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Three years of nitrous oxide and nitric oxideemissions from silandic andosols cultivated withmaize in Hokkaido, JapanKanako Kusa a b , Ronggui Hu a c , Takuji Sawamoto a d & Ryusuke Hatano a ea Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japanb National Agricultural Research Center, Tsukuba, 305-8666, Japanc College of Resource and Environment, Huazhong Agricultural University, Wuhan, Hubei,430070, Chinad Faculty of Dairy Science, Rakuno Gakuen University, Ebetsu, 069-8501, Japane Field Science Center for Northern Biosphere, Hokkaido University, Sapporo, 060-0809,Japan

Version of record first published: 17 Dec 2010

To cite this article: Kanako Kusa, Ronggui Hu, Takuji Sawamoto & Ryusuke Hatano (2006): Three years of nitrous oxideand nitric oxide emissions from silandic andosols cultivated with maize in Hokkaido, Japan, Soil Science and PlantNutrition, 52:1, 103-113

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Soil Science and Plant Nutrition (2006) 52, 103–113 dio: 10.1111/j.1747-0765.2006.00009.x

© 2006 Japanese Society of Soil Science and Plant Nutrition

Blackwell Publishing LtdORIGINAL ARTICLEN2O and NO Emissions from Andosols in HokkaidoK. KUSA et al.

Three years of nitrous oxide and nitric oxide emissions from silandic andosols cultivated with maize in Hokkaido, Japan

Kanako KUSA†, Ronggui HU‡, Takuji SAWAMOTO§ and Ryusuke HATANO¶

Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan

Abstract

We measured nitrous oxide (N2O) and nitric oxide (NO) emissions during the snow-free season (April–November) over a 3-year period (1998–2000) from a Silandic Andosols cultivated with maize (Zea mays L.)in central Hokkaido, Japan. In May, before furrowing, composted cattle manure was broadcast onto thefield at a rate of 3.0 g N m−2. After furrowing, chemical fertilizer (NH4)2SO4-N + (NH4)3PO4-N : urea-N ata ratio of 10:3 was applied to the row at a rate of 13 g N m−2. An impermeable layer lay 1.3 m belowground level. As a result, after heavy rains and during the snow-melting period, the groundwater table roseto near the ground surface. The N2O and NO emission rates ranged from 0.0 to 6.4 and from 0.00 to0.94 mg N m−2 h−1, respectively. The highest N2O emission was observed after heavy rain in summer andautumn. The magnitude and seasonal pattern of N2O emissions from the inter row were similar to thosefrom the row itself, although chemical fertilizer had not been applied to the inter row. In contrast, anincrease in NO emissions was observed only from the row. Seasonal fluctuations in soil and concentrations and the emission ratio N2O-N/NO-N suggested that N2O and NO emitted after fertilizerapplication (May to early July) were produced mainly by nitrification, whereas N2O emitted after heavyrains (after mid-July) was produced mainly by denitrification. Total N2O and NO emissions during thesnow-free season ranged from 0.7 to 2.8 and from 0.0 to 0.7 g N m-2, respectively, over a 3-year period.The N2O and NO emissions from our field were relatively high compared with those reported worldwide.In contrast, reported N2O emission rates from agricultural Andosols in Japan are typically lower than thosefrom other agricultural soils in Japan and around the world. Therefore, the results of the present studysuggest that high N2O emissions may occur from Japanese agricultural Andosols that are poorly drained.

Key words: Andosols, denitrification, nitric oxide, nitrification, nitrous oxide.

INTRODUCTION

Nitrous oxide (N2O) is a greenhouse gas and its con-centration in the troposphere is 314 ppb. The atmos-pheric concentration of N2O is lower than that of carbondioxide (CO2) or methane (CH4), but its 100-year Glo-bal Warming Potential is higher than that of CO2 and

CH4 because of its long atmospheric lifetime (approxi-mately 120 years). Therefore, the potential impact ofincreasing N2O on global warming is significant.Moreover, N2O contributes to the depletion of strat-ospheric ozone (O3) (FAO and IFA 2001; Prather et al.2001).

Nitric oxide (NO) is the main component of theatmospheric pollutant reported as NOx. In the atmos-phere, NO is oxidized to nitrogen dioxide (NO2), so theatmospheric concentration of NO varies. In general,atmospheric NOx concentration ranges from 20 to500 ppb in urban areas and from 1 to 10 ppb in ruraldistricts (Hatakeyama and Sagai 1996). Redeposition ofNOx contributes to the acidification and eutrophicationof aquatic ecosystems. In addition, NO catalyzes tropo-spheric O3 production, and is directly responsible forthe formation of a greenhouse gas (Davidson andKingerlee 1997; FAO and IFA 2001; Hatakeyama andSagai 1996; Ibusuki 1990; Prather et al. 2001).

