Differences in nitrous oxide fluxes from red soil under different land uses in mid-subtropical China

Agriculture, Ecosystems and Environment 146 (2012) 168–178

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Differences in nitrous oxide fluxes from red soil under different land uses in mid-subtropical China Shan Lin a , Javed Iqbal a , Ronggui Hu a,∗ , Leilei Ruan a , Jinshui Wu b , Jinsong Zhao a , Pengju Wang a a b

College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, PR China Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, PR China

a r t i c l e

i n f o

Article history: Received 21 March 2011 Received in revised form 30 October 2011 Accepted 31 October 2011 Available online 1 December 2011 Keywords: Dissolved organic carbon Microbial biomass carbon Nitrous oxide fluxes Red soil Soil temperature Water-filled pore space

a b s t r a c t Red soil may play an important role in nitrous oxide (N2 O) emissions due to its recent land use change pattern. To predict the land use change effect on N2 O emissions, we examined the relationship between soil N2 O flux and environmental determinants in four different types of land uses in subtropical red soil. During two years of study (January 2005–January 2007), biweekly N2 O fluxes were measured from 09:00 to 11:00 a.m. using static closed chamber method. Objectives were to estimate the seasonal and annual N2 O flux differences from land use change and, reveal the controlling factors of soil N2 O emission by studying the relationship of dissolved organic carbon (DOC), microbial biomass carbon (MBC), water filled pore space (WFPS) and soil temperature with soil N2 O flux. Nitrous oxide fluxes were significantly higher in hot-humid season than in the cool-dry season. Significant differences in soil N2 O fluxes were observed among four land uses; 2.9, 1.9 and 1.7 times increased N2 O emissions were observed after conventional land use conversion from woodland to paddy, orchard and upland, respectively. The mean annual budgets of N2 O emission were 0.71–2.21 kg N2 O-N ha−1 year−1 from four land use types. The differences were partly attributed to increased fertilizer use in agriculture land uses. In all land uses, N2 O fluxes were positively related to soil temperature and DOC accounting for 22–48% and 30–46% of the seasonal N2 O flux variability, respectively. Nitrous oxide fluxes did significantly correlate with WFPS in orchard and upland only. Nitrous oxide fluxes responded positively to MBC in all land use types except orchard which had the lowest WFPS. We conclude that (1) land use conversion from woodland to agriculture land uses leads to increased soil N2 O fluxes, partly due increased fertilizer use, and (2) irrespective of land use, soil N2 O fluxes are under environmental controls, the main variables being soil temperature and DOC, both of which control the supply of nitrification and denitrification substrates. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Nitrous oxide is among one of the important greenhouse gases, which has 296-fold higher greenhouse effect than that of CO2 (IPCC, 2001). There is a growing concern about increasing emissions of N2 O. Nitrous oxide emissions grew by about 50%, due mainly to increased use of fertilizer and the growth of agriculture (IPCC, 2007). The global emission of N2 O was estimated to be 16.2 Tg N year−1 , and the emission from agriculture soils accounted for 24% of total emissions (Mosier et al., 1998; IPCC, 2001). Intensive soil management has therefore led to a considerable increase in the exchange of N2 O between soils and the atmosphere. The primary reasons for enhanced N2 O emissions from agricultural soils are increased N inputs by mineral fertilizers, symbiotic N2 fixation,

∗ Corresponding author. Tel.: +86 27 87282152; fax: +86 27 87396057. E-mail address: [email protected] (R. Hu). 0167-8809/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2011.10.024

organic C and animal waste application (Ruser et al., 2006). With the increasing demand for food supply, cultivated area as well as input of N chemical fertilizers into agricultural ecosystems is expected to further increase. As a result, the emission of N2 O from agriculture may be intensified and its impacts on global climate may become more serious in the future (Zheng et al., 2000). One of the major parameters regulating the emission of N2 O from soils is the land use type (Skiba and Smith, 2000). Relevant aspects of land use include: input of organic or inorganic fertilizers, animal grazing (creating concentrated urea and manure patches), and the ecosystem and plants’ ability to fix molecular N from the atmosphere (Smith, 2005). Land use can affect the biogeochemical and physical controllers of trace gas fluxes, which in turn is hypothesized to influence the populations of soil microbial functional groups relevant to N2 O fluxes. Land use and agricultural practices can result in important contributions to the global source strength of atmospheric N2 O (Scheer et al., 2008). Saggar et al. (2008) showed that fertilized grasslands and pastures typically

