Fe(III) fertilization mitigating net global warming potential and greenhouse gas intensity in paddy rice-wheat rotation systems in China

Environmental Pollution 164 (2012) 73e80

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Fe(III) fertilization mitigating net global warming potential and greenhouse gas intensity in paddy rice-wheat rotation systems in China Shuwei Liu a, Ling Zhang a, Qiaohui Liu a, b, Jianwen Zou a, * a b

Jiangsu Key Laboratory of Low Carbon Agriculture and GHGs Mitigation, Nanjing Agricultural University, Nanjing 210095, China College of Environmental Science and Engineering, Nanjing University of Information Science & Technology, Nanjing 210044, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 October 2011 Received in revised form 16 January 2012 Accepted 20 January 2012

A complete accounting of net greenhouse gas balance (NGHGB) and greenhouse gas intensity (GHGI) affected by Fe(III) fertilizer application was examined in typical annual paddy rice-winter wheat rotation cropping systems in southeast China. Annual fluxes of soil carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) were measured using static chamber method, and the net ecosystem exchange of CO2 (NEE) was determined by the difference between soil CO2 emissions (RH) and net primary production (NPP). Fe(III) fertilizer application significantly decreased RH without adverse effects on NPP of rice and winter wheat. Fe(III) fertilizer application decreased seasonal CH4 by 27e44%, but increased annual N2O by 65e100%. Overall, Fe(III) fertilizer application decreased the annual NGHGB and GHGI by 35e47% and 30e36%, respectively. High grain yield and low greenhouse gas intensity can be reconciled by Fe(III) fertilizer applied at the local recommendation rate in rice-based cropping systems. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Carbon dioxide Methane Iron fertilizer NEE Nitrous oxide Rice paddy

1. Introduction Atmospheric carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) are most potent long-lived greenhouse gases (GHGs) that have significantly contributed to global warming due to their radiative forcing. Globally, atmospheric concentration of GHGs has increased at an annual growth rate of 0.5% for CO2, 0.6% for CH4 and 0.25% for N2O over the past few decades (IPCC, 2007a). Agriculture contributed 10e12% to the total global anthropogenic emissions of GHGs in 2005, with an estimated emission of 5.1e6.1 Pg CO2equivalents yr
1 (IPCC, 2007b). While agriculture releases significant amount of GHGs to the atmosphere, the global technical mitigation potential from agriculture (excluding fossil fuel offsets from biomass) is also estimated to be as high as 5.5e6.0 Pg CO2equivalents yr
1 by 2030 (Smith et al., 2008). Some agricultural practices have been proposed for targeting a specific greenhouse gas (CH4 or N2O) mitigation or soil organic carbon (SOC) sequestration (Smith et al., 2008). However, there are trade-offs among GHGs in agriculture. For example, soil carbon sequestration benefited from balanced fertilizer inputs may be offset by increased N2O emissions (Six et al., 2004; Sang et al.,

* Corresponding author. E-mail address: [email protected] (J. Zou). 0269-7491/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2012.01.029

2011). Shifting from continuous waterlogging to midseason drainage leads to a trade-off between CH4 and N2O fluxes in rice paddies (Cai et al., 1997, 1999; Yagi et al., 1997; Zheng et al., 2000; Zou et al., 2005a). Soil organic carbon (SOC) sequestration increased with crop residue amendment is accompanied by substantial CH4 emission in rice paddies (Adhya et al., 2000; Cai et al., 2000; Ma et al., 2009). No pronounced N2O fluxes due to waterlogging during the rice season is generally followed by high N2O fluxes from the upland cropping season in an annual riceupland cropping rotation system (Zou et al., 2004a, 2007; Liu et al., 2010). Given trade-offs among GHGs, a complete perspective on the agriculture impacts on radiative forcing is vital to taking effective agriculture management strategy for mitigating climatic impacts (Frolking et al., 2004; Robertson and Grace, 2004; Mosier et al., 2006; Johnson et al., 2007). The net greenhouse gas balance of CO2, CH4 and N2O (NGHGB, CO2-equivalents) in a crop production system, based on the global warming potential (GWP) of which given time horizon (e.g., 100-years in this study), was introduced to assess their climatic impacts (Robertson and Grace, 2004; Mosier et al., 2006). Furthermore, another concept, greenhouse gas intensity (GHGI) relating agricultural practices to NGHGB, was developed to assess climatic impacts of agriculture in terms of per kg of yield (Li et al., 2006; Mosier et al., 2006; Qin et al., 2010). Subsequently, agricultural practices targeting