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Correspondence: Dr K. KUSA, Graduate School ofAgriculture, Hokkaido University, Sapporo, 060-8589 Japan.Email: kusakana@affrc.go.jpPresent addresses: †National Agricultural Research Center,Tsukuba 305-8666, Japan. ‡College of Resource andEnvironment, Huazhong Agricultural University, Wuhan,Hubei 430070, China. §Faculty of Dairy Science, RakunoGakuen University, Ebetsu 069-8501, Japan. ¶Field ScienceCenter for Northern Biosphere, Hokkaido University,Sapporo 060-0809, Japan.Received 21 June 2005.Accepted for publication 7 November 2005.

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The N2O emissions from agricultural lands increasewith N application rates, which depend, in part, on cli-matic conditions and soil fertility (e.g. soil organic C andN contents) (FAO and IFA 2001). Global N2O emissionsfrom agricultural soils have been estimated to be4.2 Tg N year−1, accounting for 46% of annual anthro-pogenic N2O emissions and 20% of global annual N2Oemissions (Mosier et al. 1998). The major source of NOx

is fossil fuel combustion (22 Tg N year−1) (Delmas et al.1997). NO emissions from global and cultivated soilshave been estimated to be approximately 21 and5.5 Tg N year−1, respectively (Davidson and Kingerlee1997). Agricultural soils are one of the sources of in-creasing NO emissions (Veldkamp and Keller 1997).

Denitrification and nitrification by soil microbes arethe dominant soil processes producing N2O and NO.Activation of these processes varies in time and spacebecause they are influenced by various factors includingsoil moisture, temperature, nitrate ( ) and ammonium( ) concentrations and soil organic matter content.To more accurately estimate N2O and NO emissionsfrom agricultural soils, empirical and process models(e.g. FAO and IFA 2001; Li 2000) have been developed.However, long-term field measurements are also re-quired to validate and improve the models, and to builda global inventory of N2O and NO emissions fromsoils. In the present study, we measured N2O and NOemissions, soil moisture, soil mineral N content, soiltemperature and rainfall over a 3-year period from aSilandic Andosols cultivated with maize (Zea mays L.)in Hokkaido, Japan. The objectives of this study wereto evaluate the seasonal pattern and amounts of N2Oand NO emissions, and to compare our results withvalues obtained in previous studies conducted in Japanand around the world.

MATERIALS AND METHODS

Experimental siteThe experimental site was a maize field (1.8 ha in area)located in the National Agricultural Research Center

for Hokkaido Region (43°0′N, 141°24′E), SapporoCity, Hokkaido, Japan. The soil was Silandic Andosols(Japanese Society of Pedology 2003). Table 1 showsthe physical and chemical properties of the soil. Animpermeable layer lay 1.3 m below ground level. As aresult, the groundwater table rose to near the groundsurface after heavy rains and during the snow-meltingperiod (Kanazawa et al. 1999). The normal annual airtemperature is 8°C and the normal annual rainfall is1129 mM (including 482 mm of snow) (Sapporo Dis-trict Meteorological Observatory 1991). Each year, inmid-May, composted cattle manure was broadcast ontothe field at a rate of 3.0 g N m−2. After furrowing, achemical fertilizer ((NH4)2SO4-N + (NH4)3PO4-N : urea-Nat a ratio of 10:3) was applied to the row at a rate of13 g N m−2 (Fig. 1). The row width was 75 cm and theinter row width was 25 cm (Fig. 1). Maize was sown inmid-May and harvested at the end of Septemberthroughout the 3-year period. The maize stubbles wereplowed into the field in the spring when the field was

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Table 1 Physical and chemical properties of the soil horizons

HorizonDepth(cm)

pH(H2O)

Total-C(%)

Total-N(%) Texture

Saturated hydraulic conductivity (m s−1)

Ap 0–30 5.6 5.1 0.7 CL 3.3 × 10−6

AB 30–37 5.8 1.5 0.2 LiC 2.2 × 10−5

B 37–47 5.8 0.8 0.1 LiC 2.3 × 10−5

BC1 47–75 5.8 0.4 0.1 CL 4.3 × 10−5

BC2 75–90 5.7 0.4 0.1 LiC NDC 90–100+ 6.0 0.3 0.0 SL ND

Bulk density (0–5 cm), 0.78; (5–10 cm), 0.81 (Mg m−−−−3). ND, not determined.

Figure 1 Schematic diagram of chamber placement.

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ridged. In general, the field was monitored every 7 daysduring the snow-free season (April–November) eachyear for 3 years (1998–2000).