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have higher emission rates than forest and most natural ecosystems. However, there is no quantitative data on the emission of N2 O from red soil of different land use types in subtropical China, except for Liu et al. (2008) who studied three greenhouse gases from pine plantation and orchard in a hilly area of South China, and Tang et al. (2006) who did measure CO2 , CH4 , and N2 O fluxes in three subtropical forest ecosystems in southern China. However, seasonal changes of N2 O emissions in subtropical red soil are poorly understood. Since the subtropical climate is characterized typically by wet and dry seasons, seasonal patterns of N2 O emissions are important for better estimation of the emissions, which may be influenced by abiotic and biotic factors including temperature, soil moisture, soil organic C and microbial biomass. Understanding the effect of soil temperature, soil moisture, DOC and MBC on soil N turnover processes and associated N2 O emissions are essential in this region. Red soil, one of the typical agricultural soils in subtropical China (Lou et al., 2003), classified as Ultisols and some of the Alfisols and Oxisols in the soil taxonomy of USA (Zhang and He, 2004), can play an important role in the global soil N balance. This soil covers about 1.13 million km2 or 11.8% of the country land surface, produces 80% of the rice and supports 22.5% of the population (Lou et al., 2003). Injudicious use of red soil resources, particularly deforestation, has caused severe soil erosion, resulting in the degradation of the environment and reduced agricultural production in the red soil regions (He et al., 2001). Red soils are subject to degradation as characterized by low organic C content and low crop productivity. In addition, the red soil region, being the most densely populated, is under great pressure to increase upland area in order to meet an increasing demand for food and fiber (Zhang and He, 2004), which causes severe environmental problem. Recently, some fallow farmlands were left for natural regeneration of secondary forest in the hilly red soil region in the middle and lower reach of the Yangtze River (Zheng et al., 2008). Among the previous studies in red soil region, many investigations have focused on the dynamics of ecosystem C allocation as affected by different forest management practices (Zheng et al., 2008), the impact of land use conversion practices on nutrients (Zhang and He, 2004), and crop production (He et al., 2001). However, few reports on soil N2 O emission have been available in subtropical China. The lack of reliable data in the red soils of these regions has hampered an accurate estimate of the global soil N2 O fluxes. Therefore, it is necessary to investigate soil N2 O fluxes from red soils for better understanding the mechanisms that regulate N balance and emission processes. Different biotic and abiotic predictors control the N2 O emission from the soil (Lin et al., 2010). The DOC accounts for small proportion of the total organic matter in soil. However, it may have a significant influence on soil biological activity, which in turn can affect soil denitrifiers for denitrification (Ullah et al., 2008). Previous studies have also concluded that N2 O fluxes from soils are strongly controlled by different climatic predictors along with soil nutrient status (Lin et al., 2010). And nutrient release and immobilization depends on the microbial dynamics, the quantity and quality of plant residues, on the C cycling and efficient use of the soil microbial community (Baudoin et al., 2003). Soil MBC is the most active component of soil organic C that regulates biogeochemical processes in terrestrial ecosystems (Paul and Clark, 1996), which have been found to show seasonal variation in subtropical agriculture soils (Frazão et al., 2010; Iqbal et al., 2010). The seasonal N2 O emissions coincided with N fertilization, and N inputs may directly and indirectly alter microbial biomass and activity (Wallenstein et al., 2006; Lee et al., 2009). However, separate seasonal effect and association of MBC with soil N2 O emissions is still uncertain and needs to be assessed. In the present study, we measured soil N2 O emissions, temperature, soil moisture, DOC contents, MBC contents and rainfall over a

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2-year period from red soil with four land use types in subtropical China. As the importance of N2 O emission caused by these agricultural systems has largely been ignored, the aims of this study were to: (1) investigate the seasonal dynamics of soil N2 O emissions in different land uses; (2) quantify annual soil N2 O fluxes between disturbed and natural vegetation in mid-subtropical red soils of central China; and (3) examine the effects of soil temperature, soil moisture, DOC and MBC on N2 O emission from different land use types. 2. Methods and materials 2.1. Site description The field experiments were carried out at the experimental station of Heshengqiao, located in Xianning, Hubei Province, Central China (29◦ 53 N, 114◦ 17 E). The selected sites were representative of the regional features of land use in central China. Altitude ranges from 86 to 147 m above sea level. This region has a humid subtropical monsoon climate with an average annual temperature of 16.8 ◦ C and mean annual precipitation of 1577.4 mm. Most of the rainfall occurs between April and September (the hot-humid season), and nearly 20% falls between October and March (the cool-dry season). The mean annual radiation hours are 1856.8 h and mean radiation rate is 43%. Red soil of this area can be classified as Ultisols and some of the Alfisols and Oxisols in the soil taxonomy of USA (Zhang and He, 2004). Soils were clayey, kaolinitic thermic Typic Plinthudults with over 2 m deep profile derived from quaternary red clay, subjected to severe erosion. Four land use types having rapeseed–rice rotation (paddy), peach trees (orchard), pine forest (woodland) and sesame–peanut rotation (upland), were selected for the measurements. Rice had been planted here for more than 500 years, and unique diagnostic horizons of paddy soils have been well developed, which started to have a rotation with rapeseed in 1956, and is maintained until now. Orchard was a wasteland before 1949 when it was planted with bush until 1981. In 1981, orchard was developed with peach trees. Pine forest, which was planted by local people in the 1970s, has slight human disturbance because it is easily accessible by nearby villagers. For upland, land use change occurred to have sesame–peanut rotation in 1981, before which it had maize plantation. Distance among orchard, woodland and upland is about 500 m from each other and these sites are about 3000 m away from paddy. During the growing seasons, each land use was fertilized except woodland. Annual average rate of N, P, K were 280, 59, 187 kg ha−1 , 210, 52, 149 kg ha−1 , 120, 197, 187 kg ha−1 for paddy, orchard, and upland, respectively. In addition to the application of N, P, and K, lime material was occasionally applied to paddy and upland. Paddy and upland were conventionally tilled twice a year while orchard was not tilled and woodland was not even disturbed. Main characteristics of the different land use types are listed in Table 1. 2.2. Experimental design In January 2005, an experiment from four land use types was started to measure N2 O fluxes. In each field, three chambers were installed (each 3–5 m apart) in a triangle form, and N2 O measurements were done every two weeks over the whole experiment (5 January-2005–9 January-2007). To avoid high temperature at noon, all measurements were conducted in the morning 09:00–11:00 (a representative time in this region as described by Lou et al. (2004)). The data in 2 h was used for 14 days average. In total, there were 42 measurements for paddy, orchard, upland and woodland.