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S. Liu et al. / Environmental Pollution 164 (2012) 73e80

a specific greenhouse gas mitigation or sequestration are highly needed to be further approved on the full perspective of NGHGB and GHGI. Rice is the primary staple food for nearly 50% of the world’s people, mainly in Asia. China is the second-largest area of rice cultivation in the world, accounting for about 20% of the world’s rice-producing area and 23% of all cultivated land in China (Frolking et al., 2002; Zhang et al., 2011). Rice-based production system is typically characterized by annual paddy rice-upland cropping rotations in China, where paddy rice-growing season is conventionally followed by an upland cropping season (e.g. rice-wheat, rice-rapeseed). These rotation systems account for 60% of the total Chinese rice planting area, and 16% of which is typically dominated by an annual paddy rice-winter wheat rotation in China (Frolking et al., 2002; Liu et al., 2010). Rice paddies are important anthropogenic source of atmospheric CH4. Fe(III) fertilization has been proved to be effectively mitigating CH4 emissions from rice paddies (Jäckel and Schnell, 2000; Furukawa and Inubushi, 2004; Ali et al., 2008; Huang et al., 2009). This suppression is primarily due to both inhabitation of CH4 production and enhancement of CH4 oxidization. However, the enhancement of CH4 oxidization may lead to an increase in soil CO2 emissions, which would offset CH4 emissions decreased by Fe(III) fertilization. Given a trade-off between CH4 and N2O emissions, N2O emissions may be significantly enhanced by Fe(III) fertilization. Indeed, N2O emissions slightly increased by Fe(III) material application have been observed in previous pot and laboratory studies, which deserves to be further confirmed by field in situ measurements (Furukawa and Inubushi, 2004; Huang et al., 2009). Therefore, a complete accounting of annual NGHGB and GHGI as affected by Fe(III) fertilization is important for assessing its mitigation effectiveness and potential (Zou et al., 2004a; Mosier et al., 2006; Johnson et al., 2007; Sang et al., 2011). Here, we presented annual field measurements of CO2, CH4 and N2O fluxes as affected by Fe(III) fertilization in a typical paddy ricewinter wheat rotation cropping system in Southeast China over the 2009e2010 annual cycle. The net ecosystem exchange rate of CO2 (NEE) was determined by the difference between soil heterotrophic respiration (RH) and net primary production (NPP). The objective of this study are to gain an insight into a complete accounting of NGHGB and GHGI as affected by Fe(III) fertilization in paddy ricewinter wheat rotation systems, and thereby to examine whether Fe(III) fertilization is an effective option for mitigating climatic impacts of Chinese paddy rice-winter wheat production system on the perspective of annual NGHGB and GHGI. 2. Materials and methods 2.1. Experimental site A field plot experiment was carried out in a typical paddy rice-winter wheat rotation system on the experimental farm of Nanjing Agricultural University, Nanjing, Jiangsu province, China (31 520 N, 118 500 E). Field plots were established in the 2009e2010 annual paddy rice-winter wheat rotation cycle. In the experimental fields, hydromorphic soil consists of 6% sand (particle size >0.05 mm), 40% silt (0.002e0.05 mm) and 54% clay (<0.002 mm) with an initial pH (H2O) of 6.8 and a low iron level of 15.6 g Fe kg
1. Soil bulk density was 1.12 g cm
3, and soil total N and organic C content were 0.15% and 1.78%, respectively. Climate information was recorded by a weather station established on the experimental field. Precipitation was 520 mm for the 2009 rice season and 545 mm for the non-rice season, annually amounting to precipitation of 1065 mm over the 2009e2010 rotation cycle. The annual mean air temperature was about 16.3  C. Mean air temperature were 22.7  C and 10.9  C during the rice and winter wheat seasons, respectively. 2.2. Field experiments Rice seeds (Oryza sativa L., cv. japonica as Wuxiangjing 14) were sown in a nursery patch on May 30; seedlings were transplanted into fields on July 3 and

