2.2 1.1 1.5 1.8

22 21 3.2 20

± ± ± ±

1.8 2.2 2.6 1.4

28 29 4.7 27

± ± ± ±

2008 3.2 3.1 3.0 2.5

34.5 ± 1.5 33.5 ± 2.6 5.01 ± 2.2 31.5 ± 3.8

± refers to standard deviation within replicate OTCs.

tropospheric ozone on the emissions of methane and nitrous oxide from soils in rice and (b) quantify the effect of increased ozone concentration on growth and yield of rice. 2. Materials and methods 2.1. Experimental site and soil A field experiment was conducted growing rice in kharif (July to October) during 2007 and 2008 in the research farm of Indian Agricultural Research Institute (IARI), New Delhi, situated at 28◦ 40 N and 77◦ 12 E, at an altitude of 228 m above mean sea level. The climate of Delhi is continental type and is characterized by important annual variation in temperature, the summers are very hot and winters are cold. Average rainfall of this area is 75 cm annually, approximately 80% of which occurs during kharif season. The mean maximum and minimum temperatures from July to October are 35 and 18 ◦ C. The alluvial soil of experimental site was silty clay loam (Typic Ustochrept) with bulk density of 1.38 g cm−3 , pH (1:2 soil:water) of 8.8, electrical conductivity of 0.43 dS m−1 , cation exchange capacity of 7.3 C mol (p+ ) kg−1 ; and organic carbon, total N, Olsen P, and ammonium acetate extractable K contents of 3.5 g kg−1 , 0.32 g kg−1 , 0.009 g kg−1 , and 0.12 g kg−1 , respectively.

temperature with a constantan-copper thermocouple and relative humidity was measured using a digital humidity sensor at 10.00 and 16.00 h daily. Transplanting of seedlings of a popular Indian rice variety Pusa Sugandh-5 (PS-5) was carried out in 5 replicate crates (size 0.24 m2 ) at 15 cm by 15 cm spacing, in each chamber on 18th July, 2007 and 24th July, 2008. Crops were harvested at maturity on 6th November, 2007 and 13th November, 2008. O3 exposure began on 20th July, 2007 and 25th July, 2008 and ended on 26th October, 2007 and 30th October, 2008 respectively when it was ripe. Charcoal filters adsorbed ozone from ambient air blown inside the OTCs and lowered the ozone concentrations by 80–85% of the ambient air. The non-filtered (NF) treatment was the control treatment and a 5% decrease in concentration than the ambient ozone levels was observed in this treatment. The seasonal ozone concentrations during the experiment period i.e. in the month of July to November 2007 and 2008 are shown in Fig. 1. The peak average concentrations were observed during September and October months. Cumulative ozone exposure above 40 ppb during daylight hours was characterized by the AOT40 index (Fuhrer et al., 1997) and is listed in Table 1. Urea at the rate of 12 g m−2 was added to rice in three splits of 6, 3, and 3 g m−2 at 0, 30 and 60 d after transplanting (DAT). The soil in rice was saturated with water till 82 DAT. Weeds, pests, and diseases were controlled as required.

2.2. Treatments and crop management 2.3. Collection and analysis of gas samples Collection of gas samples for CH4 and N2 O was carried out by the closed-chamber technique (Hutchinson and Mosier, 1981). Chambers of 15 cm × 15 cm × 100 cm (L × B × H) made of 6 mm transparent acrylic sheets were placed over the plants for sampling of CH4 and N2 O. A small rotary fan was fixed in each chamber for mixing of air inside the chamber. Temperature and pressure

Mea n da ily a mbient o zo ne co ncentra tio n (ppb)

120

2008 2007

100

80

60

40

20

0 1/7 5/7 10/7 16/7 21/7 25/7 30/7 4/8 8/8 14/8 19/8 23/8 28/8 2/9 6/9 11/9 16/9 20/9 25/9 30/9 4/10 9/10 15/10 20/10 24/10 29/10 3/11 7/11 13/11 18/11 22/11 27/11