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Table 1 Description of selected physico-chemical properties of the soils in different land use types at Heshengqiao. Land use

Paddy

Orchard

Woodland

Upland

Altitude (m) Slope (◦ ) C:N-ratio Organic C (g kg−1 ) Total N (g kg−1 ) pH Bulk density (g cm−3 ) Soil texture Sand (%) Silt (%) Clay (%)

86 Terrace 6.62 ± 0.07a 16.87 ± 0.09a 2.55 ± 0.01a 5.11 ± 0.02ab 1.37 ± 0.02a Sandy loam 59.12 ± 1.50a 34.44 ± 2.81c 6.44 ± 0.45a

135 5–10 4.56 ± 0.05d 6.29 ± 0.09d 1.38 ± 0.01c 5.07 ± 0.01bc 1.24 ± 0.01b Loam 51.32 ± 1.60b 46.64 ± 1.88b 2.04 ± 0.12c

147 5–15 5.32 ± 0.07b 9.95 ± 0.10b 1.87 ± 0.02b 5.02 ± 0.01c 1.36 ± 0.02a Silt loam 18.24 ± 1.74c 79.56 ± 2.91a 2.2 ± 0.26b

130 Terrace 4.91 ± 0.05c 9.33 ± 0.05c 1.90 ± 0.02b 5.15 ± 0.02a 1.23 ± 0.01b Loam 49.01 ± 2.11b 48.63 ± 1.59b 2.36 ± 0.23b

Means in a row followed by the same letter were not significantly different (P < 0.05) by Duncan’s test method. Values are the mean ± SE (standard error).

2.3. Measurement of N2 O fluxes Nitrous oxide fluxes were measured using static closed chamber (Iqbal et al., 2009a,b) and gas chromatography techniques (Wang and Wang, 2003). The closed chamber was made from 8 mm thick stainless steel materials consisting of two parts (Lin et al., 2010). The top edges were rubber-sealed in order to prevent from leakage when the top lid was put on it. Two battery-operated fans inside the stainless steel box homogenized the air in the chamber. A white thermal insulation cover was added outside of the stainless steel cover to reduce the impact of direct radiative heating during sampling. During the experimental period, the chambers were placed on stainless steel frame that had been inserted 5 cm into the soil. Samples were taken with 100 ml plastic syringes attached to a three-way stopcock at 0, 10, 20, 30 min following chamber closure, respectively, and then injected into evacuated bags made of inert aluminum-coated plastic. Nitrous oxide concentrations in the samples were analyzed in the laboratory within 24 h following sampling using a gas chromatograph (HP 6890 Series, GC System, Hewlett Packard, USA). The gas chromatograph was equipped with an electron capture detector for N2 O analysis. Nitrous oxide flux was calculated based on the rate of change in N2 O concentration within the chamber, which was estimated as the slope of linear regression between concentration and time.

2.4. Soil sampling and analysis Ten fresh soil samples (0–20 cm) were taken from each field, at the same time of N2 O flux measurements, mixed and placed in plastic bags after manual removal of visible plant residues and roots. Soil samples were analyzed for soil water content (Ovendrying method), total organic C (dichromate oxidation method), total N (Kjeldahl method), particle size distribution (analyzed with the pipette method using pyrophosphate as a dispersing agent) and pH (1:1 soil water paste) with electrometry (pH electrode). Soil bulk density was determined as described by Iqbal et al. (2008, 2009c). Each measurement was replicated three times. For MBC and DOC determinations, the soil samples were transported on ice in a cooler, to the laboratory, and immediately stored in sealed plastic bags at 4 ◦ C. Prior to analysis, soil samples were sieved through a 2-mm sieve, adjusted to a 40% of water holding capacity, and kept at room temperature for 7 days. Microbial biomass carbon was estimated by the chloroform fumigation–extraction method (Wu et al., 1990), using alcohol free CHCl3 , followed by 0.5 M K2 SO4 extraction of both fumigated and non-fumigated soils. Both the non-fumigated and fumigated soil extracts were filtered through Whatman #40 paper and frozen until analysis of MBC. Microbial biomass carbon was analyzed by a TOC-5000A total organic C analyzer (Shimadzu, Kyoto, Japan),

and estimated using the equation: MBC = 2.22Ec , where Ec is the difference between organic C extracted from the K2 SO4 extracts of fumigated and non-fumigated soils, both expressed as ␮g C g−1 oven dry soil (Wu et al., 1990). Dissolved organic carbon was extracted and analyzed as described by Mulvaney et al. (1997). 2.5. Measurement of other environmental factors Soil temperatures (at depth 0–5 cm) were measured using soil thermometers inserted to a depth of 5 cm inside the chambers. Soil moisture content (0–10 cm) was estimated by the relative water content as the percentage of WFPS. The water mass content of soil (g g−1 ) was determined by gravimetry with oven drying at 105 ◦ C for 24 h. Soil WFPS was calculated based on the equation (Franzluebbers, 1999): WFPS =