harvested on October 31, 2009. We plowed, mixed the surface soil and leveled the ground before rice transplanting. All the field plots were under a typical water regime of flooding-midseason drainage-reflooding-moisture irrigation during the rice-growing season. Specifically, flooding was initiated for one week before rice transplanting and maintained until August 17, and followed by midseason drainage for ten days. Subsequently, all the field plots were re-flooded until September 25, 2009 and followed by maintaining moist soil status but without waterlogging (a dry-wet alteration with intermittent irrigation) until one week before rice harvesting (Fig. 1). After rice was harvested, a short fallow period was followed through November 1 to November 18, 2009. A winter wheat cultivar of Yangmai 158 (Triticum aestivum L.) was planted on November 18, 2009 and harvested on June 2, 2010. The practical fertilization regime in local rice-wheat rotation systems was adopted in this study (Cai et al., 1997; Zheng et al., 2000; Zou et al., 2004a, 2005a,b). In accord with the local conventional fertilizer application methods, urea was broadcasted on the fertilized field plots. The seasonal chemical N fertilizer totaled 250 kg N ha
1 for all the field plots, with a split of 40% of the total as basal fertilizer, 40% at turning-green and 20% at tillering stage for rice (Fig. 1). For each plot, calcium superphosphate used as phosphorus fertilizer and Potassium chloride used as potassium fertilizer were identically applied as the basal fertilizer at the local rate of 300 kg P2O5 ha
1 and 150 kg K2O ha
1 during the rice season, respectively. During the winter wheat season, chemical N input totaled 300 kg N ha
1 with a proportion of 75 kg N ha
1 as compound fertilizer (N:P2O5:K2O ¼ 12%:6%:7%) and 225 kg N ha
1 as urea. Winter wheat and rice crop residues were incorporated at the rate of 2.25 t ha
1 and 4.50 t ha
1 during the rice and winter wheat cropping seasons for all the field plots, respectively. Different Fe(III) fertilizer application rates were designed in the field treatment over the paddy rice-winter wheat rotation cycle. Ferric hydroxide and ferrihydrite selected as the iron fertilizer materials in the form of amorphous granular were amended in the rice and wheat cropping seasons, respectively. The iron fertilizer materials were prepared according to Schwertmann and Cornell (1991) and Zhou et al. (2009a). Average active and free iron concentration was as high as 52e60%. The Fe(III) fertilizer was applied at the rate of 4.0 and 8.0 t ha
1, representing the local recommendation medium (Fe-M) and high (Fe-H) application levels in the ricebased soils of Southeast China, respectively (Zhou et al., 2009a). The plots without Fe(III) fertilizer amendment were setup as the control. For the Fe(III) fertilized plots, Fe(III) fertilizer together with crop residue was incorporated at the soil depth of 10e15 cm one week before rice transplanting or winter wheat sowing. The Fe(III) material and crop residue were mixed mechanically and adequately prior to the incorporation. 2.3. Gas sampling and measurements In each plot, six aluminum flux collars (0.5 m length  0.5 m width  0.15 m height) permanently installed near the installed boardwalks ensured reproducible placement of gas collecting chambers during successive gas emission measurements over the whole annual cycle. The top edge of the collar had a groove (5 cm in depth) for filling with water to seal the rim of the chamber with leveled surface. The three collars containing crop vegetation growth with normal density were used for CH4 and N2O flux measurements, and the other adjacent three inter-row collars without covering crop vegetation growth were setup for soil CO2 flux measurements, referring to soil heterotrophic respiration (RH). The cross-sectional area of the chamber was 0.25 (0.5 m  0.5 m) m2. For CH4 and N2O flux measurements, gas samples were collected from the chambers placed over the vegetation with the rim of the chamber fitted into the groove of the collar. Gas samples were taken once a week except that they were taken once a day during the period of midseason drainage and after precipitation events. Gas samples were taken from local time 0800 to 1000 LST for rice season and 1300 to 1500 LST for wheat season (Zou et al., 2004a, 2005b). The CO2, CH4 and N2O fluxes were determined by the static chamber-GC method (Zheng et al., 2008a; Wang et al., 2010). The mixing ratios of the above three gases were analyzed with a modified gas chromatograph (Agilent 7890) equipped with a flame ionization detector (FID) and an electron capture detector (ECD) (Wang et al., 2010). The procedures for simultaneously measuring CO2, CH4 and N2O fluxes were detailed in our previous studies (Zou et al., 2005a,b). 2.4. Determination of NEE, GWPs and GHGI Net ecosystem exchange of CO2 between agroecosystem and atmosphere (NEE) refers to how much carbon lost or gained for an ecosystem, equivalent to the difference between soil heterotrophic respiration (RH) and NPP. The NPP was determined by the harvested above- and belowground biomass and litterfall over the whole annual cycle. The RH was approximately represented by soil CO2 fluxes from inter-row collars without covering crop growth. In order to assess the net effects of iron (III) fertilization on GHGs mitigation, we calculated the combined NGHGB for each treatment by adding CH4 and N2O emissions to NEE budgets using the IPCC GWP factors of which over the 100-yr time horizon based on the following equation (IPCC, 2007a):

S. Liu et al. / Environmental Pollution 164 (2012) 73e80

75

800

CO2 f lux (mg m-2 h-1)

Control

Fe-M

a

Fe-H

600

400

200

0

40

CH4 f lux (mg m-2 h-1)

b 30

20

10

0

2500

F

D

F

c

M

N2O flux (µ g m-2 h-1)

2000

1500

Fertilization

Fertilization

1000

500

27/ May /10

29/A pr/10

13/ May /10

15/A pr/10

01/A pr/10

18/ Mar/10

04/ Mar/10

18/ Feb/10

21/J an/10

04/ Feb/10

07/J an/10

24/ Dec /09

10/ Dec /09

26/ Nov /09

29/ Oc t /09

12/ Nov /09

15/ Oc t /09

01/ Oc t /09

17/ Sep/09

03/ Sep/09

20/ Aug/09

23/J ul/09

06/ Aug/09

09/J ul/09

0

Date (dd-mm-yy) Fig. 1. Annual fluxes (mean  1SE) of soil CO2, CH4 and N2O in paddy rice-winter wheat rotation systems under Fe(III) fertilizer applied at the different levels. Water regime in rice season: F e flooding; D e midseason drainage; M e moisture irrigation without waterlogging.

NGHGB ¼ NEE þ 25  CH4 þ 298  N2 O

  kg CO2
equivalent ha
1 yr
1

Further, the GHGI is calculated by dividing NGHGB by grain yield (Li et al., 2006; Mosier et al., 2006; Sang et al., 2011): GHGI ¼ NGHGB=grain yield



kg CO2
equivalents kg
1

 grain yr
1 :

2.5. Statistical analyses Differences in seasonal CO2, CH4 and N2O emissions as affected by iron (III) application were examined by one-way analysis of variance (ANOVA). Statistical significance was determined at the 0.05 probability level. Differences in seasonal and annual GHGs, grain yield, NEE, NGHGB, and GHGI among treatments were

further examined by the Tukey’s multiple range tests. All statistical analyses were carried out using JMP version 7.0 (SAS Institute, USA, 2007).