Rice crop was grown in open-top chambers (OTCs) of 3 m diameter and 2.5 m height consisting of a circular aluminum frame covered with transparent film. The experiment was carried out with four treatments arranged in randomized block design with three replications. The treatments were: charcoal filtered air (CF), elevated ozone (EO) and non filtered air (NF) and chamber less ambient control (AA) (Table 1). The OTCs were fitted with an inert PVC pipe of 10 cm diameter (adjustable height) with many small holes which released either charcoal filtered air (CF), non-filtered air (NF) or elevated ozone along with non-filtered air (EO) at the crop canopy level. Air was blown into the OTCs through a fan that provided uniform air speeds. The ventilation rates were kept at 3 air changes per minute to keep the leaf boundary layer resistances down and the chamber temperature close to ambient. In the EO treatment 25–35 ppb of additional ozone was maintained over the non-filtered air levels. O3 was applied for 7 h d−1 for 5 d week−1 (09.30–16.30 h) in the elevated O3 chambers. Additional O3 was generated from oxygen with the help of reaction with UV radiation < 200 nm using ozone generators (Systocom, Varanasi, India). Air was sampled from the middle of each OTC at the crop canopy level and fed to an O3 analyzer (Model APOA-370, Horiba, Germany) for measuring the ozone concentrations daily from 9.30 to 16.30 h. In order to segregate treatment effects from chamber effects, and to reduce the effect of environmental heterogeneity within the chambers, plants were randomized within the chambers, on weekly basis throughout the experiment. The light intensity inside and outside the OTCs was measured using a portable light meter (Metravi 1332),

Date (Day/month)

Fig. 1. Mean daily ambient ozone concentrations during crop growth period in 2007 and 2008.

A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

measurement inside the chambers were made during the sampling of gases. Head space volume inside the chamber was recorded, which was used to calculate flux of CH4 and N2 O. Gas samples were drawn with 50 ml syringe with the help of a hypodermic needle (24 gauge) at 0, 15, and 30 min for CH4 and 0, 30, and 60 min for N2 O. The samples of gases were collected and brought to the laboratory where they were analyzed within two hours. Concentration of CH4 in the gas samples was estimated by gas chromatograph fitted with a flame ionization detector (FID) (Pathak et al., 2003) and N2 O samples were analyzed using electron capture detector (ECD) (Pathak et al., 2002). A GC-computer interface was used to plot and measure the peak area. Methane standards of 2 and 5 ppmV and N2 O standard of 500 ppbV and 1 ppmV obtained from Spectra Gases (NIST standards) were used for calibration. Samples for GHG analysis were collected between 10 and 11 am from each treatment replicate by placing one box per replicate on, 1, 3, 7, 10, 15, 17, 24, 27, 29, 36, 43, 50, 52, 64, 78, 84, 92, 99 and 108 DAT in 2007 and on 1, 3, 6, 9, 11, 15, 19, 24, 28, 31, 36, 44, 50, 54, 61, 68, 75, 82, 89, 96 and 103 DAT in 2008. Estimation of total N2 O and CH4 emissions during the crop season was done by successive linear interpolation of average emission on the sampling days assuming that emission followed a linear trend during the periods when no sample was taken (Pathak et al., 2002). 2.4. Soil sampling and analysis Soil samples from 0 to 15 cm soil layer at 3 locations in each treatment were collected using a core sampler of 8 cm diameter at different stages. The samples were analyzed for soil available N, total N, soil organic carbon, dissolved organic carbon and moisture content. Initial soil samples were analyzed to determine the physico-chemical properties using standard procedures (Page et al., 1982). 2.5. Plant sampling and analysis Plant samples were collected for recording of root dry weight and shoot dry weight at different growth stages. Root activity was measured using the TTC (triphenyl tetrazolium chloride) method (Chen, 2003) and expressed as the deoxidization ability (mg/g/h). Dehydrogenase was expressed as the deoxidized TTC quantity, which was an index of root activity (Chen et al., 2008). To 0.5 g of root sample was added 10 ml solution of equal quantities (0.4%) of TTC and phosphate buffer and kept in the dark for 3 h at 37 ◦ C. The reaction was stopped with 1 M H2 SO4 . The roots were ground and transferred into a tube with ethyl acetate to a total volume of 10 ml. The solution absorbance was read as 485 nm, with a spectrophotometer. Yield related parameters such as number of tillers, number of panicles per hill, number of filled grains per panicle, grain yield, straw yield and harvest index were recorded after the final harvest. The grains were separated from the straw, dried, and weighed. The dry weight was determined by oven-drying at 65 ◦ C to constant weight. 2.6. Global warming potential Global warming potential is an index defined as the cumulative radiative forcing between the present and some chosen later time ‘horizon’ caused by a unit mass of gas emitted now. It is used to compare the effectiveness of each greenhouse gas to trap heat in the atmosphere relative to some standard gas, by convention CO2 . The GWP for N2 O is 298 and GWP for CH4 is 25 when GWP value for CO2 is taken as 1. The GWP of different treatments were calculated using the following equation (IPCC, 2007): GWP = N2 O × 298 + CH4 × 25