SWC × BD 1 − BD/PD

where SWC is the soil water content (g g−1 ), BD is the soil bulk density (g cm−3 ), and PD is the soil particle density. Precipitation and air temperature were also monitored throughout the experimental period. 2.6. Statistical analysis All the statistical analyses were performed by using the SPSS 11.0 package (SPSS, Chicago, IL, USA). The data were subjected to an analysis of variance, and the means and the standard error of the three replicates were calculated. Simple regression procedure was used to evaluate the contribution of soil temperature, WFPS, DOC and MBC to soil N2 O flux. A Duncan’s Multiple Range Test was used to compare the mean soil N2 O fluxes, soil temperature, WFPS, DOC and MBC among the four land use types, accepted the 0.05 probability as significant. Water-filled pore space of 0–10 cm depth was used as the moisture variable in all analyses, as this property integrates porosity and moisture variables (Franzluebbers, 1999). 3. Results 3.1. Rainfall, temperature, soil moisture, DOC and MBC During 2-years-study period, the annual precipitation was significantly lower (1320 mm) than in normal years (1577 mm). The largest monthly precipitation (245.5 mm) occurred in July-2005 (Fig. 1), whereas the smallest monthly precipitation in December-2005 (27.3 mm). Precipitation during the April–September accounted for 75% and 71% of total rainfall in 2005 and 2006, respectively. Annual air temperature was 20.2 ◦ C, with monthly temperature ranging from 6.3 ◦ C to 30.7 ◦ C (Fig. 1).

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Fig. 1. Seasonal variations of precipitation and temperature at Heshengqiao.

Soil temperature depicted clear seasonal variation (Fig. 2C). Soil was warm from April through September 2005 and became cool from October 2005 to March 2006. The seasonality of soil temperature was consistent with the seasonal pattern of air temperature (Figs. 1 and 2C). There were no significant differences in soil temperature among the four land use types. Significant differences in the soil moisture content (expressed as % of WFPS) were found among the four land use types following the order of

paddy > woodland > upland > orchard at P < 0.05 (Fig. 2B, n = 42). Soil in orchard was significantly drier than other three land use types. Soil moisture contents in cool-dry season (October–March) were significantly lower than in hot-humid season (April–September). Soil DOC varied from 11.8 to 272.5 mg C kg−1 (Fig. 3A) in four land use types, and the lowest value was observed at the end of May 2005 in upland. The DOC contents were significantly lower in cool-dry season than in hot-humid season from all land use types.

Fig. 2. Seasonal variation of (A) soil N2 O flux, (B) soil temperature at 5 cm depth and (C) water-filled pore space (% WFPS, 0–10 cm). Values are mean ± SE (standard error) determined in the morning (09:00–11:00 a.m.) on sampling dates.

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Fig. 3. Seasonal variation of (A) DOC and (B) MBC in different land uses. Values are mean ± SE (standard error) determined in the morning (09:00–11:00 a.m.) on sampling dates. Table 2 Seasonal and annual means of N2 O fluxes (␮g N2 O-N m−2 h−1 ) among four land use types. Land use types

Paddy

Orchard

Woodland

Upland

Hot-humid season Cool-dry season Annual mean

30.3 ± 4.2a 18.0 ± 3.1a 24.1 ± 3.7a

22.1 ± 2.1ab 9.1 ± 1.2b 15.6 ± 1.4b

11.6 ± 1.1c 4.7 ± 0.6c 8.2 ± 0.9c

18.8 ± 1.5b 9.8 ± 1.1b 14.3 ± 1.3b

Different letters in a row indicate significant differences (P < 0.05) of N2 O fluxes among land use types.

Highest DOC contents were observed from paddy that had high soil moisture values as compared to other land use types, and the lowest DOC contents were observed from orchard which has lower moisture values (Figs. 2B and 3A). Microbial biomass carbon showed clear seasonal variation during the study period. Microbial biomass carbon peaked in June 2005 when there was maximum air temperature with some intense rainstorms. The lowest level occurred in December 2005 when there was lesser precipitation. Throughout the study period, the highest MBC contents (from 104.5 to 876.5 mg C kg−1 ) were observed from paddy and lowest MBC contents (from 46.1 to 237.3 mg C kg−1 ) were observed from orchard (Fig. 3B).

3.2. Seasonal variations of N2 O fluxes During two years of measurements, soils showed N2 O emission except some negative values in January and December when the lowest temperature and precipitation were observed. Significant differences of N2 O fluxes between hot-humid season and cooldry season were observed in all land use types (Table 2). From all land uses, N2 O fluxes during cool-dry season were significantly reduced compared to hot-humid season. The highest mean N2 O flux (30.3 ± 4.2 ␮g N2 O-N m−2 h−1 ) was found from paddy during