3. Results 3.1. NEE Seasonal pattern of soil CO2 fluxes was similar among the field plots, which was independent of Fe(III) fertilizer application (Fig. 1a). Over the whole annual rotation cycle, soil CO2 emissions were primarily affected by temperature, and thus soil CO2 fluxes were generally greater in the summer season than in the winter

76

S. Liu et al. / Environmental Pollution 164 (2012) 73e80

season. Besides temperature, soil water status was another important factor influencing soil CO2 emissions during the ricegrowing season. High flooding layer (about 10 cm depth) lowered soil CO2 fluxes in the rice early stage, and thereafter midseason field drainage triggered much CO2 emission for all the treatments. Soil CO2 fluxes were maintained at relatively high level due to moisture irrigation without waterlogging in the late stage of rice. Similar seasonal trend of soil CO2 emissions among the field treatments was also observed during the wheat-growing season. Temperature lowered CO2 fluxes during the early period of wheat-growing season. As the temperature ascending, thereafter, soil CO2 emission increased steadily. Fe(III) fertilization slightly or significantly decreased soil total CO2 emissions during the rice-growing season (one-way ANOVA, P ¼ 0.07), the non-rice season (P ¼ 0.02) or over the whole annual rotation (P ¼ 0.03), while the difference in soil CO2 emissions was not significant between the two Fe(III) fertilized treatments (Tukey’s multiple range tests, Table 1). During the ricegrowing season, soil CO2 fluxes averaged 233.2 mg m
2 h
1, 156.1 mg m
2 h
1 and 144.4 mg m
2 h
1 for the control, Fe-M and Fe-H treatments, respectively. Relative to the control, soil CO2 emissions were decreased by 33% and 38% for the Fe-M and Fe-H plots, respectively. During the non-rice season, soil CO2 fluxes averaged 241.7 mg m
2 h
1, amounting to 11.95 t CO2 ha
1 for the control plots. Soil CO2 fluxes were, on average, 188.0 mg m
2 h
1 and 174.2 mg m
2 h
1 for the Fe-M and Fe-H plots, 22% and 28% lower than those from the control plots, respectively. Over the whole annual rotation cycle, soil CO2 emissions totaled 18.66 t CO2 ha
1, 13.79 t CO2 ha
1 and 12.77 t CO2 ha
1 for the control, Fe-M and Fe-H treatments, respectively. Compared with the control, Fe(III) fertilization decreased annual soil CO2 emissions by 26% for the Fe-M plots and 32% for the Fe-H plots. About 33e36% of the annual total soil CO2 emission was contributed by the rice-growing season, and the other 64e67% occurred during the non-rice season. The yield and NPP of rice and wheat were not significantly different among field treatments in this study (Tables 1 and 2). The yields of rice and wheat were, on average, 5e10% and 2e4% greater in the Fe(III) fertilized plots than in the control, respectively. Similarly, Fe(III) fertilizer application increased the NPP of rice and wheat by 8% and 5e12%, respectively. Over the whole annual cycle, atmospheric CO2 assimilated into NPP of the rice and winter wheat crops together totaled 13.6 t C ha
1, 14.6 t C ha
1 and 15.0 t C ha
1 for the control, Fe-M and Fe-H treatments, respectively. Nevertheless, the amount of root exudates was not taken into account in this study, and thus the NPP might have been underestimated. Net ecosystem exchange of CO2 (NEE) was significantly affected by Fe(III) fertilizer application over the whole annual cycle (P < 0.01). The negative net annual NEE suggested that atmospheric CO2 captured into biomass exceeded soil heterotrophic CO2 effluxes over the whole rice-winter wheat cropping season. The lower negative NEE indicated that rice production system sequestrated atmospheric CO2 more efficiently than winter wheat cropping system. Over the whole annual rotation cycle, the NEE was