Measurement of N2O and NO emissions and soil respirationGas emissions from the soil surface were measuredusing a closed-chamber technique. A cylindrical stain-less steel chamber, 0.2 m in diameter and 0.2 m high,was used. Almost all of the sampling was conductedat approximately 11.00 am. The chamber positions areshown in Fig. 1. The chamber was not placed over themaize shoot. Fifteen minutes after placement of thechamber, gas samples were withdrawn from the enclosedatmosphere. Ambient air was collected at the soil surfaceand 2 m above the soil surface, and the mean of the twovalues was used as the background concentration in thecalculation of gas emissions. The gas sampling methodand the calculation of gas emissions are described indetail in our previous paper (Kusa et al. 2002). A gaschromatograph equipped with an electron capturedetector (GC-14B, Shimadzu Corp., Kyoto, Japan) wasused for the N2O analysis. Concentrations of NO andCO2 were analyzed using a chemiluminescence nitrogenoxide analyzer (Model 265P, Kimoto Electric Co. Ltd.,Osaka, Japan) and a portable infrared gas analyzer(ZFP-5, Fuji Electric Co. Ltd., Tokyo, Japan), res-pectively. Four chambers were used and two wereplaced on the row and the other two in the inter row,and the average of the two replicates was calculated.Both chambers were placed in the same row and interrow, and the placements of the chambers in the rowand inter row were adjacent (Fig. 1). The cumulativevalue of emissions was calculated using linear interpola-tion. NO emissions were not measured in 1998.

Ancillary measurementsSoil temperature was measured at a depth of 10 cmwith a digital thermometer. Undisturbed soil samples(0–5 cm depth) were collected near the chamber(Fig. 1) with a 100-mL steel cylinder, and the solid,water and gaseous phases and the water-filled porespace (WFPS) were measured. Disturbed soil sampleswere taken from 0–10 cm depth (1998) and 0–15 cmdepth (1999–2000) to measure the concentrations ofsoil and . In the rows, these soil samples weretaken near the area where the chemical fertilizer hadbeen applied (Fig. 1). Field-moist soil samples wereextracted in deionized water (1:5, soil : water), and

and concentrations in the extracted solutionwere determined using ion-exchange chromatographyand colorimetry with indophenol blue, respectively.Meteorological data (air temperature and rainfall) wererecorded at the National Agricultural Research Center

for Hokkaido Region. The dry weight of maize wasmeasured from the emergence to the harvest stage, andN uptake by maize was determined using the Kjeldahlmethod.

RESULTS

Environmental factorsThe frequency of rain increased after July every year(Fig. 2a). The amount of rain in the snow-free seasonwas greater in 2000 than in 1998 or 1999 (Table 2). Inmid-September 1998 and mid-July 1999 and 2000,heavy rain caused high soil moisture (high WFPS) (morethan 80% in the inter row and more than 60% in therow) (Fig. 2a). The WFPS values during the relativelydry season (May–June) were lower than those duringthe relatively wet season (July–October). The WFPSvalues in the inter row were higher than those in therow (paired t-test, t = 4.22, P < 0.01, n = 52; Fig. 2a).Soil temperature increased from spring to summer anddecreased from summer to autumn (Fig. 2b). The meansoil temperature during the 3-year study period was16.6°C (range 0.6–26.4°C) in the row and 16.5°C(0.6–25.6°C) in the inter row. Soil temperature in therow was significantly higher than that in the inter row(paired t-test, t = 1.98, P = 0.05, n = 56). There were nosignificant annual differences in WFPS values or soiltemperature (Table 2).

Maize N uptake and mineral N in the soilNitrogen (N) uptake by maize increased from July toSeptember (Fig. 2b). The average N uptake was20 g N m−2 (range 13–29 g N m−2). In the row, the soil

concentration increased to its maximum value(210–460 mg N kg−1) just after fertilizer applicationand then rapidly decreased to below 10 mg N kg−1.Similarly, soil concentration increased to itsmaximum value (180–230 mg N kg−1) in June or Julyand then rapidly decreased to below 10 mg N kg−1

(Fig. 2c,d). In the inter row, where no chemical fertilizerhad been applied, the soil concentration wasapproximately constant (we removed an exceptionallylarge value). Soil concentration in the inter rowincreased slightly in June and July.