hot-humid season, and the lowest mean N2 O flux (4.7 ± 0.6 ␮g N2 ON m−2 h−1 ) was from woodland in cold-dry season (Table 2). 3.3. Land use effect on N2 O fluxes Soil N2 O fluxes differed among the four land uses following the order of paddy > orchard ∼ upland > woodland (P < 0.05, Fig. 2A and Table 2). Soil N2 O fluxes averaged 24.1 ± 3.7, 15.6 ± 1.4, 14.3 ± 1.3 and 8.2 ± 0.9 (±S.D.; n = 42) ␮g N2 O-N m−2 h−1 from paddy, orchard, upland and woodland, respectively. Nitrous oxide flux was 2.9 times greater in paddy than in woodland and 1.7 times greater in upland than in woodland, while there was no significant difference in N2 O flux between upland and orchard. The cumulative N2 O emission was highest (2.21 kg N2 O-N ha−1 year−1 ) in paddy soil with highest fertilization applied among all four land use types in a period of two years, followed by orchard (1.40 kg N2 ON ha−1 year−1 ) and upland (1.24 kg N2 O-N ha−1 year−1 ), which had received second and the third highest fertilization dosage in the entire study period, respectively. The lowest (0.71 kg N2 ON ha−1 year−1 ) N2 O emissions were observed in woodland that did not receive any fertilizer. 3.4. Relationships between soil N2 O fluxes and environmental factors Nitrous oxide fluxes had strong positive correlation with soil temperature at 5 cm depth in all land uses (P < 0.01, n = 42, Fig. 4). Linear regression between N2 O fluxes and soil temperature explained 22%, 48%, 40% and 34% of the variability, for paddy, orchard, woodland, and upland, respectively (Fig. 4). A significant influence of WFPS on the soil N2 O fluxes was observed for woodland and upland (P < 0.05, n = 42, Fig. 5), while the poor relationship was found for paddy and orchard (P > 0.05, Fig. 5) due to extremely higher and lower WFPS, respectively (Fig. 2B). Nitrous oxide flux had positive linear relationship with DOC among four land use

100 90 80 70 60 50 40 30 20 10 0 -10

A N2O flux (µg m-2 h-1)

N 2O flux (µg m-2 h-1)

S. Lin et al. / Agriculture, Ecosystems and Environment 146 (2012) 168–178

y = 1.4817x - 3.7925 R2 = 0.2186, P=0.002

50

B

40

y = 0.9936x - 3.9194 R2 = 0.4754, P<0.001

30 20 10 0 -10

0

10

20

30

40

0

10

Soil temperature (ºC)

N 2O flux (µg m-2 h-1)

N2O flux (µg m-2 h-1)

60

25 y = 0.5661x - 1.841 R2 = 0.3989, P<0.001

20 15

20

30

40

Soil temperature (ºC)

C

30

10 5 0

D

50

y = 0.7214x + 0.08 R2 = 0.3398, P<0.001

40 30 20 10 0

-5 -10

173

-10 0

10

20

30

40

0

10

Soil temperature (ºC)

20

30

40

Soil temperature (ºC)

100 90 80 70 60 50 40 30 20 10 0 -10

50

A N 2O flux (µg m-2 h-1)

N 2O flux (µg m -2 h -1)

Fig. 4. Relationship between soil N2 O flux and soil temperature at 5 cm depth in different land uses. (A) Paddy, (B) Orchard, (C) Woodland, (D) Upland.

0

50

100

30 20 10 0 -10

150

B

40

0

10

Soil moisture (% WFPS) 60

C

25

y = 0.1492x - 0.7495 R2 = 0.1606, P=0.009

20

N 2O flux (µg m -2 h-1)

N 2O flux (µg m -2 h-1)

30

15 10 5 0 -5 -10

0

50

Soil moisture (% WFPS)

20

30

40

Soil moisture (% WFPS)

100

D

50

y = 0.3179x - 0.6728 R2 = 0.1139, P=0.029

40 30 20 10 0 -10

0

20

40

60

80

Soil moisture (% WFPS)

Fig. 5. Relationship between soil N2 O flux and soil moisture at 0–10 cm depth in different land uses. (A) Paddy, (B) Orchard, (C) Woodland, (D) Upland.

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100 90 80 70 60 50 40 30 20 10 0 -10

A

50 y = 0.2219x - 3.1659 R2 = 0.4193, P<0.001

N 2O flux (µg m-2 h-1)

N 2O flux (µg m-2 h-1)

174

B

40 30 20 10 y = 0.2209x + 0.7005 R2 = 0.3204, P<0.001

0 -10

0

100

200

300

0

50

DOC (mg kg -1) 60

C

25

N 2O flux (µg m -2 h -1)

N 2O flux (µg m-2 h-1)

30

20 15 10 5

y = 0.1097x + 0.4032 R2 = 0.4601, P<0.001

0 -5 -10 0

100

200

100

150

DOC (mg kg -1)

300

DOC (mg kg -1)

D

50

y = 0.0983x + 5.212 R2 = 0.2961, P<0.001

40 30 20 10 0 -10

0

100

200

300

DOC (mg kg -1)

Fig. 6. Relationship between soil N2 O flux and DOC in different land uses. (A) Paddy, (B) Orchard, (C) Woodland, (D) Upland.