estimated to be
8.51 t C ha
1,
10.80 t C ha
1 and
11.48 t C ha
1 for the control, Fe-M and Fe-H plots, respectively. Compared with the control, Fe(III) fertilization significantly benefited for ecosystem CO2 sequestration, with 19e21% greater in the rice-growing season and 57e90% greater in the non-rice season. 3.2. CH4 Methane fluxes were pronounced only during the rice-growing season, while no significant emission and/or uptake of CH4 were detected in the wheat-growing season (data not shown, Fig. 1b). Fe(III) fertilization did not change seasonal pattern of CH4 emission, rather mainly varied with water regime in rice paddies. Much CH4 emission was pronounced within two weeks after transplanting (Fig. 1b), which was largely contributed by the organic residues retained from the previous season and the applied crop residues. Thereafter, CH4 emission was dramatically decreased by midseason drainage and then remained at a lower release level (Fig. 1b). Although the seasonal trend of CH4 emission was similar, a considerable difference in seasonal total of CH4 flux was observed among the treatments (Table 1). Compared with the control, Fe(III) fertilization significantly decreased CH4 emissions from rice paddies (P < 0.01). Seasonal CH4 emissions averaged 7.03 mg m
2 h
1 and totaled 202.4 kg ha
1 for the control. Relative to the control, Fe(III) fertilization decreased CH4 by 27% and 44% for the Fe-M and Fe-H plots, respectively (Table 1). There was no significant difference in CH4 emissions between the two Fe(III) fertilization treatments, with an average of 5.16 mg m
2 h
1 and 3.95 mg m
2 h
1 for the Fe-M and Fe-H plots in the rice-growing season, respectively (Table 1). 3.3. N2O Seasonal pattern of N2O flux was primarily dependent on water regime during the rice-growing season and synthetic fertilizer application during the winter wheat season, while it did not vary with Fe(III) fertilization (Fig. 1c). Heavy flooding led to unperceivable N2O emission flux although basal fertilizer applied at the beginning of rice transplanting. Intensive N2O emission happened during the non-waterlogged period of rice-growing season, i.e. the drainage and dryewet alteration periods. The episode of midseason drainage resulted in N2O flux peak during the rice-growing season (Fig. 1c). During the winter wheat-growing season, N2O flux peaks were generally observed after topdressing synthetic fertilizer application. A one-way ANOVA showed that Fe(III) fertilization significantly increased N2O emissions during the rice-growing season (P ¼ 0.02), non-rice season (P < 0.01) or over the whole annual cycle (P < 0.001). Over the whole annual cycle, N2O emissions from the control plots averaged 31.8 mg N2OeN m
2 h
1 during the ricegrowing season and 58.6 mg N2OeN m
2 h
1 during the non-rice season. During the rice-growing season, seasonal N2O fluxes from the Fe-M and Fe-H treatments averaged 51.3 mg N2OeN m
2 h
1 and 75.1 mg N2OeN m
2 h
1, 61% and 136% greater than those

Table 1 Seasonal NEE, CH4 and N2O emissions from paddy rice-winter wheat cropping rotation systems (Mean  SE, n ¼ 3). Treatments

Control Fe-M Fe-H

Rice season

Winter wheat season

RH

NPP (t C ha
1)

NEE

CH4 (kg ha
1)

N2O (kg N2OeN ha
1)

RH

NPP (t C ha
1)

NEE

N2O (kg N2OeN ha
1)

1.83  0.25a 1.23  0.09ab 1.13  0.17b

8.67  0.38a 9.39  0.64a 9.43  0.49a


6.83  0.26a
8.17  0.55b
8.29  0.47b

202.40  13.30a 148.47  9.95b 113.63  10.31b

0.92  0.17b 1.48  0.10ab 2.16  0.32a

3.26  0.19a 2.54  0.18b 2.35  0.15b

4.93  0.14a 5.17  0.20a 5.54  0.37a


1.67  0.11a
2.63  0.10b
3.19  0.19c

2.90  0.01b 4.80  0.45a 5.45  0.16a

Different letters in a single column indicate significant difference between treatments at the 0.05 probability level.

S. Liu et al. / Environmental Pollution 164 (2012) 73e80

77

Table 2 Seasonal and annual NGHGB (t CO2-equalivent ha
1 yr
1), yield (t ha
1) and GHGI (t CO2-equivalent t
1 grain yield yr
1) in the paddy rice-winter wheat cropping rotation system (Mean  SE, n ¼ 3). Treatments

Control Fe-M Fe-H

Rice season

Winter wheat season

Annual

NGHGB

Yield

GHGI

NGHGB

Yield

GHGI

NGHGB

Yield

GHGI


19.6  0.8a
25.5  2.0b
26.5  1.9b

7.28  0.29a 7.65  0.25a 7.97  0.15a


2.70  0.21a
3.34  0.25a
3.34  0.26a


4.8  0.4a
7.4  0.5b
9.1  0.4c

4.86  0.22a 4.94  0.18a 5.03  0.16a


0.99  0.13a
1.51  0.16b
1.82  0.05b


24.3  1.1a
32.9  1.5b
35.7  1.5b

12.14  0.44a 12.59  0.36a 13.01  0.30a


2.02  0.16a
2.62  0.08b
2.75  0.16b

Different letters in a single column indicate significant difference between treatments at the 0.05 probability level.