Nitrous oxide and NO emission ratesNitrous oxide emission rates increased markedly inmid-September 1998 and in July and August 1999 and2000; these increases took place after heavy rain ofmore than 80 mm day−1 (Fig. 2a,e). The mean N2Oemission rate from the row during the 3-year periodwas 0.30 mg N m−2 h−1 (range 0.00–6.42 mg N m−2 h−1),and from the inter row was 0.26 mg N m−2 h−1 (range0.00–5.87 mg N m−2 h−1). The difference in N2O emission

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rates between the row and the inter row was not sig-nificant (paired t-test: t = 0.74, p = 0.46, n = 66). Incontrast, the seasonal pattern and magnitude of NOemission rates differed between the row and inter row(Fig. 2f). NO emission rates increased markedly in therow in June and July, just after fertilizer application,but did not increase in the inter row. The mean NOemission rate from the row over 2 years (1999–2000)was 0.07 mg N m−2 h−1 (range 0.00–0.94 mg N m−2 h−1),and from the inter row was 0.00 mg N m−2 h−1

(0.00–0.05 mg N m−2 h−1). This difference in emissionrates between the row and inter row was significant(paired t-test: t = 2.79, P < 0.01, n = 43).

Soil respiration ratesSoil respiration rates increased from May to July anddecreased from September to November (Fig. 2g). Overthe 3-year study period, soil respiration rates from therow ranged from 0 to 520 mg C m−2 h−1, and thosefrom the inter row ranged from 0 to 200 mg C m−2 h−1.

Figure 2 Seasonal pattern of (a) rainfall and soil moisture (WFPS), (b) soil temperature, (c) soil NO3-N concentration, (d) soil NH4-Nconcentration, (e) nitrous oxide (N2O) and (f) nitric oxide (NO) emission rates and (g) soil respiration rate from 1998 to 2000.Closed circles (�) and open triangles (�) denote the data observed in the row and inter row, respectively. Bars in (a) and crosses(+) in (b) denote the rainfall and maize N uptake, respectively. F.A. and H. denote the times of fertilizer application and harvest,respectively. WFPS, water-filled pore space.

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Mean values of soil respiration rates from the row andinter row were 130 and 95 mg C m−2 h−1, respectively.After emergence of the maize seedlings, soil respirationrates from the row became significantly higher than thosefrom the inter row (paired t test: t = 5.93, P < 0.01, n = 56).

Emission ratio of N2O-N to NO-NThe emission ratio of N2O-N to NO-N (N2O-N/NO-N)was higher after mid-July than during the period frommid-May (just after fertilizer application) to early July(Fig. 3). The mean emission ratio from the row fromjust after fertilizer application to early July was 3.0 in1999 and 1.4 in 2000, whereas the corresponding val-ues in the inter row were 5.4 and 4.4 (Table 3). Frommid-July to October, the mean ratios in 1999 and 2000were 290 and 46 in the row, respectively, and 130 and180 in the inter row. Thus, N2O-N/NO-N values in therow were lower than those in the inter row just afterfertilizer application (paired t test: t = 2.02, P = 0.06,n = 14), but they became similar after mid-July (pairedt test: t = 0.14, P = 0.89, n = 15).

Relationships between gas emission rates and environmental factorsIn the row, the N2O emission rate was significantlycorrelated only with soil temperature (Table 4). In the

inter row, the relationship between WFPS values andthe N2O emission rate was significant. In the row, theNO emission rate was positively correlated with soiltemperature, soil and soil concentrations, andnegatively correlated with WFPS values (Table 4). Inthe inter row, the NO emission rate was correlated withsoil concentration and also negatively correlatedwith WFPS values. Soil respiration rate was positivelycorrelated with soil temperature and negatively

Table 2 Air temperature, rainfall, soil temperature and water-filled pore space (WFPS) in the snow-free season from 1998 to 2000

Year (Unit) 1998 1999 2000

Climatic parameters (April–November)

Mean air temperature (οC) 13.2 13.8 13.6Rainfall (mm) 765 769 1035

RowSoil temperature

Mean (οC) 16.0 16.2 17.7Range (οC) (3.0–22.8) (6.1–24.6) (0.6–26.4)Variance 20.9 31.4 37.3anova among three years n.d. n.d. n.d.

WFPSMean (%) 50.5 47.4 48.1Variance 200 178 257anova among three years n.d. n.d. n.d.

Inter rowSoil temperature

Mean (οC) 16.0 16.3 17.4Range (οC) (2.9–23.0) (6.2–23.8) (0.6–25.6)Variance 19.7 30.7 33.9anova among three years n.d. n.d. n.d.

WFPSMean (%) 62.8 64.2 66.1Variance 224 148 233anova among three years n.d. n.d. n.d.

n.d., no difference (level of confidence was 5%).

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Figure 3 Emission ratios of N2O-N to NO-N from 1999 to2000. Triangles (�) and circles (�) denote the data collectedin 1999 and 2000, respectively. Closed and open symbolsdenote the data observed in the row and inter row,respectively. F.A. and H. denote the times of fertilizerapplication and harvest, respectively.

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correlated with WFPS values in both the row and interrow (Table 4). Moreover, the N2O-N/NO-N ratio andWFPS values were significantly correlated in both therow and inter row (Table 4). In the row, the N2O-N/NO-Nratio was also negatively correlated with soil and

concentrations.