types (P < 0.001, Fig. 6). The DOC content accounted for 30–46% of soil N2 O flux variability in four land uses (Fig. 6). Nitrous oxide fluxes correlated significantly with MBC from paddy, woodland and upland (P < 0.01, n = 42, Fig. 7), but not for orchard, since WFPS was lower (<32%) in orchard during study period. 4. Discussion 4.1. Comparison with other studies on soil N2 O fluxes The annual mean N2 O emissions from different land uses in Xianning ranged from 0.71 to 2.21 kg N2 O-N ha−1 year−1 . On average, soils in Xianning released about 1.39 kg N2 O-N ha−1 year−1 (arithmetic average of four sites) into the atmosphere. The annual N2 O emissions observed from pine forest 0.71 kg N2 ON ha−1 year−1 , were within the range of emissions observed from secondary forest site in Xishuangbanna region, tropical Southeast Asia (Werner et al., 2006) and oak forest (0.8 kg N2 ON ha−1 year−1 ) in a humid temperate region of southern Europe (Merino et al., 2004). However, these values were lower than the emissions (3.2 kg N2 O-N ha−1 year−1 ) reported from Dinghushan Nature Reserve in south subtropical monsoon climate region of Guangdong southern China (Tang et al., 2006). The lower emission observed in Xianning were probably due to less average annual rainfall (1577 mm) than in Guangdong (1927 mm), as more precipitation generally supports greater N2 O emissions (Zheng et al., 2000). However, higher pH in Xianning (pH = 5.02) than in Guangdong (pH = 3.80–4.02) could also have partly explained the differences of fluxes between the two studies. On the other hand, the annual N2 O emissions from pine forest (0.71 kg N2 ON ha−1 year−1 ) of red soil in Xianning were higher than the

emissions (0.13 kg N2 O-N ha−1 year−1 ) found in our previous study from Zigui (Lin et al., 2010). This difference can be attributed to a soil pH difference between the two sites (5.02 at Xianning versus 6.75 at Zigui). In this study, red soil through various mechanisms may have enhanced the N2 O emission. Firstly, the red soil is an acidic soil, with the possibility of enhanced N gases emissions (Macdonald et al., 2010). The acidification may severely inhibit N2 O reductase with the result that denitrification yields more N2 O than N2 (Weier and Gilliam, 1986). Increased soil acidity may also lower the decomposition rate of soil organic matter (Persson et al., 1989) which have been reported to promote N2 O emissions by increasing microbial O2 consumption (Jäger et al., 2011). Secondly, the red soil is an iron-rich soil. Iron oxide is the most important electron acceptor in soil (Furukawa and Inubushi, 2004). A pot experiment showed that ferrihydrite amendment stimulated N2 O fluxes (Huang et al., 2009). Nitrous oxide annual emissions from upland and orchard were 1.24 kg N2 O-N ha−1 year−1 and 1.40 kg N2 O-N ha−1 year−1 , respectively, which were less than the values (5.56 kg N2 O-N ha−1 year−1 ) reported from an onion field with chemical N fertilization and organic matter application in Mikasa, Hokkaido Japan (Toma et al., 2007). The lower values in our study were probably due to lower amount of applied fertilizer N (from 120 to 210 kg N ha−1 year−1 ) than those in Mikasa (475 kg N ha−1 year−1 ). The N2 O emission from agricultural soils usually increases with increase in the application of fertilizer N (Zou et al., 2005). Nitrous oxide annual emissions from upland and orchard reported in this study are significantly lower to medium range of reported N2 O emissions from cornfield in Southern Hokkaido, Japan (Katayanagi et al., 2008). This discrepancy is most likely due to the differences in SOC (6.29–9.33 g kg−1 in Xianning versus 41.8–100 g kg−1 in Hokkaido),

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y = 0.0403x + 4.728 R2 = 0.1848, P=0.004

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Fig. 7. Relationship between soil N2 O flux and MBC in different land uses. (A) Paddy, (B) Orchard, (C) Woodland, (D) Upland.

as the soil with higher SOC generally supports greater N2 O emissions (Bouwman et al., 2002; Li et al., 2005). The annual mean N2 O emission from paddy was 2.21 kg N2 O-N ha−1 year−1 in our study, which was within the range of N2 O fluxes at paddy field site in the tropical peatland in South Kalimantan, Indonesia (Inubushi et al., 2003). However, it was lower than a paddy field with rice–winter wheat rotation in Nanjing, Southeast China (Zou et al., 2005). The differences in N2 O emissions with different rotation (Xianning versus Nanjing) were probably due to different managements and soil physicochemical properties (i.e., soil texture).

4.2. Effect of land use on soil N2 O fluxes Differences in the land use types seem to exert some controls on potential N2 O fluxes from soils. Land use had a significant impact on soil N2 O flux, which was in agreement with the previous findings (Hadi et al., 2000; Scheer et al., 2008). Hadi et al. (2000) showed that the N2 O emission was strongly influenced by landuse management, soil moisture contents, addition of ammonium fertilizer or rice straw. Scheer et al. (2008) underlined that N2 O emission in land-use systems can be controlled by fertilization and soil water content. Intensive soil management has therefore led to a considerable increase in the exchange of N2 O between soils and the atmosphere (IPCC, 1995). Our results confirm the idea, developed in previous studies that soil N2 O flux was significantly lower for woodland (unmanaged) than agriculture land use types (managed). Among all land uses, the cumulative N2 O emission was less (0.71 kg N2 O-N ha−1 year−1 ) in woodland soil with no fertilization. Addition of fertilizer N to soils generally leads to increased N2 O