23

The GWP/unit of yield was calculated by dividing GWP of a treatment with rice grain yield. 2.7. Data analysis Statistical analysis of the data were done using MSTATC statistical package. Analysis of variance was done to test whether the differences were statistically significant. Unless indicated otherwise, differences were considered only when significant at P < 0.05. 3. Results and discussion Mean hourly ozone concentrations in the CF chambers did not exceed 5 ppb as the charcoal filters removed 80–85% of ambient ozone, sulphur dioxide and nitrogen dioxide from the OTCs. The 7-h concentration of ozone, sulphur dioxide and nitrogen dioxide in non-filtered air during the growing season was 26.2 ± 1.9, 18 ± 1.1 and 29 ± 3.1 ppb in 2007 and 37.2 ± 2.5, 21 ± 2.2 and 33.5± 2.6 ppb in 2008. The 7-h ozone concentration in the EO treatment was 59.1 ± 4.2 and 69.7 ± 3.9 ppb in 2007 and 2008, respectively (Table 1). Levels of sun light on the crop canopy were, on an average, reduced by 11% inside the OTC, whereas mean air temperature inside the chamber was 0.8 ± 0.1 ◦ C higher than that of outside the chambers (Table 2). Relative humidity was 7.2 and 8.1% higher inside the chambers in 2007 and 2008, respectively (Table 2). Ozone concentrations were low during the monsoon season (July and August) in 2007, with mean concentrations of 22.4 ± 0.9 and 16.9 ± 2.7 ppb, respectively in ambient air (Fig. 1). The mean concentrations of ozone increased in ambient air to 44.6 ± 2.1 ppb during September 2007. Ozone concentrations then fell during October and November 2007. Higher concentrations of ozone were observed throughout the kharif season (July to October) in 2008 as compared to the previous year (Fig. 1). In the leaves of rice plants exposed to the EO treatment, the onset of senescence advanced as compared to the NF treatment from 80 DAT to 71 DAT in 2007 and from 82 to 76 DAT in 2008. 3.1. Methane emission from soil under different ozone levels Lower emissions of methane were observed during the initial crop growth period and the methane fluxes were almost same in all the treatments till 24 DAT in both years. Subsequently significant differences in the methane flux were observed and the maximum emission of methane occurred between 36 and 52 DAT in 2007 and between 28 and 54 DAT in 2008 in the different treatments (Fig. 2a). The peak emission of 168.8 mg m−2 d−1 and 159 mg m−2 d−1 was obtained on 43 and 44 DAT in the CF treatment in 2007 and 2008 respectively. This coincided with the maximum tillering stage in rice. The peak CH4 emissions during the growing season may be associated with high growth and root activity of the rice plants that supplied soil bacteria with fresh organic matter via root exudation (Holzapfel-Pschorn and Seiler, 1986; Schütz et al., 1991). The temporal flux of CH4 in the different treatments fluctuated between −13.31 mg m−2 d−1 in the EO treatment and 168.8 mg m−2 d−1 in the CF treatment during the crop growing period in 2007. Similar magnitude of methane fluxes was observed in year 2008 also. Increased shoot and root biomass (Fig. 3a) was observed in the CF over the NF treatment probably due to higher photosynthetic activity (results not shown) in this treatment. More below ground biomass might have resulted in higher amount of root exudates providing substrates for methanogens resulting in increased methane emissions in the CF treatment. There was a decline in root biomass under elevated ozone from 25 to 50 DAT (Fig. 3a). Many O3 -induced reactions, such as repair processes and production of secondary compounds in leaves, cause an increase in C demand, and

