Nitrous oxide emission from tea soil under different fertilizer managements in Japan

Catena 135 (2015) 304–312

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Nitrous oxide emission from tea soil under different fertilizer managements in Japan☆ Mudan Hou a, Naoko Ohkama-Ohtsu b, Sohzoh Suzuki b, Haruo Tanaka b, Urs Schmidhalter c, Sonoko Dorothea Bellingrath-Kimura d,⁎ a

Graduate School of Agriculture, Department of Biological Production Science, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan Institute of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, Japan Technical University Munich, School of Life Sciences Weihenstephan, Institute of Plant Nutrition, Freising-Weihenshephan 85354, Germany d Leibniz Centre for Agricultural Landscape Research, Institute of Land Use Systems, Head of Institute, Eberswalder str. 84, 15374 Muencheberg, Germany b c

a r t i c l e

i n f o

Article history: Received 5 December 2014 Received in revised form 16 July 2015 Accepted 20 July 2015 Available online 2 September 2015 Keywords: Chemical fertilizer Chicken manure Nitrous oxide Tea field Row Canopy

a b s t r a c t A field experiment was conducted to assess N2O emissions in response to different fertilizer types and amounts in a heavily fertilized tea field in Japan. Four treatments were implemented: CONT: no fertilizer, CONV: conventional fertilization, 1/2CONV, and CHEM: chemical fertilization. Gas samples were collected 5–8 times after every fertilizer application using the closed chamber method. The results revealed high seasonal variation in N2O emissions driven by soil temperature rather than the fertilizer application time. The soil temperature at a depth of 0–10 cm was significantly correlated with N2O emission (P b 0.01). The highest cumulative N2O emission (73.2 kg N ha−1 yr−1) was observed in the CHEM treatment, followed by the CONV treatment (65.0 kg N ha−1 yr−1), the 1/2CONV treatment (18.6 kg N ha−1 yr−1) and the CONT treatment (1.8 kg N ha−1 yr−1). The highest N2O emission factor (7.9%) was found in the CHEM treatment, followed by the CONV treatment (7.0%) and the 1/2CONV treatment (3.7%). There were spatial differences in the soil characteristics across the tea field. Accurate estimates of the ratios of N2O emitted from the four treatments during the two crop seasons were 47.9% and 52.1% from the soil on the rows (108.6 kg N ha−1) and under the canopies (118.3 kg N ha−1), respectively. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Nitrous oxide (N2O) is one of the major greenhouse gasses, and its concentration in the atmosphere has been increasing during the past several decades as a result of human activities. Global anthropogenic N2O emissions are increasing rapidly and are expected to almost double by 2050 unless mitigating action is accelerated. A total of 53% of all N2O emissions originate from the soil (IPCC, 2007), and 35% of the global annual N2O emissions originate from agricultural land, especially fertilized soils, which account for 6.3 Tg N yr−1 (Kroeze et al., 1999). Among all agricultural fields in Japan, the highest amount of nitrogen (N) fertilizer has been applied to tea (Camellia sinensis) fields (Mishima et al., 2012), as the amino acid content in green tea is a major factor in its quality; approximately 20 different amino acids contribute to the overall content (Muhammad and Kumazawa, 1974; Ruan

☆ This paper belongs to the special section ‘Key Processes and Factors to Mitigate Land Degradation’. ⁎ Corresponding author. E-mail addresses: [email protected] (M. Hou), [email protected] (N. Ohkama-Ohtsu), [email protected] (S. Suzuki), [email protected] (H. Tanaka), [email protected] (U. Schmidhalter), [email protected] (S.D. Bellingrath-Kimura).

http://dx.doi.org/10.1016/j.catena.2015.07.014 0341-8162/© 2015 Elsevier B.V. All rights reserved.

et al., 2010). Tea fields also receive a large amount of poultry manure (Mishima et al., 2012). Poultry manure degrades more easily and releases inorganic N more rapidly than other manures (Uenosono et al., 2004). Nitrogen in the form of mineral and organic fertilizers has been applied at rates as high as 450–1000 kg N ha−1 yr− 1 in tea fields (Li et al., 2013; Tokuda and Hayatsu, 2001; Xue et al., 2006), which is significantly higher than the rate recommended by extension officers, i.e., 250–375 kg N ha−1 yr−1 (Malenga, 1987). Moreover, in addition to direct N fertilizer, N is also supplied to the soil by trimmed leaves and branches, and through natural litter fall (Yamamoto et al., 2014). In Japan, the N absorbed by mature tea plants amounts to approximately 200–300 kg N ha−1 yr−1, and hence the residue leads to diffused pollution and even damages the growth of tea plants (Nakasone and Yamamoto, 2004; Oh et al., 2006). Although there is increasing information regarding N2O emission from tea fields, little is known about N2O emission from different types of fertilizers. The major controlling factors for N2O production − are temperature and the amount of NH+ 4 –N, NO3 –N, water, and organic matter in the soil (Kaiser et al., 1998; Signor and Cerri, 2013; Smith et al., 1998). The addition of inorganic N increases N2O emission by affecting the processes of nitrification and denitrification by increasing the − available NH+ 4 –N and NO3 –N substrates (Chadwick et al., 2000).