emission (Zou et al., 2005). These activities increase the amount of N available for nitrification and denitrification, and ultimately the amount of N2 O emitted by these processes (IPCC, 1995). Merino et al. (2004) reported that N2 O fluxes in the forest soil were very low in comparison with those in the agricultural soil throughout their study, which is in agreement with our results. Highest N2 O fluxes were observed from paddy field where highest amount of N fertilizer was applied and highest soil water contents (Fig. 2B) were observed. It agrees with the other findings that N fertilization and soil moisture increased the N2 O fluxes in the soils (Weitz et al., 2001; Werner et al., 2006). Zheng et al. (2000) also reported that soil moisture is the most sensitive factor to regulate N2 O emission from croplands. Maximum DOC contents were observed from paddy that had high soil moisture (Fig. 2B) and total organic C values (Table 1) as compared to other three soils. This resulted in high N2 O fluxes from paddy soil. Dissolved organic carbon and MBC were also significantly higher in paddy than the other land use types (Fig. 3). Studies have shown that N2 O emissions from the soil significantly positively related to DOC and MBC (Lou et al., 2007; Zhang et al., 2008). The higher level of DOC concentrations may have enhanced C availability, as C availability controlled N2 O emissions through its influence on microbial activity (Burger et al., 2005). Nevertheless, the N2 O differences among different land uses can also be due to distinct soil textural class (Xu et al., 2000). The effect of soil texture on N2 O emission likely results from physical variations in air and water proportions. The higher soil N2 O flux under paddy can be attributed to its moderate soil (sandy loam) conditions making it suitable for soil microorganisms to produce N2 O efficiently, while lower soil N2 O flux under woodland can be attributed to its restricted soil (silt loam) conditions having depressed microbial activities.

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Fig. 8. Regression analysis between N2 O flux and DOC content in 0–20 cm soil depth for different categories of water-filled pore space (WFPS).

4.3. Effect of environmental variables on soil N2 O fluxes Soil environmental and biological variables such as soil temperature, WFPS, DOC and MBC, that affects microbial activities, in turn nitrification and denitrification, are most important in terms of N2 O production. The relationships we found between soil temperature and soil N2 O fluxes are consistent with other field studies (Zheng et al., 2000; Werner et al., 2006). In this study, soil N2 O flux increased as soil temperature increased from April to September of each year (Fig. 2). Kesik et al. (2006) showed that N2 O production increased with temperature between 4 and 32 ◦ C. Papen and Butterbach-Bahl (1999) also found that during a 3-year continuous measurement period of N2 O emissions from untreated and limed soil of an N-saturated spruce and beech forest site, soil temperature was the most important factor modulating N2 O emissions closely followed by WFPS. Zheng et al. (2000) observed that soil moisture was the most sensitive factor to regulate N2 O production from croplands. Soil moisture controlled N2 O emissions through its influence on both microbial activity and on gas transport (Burger et al., 2005). However, soil moisture has shown contradictory effects on soil N2 O flux: enhancement (Zheng et al., 2000; Merino et al., 2004), or weak effects (Weitz et al., 2001; Tang et al., 2006). Because of high WFPS (i.e. >60%) during rice growing season (April to August), N2 O fluxes had no significant correlation with WFPS in paddy field (Fig. 5). Similarly, due to lower WFPS (i.e. <32%), N2 O fluxes were weakly correlated with WFPS in orchard. The inhibition of soil moisture content on N2 O flux may be significant at its lower end (dry soil) or high end (wet soil). Simojoki and Jaakkola measured higher N2 O emissions at WFPS between 60 and 90% in agricultural soils (Simojoki and Jaakkola, 2000). Werner et al. (2006) found a positive correlation between N2 O emissions and WFPS in tropical rainforest soils of Southwest China. Soil moisture in our study had a significant correlation with N2 O fluxes in woodland and upland only, which was in agreement with the results from our previous study in Zigui (Lin et al., 2010). Changes in soil moisture ultimately control soil aeration and effect nutrient availability (Werner et al., 2006). This finally feeds back into the spatial and temporal differences in the occurrence and magnitude of the oxidative nitrification and reductive denitrification processes and associated N trace gas emissions (Conrad, 1996). High N2 O fluxes have been reported from manure fields with high C availability (Mogge et al., 1999). Granli and Bøchman (1994) reported that the rate of N2 O production was partially controlled by C susceptible to mineralization. Several studies have implied