from the control, respectively. During the non-rice growing season, similarly, seasonal N2O emissions from the Fe-M and Fe-H treatments were 66% and 88% greater than those from the control, with an average flux of 97.2 mg N2OeN m
2 h
1 and 110.2 mg N2OeN m
2 h
1, respectively. Over the whole annual paddy rice-winter wheat rotation cycle, N2O emissions were 65e100% greater in the Fe(III) fertilizer applied plots than in the non-amendment control plots. Relative to the rice-growing season, seasonal mean N2O fluxes during the non-rice growing season were 84%, 89% and 47% higher for the control, Fe-M and Fe-H plots, respectively. 3.4. NGHGB and GHGI The annual NGHGB was negative for all the field treatments, suggesting that net ecosystem production exceeded the CO2equivalents due to annual CH4 and N2O emissions from paddy rice-winter wheat rotation systems (Table 2). Although Fe(III) fertilizer application increased annual N2O emissions, it remarkably decreased CH4 emission and increasingly assimilated atmospheric CO2 into agroecosystems, which led to the significant decease in the annual NGHGB over the 100-year time (P < 0.01, Table 2). Compared with the control, Fe(III) fertilizer application decreased the NGHGB by 30e36% and 55e91% during the rice and non-rice seasons, respectively. Over the whole rotation cycle, the annual NGHGB was decreased by 35e47% due to Fe(III) fertilizer application relative to the control. No significant difference in GHGIs was found between the two Fe(III) fertilization treatments, while the GHGIs were lower for the Fe(III) fertilization plots relative to the control since the NGHGB was significantly decreased by Fe(III) fertilizer application (Table 2). Relative to the control, the Fe(III) fertilizer application decreased GHGIs by 24% and 52e83% during the rice and non-rice seasons, respectively. Over the whole rotation cycle, annual GHGIs were decreased by 30e36% due to the Fe(III) fertilizer application as compared with the control. 4. Discussion 4.1. Effects of Fe(III) fertilization on NEE Net ecosystem exchange of CO2 (NEE) refers to the balance between outputs by heterotrophic oxidation of organic material and C inputs by autotrophic fixation. Similar as previous studies (Lund et al., 1999; Zou et al., 2004b; Mosier et al., 2006; Zheng et al., 2008b; Nishimura et al., 2008), the NEE was determined by the static chamber method in this study, in which soil heterotrophic respiration was roughly represented by soil CO2 fluxes from plots without crop growth involvement. Some previous studies suggested that the NEE determined by the chamber method was comparable to that estimated by the micrometeorological techniques, such as eddy covariance tower (Frolking et al., 1998; Anthoni et al., 2004; Zou et al., 2004b; Zheng et al., 2008b).

The NPP, RH and NEE estimates in this study were generally comparable to those reported in the paddy rice-winter wheat rotation systems in this area (Zou et al., 2004b; Zheng et al., 2008b). In the present study, the RH during rice-growing season was estimated to be 1.83 t C ha
1 for the control, falling within our previous estimates (1.38e2.10 t C ha
1) in the 2001 and 2002 rice seasons (Zou et al., 2004b). The NEE was estimated to be
6.83 t C ha
1 during the rice season and
8.51 t C ha
1 over the entire cycle for the control in this study, close to the results in annual paddy rice-winter wheat rotation systems obtained by Zheng et al. (2008b), showing that the total NEE was estimated to be
7.08 to
7.54 t C ha
1 during the 2001 rice-growing season and
7.91 to
8.46 t C ha
1 over the 2001e2002 annual rotation cycle, and
7.35 to
7.82 t C ha
1 during the 2002 rice-growing season and
9.51 to
10.15 t C ha
1 over the 2002e2003 annual rotation cycle. Basically, the decreases in NEE might be achieved through increasing NPP, decreasing soil CO2 emissions or both. In the present study, the NEE decreased by Fe(III) fertilizer application was achieved mainly through decreasing soil CO2 emissions rather than increasing NPP (Table 1). Over the whole annual rotation cycle, NPP and crop yields of rice and wheat were not significantly affected by Fe(III) fertilizer application, which is in agreement with previous pot and field studies (Jäckel et al., 2005; Fang et al., 2008; Liu et al., 2008; Shao et al., 2008; Fu et al., 2010). A pot experiment study showed that no significant differences in shoot and root biomass of rice were found between the control and iron fertilizer treatments (Liu et al., 2008). Shao et al. (2008) and Fu et al. (2010) reported that plant growth and rice grain yield were not suppressed by the iron fertilizer application. Also, grain yield, harvest index, and iron content of rice grains were not different in the rice paddies with Fe(III) fertilizer application as compared with the control in the Jäckel et al.’s (2005) and Huang et al.’s (2009) rice paddy studies. Nevertheless, excessive Fe(III) material inputs may display adverse impacts on crop growth and grain yield, particularly in the iron abundant soils (Benckiser et al., 1984). When Fe(III) material was incorporated into soil, soil CO2 emissions were significantly decreased over the whole annual rotation cycle, suggesting that Fe(III) fertilizer application might have suppressed soil carbon mineralization in this study. Soil carbon mineralization suppressed by Fe(III) fertilizer application was also found in some pot and laboratory studies (Jäckel and Schnell, 2000; Furukawa and Inubushi, 2002; Qu et al., 2005; Zhou et al., 2009a), revealing the important controls of chemical stabilization (e.g. Fe oxyhydrates) on SOC sequestration (Olk et al., 2006; Jastrow et al., 2007; Bierke et al., 2008; Zhou et al., 2009a,b). Indeed, chemical protection by Fe oxyhydrates on newly accumulated C has been well documented to facilitate soil C sequestration and stabilization (Jastrow, 1996; Torn et al., 1997; Spaccini et al., 2001; Osher et al., 2003). Some studies showed the positive correlation of SOC with Fe oxyhydrates, supporting that accumulation of SOC in the paddy soils was closely associated