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Conventional ammonium turnover in soil consists of two steps: nitrification by autotrophs under aerobic conditions, which is followed by denitrification by heterotrophs under anaerobic conditions (Chen and Ni, 2011). However, aerobic denitrification has recently been found in soil with a soil water content of 20% water filled pore space (WFPS) (Baggs et al., 2010). Organic fertilizers with a high and easily mineralizable organic C content stimulate microbial activity and increase N2O emission (Chadwick et al., 2000). Tea fields, with their high N fertilizer requirements, provide potentially favorable conditions for nitrifying and denitrifying microbes that could result in high N2O emission. The number of denitrifiers has been shown to be much higher in tea soil than in potato or pine soils, and both N mineralization and nitrification processes were more active in tea soil than in other soils investigated (Oh et al., 2006). The N2O emission rates in tea fields are much higher than those in other upland fields and paddy fields (Jumadi et al., 2005). The annual N2O emissions from fields of wheat, corn, vegetables, and fruits averaged 0.05–0.4 mg N m−2 h−1 (JSSS, 1996), whereas emissions from tea fields were 2.0–8.5 mg N m−2 h−1 (Oh et al., 2006). Akiyama et al. (2006) reviewed previous studies and reported that the estimated annual fertilizer-induced N2O emission factors for tea fields in Japan are 2.82 ± 1.80%. The tea fields accounted for only 1% of the total agricultural field area, but 3.7% of the total N fertilizer used in Japanese agricultural fields was applied to tea fields. The N2O emission from tea fields accounts for approximately 16% of the total N2O emission from Japanese agricultural fields (NIES, 2012). Therefore, a reduction in N2O emissions from tea fields will contribute greatly to a reduction in the total N2O emission from Japanese agricultural fields. Because various types of fertilizer are applied to tea fields, it is important to determine their effectiveness in enhancing tea growth and the N lost by N2O emission. The tea plant in Japan is cultivated as continuous canopies in rows. The distance between rows of tea plants commonly ranges between 1.5 and 2.0 m. The tea canopy covers a width of 1.0–1.5 m and leaves a region of bare soil between the rows. All fertilizers are applied to the bare soil between the rows of tea plants (Hirono and Nonaka, 2012). No fertilizer is applied to the soil area under the canopy. The soil characteristics on the row and under the tea canopy must be different. First, fertilizers are applied and cultivation occurs through direct sunlight and rainfall. Then, the soil on the row is compacted by the movement of the trimming machine. However, no fertilizer is applied directly to the soil under the canopy except for the trimmed leaves. The soil has high porosity because there is no disturbance; in addition, conditions are shady. Most of the studies on N2O emission from tea fields were based on emission only from the soil between the rows where the fertilizer is applied (Akiyama et al., 2006). However, some studies have suggested that there is considerable N2O emission from the soil under the canopy (Hirono and Nonaka, 2012; Yamamoto et al., 2014). The estimation of N2O emission for a whole tea field using only N2O emission from the soil on a row might result in an overestimate if it is assumed that the soil conditions on the row and under canopy are the same. Thus, the objectives of this study were to assess N2O emissions and their sources under different fertilizer types and amounts in tea fields and to extend the N2O measurement to the soil under the canopy to accurately estimate the N2O emission from the whole tea field.

The experiment was laid out in a randomized complete block design with three replications. The plot size was approximately 5 × 6.4 m. The width between rows was 0.4 m and the width of the tea plant canopy was 1.2 m. Tea plants were planted in 1998, fertilized using a conventional method with more than 600 kg N ha−1 yr−1 in the first 10 years, and then did not receive fertilizer until 2011. Four treatments were implemented with different types and amounts of N fertilizers: control (CONT), conventional (CONV), chemical (CHEM), and half conventional (1/2CONV) fertilizer. No fertilizer was applied to the CONT treatment. The amounts of fertilizer were 600 kg N ha− 1 yr− 1 applied as (NH4)2SO4 and 300 kg N ha− 1 yr− 1 applied as chicken manure for CONV, 900 kg N ha− 1 yr−1 applied as (NH4)2SO4 for CHEM, and 300 kg N ha−1 yr−1 applied as (NH4)2SO4 and 150 kg N ha−1 yr−1 applied as chicken manure for 1/2CONV. The nutritional component of the chicken manure applied in this field was as follows: TN was 2.64%, P2O5 was 5.96%, K2O was 3.95%, TC was −1 27.92%, C/N was 10.58, NH+ , NO− 4 –N was 4.02 mg kg 3 –N was 0.04 mg kg−1, and the pH was 8.11 and water content was 22.35%. The fertilizer was applied to the soil between the tea plant rows, which is the conventional practice for tea cultivation in Japan. After fertilizer application, the soil on rows was cultivated to a depth of 10 cm below the soil surface. In 2011, the spring fertilizer (660 kg N ha−1 yr−1) was applied to all the fertilized treatments in March 4, 2011, which represented 2/3 of the total amount of annual fertilizer. The fertilizer in the summer season (60 kg N ha− 1 yr− 1) was applied on June 21, 2011, the autumn fertilizer (120 kg N ha−1 yr−1) was split into two applications, i.e., August 12 and October 15, 2011, and the winter fertilizer (60 kg N ha−1 yr−1) was applied on November 6, 2011. In 2012, the spring fertilizer (660 kg N ha−1 yr−1) was applied on March 13, 2012 and the summer fertilizer (60 kg N ha− 1 yr−1) was applied on May 16, 2012 (Table 2).