Emissions of N2O, NO and CO2 during the snow-free seasonTotal mean N2O emissions from the row and inter rowduring the snow-free season for the 3 years were1.6 g N m−2 (0.87–2.2 g N m−2) and 1.5 g N m−2 (0.73–2.8 g N m−2), respectively, (Table 5). The total amountand seasonal pattern of N2O emissions were similar(Fig. 4) in both the row and inter row, even thoughchemical fertilizer was not applied to the inter row.

Cumulative N2O emissions from May to early July, whenthe N2O-N/NO-N ratio was relatively low, were lessthan 20%, and emissions from mid-July to October,when the N2O-N/NO-N ratio was relatively high, weremore than 80% of the total emissions during the snow-free season (Table 3, Figs 3,4). The total N2O emissionsrelative to the amount of applied N in the row and interrow ranged from 5.4% to 14% and from 24% to 94%,respectively, during the 3-year study period (Table 5).

During the snow-free season, the total NO emissionsfrom the row were greater than those from the interrow (Table 5, Fig. 4). Just after fertilizer application(from mid-May to early July), when the N2O-N/NO-Nratio was relatively low, cumulative NO emissionsaccounted for 80–90% of the total emissions duringthe snow-free season (Table 3, Fig. 3). The total NO

Table 3 Cumulative nitrous oxide (N2O) and nitric oxide (NO) emissions and the emission ratio of N2O-N/NO-N

Middle May–Early July Middle July–October

Year 1999 2000 1999 2000Row

N2O-N/NO-N emission ratioMean 3.0 1.4 290 46

Gas emissionsN2O (g N m−2) 0.34 0.15 1.77 1.45NO (g N m−2) 0.24 0.55 0.03 0.11

Cumulative gas emissions as a percentage of the total gas emission during the snow-free seasonN2O (%) 16 8.5 82 84NO (%) 89 83 10 17

Inter row N2O-N/NO-N emission ratio

Mean 5.4 4.4 130 180Gas emissions

N2O (g N m−2) 0.13 0.15 2.57 0.84NO (g N m−2) 0.04 0.02 0.01 0.03

Cumulative gas emissions as a percentage of the total gas emission during the snow-free seasonN2O (%) 4.7 6.6 91 79NO (%) 72 34 18 64

Table 4 Relationships (correlation coefficient, r) between gas emission rates and environmental factors

Log(N2O emission rate) Log(NO emission rate) Log(Soil respiration rate)Log(N2O-N/NO-N

emission rate)

Row Inter row Row Inter row Row Inter row Row Inter row

Soil temperature 0.47** 0.17 0.47** 0.27 0.76** 0.73** −0.10 0.16WFPS 0.00 0.30* −0.48** −0.32* −0.44** −0.44** 0.52** 0.55**Soil NO3-N 0.17 0.06 0.64** 0.40* 0.24 0.19 −0.57** −0.17concentrationSoil NH4-N 0.09 0.25 0.33* 0.09 –0.04 0.03 −0.33* 0.17concentration

*p < 0.05; **p < 0.01. WFPS, water-filled pore space.

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emissions relative to the amount of applied N were1.7% and 4.1% in 1999 and 2000, respectively, inthe row and 1.7% in both years in the inter row(Table 5). In both the row and inter row, cumulativeN2O-N emissions were greater than cumulative NO-Nemissions. The total N2O emissions, weighted by area,of row + inter row during the snow-free season rangedfrom 0.84 to 2.3 g N m−2, and the total emissions ofNO ranged from 0.21 to 0.51 g N m−2. The weightedtotal N2O + NO emissions from this field correspondedto approximately 20% of the amount of applied N(as chemical fertilizer and compost).

The total amount of soil respiration from the rowand inter row during the snow-free season for the 3-year

study period ranged from 0.53 to 0.82 and from 0.40 to0.50 kg C m−2, respectively (Table 6). The total amountof soil respiration from the row was larger than thatfrom the inter row. The total amount of soil respirationweighted by the area of row + inter row during thesnow-free season for the 3-year period ranged from0.50 to 0.73 kg C m−2. Annual changes in the totalamount of soil respiration were smaller than those inN2O and NO emissions. The seasonal pattern of cumu-lative soil respiration showed a sigmoidal curve (Fig. 4).The cumulative rainfall from April to June and fromJuly to September corresponded to 25% and 50%,respectively, of the total rainfall during the snow-freeseason (Fig. 4).