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A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

Table 2 Mean monthly microclimatic conditions inside and outside the open top chambers (OTCs) during 2007 and 2008 rice season. Month

7-Jul 7-Aug 7-Sep 7-Oct 7-Nov 8-Jul 8-Aug 8-Sep 8-Oct 8-Nov

Temperature ◦ C

Light intensity (␮mol m−2 s−1 )

Relative humidity (%)

Outside

Inside

Difference

Outside

Inside

Difference

Outside

Inside

Difference

28.7 29.4 28.2 27.3 25.6 29.2 29.7 28.3 27.1 26.2

29.5 30.2 29.1 28.1 26.4 30.1 30.5 29.1 28 27.1

0.8 0.8 0.9 0.8 0.8 0.9 0.8 0.8 0.9 0.9

1267 1250 1257 1274 1246 1272 1261 1276 1291 1250

1128 1109 1119 1141 1119 1130 1120 1133 1148 1122

139 141 138 133 127 142 141 143 143 128

71.6 74.3 69.4 67.8 66.3 70.9 69.4 68.8 67 66.1

76.8 79.7 73.9 72.3 70.5 76.6 75 74.4 72.4 70.2

5.2 5.4 4.5 4.5 4.2 5.7 5.6 5.6 5.4 4.1

Values are monthly average of two daily readings taken at 10.00 and 16.00 h.

thus a reduction in C allocation below-ground (Andersen, 2003). The temporal and spatial distributions of methane production were related to root biomass (Sass et al., 1990) and above ground biomass (Huang et al., 1997). Zheng et al. (2011) attributed reduction in CH4 emission to reduction in underground and above ground biomass. The decline in methane emission under elevated ozone was thus due to the lower availability of substrate for methanogenic bacteria. The amount of methane formed in paddy soils is positively correlated with organic-C, mineralizable N and redox potential of soil (Kimura et al., 1992). No significant change, however was observed in soil organic carbon in any of the treatments in this study, but

Fig. 2. Effect of ozone levels on (a) temporal emission of CH4 from rice soil and (b) temporal emission of N2 O–N from rice soil in 2007 and 2008. *CF – charcoal filtered air; NF – non filtered air; EO – elevated ozone; AA – ambient air.