2. Materials and methods

2.3. Sample collection, soil parameters, and N2O analysis

2.1. Experimental site

The collection of gas samples from the soil surface for N2O emission measurements began before fertilization on February 23, 2011 and continued until July 3, 2012 using the closed-chamber method. Two chambers were inserted under the canopy and two were placed on the row for each of the 2 replications. The gas was sampled between 11:00 am and 3:00 pm to measure the daily average gas emission in the field. The chambers used in this study comprised a polyvinyl nontransparent circle cylinder with a diameter and height of 20 cm. The bases of the chambers were inserted into the soil between the

A field experiment was conducted in a tea field from February 2011 to July 2012 at the experimental farm of the Tokyo University of Agriculture and Technology (TUAT) in Fuchu, Japan (Latitude 35° 40′ N, Longitude 139° 37′ E). The average precipitation during this period was 1561.8 mm, and the highest and lowest air temperatures for these two years were 36.7 °C and − 6.2 °C, respectively. The soil was classified as a Silandic Andosol according to the World Reference Base

Table 1 Physico-chemical characteristics of tea soil profile in different depths. Horizon

Depth (cm)

pH

EC (dS m−1)

Total N (g kg−1)

Total C (g kg−1)

CEC (cmolc kg−1)

Bulk density (g cm−3)

Ap A2 B1 B2 B3

0–18 18–40 40–55 55–74 74–95

6.13 a 6.02 a 6.03 a 5.98 a 6.13 a

3.59 bc 4.08 d 2.72 ab 2.57 a 3.18 abc

5.06 d 4.27 d 4.01 b 2.96 c 1.51 a

65.80 c 59.51 c 59.36 c 39.89 b 17.47 a

15.89 bcd 15.23 bc 15.34 bcd 13.59 b 10.64 a

0.69 c 0.69 c 0.62 c 0.47 b 0.46 a

EC is electrical conductivity; CEC is cation exchange capacity. Values are the means of 3 replications from each depth. The same letters indicate that the values are not significantly different at p b 0.05 (Fisher LSD test).

for Soil Resources 2006 by the IUSS Working Group WRB (2007). The topsoil (1–18 cm) of the tea fields is loam (percentages of sand, silt and clay are 23.2%, 74.3% and 2.5%, respectively) with a pH of 6.1. The levels of soil organic carbon (SOC) and total N are 33 and 2.5 g kg−1, respectively. The chemical and physical characteristics of the soil profile at 5 depths from 0 to 94 cm are shown in Table 1. 2.2. Experiment design

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Table 2 Amount and types of fertilizers applied in different seasons in four treatments. Treatment

Practices

Spring

Summer

Autumn

Winter

Total amount

Fertilizer amount (kg N ha−1 yr−1) CONT CONV CHEM 1/2 CONV

Control Poultry and (NH4)2SO4 (NH4)2SO4 Poultry and (NH4)2SO4

0 660

0 60

0 120

0 60

0 900

660 330

60 30

120 60

60 30

900 450

F ¼ ρ  h  ðΔC=ΔtÞ  ½273=ð273 þ TÞ where F is the gas flux (μg N m−2 h− 1 for N2O), ρ is the gas density (N2O–N = 1.26 × 109 μm−3), h is the height of the chamber from the soil surface (m), △C/△t is the slope of the change of the gas concentration inside the chamber during the sampling period (m3 m−3 h−1), and T is the average air temperature during the sampling period (°C). The emission factor (EF) is defined as the cumulative amount of N2O emitted from the fertilized treatment minus that from the control treatment and is expressed as a percentage of the N applied (Akiyama et al., 2006). The cumulative amount of N2O gas measured during one crop season was calculated by multiplying the daily gas emission for each measurement with the time interval, and then adding all of these values. The whole experimental period was divided into two crop seasons. The 1st crop season was from February 23, 2011 to January 20, 2012, which was further divided into four seasons: spring (February 23–April 12 2011), summer (May 2–July 23, 2011), autumn (August 4–October 31, 2011) and winter (November 7 2011–January 20 2012). The 2nd crop season was from Feb 10, 2012 to July 3, 2012, which was divided into two seasons, i.e., spring (Feb 10–April 23, 2012) and summer (May 10–July 3 2012). The equation used for the calculation is as follows: n X ðRi  24  DiÞ i¼1

where Ri Di n

WFPS ¼ Vol=ð1−SBD=2:65Þ where

rows and under the canopy of the tea plants to a depth of 5 cm. The bases that had been inserted into the soil between the rows were removed prior to harvesting and fertilizer application, and then returned after the completion of these activities. Vials (20 ml) were vacuumed for 15 min before gas sampling. The 40 ml of air inside the chambers was collected with a 50-ml syringe using a three-way cock. After washing the passage way, 30 ml of air was inserted into the vials such that the internal pressure of the vial was higher than the atmospheric pressure. The gas samples in each chamber were collected three times at 10-min intervals, immediately after the closure of the chamber, and 10 and 20 min after placement. The vials were transported to the laboratory and stored at room temperature until analysis. The gas samples were collected at 1, 2, 4, 7, 10, 20, 35 and 50 days after every fertilizer application, except for some samples that were delayed for a few days. The nitrous oxide samples were analyzed using a gas chromatograph (GC-2014, Shimadzu, Kyoto, Japan) equipped with an electron capture detector (ECD) held constant at 350 °C. A carrier gas of 5% methane in argon was supplied at a flow rate of 10 ml min−1. The injection temperature was 80 °C. Gas emissions were calculated from the change in the gas concentration in the chamber versus the closure time:

Cumulative N2 O emission ¼

Air temperature was measured using an OPTEX thermometer in each chamber, and soil temperature was measured at a depth of 10 cm near the chamber. The volumetric soil water content was measured at a depth of 10 cm when the gas samples were collected, using a soil sensor (HydroSense CS620 sensor, CD620 display, made in Australia). The volumetric soil water content was converted into WFPS using the following formula:

the mean gas flux (mg N m−2 h−1) of two successive sampling dates; the number of days in the sampling interval; and the number of sampling periods.