Table 5 Amount of applied nitrogen (N), gas emissions and maize N uptake during the snow-free season (April–November) from1998 to 2000

Year (Unit) 1998 1999 2000

Period of measurement (days) 198 199 197Row

Applied NChemical Fertilizer (g N m−2) 13.0 13.0 13.0Manure (g N m−2) 3.0 3.0 3.0

Gas emissionsN2O (g N m−2) 0.87 ± 0.09 2.17 ± 0.24 1.71 ± 0.15NO (g N m−2) ND 0.27 ± 0.16 0.66 ± 0.06N2O + NO (g N m−2) ND 2.44 ± 0.29 2.37 ± 0.16

Percentage of emitted N to applied NN2O (%) 5.4 13.6 10.8NO (%) ND 1.7 4.1N2O + NO (%) ND 15.0 15.0

Inter rowApplied N

Chemical Fertilizer (g N m−2) 0.0 0.0 0.0Manure (g N m−2) 3.0 3.0 3.0

Gas emissionsN2O (g N m−2) 0.73 ± 0.17 2.82 ± 0.86 1.07 ± 0.10NO (g N m−2) ND 0.05 ± 0.01 0.05 ± 0.02N2O + NO (g N m−2) ND 2.87 ± 0.86 1.12 ± 0.10

Percentage of emitted N to applied NN2O (%) 24.3 94.0 35.7NO (%) ND 1.7 1.7N2O + NO (%) ND 95.7 37.3

Row + Inter row†

Applied NChemical Fertilizer (g N m−2) 9.8 9.8 9.8Manure (g N m−2) 3.0 3.0 3.0Maize N uptake (g N m−2) 13 17 29

Gas emissionsN2O (g N m−2) 0.83 ± 0.08 2.33 ± 0.28 1.55 ± 0.12NO (g N m−2) ND 0.21 ± 0.12 0.51 ± 0.05N2O + NO (g N m−2) ND 2.55 ± 0.30 2.06 ± 0.13N2O + NO (% for applied N) ND 20 16

†Row and inter row widths were 75 and 25 cm, respectively (see Fig. 1). ND, not determined; ±, standard deviation.

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DISCUSSION

Seasonal pattern of N2O and NO emissionsMany researchers have reported that remarkableincreases in N2O emission rates occur just after ferti-lizer application because the nitrification process isactive after is applied to agricultural soils. Previ-ously reported values of N2O emission rates range from0.1 to 1.0 mg N m−2 h−1 (Akiyama and Tsuruta 2003;Jambert et al. 1997; Lessard et al. 1996; Minami 1997;Skiba et al. 1996; Smith et al. 1998; Thornton andValente 1996; Williams et al. 1999; Yamulki et al. 1995;Yoh et al. 1997). In some reports, the highest N2Oemission rates were observed just after fertilizer applica-tion (Akiyama et al. 2000; Akiyama and Tsuruta 2002,2003; Jambert et al. 1997; Skiba et al. 1996). In thestudy field, the maximum N2O emission rates within

1 month after fertilizer application ranged from 0.08 to0.54 mg N m−2 h−1, and the increase in N2O emissionrates just after fertilizer application in this field studywas similar to previously reported values.

In contrast, N2O emission rates just after heavy rainranged from 1.73 to 6.42 mg N m−2 h−1, values whichwere much higher than those measured just after fer-tilizer application (Figs 2a,e,4). Some previous studieshave reported a similar phenomenon. For example, aremarkable increase in N2O emission rates, higherthan that just after fertilizer application, was observedduring the harvest season when the frequency of rainwas high, for a gray lowland soil in central Hokkaido(Hatano and Sawamoto 1997; Kusa et al. 2002;Sawamoto and Hatano 2000) and for Andosols ineastern Hokkaido, Japan (Koga et al. 2004). Althoughthe N2O emission rate (0.3 mg N m−2 h−1) observedfor the Andosols in eastern Hokkaido was lower than thatobserved in the present study, the highest N2O emissionrate was observed during the harvest season after aheavy rain. However, in Honshu (the largest island ofJapan), the highest N2O emission rates have beenobserved just after fertilizer application in manyagricultural fields amended with chemical fertilizer(Akiyama and Tsuruta 2003; Tsuruta 2000). High N2Oemission rates in the harvest season, when rain fallswith a high frequency, and after heavy rain are probablycharacteristic in Hokkaido. In Hokkaido, there is nodistinct rainy season in early summer and most rain

NH4+

Figure 4 Cumulative nitrous oxide (N2O)and nitric oxide (NO) emissions, soilrespiration and rainfall (1998–2000). Rand F denote the data observed in therow and inter row, respectively. F.A.and H. denote the times of fertilizerapplication and harvest, respectively.

Table 6 Amount of soil respiration during the snow-freeseason (April–November) from 1998 to 2000

Soil respiration (kg C m−2)Plot/Year 1998 1999 2000

Period of measurement (days) 198 199 197Row 0.53 0.82 0.73Inter row 0.40 0.44 0.50Row + Inter row† 0.50 0.73 0.67

†Row and inter row widths were 75 and 25 cm, respectively.