the dissolved organic carbon content was lower (Fig. 4a) under the EO treatment in both the years. This was probably because of lower carbon allocation to the roots resulting in lower root biomass and lesser amount of root exudates. Reducing root growth upon exposure to elevated O3 has been reported to decrease the amount of root exudates (Edwards et al., 1990). In the current study lower root activity, as measured by dehydrogenase activity, was observed at 25 and 50 DAT (Fig. 3b) under elevated ozone. Negative fluxes of methane emission were observed during the later stage of crop growth in both the years. The aerobic conditions prevailing in soil after 84 DAT led to favorable conditions for the growth of methanotrophs resulting in an uptake of CH4 and thus negative flux of methane were observed on 99 DAT in the CF, NF and AA treatments and from 92 DAT onwards in the EO treatment in 2007. Similar negative fluxes were also observed in 2008 crop season as well. Pathak et al. (2003) also observed negative fluxes of methane on days when soil became aerobic. Cumulative seasonal methane emission was significantly affected by different ozone concentrations. The highest emission (5.31 g m−2 ) was observed in the CF treatment and the lowest (3.07 g m−2 ) in the EO treatment in 2007. In 2008 the highest emission was 4.8 g m−2 in the CF and lowest (2.6 g m−2 ) was in the EO treatment (Table 3). Cumulative methane emission was 29.7% less in the EO than the NF treatment while in the CF treatment methane emission was higher by 21.5% over the NF treatment. Zheng et al. (2011) observed a 38–51% decrease in methane emission under the elevated ozone. Reduced methane emissions have also been observed in peat bogs under higher ozone concentrations (Derwent et al., 2009).Nitrous oxide emission from soil under different ozone levels Nitrous oxide emission ranged from 109 ␮g m−2 d−1 in the EO treatment to 1667 ␮g m−2 d−1 in the CF treatment during the crop growth period in 2007 and from 101 ␮g m−2 d−1 in the EO to 1453 ␮g m−2 d−1 in the CF treatment in 2008 (Fig. 2b). Significant impact of ozone filtration was obtained on the emission of nitrous oxide from soil. The N2 O–N flux during initial crop growth period was influenced by fertilizer N application. First peak flux of nitrous oxide emission varied from 1522 to1667 ␮g m−2 d−1 on 3 DAT in 2007 and from 1336 to 1398 ␮g m−2 d−1 on 5 DAT in 2008 under the different treatments. This coincided with the first dose of fertilizer N application. Subsequently there was a low emission till the next date of fertilizer application. Similar peaks of N2 O–N flux were observed after every dose of N application, which supplied the substrate (NH4 + –N) for nitrification and subsequently substrate (NO3 − –N) for denitrification. Average daily emissions of N2 O–N during the rice crop ranged from 543 ␮g m−2 –d−1 in the EO to 640 ␮g m−2 –d−1 in the CF

A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

root dry weight (g palnt-1)

0.9

(a)

CF

NF

EO

AA

0.8

0.8 0.7

0.7

0.6

0.6 0.5

0.5

0.4

0.4

0.3

0.3

0.2

0.2

0.1

0.1

0

0 25

shoot dry weight (g plant-1)

25

50

5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

80

24 5.5 5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0

2007

25

9

50 Days after transplanting

CF

(b)

24

EO

AA

50 Days after transplanting

78

10 9

8

Root activiity (TPF ppm)

78

2008

80

NF

50

7

2007

6

8

2008

7 6

5

5

4

4

3

3

2

2

1

1 0

0 25

50

24

80

50

78

Days after transplaning

Days after transplaning

Fig. 3. Effect of ozone levels on (a) root and shoot dry weight and (b) rice root activity in 2007 and 2008. *CF – charcoal filtered air; NF – non filtered air; EO – elevated ozone, AA – ambient air.

treatment in 2007. As soil nitrification and denitrification are major pathways of N2 O emissions, decrease in substrate availability (i.e., changes in quantity of root exudates and root biomass) for nitrifying and denitrifying bacteria may have decreased N2 O emissions

under elevated ozone. Lowering in biomass in the EO treatment may have also caused modifications in the mineralization of organic N thereby reducing the availability of soil N and affecting the N cycle (Booker et al., 2005).

Table 3 Effect of ozone on cumulative emission of methane, nitrous oxide and global warming potential of rice soil. Treatments

CH4 emission (g m−2 ) 2007

Charcoal filtered air Elevated ozone Non filtered air Ambient air

5.31 3.07 4.37 3.82

N2 O emission (mg m−2 )

2008 ± ± ± ±

0.43a* 0.32c 0.18b 0.38b

4.9 2.5 4.2 3.7

± ± ± ±

2007 0.20a 0.09c 0.24b 0.41b

85.8 75.1 81.4 79.9

GWP (g CO2 eq. m−2 )

2008 ± ± ± ±

3.5a 1.7c 1.4b 1.9b

97.6 72.9 83.4 84.5

2007 ± ± ± ±

4.6a 2.7c 4.9b 3.6b

158 99 134 119

± ± ± ±

GWP/unit of yield g CO2 eq. g−1 yield

2008 11.8a 8.5c 4.9b 10.1b

± refers to standard deviation within replicate OTCs. * In a column values followed by the same letter are not significantly different at P < 0.05 by Duncan’s multiple range test.