WFPS Vol SBD 2.65

is the water-filled pore space (%); is the volumetric water content (%); is the soil bulk density (g cm−3); and is the soil particle density (g cm−3).

The soil profile was excavated in the tea fields at 1-m intervals. The resulting trench measured 1 × 2 m with a depth of 1 m. Soil samples from the profiles were collected from the trench wall at the following depths: 0–18 cm, 18–40 cm, 40–55 cm, 55–74 cm, and 74–94 cm. The samples were air dried and passed through a 2-mm sieve for further analysis. Soil samples were collected from the rows in the different treatments at a depth of 0–10 cm, approximately 4 times after every fertilizer application. Various physico-chemical properties of the soil were measured, including pH, total carbon concentration (TC), total nitrogen + (TN), as well as the levels of nitrate (NO− 3 ), and ammonium (NH4 ) ions. The procedures used for the laboratory analysis were as follows. The pH of 1:2.5 air-dried soil (weight) to deionized water (volume) (i.e., 20 g soil, 50 ml deionized water) was determined using a glass + electrode. The concentrations of NO− 3 and NH4 were determined by extracting the mineral N in the soils with a 2 mol l−1 KCl solution (1:10 soil to KCl solution), which was then filtered through Whatman #42 filter paper and analyzed using a colorimetric method. The absorbance of the extracted solution was measured using a UV–VI spectrophotometer (Shimadzu UVmini 1240, Shimadzu Corporation, Kyoto, Japan) at 220 nm to determine the concentration of NO− 3 ions. For NH+ 4 analysis, 5 ml of the soil extraction, 3 ml of buffer solution, and 2 ml of phenol-nitroprusside were mixed, and the absorbance of the mixed solution was measured after 45 min at a wavelength of 635 nm using a UV–VI spectrophotometer (Shimadzu UVmini 1240, Shimadzu Corporation, Kyoto, Japan). Total carbon and TN were measured using a Sumigraph NC-80 Auto Gas Chromatograph GC-4C device after the soil samples were sieved through a 0.5-mm mesh. The carbon:nitrogen ratio (C:N ratio) of the soil was used in subsequent analyses. 2.4. Statistical analysis of the data All data were subjected to analysis of variance (ANOVA) using CropStat 7.2 statistical software. A comparison of treatment means was performed using the least significant differences (LSD) at p = 0.05. Spearman rank order correlation analysis was performed using Sigma Plot 11.0 statistical software. 3. Results 3.1. Soil properties and N2O flux The average soil temperature during the study period was 15.2 °C. The highest and lowest soil temperatures were 29.8 °C in August and 3.3 °C in March, respectively. The average soil temperatures in different seasons were 7.1 °C, 24.9 °C, 24.5 °C and 6.2 °C in spring, summer, autumn and winter in 2011, and 8.8 °C and 18.5 °C in the spring and summer seasons in 2012, respectively (Fig. 1a). The total precipitation from February 2011 to June 2012 was 2181 mm. The average daily precipitation in different seasons was 2.1 mm, 6.0 mm, 6.2 mm and 2.3 mm

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Fig. 1. Time course (February 2011–July 2012) of (a) soil temperature (the average soil temperatures were shown by different seasons), (b) precipitation, (c) WFPS, (d) pH, (e) NH+ 4 –N + − concentration in soil, (f) NO− 3 –N concentration in soil (the time course of concentration of NH4 –N and NO3 –N were till June, 2012) and (g) N2O emission from soil. Solid arrows represent basic fertilizer and dotted arrows represent added fertilizer.

from spring to winter season in 2011, and 4.1 mm and 7.1 mm in the spring and summer seasons in 2012, respectively (Fig. 1b). There were no significant seasonal changes in the WFPS in 2011; this value was relatively low in autumn (31.3%) compared with the spring (34.2%), summer (35.8%), and winter seasons (33.5%) (Fig. 1c). The pH values were generally the same in the CONT, CONV and 1/2CONV treatments (average values for the whole study period were 6.7, 6.5 and 6.7, respectively) and were lowest (6.1) in the CHEM fertilizer treatment; however, there was no significant change between the different seasons (Fig. 1d). The concentrations of NH+ 4 –N in the soil between the plant rows increased rapidly after fertilizer application in June 2011, and March and May 2012. Particularly high values were

found in the CHEM treatment. The general NH+ 4 –N trend indicated low values in the spring and summer seasons, which then increased to the high value of 69.3 mg kg−1 in autumn followed by a decrease in the winter season in 2011. However, relatively higher concentrations of 30.0 mg kg−1 were measured in spring and 105.0 mg kg−1 was measured in 2012 (Fig. 1e). The trend in the NO− 3 –N concentrations was less variable than that of NH+ 4 –N; however, the highest average values were found in the summer season in 2012 (Fig. 1f). Low N2O emission from the CONT treatment was recorded during the experimental period, whereas the fertilized treatments showed high peaks during the summer and autumn seasons, even though the highest amounts of fertilizers were applied in spring (Fig. 1g). The CONV