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with the steady binding of SOC with Fe oxyhydrates (Kiem and Kögel-Knabner, 2002; Wiseman and Puttmann, 2005; Zhou et al., 2009a,b). 4.2. Effects of Fe(III) fertilization on CH4 Fe(III) fertilizer application has been widely approved as an effective option for CH4 suppression in rice paddies. In the present study, Fe(III) fertilizer application decreased seasonal CH4 emissions by 27e44% during the rice-growing season, comparable to the results of previous field and pot studies. The results of a field plot experiment showed that seasonal total CH4 emissions during the vegetation period of rice were 50% lower in the Fe(III) fertilized plot than in the non-supplemented control plot (Jäckel et al., 2005). Similar results were also found in outdoor pot experiments, showing that Fe(III) fertilizer application relative to the control decreased seasonal CH4 emissions by 43e84% (Jäckel and Schnell, 2000), 25e50% (Furukawa and Inubushi, 2004), or 26e69% (Huang et al., 2009). The suppression effect of methanogenesis by Fe(III) fertilizer amendment was consider as a principal reason for lower CH4 emissions (Jugsujinda and Patrick, 1996; Achtnich et al., 1995a,b; Roy and Conrad, 1999; Jäckel and Schnell, 2000; Furukawa and Inubushi, 2004; Ali et al., 2008; Huang et al., 2009). When rice paddies are flooded, CH4 production is a microbial process where a series of sequential reduction processes are initiated (Ponnamperuma, 1981; Watanabe, 1984). In these reduction processes, the electron acceptors are ordered by their redox potential, and substrate is possibly utilized at lower concentrations by electron acceptors with a higher redox potential (Cord-Ruwisch et al., 1988; Lovley and Phillips, 1988). It is well documented that ferric-iron reducing bacteria have lower threshold concentrations for the utilization of H2 and acetate than do methanogens, revealing that microbial Fe(III) reduction is an energetically more competitive electron accepting process than methanogenesis (Wang et al., 1993; Frenzel et al., 1999; Yao et al., 1999). On the other hand, CH4 emissions decreased by Fe(III) application might also be attributed to the enhancement of CH4 oxidation (Furukawa and Inubushi, 2002; Jäckel et al., 2005; Smemo and Yavitt, 2011). Some studies showed that Fe(III) is mechanistically linked to anaerobic oxidization of methane in wetlands since Fe(III) could serve as the electron acceptor for anaerobic oxidization of methane under anaerobic environments (Zehnder and Brock, 1980; Miura et al., 1992; Daniel et al., 1999; Murase and Kimura, 1994; Beal et al., 2009). 4.3. Effects of Fe(III) fertilization on N2O While Fe(III) fertilizer application significantly suppressed soil CO2 and CH4 emissions, soil N2O emissions were facilitated by Fe(III) fertilizer application during the rice and non-rice seasons. Over the whole annual paddy rice-winter wheat rotation cycle, N2O emissions were 65e100% greater in the Fe(III) fertilizer applied plots than in the non-amendment control plots, which confirmed the findings in previous pot and laboratory studies. In a rice paddy pot study, N2O emissions were increased by 30e95% due to Fe(III) material amendment (Furukawa and Inubushi, 2004). Previous laboratory and pot studies also found that soil N2O emissions were facilitated by Fe(III) fertilizer amendment in Huang et al. (2009). A trade-off between CH4 and N2O emissions due to agricultural practices has been well documented in rice paddies (Cai et al., 1997, 1999; Yagi et al., 1997; Zou et al., 2004a, 2005a). In the present study, Fe(III) fertilizer amendment decreased CH4 while increased N2O emissions from rice paddies, suggesting a trade-off between them as well (Furukawa and Inubushi, 2004; Huang et al., 2009).

Several explanations may be given for higher N2O emissions due to Fe(III) fertilizer amendment. First, lower N2O emission may be in part attributed to a toxic effect of Fe(III) material on enzymatic activity in soil nitrification and denitrification processes, in which N2O is produced (Brons et al., 1991; Furukawa and Inubushi, 2004; Huang et al., 2009). Second, Fe(III) fertilizer amendment has impacts on soil pH and Eh that are two factors important to N2O emissions (Frenzel et al., 1999; Furukawa and Inubushi, 2004). Given that Fe(III) lowered soil C decomposition, in addition, Fe(III) fertilizer would alleviate immobilization of fertilizer N accompanying the decomposition of incorporated crop residue with high C/N ratio, and thereby making more mineral N available to nitrification and denitrification (Zou et al., 2004a, 2005a; Qu et al., 2005). Finally, Fe(III) may interact with other heavy metals (e.g. Al, Cd), and these heavy metals functioning together would be involved in soil nitrification and denitrification processes (Qu et al., 2005; Huang et al., 2009). 4.4. Effects of Fe(III) fertilization on NGHGB and GHGI The negative annual NGHGB for all the field treatments in this study is contrary to the positive GWP (analogous to NGHGB) in some previous field and model studies for rice paddies, which was based on the accounting of annual changes in SOC and CH4 and N2O emissions (Li et al., 2006; Sang et al., 2011). Clearly, the divergent results of GWP/NGHGB are due to the ecosystem C balance estimate methods (West and Marland, 2002; Mosier et al., 2006; Johnson et al., 2007; Wang et al., 2011). In the present study, the NEE referred to the difference between the soil CO2 emissions and NPP. In our previous study on double rice paddies under long-term fertilizer experiment, in contrast, the CO2 balance was estimated by the annual changes in SOC, referring to the net ecosystem carbon balance (NECB) since atmospheric CO2 captured into crop biomass removed from the fields and other C losses were not considered (Sang et al., 2011). Shifts from the net sinks to the sources for GWP due to the differential C balance estimate methods (NEE vs. NECB) were also reported in irrigated cropping systems in Northeastern Colorado (Mosier et al., 2005, 2006; Johnson et al., 2007). The Ecological Society of America defined C sequestration as long-term storage (ESA, 2000), although the term “sequestration” may sometimes refer to short-term removal of CO2 from the atmosphere as well (Johnson et al., 2007). In this perspective, agricultural ecosystem C sequestration estimates should be strictly based on the NECB, while considering NEE as a major component (Chapin et al., 2006; Zheng et al., 2008b). The NECB represents the net rate of organic C accumulation in (or loss from) an ecosystem, including inorganic C fluxes that contribute to or derive from organic C plus inputs and outputs of organic C. In order to increase agricultural ecosystems C sequestration, therefore, crop biomass is increasingly retained in the fields in China (Zhang et al., 2011). Also, much crop biomass is currently used to produce bio-energy and black carbon material (Zhang et al., 2010). These parts of carbon would be considered into the C sequestration calculations when upscaling from the landscape to the region (Baker and Griffis, 2005; Johnson et al., 2007). Compared with the control, Fe(III) fertilizer application decreased NGHGB and GHGI without adverse effects on grain yields of rice and wheat. Based on the results of grain yield, NGHGB and GHGI, Fe(III) fertilizer application would be employed to simultaneously achieve grain yield and mitigating climatic impacts of paddy rice-winter wheat rotation cropping system. Nevertheless, the annual NGHGB and GHGI were not significantly different between the Fe-M and F-H treatments. In order to avoid possible adverse effects on grain yield due to Fe(III) material amended at high rates, therefore, Fe(III) fertilizer would be applied at the local