152 84 130 118

± ± ± ±

6.4a 3.1c 7.5b 11.3b

2007

2008

0.25a 0.20b 0.25a 0.23a

0.22a 0.17b 0.23a 0.22a

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A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

Dissolved organic carbon (%)

CF

0.030 0.028 0.026 0.024 0.022 0.020 0.018 0.016 0.014 0.012 0.010 0.008 0.006

NF

EO

(a)

AA

0.030 0.028 0.026 0.024 0.022 0.020 0.018 0.016 0.014 0.012 0.010 0.008 0.006

2007

0

36

69

80

111

2008

0

35

Days after transplanting

(b)

CF

NF

EO

AA

280

2007 Total N (kg ha -1 )

70

85

110

Days after transplanting

320

2008

300

260 280 240

260

240

220

220 200

200 180

180 0

36

69

80

111

Days after transplanting

0

35

70

85

110

Days after transplanting

Fig. 4. Effect of ozone levels on (a) soil dissolved organic carbon and (b) total soil nitrogen in 2007 and 2008. *CF – charcoal filtered air; NF – non filtered air; EO – elevated ozone, AA – ambient air.

Cumulative seasonal emission of N2 O in 2007 ranged from 75.1 mg m−2 in the EO to 85.8 mg m−2 in the CF treatment (Table 3). The cumulative emissions in 2008 were higher than the previous year and increased by 17% in the CF as compared to the NF treatment. Increased C input due to more root biomass under the CF treatment may have increased N availability by enhancing N mineralization (Hungate et al., 1996; Holmes et al., 2003) resulting in higher emission of N2 O–N in the CF treatment. Lower total N in soil was observed under elevated ozone (Fig. 4b) during the crop growth period. Kanerva et al. (2006) observed lower inorganic N content in soil under elevated ozone.

the roots to uptake N from soil resulting in reduced grain and straw yield than that in the CF treatment. Nouchi et al. (1991) observed that O3 exposure at 100 ppbV inhibited NH4 + –N uptake by roots. Besides reduction in root biomass, root activity was significantly reduced under elevated O3 concentration as compared to the CF and NF treatments (Fig. 3b). Reduction in root activity reflected a decline in root function after elevated O3 exposure. Chen et al. (2008) observed decreased rice root activity under the elevated ozone due to less organic matter partitioning to roots.

3.3. Effect of ozone on root biomass and activity

Grain yield of rice ranged from 483 to 637 g m−2 under different levels of ozone in 2007 (Table 4). The presence of higher ozone led to 11.4% and 12.3% decrease in rice yield in 2007 and 2008, respectively. Charcoal filtration of air increased rice yield by 16.9% and 21.8% in 2007 and 2008, respectively. Removal of ozone from ambient air increased rice yield. Wahid et al. (1995) observed reduction of 42% and 37% in the grain yield of two cultivars of rice under higher ozone concentrations. The decline in grain yield was due to decrease in the various yield parameters under elevated ozone (Table 3). The number of tillers decreased by 11.9% in the EO and increased by 22.5% in the CF over the NF treatment, respectively in 2007. Average number of panicles hill−1 was the lowest in the

Elevated ozone had a negative impact on root and shoot biomass of rice crop. Injury to the lower leaves, which acted as the main source of photosynthate, might explain decrease in root and shoot biomass under elevated zone (Andersen, 2003). The decreasing biomass partitioning to roots resulted in a decline (14%) in root/shoot ratio at 50 DAT under elevated ozone. Root dry weight and shoot dry weight ranged from 0.56 to 0.76 g per plant and 3.08 to 4.14 g per plant respectively at 80 DAT (Fig. 3a) in 2007 and from 0.48 to 0.74 g per plant and 2.97 to 5.01 g per plant respectively at 78 DAT in 2008. Lesser root biomass in the EO treatment inhibited