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treatment showed the highest N2O emission with 3.13 mg N m−2 h−1 on June 23, 2011, and the second highest peak of 1.81 mg N m−2 h−1 on June 28, 2011. The emission peak in 2012 was lower than that in 2011, and the highest amount of 1.13 mg m−2 h−1 was recorded on May 17, 2012. The CHEM and 1/2CONV treatments showed N2O emission trends similar to those of the CONV treatment, while the amount of N2O was higher in the CHEM and lower in the 1/2CONV compared with the CONV treatment. The CHEM treatment showed the highest N2O peaks compared with the other treatments for most of the sampling times; however, the highest peak (2.47 mg m−2 h−1 on August 20, 2011) was lower than that detected in the CONV treatment. The N2O emitted from the fertilized treatments declined to almost the same level as the CONT treatment after 30 to 40 days after fertilizer application. No remarkable emissions of N2O were measured for any of the other fertilizer application times. When the soil temperature was less than 12 °C, the N2O emission in all treatments was at a low level, i.e., less than 50 μg N m−2 h−1, and there were no significant differences among treatments. When the soil temperature was higher than 12 °C, both the CONV and CHEM treatments showed a similar trend and exhibited a much higher N2O emission compared with the 1/2CONV and CONT treatments. The Spearman rank order correlation analysis showed that N2O emission was significantly correlated with the soil temperature and NO− 3 –N concentration of the soil at a depth of 0–10 cm (P b 0.01, Table 3).

Fig. 2. Accumulated amount of N2O emission in the 1st crop season which was calculated by the ratio (1:3) of row and canopy width. One crop season was divided into 4 seasons (spring, summer, autumn and winter).

3.3. N2O emissions from the row and under the canopy There were no significant differences in the N2O emitted from the soil on the rows and the soil under the canopy in the CONT plot (P N 0.05) (Fig. 3a). Nitrous oxide emissions from the soil between the rows were significantly higher (P b 0.05) than those from the soil under the canopy in the CONV and 1/2CONV treatments (Fig. 3b, d). Higher N2O emissions were measured from the soil on the row compared with that under the canopy in the CHEM treatment; however, these were not significantly different (P N 0.05) (Fig. 3c). The average WFPS was significantly higher for the soil on the tea plant rows (51.9%) compared with that under the tea plant canopy (45.4%) (p b 0.05, Fig. 3e). No large differences were found for soil temperature (P N 0.05), but the temperature was sometimes lower under the canopy (Fig. 3f). The N2O emission trend for the soil under the canopy was similar to that for the soil on the rows during the 1st crop season, and no high peak was observed for the summer and autumn fertilizer application times from the soil under canopy, although there were sharp peaks for the soil on the plant rows during the same time period (Fig. 3a, b, c, d). The ratio of the cumulative amount of N2O emitted from the soil under the canopy in whole cumulative amount of N2O emitted from entire tea field was lowest in the CHEM fertilizer treatment (35.9%), whereas the ratios for the three other treatments ranged from 48.4 to 57.2% (Fig. 4).

3.2. Cumulative N2O emissions The cumulative amount of N2O during the 1st crop season is shown in Fig. 2. In the first crop season, the highest cumulative N2O emission (73.2 kg N ha−1 yr−1) was observed for the CHEM treatment, followed by the CONV treatment (65.0 kg N ha−1 yr−1), the 1/2CONV treatment (18.6 kg N ha−1 yr−1) and the CONT treatment (1.8 kg N ha−yr−1). In the following years, the highest cumulative N2O emission (31.8 kg N ha−1 127 day− 1) was observed for the CHEM treatment, followed by the CONV treatment (24.6 kg N ha− 1 127 day− 1 ), the 1/2CONV treatment (11.6 kg N ha−1 127 day−1) and the CONT treatment (0.4 kg N ha−1 127 day−1). The highest cumulative N2O emission was observed in the CHEM treatment followed by CONV treatments in both years. During the whole experimental period, much higher cumulative N2O emissions in the summer season were observed in four treatments. There were differences in percentage values of cumulative N2O emission in the summer season among four treatments: the highest value (73.5%) was found in CONV treatment, then that in CHEM treatment (61.6%), 55.9% in 1/2CONV treatment and the lowest value (40.5%) was found in CONT. The average values of the percentage of cumulative N2O emission of four treatments in the summer and autumn seasons in 2011 were, 65.6% (104.0 kg N ha−1) and 32.2% (51.0 kg N ha-1) of the total N2O emissions, while for those recorded in the spring and winter seasons they were 1.7% (2.7 kg N ha−1) and 0.6% (0.9 kg N ha−1), respectively (Fig. 2). The cumulative N2O emission in the CHEM treatment was significantly higher than that in the CONT treatment (P b 0.05); however, there were no significant differences among the three fertilized treatments (P N 0.05) (Fig. 2). The differences in cumulative N2O emission among the four treatments were greater in the summer season.