that the amount of DOC is a measure of the readily available resource for microbial growth and biological decomposition, often being considered as a good index of C availability (Liang et al., 1996; Jensen et al., 1997). Similarly, DOC has been proposed as an indicator of the C available to soil microorganisms (Boyer and Groffman, 1996). Nitrous oxide fluxes measured from four land use types significantly correlated with soil DOC contents (Fig. 6). The positive relations observed between soil N2 O flux and DOC were consistent with the results of other studies (Huang et al., 2004; Ullah et al., 2008). Huang et al. (2004) found that addition of synthetic N affected DOC transformation which was dependent on C:N ratio of the incorporated residues, and the change in N2 O emission was related to change in DOC, as higher N2 O emissions were observed with higher DOC concentration. Meijide et al. (2007) found that denitrification was the process responsible for most of the N2 O emissions, and DOC and NO3 − -N contents explained 40% of variability in the denitrification rate. The production of N2 O via denitrification could have been enhanced by the supply of C (Toma and Hatano, 2007). Water-filled pore space and organic C supply both were significantly related to denitrification rate (Weier et al., 1993; Elmi et al., 2005). The DOC content explained up to 49% of soil N2 O flux when WFPS was higher than 45% (P < 0.0001, n = 97, Fig. 8), while it only accounted for 6% of N2 O flux when WFPS was lower than 45% (P = 0.040, n = 71, Fig. 8). Wetter soils (WFPS > 45%) may have enhanced DOC and, in turn denitrification rates in this study. Therefore, we think that the relationship between N2 O fluxes and soil DOC contents had strong dependence on soil moisture contents. However, the types and amounts of C and N are likely to influence N2 O emissions (Burger et al., 2005). Microbial biomass carbon is the most active component of soil organic C that regulates biogeochemical processes in terrestrial ecosystems (Paul and Clark, 1996). In our study, DOC contents were found to correlate with MBC contents among different land uses (Fig. 3), MBC contents and N2 O emissions were found to strongly correlate with DOC, which was consistent with the reports of Zak et al. (1990), Barton and Schipper (2001) and Huang et al. (2004). It suggests that MBC might play an important role on N2 O production in red soil. The seasonal pattern of MBC was similar with the results of Burger et al. who found higher MBC concentrations in June, and the lowest in October (Burger et al., 2005). The seasonal pattern of MBC contents was similar to that of soil N2 O flux during the whole study period. Both had the maximum value in humid season and the minimum in dry season (Figs. 2 and 3). In our study, N2 O fluxes had positive correlation with soil MBC contents in all land use types except orchard that had low WFPS (<32%). Our study confirmed the

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previous observation that higher N2 O emissions were associated with higher MBC contents in some soils (Lou et al., 2007; Zhang et al., 2008). 5. Conclusion Soil temperature and DOC were the significant positive factors controlling soil N2 O fluxes in all land use types. To have a control on N2 O flux, DOC had strong dependence on soil moisture contents of the soils, as a positive correlation between N2 O flux and DOC was observed when WFPS was more than 45%, while poor correlation was found when WFPS was lower than 45%. Microbial biomass carbon showed a significant effect on soil N2 O flux from all land uses except orchard which had lowest WFPS contents. Overall, driven by seasonality of environmental factors, soil N2 O fluxes showed a seasonal pattern, with significantly higher fluxes being observed from humid season. Differences in land use always lead to differences in the vegetation, density of below ground microbial biomass, amount of C and N available for soil microbes, physical and chemical characteristics of the soil and so on. In this study, variations of environmental effects on N2 O emissions were observed from different land uses. This shows that land use types had great influence on N2 O flux, and the relationships between soil N2 O fluxes and environmental factors caused by land use changes are important when estimating variations in the N cycle and its response to environmental changes. The phenomenon observed in this study can be used for estimating soil N2 O fluxes and developing N budget for similar subtropical areas. However, whether landscape heterogeneity and different agriculture practices at large spatial scales may alter these results, still need to be tested. Acknowledgements This research was jointly supported by National Natural Science Foundation of China (Nos. 41090283 and 40930529). The authors are grateful to the president and staff members of the experimental station of Heshengqiao, located in Xianning, Hubei province, central China, for assistance during the field investigations. References Barton, L., Schipper, L.A., 2001. Regulation of nitrous oxide emissions from soils irrigated with dairy farm effluent. J. Environ. Qual. 30, 1881–1887. Baudoin, E., Benizri, E., Guckert, A., 2003. A impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol. Biochem. 35, 1183–1192. Bouwman, A.F., Boumans, L.J.M., Batjes, N.H., 2002. Emissions of N2 O and NO from fertilized fields: summary of available measurement data. Global Biogeochem. Cycl. 16 (4), 1058–1070. Boyer, J.N., Groffman, P.M., 1996. Bioavailability of water extractable organic carbon fractions in forest and agricultural soil profiles. Soil Biol. Biochem. 28, 783–790. Burger, M., Jackson, L.E., Lundquist, E., Louie, D.T., Miller, R.L., Rolston, D.E., Scow, K.M., 2005. Microbial responses and nitrous oxide emissions during wetting and drying of organically managed soil under tomatoes. Biol. Fertil. Soils 42, 109–118. Conrad, R., 1996. Soil microorganisms as controllers of atmospheric trace gases (H2 , CO, CH4 , OCS, N2 O, and NO). Microbiol. Rev. 60, 609–640. Elmi, A., Burton, D., Gordon, R., Madramootoo, C., 2005. Impacts of water table management on N2 O and N2 from a sandy loam soil in southwestern Quebec, Canada. Nutr. Cycl. Agroecosyst. 72, 229–240. Franzluebbers, A.J., 1999. Microbial activity in response to water-filled pore space of variably eroded southern Piedmont soils. Appl. Soil Ecol. 11, 91–101. Frazão, L.A., Piccolo, M.C., Feigl, B.J., Cerri, C.C., Cerri, C.E.P., 2010. Inorganic nitrogen, microbial biomass and microbial activity of a sandy Brazilian Cerrado soil under different land uses. Agric. Ecosyst. Environ. 135, 161–167. Furukawa, Y., Inubushi, K., 2004. Effect of application of iron materials on methane and nitrous oxide emissions from two types of paddy soils. Soil Sci. Plant Nutr. 50, 917–924. Granli, L., Bøchman, O.C., 1994. Nitrous oxide from agriculture. Norw. J. Agric. Sci. (Suppl. 12), 1–128.

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