3.4. Effect of ozone on yield

A. Bhatia et al. / Agriculture, Ecosystems and Environment 144 (2011) 21–28

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Table 4 Effect of ozone on yield and yield components of rice. Parameters

Non filtered 2007

No. of filled grains panicle−1 No. of tillers hill−1 1000 grain weight Grain yield (gm−2 ) Straw yield (gm−2 )

144 15.3 21.4 545 1214

Charcoal filtered 2008

± ± ± ± ±

12a* 1.1b 0.7a 20b 35a

148 16 22 567 1196

2007 ± ± ± ± ±

8a 1.3b 1.1a 18b 29a

152 18.7 22.7 637 1330

Elevated ozone 2008

± ± ± ± ±

11a 0.9a 0.4a 25a 39a

155 19.2 23 691 1358

2007 ± ± ± ± ±

16a 1.2a 0.6a 16a 62a

124 13.5 19.2 483 1039

Ambient 2008

± ± ± ± ±

9b 0.6c 0.3b 31c 48b

118 13.9 18.9 497 1072

2007 ± ± ± ± ±

14b 0.9c 0.7b 22c 37b

146 15.1 20.7 528 1199

2008 ± ± ± ± ±

10a 1.3b 0.2a 22b 41a

142 16 21.1 525 1151

± ± ± ± ±

8a 0.8b 0.4a 35b 23a

± standard deviation within replicate OTCs. * In a row values followed by the same letter are not significantly different at P < 0.05 by Duncan’s multiple range test.

EO treatment in both the years. Decreased photosynthates production under the EO resulted in less translocation of carbohydrates to the grains resulting in a decrease in filled grains panicle−1 by 13.8 and 20.2% over the NF treatment in 2007 and 2008, respectively. The filled grains panicle−1 increased upon charcoal filtration of air. This was due to the higher translocation of carbohydrates to sink leading to higher grain filling (Reddy and Reddy, 1989) in the CF treatment. Elevated ozone also decreased the 1000 grain weight of the rice (Table 4). Ariyaphanphitak et al. (2005) reported that Thai Jasmine rice cultivars exposed to elevated O3 suffered a significant reduction in filled seeds per panicle, and grain yield. Thus elevated levels of ozone had a negative impact on grain yield. No significant difference was observed in grain yields in the AA and NF treatments. Straw yield was the highest under charcoal filtration and low under elevated ozone concentrations in both the years (Table 4). Increased C input in the CF treatment could have increased the N availability by enhancing N mineralization (Hungate et al., 1996). Also higher tiller production due to favorable condition in the CF treatment increased the photosynthetic assimilation resulting in enhanced dry matter production.

3.5. Effect of ozone on soil carbon and nitrogen Dissolved organic carbon (DOC), a labile form of carbon, is affected by any short-term change in carbon dynamics. The DOC ranged from 0.008% to 0.023% under different treatment and the minimum was observed under the EO treatment in 2007 (Fig. 4a). The decline in DOC under EO in both the years was probably due to lower root activity. In addition to reducing root growth and activity, exposure to elevated O3 is also known to decrease the amount of root exudates (Edwards et al., 1990; McCool et al., 1983) and the labile C pool. Higher DOC levels were observed in the charcoal filter treatment in 2008 (Fig. 4a). The reduced ozone concentration of ozone in the CF treatment led to an increase in the DOC in soil, probably because of increased root exudation due to higher root carbon allocation as compared to the NF treatment. No significant impact of different ozone levels was observed on soil organic carbon (SOC). Soil organic carbon being a stable parameter was not impacted by short-term changes in soil (Banerjee et al., 2006). Total N in soil decreased significantly under elevated ozone after 69 DAT (Fig. 4b) probably due to reduced carbon allocation below ground which affected the soil carbon and nitrogen mineralization processes. Elevated O3 decreased soil mineral N through a reduction in quantity and quality of plant litter input (Kanerva et al., 2005). A decrease in N availability suggested that O3 stress created a deficiency of available N for the soil microbes and N2 O emissions decreased which are the first signs of a disturbance in the N cycle. Soil N content was the highest under the CF treatment but it was not significantly different from the NF treatment in both the years. More root growth and activity in the CF treatment may have led to a higher uptake of N by the plant. Soil NH4 + –N concentration varied