4. Discussion 4.1. The factors controlling N2O emission The seasonal patterns of N2O emission were mainly driven by the seasonal variation in soil conditions such as soil temperature and soil NO− 3 –N concentration rather than the time or amount of fertilizer

Table 3 − Spearman rank order correlation analysis for the relationship between nitrous oxide (N2O) emission and soil NH+ 4 –N content, soil NO3 –N content, pH, soil TC content, soil TN content, water-filled pore space (WFPS), and soil temperature at 10 cm depth. Soil parameters

NO− 3 –N

NH+ 4 –N

Unit

(mg N kg soil

N2O (mg N m−2 h−1) Correlation coefficient

−0.03 ns

−1

)

(mg N kg soil 0.51 **

pH −1

)

TC (g kg

−0.08 ns

TN −1

−0.08 ns

)

(g kg

−1

−0.14 ns

)

WFPS

Soil temperature

(%)

(°C)

−0.01 ns

0.47 **

**, * and ns stand for significant at 1%, 5% and non-significant, respectively. The significant positive correlations at 5% were shown between N2O and NO− 3 –N and soil temperature at 10 cm depth.

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Fig. 3. N2O emission from the soil on a row and under a canopy in (a) CONT treatment: not significantly different, (b) CONV treatment: significantly different, (c) CHEM treatment: not significantly different, (d) 1/2CONV treatment: significantly different, (e) soil water content: significantly different, and (f) soil temperature; not significantly different between soil on a row and under a canopy. The solid arrows represent basic fertilizer and dotted arrows represent added fertilizer.

application (Fig. 1, Table 2). The optimum temperature for the production of N2O is 28 °C (Kesik et al., 2006). Increased temperature stimulates temperature-sensitive microbial processes within the nitrogen cycle, which cascade reactive N compounds through their different oxidation states and lead to an increase in N2O fluxes in the soil (Butterbach-Bahl et al., 2013). Nitrification can take place in the temperature range of 5–35 °C and is reduced by 50% at 12 °C (Shammas, 1986). The average soil temperatures were 7.1 °C and 8.8 °C in the spring season of 2011 and 2012, respectively, which resulted in little N2O emission even though 660 kg N ha−1 yr−1 of fertilizer was applied in the CONV and CHEM treatments. However, highest emission peaks were observed in the three fertilized treatments in the summer seasons when the average soil temperatures were 24.9 °C in 2011 and 18.5 °C in 2012 (Fig. 1a).

Fig. 4. Ratios of N2O emissions from the soil on rows and the soil under the canopies from four treatments.

In the CONV treatment, a sharp N2O emission peak occurred in the first few days after the summer and autumn fertilizer applications. As mentioned in the Introduction, the contents of TC, NH+ 4 –N −1 and NO− and 3 –N in chicken manure were 27.92%, 4.02 mg kg 0.04 mg kg−1, respectively. When the manure was applied to the soil during summer, NH+ 4 –N oxidized with an increasing soil temperature and produce N2O gas. On the other hand, the NO− 3 –N and the readily available C in the manure increased microbial activity and resulted in oxygen depletion and the creation of anaerobic microsites in the soil, which caused denitrification and the production of high amounts of N2O. A large amount of applied NH+ 4 –N can be easily nitrified under aerobic conditions before being taken up by the tea plant. Thus, the nitrification process with increasing soil temperature is considered to be the main contributing factor to the high N2O emission in the CHEM treatment. There was no added C substrate as in the CONV treatment, and denitrification in the CHEM treatment was therefore assumed to be lower than that in the CONV treatment, which resulted in a lower peak observed for the CHEM treatment in comparison to the CONV treatment. The 1/2CONV treatment did not show sharp peaks due to the lower + concentrations of NO− 3 –N (Fig. 1f) and NH4 –N (Fig. 1e). The N2O emission was lower than that of the CONV treatment, confirming that N2O emissions decrease with decreasing N fertilizer rate, although they did not decrease in a linear manner. There was a seasonal change in the cumulative amount of N2O emissions. The highest cumulative amounts of N2O were found in the summer season in both 2011 and 2012. However, there was a difference between the cumulative amount of N2O emissions in spring in the two crop seasons, i.e., 2.7 kg N ha−1 and 9.7 kg N ha−1 in 2011 and 2012, respectively. Obviously, residual fertilizer from 2011 influenced the N2O emission in the spring season in 2012. Surprisingly, the cumulative