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tends to fall in September, although there are two majorrainy seasons, in early summer and in autumn inHonshu (Kurashima 1966). Thus, the difference in theseasonal pattern of N2O emission rates may be relatedto differences in the amount and pattern of rainfall.It has also been suggested that not only in Hokkaidobut also in Honshu and other regions, high N2Oemission rates could be recorded in the harvest seasonif the conditions were suitable for denitrification, that is,frequent or heavy rain and persistence of NO3 in soil.

High NO emission rates just after fertilizer applica-tion have been observed in agricultural fields amendedwith chemical fertilizer (Akiyama et al. 2000; Akiyamaand Tsuruta 2002; Akiyama and Tsuruta 2003; Thorntonand Valente 1996; Tsuruta 2000; Veldkamp and Keller1997; Watanabe et al. 1997). Because chemical ferti-lizer was applied only to the row in the present study,the increase in NO emission rates just after fertiliza-tion occurred only from the row (Fig. 2f).

Nitrous oxide and NO production in soilSeveral studies have shown that N2O is produced byboth denitrification and nitrification, whereas NO isproduced mainly by nitrification (Bremner 1997; Dav-idson 1992). Lipschultz et al. (1981) reported that theproduction ratio of N2O-N to NO-N by nitrificationwas in the range of 0.2–1.0, but was 100 by denitrifica-tion, indicating that the activity of denitrifying bacteriawas higher than that of nitrifying bacteria when theemission ratio (N2O-N/NO-N) was relatively high. Otherstudies have shown that nitrification activity increasedin proportion to soil moisture at WFPS values less than60% and that it drastically decreased when the WFPSvalues exceeded 60%. In contrast, denitrificationactivity often remained negligible when the WFPS valueswere less than 60%, but increased dramatically whenthe values exceeded 60% (Aulakh et al. 1992; Linn andDoran 1984). Judging from these previous reports andfrom the significant relationships between WFPS valuesand N2O-N/NO-N ratios in the present study field(Table 4), denitrification was activated by high watercontent in the field.

In the row, a drastic increase in NO emission ratescoincided with an increase in soil concentrationand a decrease in soil concentration, derived fromnitrification just after fertilizer application (mid-May toearly July) (Fig. 2c,d,f). The N2O-N/NO-N ratio remainedlow during this period (Fig. 3). This suggests that nitri-fication may have been mainly responsible for N2Oand NO production just after fertilizer application.However, N2O emission rates drastically increased aftermid-July when the N2O-N/NO-N ratio increased,indicating that denitrification may have been mainlyresponsible for N2O production after mid-July.

Soil in the inter row was probably much more anaer-obic than soil in the row (Fig. 2a) because oxygen diffusionwould have been inhibited by the high water content inthe soil of the inter row. Soil concentration in theinter row was lower than that in the row because was not supplied by chemical fertilizer. These condi-tions in the inter row probably promoted denitrificationbut limited nitrification, accounting for the increase inthe N2O emission rate and the lack of an increase in theNO emission rate in the inter row (Fig. 2e,f).

The N2O-N/NO-N ratio increased after mid-July(Fig. 3). If it is assumed that N2O emitted after mid-Julywas produced by denitrification, then 80% of the totalN2O emissions was produced by denitrification (Table 3).

Heavy rain as a factor responsible for high N2O emission ratesThe annual change in the N2O emission rate was greaterthan the change in soil respiration rate (Tables 5,6 andFigs 2,4), suggesting that the annual change in thosefactors responsible for N2O emission rate was greaterthan that affecting root and microbial respiration insoil. Sawamoto and Hatano (2000) observed the sameresult in a gray lowland soil with cultivated onions incentral Hokkaido. An increase in the N2O emission rateafter wetting of dry soil has been reported in incubationstudies and dry-season investigations of savanna(Davidson 1992; Scholes et al. 1997). Other studieshave shown that annual changes in the N2O emissionrates in the 30 days after fertilizer application werecaused by changes in the rain pattern: the N2O emissionrate markedly increased after rain when no rain hadfallen just after fertilizer application (Akiyama andTsuruta 2003; Williams et al. 1999). In Hokkaido,N2O emission rates increase remarkably in the rainyseason (summer and autumn) (Koga et al. 2004; Kusaet al. 2002). These results indicate that water suppliedby rain significantly affects N2O emission. In the presentstudy, the pattern of daily and cumulative rainfall wasdifferent over the 3-year period (Figs 2,4). Therefore,variability in the amount of water added to soil by rainmay be one major reason for the considerable variationin N2O emission.