between 18.91 kg ha−1 to 37.72 kg ha−1 under the different ozone treatments (results not shown). At harvest the NH4 + –N concentration in the CF was higher by 20.93% than the NF treatment in 2007 and was the lowest under the EO treatment. 3.6. Global warming potential (GWP) The GWP ranged from 99 to 158 in 2007 and from 84 to 153 g CO2 eq. m−2 in 2008. The GWP increased by 17.9 and 16.9% in the CF treatment and decreased by 26.1 and 35.4% in the EO treatment over the NF treatment in 2007 and 2008, respectively (Table 3).The GWP per unit of yield was the lowest in the EO treatment at 0.20 and 0.17 gCO2 eq. g−1 yield in 2007 and 2008 respectively. 4. Conclusions Rising O3 in the troposphere is a potential threat to crop production. However, it could also decrease emissions of GHGs from soil. The current study showed that elevated tropospheric ozone altered the plant carbon allocation and decreased emission of methane and nitrous oxide in rice. Comparison of responses of rice plants grown in environments with filtered and non-filtered air showed that the current levels of ozone are impacting the growth, productivity and GHG emission in rice. Rice yields decreased under elevated ozone but the GHG emissions were also lowered resulting in a lowering in GWP per unit of rice yield. Acknowledgements The authors are grateful to the Post Graduate School, Indian Agricultural Research Institute, New Delhi, India and Department of Science and Technology, Government of India, for providing funding during the course of the study. References Andersen, C., 2003. Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol. 157, 213–228. Ariyaphanphitak, W., Chidthaisong, A., Sarobol, E., Bashkin, V., Towprayoon, S., 2005. Effects of elevated ozone concentrations on Thai jasmine rice cultivars (Oryza sativa L.). Water Air Soil Poll. 167, 179–200. Banerjee, B., Aggarwal, P.K., Pathak, H., Singh, A.K., Chaudhary, A., 2006. Dynamics of organic carbon and microbial biomass in alluvial soil with tillage and amendments in rice wheat systems. Environ. Monit. Assess. 119, 173–189. Booker, F.L., Prior, S.A., Torbert, H.A., Fiscus, E.L., Pursley, W.A., Hu, S., 2005. Decomposition of soybean grown under elevated concentrations of CO2 and O3 . Global Change Biol. 11, 685–698. Chen, C.L., 2003. Measurement of plant root activity (TTC). In: Li, H.S. (Ed.), Principle and Technology of Plant Physiological and Biochemical Experiments. Higher Education Press, Beijing, pp. 119–120. Chen, Z., Wang, X., Feng, Z., Zheng, F., Duan, X., Yang, W., 2008. Effect of elevated ozone on growth and yield of field-grown rice in Yangtze River Delta, China. J. Environ. Sci. 20, 320–325. Derwent, R.G., Simmonds, P.G., Manning, A.J., Doherty, S.O., Spain, G., 2009. Methane emissions from peat bogs in the vicinity of the Mace Head Atmospheric Research Station over a 12-year period. Atmos. Environ. 43, 2328–2335. Edwards, N.T., Taylor Jr., G.E., Adams, M.N., Simmons, G.L., Kelly, J.M., 1990. Ozone, acidic rain, and soil magnesiums effects on growth and foliar pigments of Pinus taeda L. Tree Physiol. 6, 95–104.

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