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amount of N2O in the summer season in 2012 (58.7 kg N ha− 1) was lower than that in 2011 (104.0 kg N ha−1). The most probable reason for this result was the average soil temperature, which was 24.9 °C in 2011 and 18.5 °C in 2012 (Fig. 1a). The differences of the mineral N contents in different fertilizers resulted in the different percentage values of cumulative N2O emission in the summer season among different treatments. The highest value (73.5%) was found in CONV treatment. The contents of NH+ 4 –N and −1 NO− and 0.04 mg kg−1, re3 –N in chicken manure were 4.02 mg kg spectively. When the manure was applied to the soil during summer, NH+ 4 –N oxidized with an increasing soil temperature and produce N2O gas. On the other hand, the content of TC was 27.92%, therefore, the NO− 3 –N and the readily available C in the manure increased microbial activity and resulted in oxygen depletion and the creation of anaerobic microsites in the soil, which caused denitrification and the production of high amounts of N2O. Both nitrification and denitrification processes under high soil temperature in the summer season resulted in the higher percentage of cumulative N2O emission in CONV treatment. The percentage value of cumulative N2O emission in the summer season in CHEM treatment was 61.6%, which was lower than that of CONV treatment, and might be due to no C substrate added as in the CONV treatment, and denitrification in the CHEM treatment was therefore assumed to be lower than that in the CONV treatment. Obviously, the + lower contents of NO− 3 –N and NH4 –N resulted in the lower percentage value of cumulative N2O emission in the summer season in 1/2CONV treatments (55.9%) and the lowest value (40.5%) was found in the CONT treatment. Higher peaks of N2O flux in the fertilized treatments during the summer and autumn seasons were due to increased N input from the fertilizer applications and the high soil temperature in this study. Akiyama and Tsuruta (2002) also showed that N2O emitted from a Chinese vegetable field was positively correlated with soil temperature. Furthermore, other studies have shown that N2O emissions are significantly and positively correlated with temperature for all land use types, suggesting that environmental temperature might play a more important role (Han et al., 2013). Yamamoto et al. (2014) indicated that 40% of the total amount of fertilizer was applied at the beginning of March, only 20% was applied in the summer season, and the remaining 40% was applied in autumn. However, the seasonal fluctuations of the N2O emissions showed that the highest peak was recorded after the application of fertilizer in autumn, and not after the fertilizer application in spring. This result highlights the fact that N2O emission is driven by temperature and not by fertilizer application time. 4.2. The effect of fertilization on cumulative N2O emission Animal manure is known to release N slowly compared with chemical fertilizer, and the N is less available to microbes as an immediate resource. Only a small amount of N in the form of NH3 and urea will be utilized immediately after application. Approximately 50% of the total nitrogen is available in the first year, and the remainder is released slowly over several subsequent seasons (Snyder et al., 2007). On the + other hand, NO− 3 , which is oxidized from NH4 , would undergo denitrification. However, the denitrifiers produce N2O instead of N2 under aerobic conditions. The isolated and characterized novel aerobic denitrifiers produce low levels of N2O under aerobic conditions (Takaya et al., 2003). Therefore, both slower nitrification and denitrification resulted in a lower cumulative amount of N2O in the CONV treatment. Most of the released NH+ 4 in the CHEM treatment could still have been nitrified before being taken up by the tea plants, which could have led to high and longer nitrification activity and consequently, to a lower soil pH. The average pH of the CONV treatment was 6.5, while the average soil pH of the CHEM fertilizer treatment was 6.1 (Fig. 1d). The microflora in tea field soils is adapted to an acidic environment (Tokuda and Hayatsu, 2004). Greater N2O emission occurs under lower pH conditions; the soil pH value in tea fields ranges from 3.3 to

4.5 (Tokuda and Hayatsu, 2001); however, the average pH value in this tea field was 6.5, which is much higher than that in other fields. The repeated application of NH+ 4 –N increased N2O emission through the coupled processes of nitrification and denitrification. Therefore, the cumulative emission over the whole experimental period was higher in the CHEM treatment relative to the CONV treatment. Akiyama et al. (2006) showed that the average N2O emission factor for tea fields in Japan was 2.82%, which is higher than that of other upland fields. The emission factors in this study were 1.3–2.8 times higher than those recorded by Akiyama et al. (2006). Other studies have shown that N2O emissions are usually below 10 kg N ha−1 yr−1 (Eichner, 1990; JSSS, 1996; Kaiser et al., 1998), but this study showed that the tea field had N2O emissions in the range 1.8–73.2 kg N ha−1 yr−1. Several studies have recorded different ranges for annual N2O emissions. Tokunaga et al. (1996) reported that N2O emissions from tea fields were 39–45 kg ha−1 yr−1. Nitrous oxide emissions from tea fields range from 32.3 to 96.6 kg N ha−1 yr−1 for long-term tea cultivation in the Shizuoka prefecture, where the highest N fertilizer application was 1100 kg N ha−1 yr−1 (Oh et al., 2006). Akiyama et al. (2006) reviewed previous studies and derived an estimated mean N2O emission of 24.3 ± 16.3 kg N ha−1 yr−1 from tea fields in Japan. There are significant uncertainties and variability in these studies, which suggest that N2O emitted from arable soils is affected by various factors such as the type of fertilizer, temperature, pH and soil type (Akiyama et al., 2006). On the other hand, nitrification and denitrification were both found to be inhibited under acidic conditions, and these processes were positively correlated with soil pH (Müller et al., 1980). The tea field was not fertilized for three years before this experiment; therefore, the average pH values were higher than those of other tea fields, as mentioned in the Results section. Consequently, the cumulative amounts of N2O in all treatments were relatively higher than in other tea fields. The N2O emission factor for the CONV treatment was 1.9-fold (2011) and 2.2-fold (2012) higher than that of the 1/2CONV treatment, which received half the amount of fertilizer than that applied to the CONV treatment. Kaiser et al. (1998) reported that the linear reduction in N fertilizer applied to arable soil did not result in a linear decrease in N2O losses because of the high N mineralization potential of the soil. Other researchers have found that increasing the amount of N added to the soil resulted in increased emissions of N2O (Mosier et al., 2006). However, no clear linear relationship has been observed between N2O emission and the fertilizer rate (Xu et al., 2014), and an exponential relationship has been observed between emissions and soil mineral N (Mu et al., 2009). Therefore, it can be concluded that the emission factor is not linearly related to the fertilizer application rate, and higher application rates result in higher emission factors. 4.3. The effect of field position on N2O emission The lowest amount of N2O was emitted from the CONT treatment compared with the three fertilized treatments, but there was no obviously higher peak throughout the whole experimental period because N was not directly supplied by fertilizer. The N2O emissions from the soil on the row were higher than those from under the canopy for most of the sampling periods in the CONT fertilizer treatment. The WFPS of the soil between the plant rows was higher than that of the soil under the plant canopy due to the compaction of the soil between the rows and the interception of rainfall by the canopy. The WFPS is thought to be a reason for higher N2O emitted from the soil between plant rows because N2O emission increases steeply with an increase in the water content of the soil (Luo et al., 2013; Smith et al., 1998). However, there was no significant difference between the N2O emitted from the soil on the row and under the canopy (P N 0.05) (Fig. 3a). The soil surface under the canopy directly underneath the tree stem was only slightly higher than the soil surface of the other areas under the canopy and on the row. The chambers under the canopy were placed in an area where thick roots allowed the chamber to be inserted