Nitrous oxide emission rates increased markedly justafter heavy rain (> 80 mm day−1) each year, but theemission rates differed greatly (Figs 2,4). In 1999 and2000, heavy rain occurred when considerable produced by nitrification still remained in the soil. Incontrast, heavy rain was also observed when relativelyless remained in the soil around harvest time(Fig. 2). Because the N2O emission rate after heavyrain is considered to have been produced by denitrifica-tion, a higher soil concentration should lead togreater N2O production through denitrification.

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Therefore, the remarkably high N2O emission rates, upto 2–6 mg N m−2 h−1, in 1999 and 2000 probably resultedfrom the promotion of N2O production by a high con-centration of soil combined with the addition ofa large amount of water to the soil by heavy rain.

Comparison of N2O and NO emissions at other sitesIn Japan, N2O emissions from upland fields for variousperiods ranged from 0.01 to 0.87 g N m−2, with mostmeasured values less than 0.1 g N m−2. Moreover, mostvalues corresponded to less than 1% of the amount ofapplied N (Akiyama and Tsuruta 2002; Akiyama andTsuruta 2003; Koga et al. 2004; Tsuruta 1997; Tsuruta2000). Akiyama and Tsuruta (2003) pointed out thatthe ratios of N2O emissions to chemical fertilizer N inJapanese Andosols were lower than those in other soilsin Japan and around the world. However, in the presentstudy, the amount of N2O emission relative to theamount of applied N ranged from 5.4% to 94.0%(Table 5). These values were markedly higher thanthose previously reported for Japanese Andosols. Kogaet al. (2004) suggested that the large difference in theratio of N2O emission to chemical fertilizer N betweenAndosols (0.36%) and gray lowland soils (2.8%; Kusaet al. 2002; Sawamoto and Hatano 2000) was causedby differences in the physical properties of the soils,such as bulk density and texture. However, the bulkdensities of the row and inter row at 0–5 cm depth were0.78 and 0.85 Mg m−3, respectively. These values arewithin reported bulk densities of Japanese Andosols(0.70–0.92 Mg m−3) where N2O emissions have beenmeasured (Akiyama et al. 2000; Koga et al. 2004). Inthe study field, an impermeable layer lay at 1.3 mdepth. As a result, the groundwater table rose to nearthe ground surface after heavy rains, when remarkableincreases in N2O emission were observed. In contrast,the Andosols where low N2O emissions were observed,were in well-drained fields (Akiyama and Tsuruta 2003;Koga et al. 2004), suggesting that a difference in waterpermeability strongly influenced N2O emission.Therefore, high N2O emission can occur from Japaneseagricultural Andosols when they are poorly drained. Inthis study, N2O emissions during the snow-free season(Table 5) were relatively high; for example, Bouwman(1996) reported that annual N2O emissions exceeded1.0 g N m−2 in only 4.5% of 249 agricultural fields.Annual NO emissions from Japan and the worldranged from 0.01 to 2.3 g N m−2, and most measuredvalues were around 0.1 g N m−2 (Akiyama and Tsuruta2002; Akiyama and Tsuruta 2003; Davidson andKingerlee 1997). Thus, NO emissions from the studyfield were relatively large compared with global data(Table 5).

CONCLUSION

The magnitude and seasonal pattern of N2O emissionrates from the row were similar to those from the interrow, even though chemical fertilizer was not applied tothe inter row. In contrast, an increase in NO emissionswas recognized only from the row. Seasonal fluctua-tions in soil and concentrations and in theemission ratio (N2O-N/NO-N) suggested that N2O andNO emitted after fertilizer application (mid-May toearly July) were mainly produced by nitrification andthat N2O emitted after heavy rain was mainly producedby denitrification. Remarkably high N2O emission ratesof up to 2–6 mg N m−2 h−1 probably resulted fromthe promotion of N2O production by a relatively highconcentration of soil together with a large amountwater added to the soil by heavy rain. Thus, high N2Oemission rates can occur from poorly drained Japaneseagricultural Andosols. The N2O and NO emissionsfrom our study field were relatively high compared withthose reported worldwide.

ACKNOWLEDGMENTS

We thank Dr Y. Ohashi (Hokkaido Agricultural Exper-iment Station), Dr K. Yoshida, Dr Y. Hayakawa and DrK. Kanazawa (National Agricultural Research Centerfor Hokkaido Region) and Dr H. Tsuruta (NationalInstitute for Agro-Environmental Science) for theirassistance in the gas chromatography analysis and forvaluable discussions. This study was partly supportedby a Japanese Grant-in-Aid for Science Research fromthe Ministry of Education (08456038) and by theGlobal Environment Research Fund from the Environ-mental Agency (Ministry) of Japan, grant B-51(6).

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