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recommended rate in the annual paddy rice-winter wheat rotation system. 5. Conclusion A complete perspective of the agriculture impacts on radiative forcing is vital to taking effective agriculture management strategy for mitigating climatic impacts. This study provided an insight into a complete accounting of annual NGHGB and GHGI as affected by Fe(III) fertilizer application in typical annual paddy rice-winter wheat rotation cropping systems. Fe(III) fertilizer application significantly decreased soil CO2 emissions without adverse effects on NPP of rice and winter wheat, and thus atmospheric CO2 captured into cropping systems were significantly increased by Fe(III) fertilizer amendments. Total CH4 emissions were significantly suppressed by Fe(III) fertilizer application during the ricegrowing season although it increased N2O emissions over the whole annual paddy rice-winter wheat rotation cycle. Fe(III) fertilizer application remarkably decreased the annual NGHGB, largely due to decreases in CH4 and soil CO2 emissions. The NGHGB and GHGI were lower for the Fe(III) fertilizer applied plots relative to the non-amendment control plots. No significant differences in NGHGB and GHGI were found between the two Fe(III) fertilizer applied treatments. Therefore, Fe(III) fertilizer applied at the local recommendation rate would be an effective option to simultaneously achieving high grain yield and low greenhouse gas intensity in Chinese rice paddies. Acknowledgments This work was supported by the National Basic Research Program of China (2012CB417102, 2009CB118608), the National Natural Science Foundation of China (NSFC, 40971140, 41171194), the NCET-08-0798 and PADA. References Achtnich, C., Bak, F., Conrad, R., 1995a. Competition for electron donors among nitrate reducers, ferric iron redures, sulfate reducers, and methanogens in anoxic paddy soil. Biology and Fertility of Soils 19, 65e72. Achtnich, C., Schuhmann, A., Wind, T., Conrad, R., 1995b. Role of interspecies H2 transfer to sulfate and ferric iron-reducing bacteria in acetate consumption in anoxic paddy soil. FEMS Microbiology Ecology 16, 61e70. Adhya, T.K., Bharati, K., Mohanty, S.R., Ramakrishnan, B., Rao, V.R., Sethunathan, N., Wassmann, R., 2000. Methane emission from rice fields at Cuttack, India. Nutrient Cycling in Agroecosystems 58, 95e105. Ali, M.A., Lee, C.H., Kim, P.J., 2008. Effect of silicate fertilizer on reducing methane emission during rice cultivation. Biology and Fertility of Soils 44, 597e604. Anthoni, P.M., Freibauer, A., Kolle, O., Schulze, E.D., 2004. Winter wheat carbon exchange in Thuringia, Germany. Agricultural and Forest Meteorology 121, 55e67. Baker, J.M., Griffis, T.J., 2005. Examining strategies to improve the carbon balance of corn/soybean agriculture using eddy covariance and mass balance techniques. Agricultural and Forest Meteorology 128, 163e177. Beal, E.J., House, C.H., Orphan, V.J., 2009. Manganese- and iron-dependent marine methane oxidation. Science 325, 184e187. Benckiser, G., Ottow, J.C.G., Watanabe, I., Santiago, S., 1984. The mechanism of excessive iron-uptake (iron toxicity) of wetland rice. Journal of Plant Nutrition 7, 177e185. Bierke, A., Kaiser, K., Guggenberger, G., 2008. Crop residue management effects on organic matter in paddy soils-The lignin component. Geoderma 146, 48e57. Brons, H.J., Hagen, W.R., Zehnder, A.J.B., 1991. Ferrous Fe dependent nitric-oxide production in NO
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