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into the soil. This area has the same surface height as the row and has higher porosity compared with the soil on the row. The probable reason for the higher peaks measured in the soil under the canopy in the 3 fertilized treatments after spring and autumn fertilization was that fertilizer applied to the row ran off during the rainy season and reached the soil under the canopy. Organic fertilizer is a source of N, which can be transformed into inorganic forms through biological processes as follows: NH+ 4 → − NH2OH → NOH → NO− 2 → NO3 (Glinski et al., 2007). In dry soils under aerobic conditions, ammonification (R-NH2 (organic N) → NH3 (ammonia) → NH+ 4 (ammonium)) occurs faster than the oxidation − − of ammonium to nitrate (NH+ 4 (ammonium) → NO2 (nitrite)→NO3 − (nitrate)), resulting in minimal NO3 accumulation (Angria et al., 2012). Therefore, less NO− 3 runoff to the soil under the canopy resulted in significantly lower amounts of N2O being emitted from the soil under the canopy compared with the soil on the row in the CONV and 1/2CONV treatments (P b 0.05) (Fig. 3b, d). The cumulative amount of N2O emitted from the soil on the row and under the plant canopy was calculated using a ratio of 1:3 (N2Orow + (N2Ocanopy × 3)), which corresponds to the ratio of the width between the plant rows (0.4 m) and the plant canopy (1.2 m). The area on row and under the tea plant canopy is directly proportional to the width of the row and canopy, as the lengths of the row and canopy are the same. The ratio of the cumulative amount of N2O emitted from the soil under the canopy in the CONV treatment was 56.9% (Fig. 4). A high rate of chemical fertilizer applied to the soil between tea plant rows made a major contribution to the high concentration of inorganic N in the CHEM fertilizer treatment. Ammonium easily ox− − idizes to nitrate (NH + 4 (ammonium) → NO 2 (nitrite) → NO 3 (nitrate)), and NO− is soluble, mobile and susceptible to being 3 transported to the soil under the canopy. This is the reason for the higher N2O emission from the soil on the row and under the canopy, but there was no significant difference (P N 0.05) in the CHEM fertilizer treatment (Fig. 3c). Accurate estimates of the ratios of N2O emitted from the soil on the rows (108.6 kg N ha−1) and under the canopies (118.3 kg N ha−1) were 47.9% and 52.1%, respectively, for the two crop seasons (419 days). The exact amounts of N2O emitted from the soil under the canopy in each treatment were 57.2% in the CONT treatment, 56.9% in the CONV treatment, 35.9% in the CHEM treatment and 48.4% in the 1/2CONV treatment. The larger area is an important reason for the high ratio of N2O emitted from the soil under the plant canopy in all the treatments, even though no fertilizer was applied to this area. Hirono and Nonaka (2012) showed that the ratio of N2O emitted from the soil under the plant canopy was 35% when the widths of the row and canopy in a tea field were 0.3 m and 1.5 m, respectively. Other researchers have found that the soil under the canopy contributed 35.5% of the total N2O emitted from a tea field when the widths of the row and canopy were 0.6 m and 1.2 m, respectively (Yamamoto et al., 2014). The ratios of N2O emitted from the soil under the plant canopy for both of these studies were lower than those recorded in our experiment. The most important reason for this is that the aforementioned studies used lower amounts of fertilizers, totaling 510 and 450 kg N ha−1 yr−1, respectively, whereas a total of 900 kg N ha− 1 yr− 1 was applied in our experiment. There would be a relatively smaller amount of fertilizer runoff (caused by rain) onto the soil under the canopy if a low amount of fertilizer was applied between the plant rows. Furthermore, the widths of the row and canopy investigated in the aforementioned studies differed from those in our experiment. The ratio of the area of the soil under the plant canopy was highest in the study of Hirono and Nonaka (2012), followed by the current experiment, and the lowest ratio was used in the research conducted by Yamamoto et al. (2014). However, a clear relationship was not found between the area of soil under the canopy and the level of N2O emitted from that region. Measurements of N2O emissions from both the soil under the canopies and the soil between the canopies are needed to estimate N2O emissions from the entire tea field.

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5. Conclusions The seasonal patterns of N2O emissions were mainly driven by the seasonal variation in soil temperatures rather than the fertilizer application time. The cumulative amount of N2O was highest in the summer season compared with the other three seasons. Both chemical fertilizer and manure increased N2O emission due to increased soil N availability associated with the application of N. Chemical fertilizer emitted more N2O than organic fertilizer. Nitrous oxide emission increased with an increase in the N application rate during the relatively higher emission periods (summer and autumn). It can be concluded that the use of organic manure, such as chicken manure, is a better option to mitigate N2O emission from a tea field with a Silandic Andosol soil. There was a spatial variation in the N2O emission within the tea field, i.e., from the soil on the row to the soil underneath the canopy. It is necessary to extend the measurement of N2O emissions to the soil underneath the plant canopy to accurately estimate N2O emissions from tea fields.

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