ARTICLE IN PRESS

1352-2310/$ - se

doi:10.1016/j.at

�Correspondfax: +8610 825

E-mail addr

Atmospheric Environment 42 (2008) 291–302

www.elsevier.com/locate/atmosenv

N2O emission from the semi-arid ecosystem under mineralfertilizer (urea and superphosphate) and increased

precipitation in northern China

Jinfeng Zhang, Xingguo Han�

Laboratory of Quantitative Vegetation Ecology, Institute of Botany, The Chinese Academy of Sciences, Nanxincun 20,

Xiangshan, Beijing 100093, PR China

Received 13 July 2007; received in revised form 14 September 2007; accepted 15 September 2007

Abstract

Soil management and climate change affect N2O emission significantly. The semi-arid grassland in northern China is

under strong anthropogenic disturbance (fertilization and land use) and toward a 30% increase in precipitation in future.

To investigate their impacts on N2O emission, N2O fluxes were measured monthly in the grassland and abandoned

cropland under mineral fertilizer (urea and superphosphate) and increased precipitation during the growing season.

During the measured period, WFPS (water filled pore space) from all the treatments never exceeded 70%, suggesting that

nitrification was the predominant source of N2O for all the treatments. Increased precipitation induced an additional

growing season emission of 0.28–0.30 kgN2O-Nha�1 y�1. N2O emission increased linearly with nitrogen application rate

and emission factors (EFs) for grassland and abandoned cropland averaged 0.35% and 0.52%, respectively.

Superphosphate addition induced N2O emission from abandoned cropland (Po0.05), but had no significant effect in

the grassland (P40.05). Despite of substantial differences in soil properties, N2O emissions were not significantly different

between the grassland and abandoned cropland (P40.05). Increased precipitation and nitrogen application at

15 gNm�2 y�1 across the grassland and abandoned cropland of northern China will increase the growing season

emissions of 71.4–76.5 and 139.23GgN2O-N into atmosphere annually. These increased emissions are about 40% and

75% of the annual emission of 186.15GgN2O-N from untreated soils, respectively. Therefore, in the temperate semi-arid

ecosystem, abandoned cropland does not constitute a potent source for increasing N2O while the effect of nitrogen

fertilization and increased precipitation cannot be neglected from the regional or national emission.

r 2007 Elsevier Ltd. All rights reserved.

Keywords: Nitrous oxide; Precipitation; Nitrogen; Phosphorus; Grassland; Abandoned

1. Introduction

Atmospheric N2O has increased from 270 to316 ppb over 200 years (IPCC, 2001). Increasing

e front matter r 2007 Elsevier Ltd. All rights reserved

mosenv.2007.09.036

ing author. Tel.: +8610 62836283;

95771.

ess: xghan2004@hotmail.com (X. Han).

N2O is a potent threat to global environmentbecause of its strong global warming potential(320 times greater than CO2) and the depletion toozone layer (IPCC, 2001). Soil is the major source ofN2O, accounting for about 70% of total emission(Bouwman, 1990). N2O from soil is mainly pro-duced as the byproduct of microbial nitrificationand denitrification. It has been discerned that

.

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302292

anthropogenic disturbances (land use, irrigation,tillage, fertilization, etc.) to soil are mainly respon-sible for increased atmospheric N2O (IPCC, 2001).But the responses of N2O to disturbances are highlyvariable depending on the specific conditions ofstudied ecosystem (Dowrick et al., 1999; Hellebrandet al., 2003; Castaldi et al., 2004) and the sources ofN2O are different (Maljanen et al., 2003; Du et al.,2006). Thus, it is essential to examine the responsesof N2O to disturbances before exporting theoptimum mitigation choices for a certain ecosystem.

The temperate grassland represents a significantsource of N2O (Mosier et al., 1991, 1997). Thetemperate semi-arid land (mainly as grassland) innorthern China covers an area of 3.1� 108 ha,accounting for 32% of the national land area (Wanget al., 2005). Despite its large coverage, the measure-ments of N2O from this area are quite few (Du et al.,2006). Several investigations showed that cultivatedcropland emitted more N2O than the native grass-land due to the impact of agriculture practices (e.g.Mosier et al., 1997; Wang et al., 2001). But it is notclear whether the former cropland still emits moreN2O after all agriculture practices are ceased.

The semi-arid grassland in northern China isdeficient in both nitrogen (N) and phosphorus (P).Its potential as carbon stock is not exerted fully dueto the limitation of nutrition (Zhu et al., 2004). N andP addition can significantly improve the productivityand is expected to sequester more atmospheric CO2

(Chen et al., 2000; Yu et al., 2006). However, Napplication generally increases another greenhousegas—N2O emission (e.g. Zheng et al., 2004; Dusen-bury, 2006), which counterbalances the gains fromCO2 and depletes atmospheric ozone. Increasednitrification rate or N2O emission to P addition alsohave been observed in several ecosystems (Kelleret al., 1988; Bauhus et al., 1993). To date, noinformation is available about the impact of fertiliza-tion on N2O emission for this vast semi-arid area.

In addition to anthropogenic disturbances, cli-mate also affects N2O emission through soil waterand temperature (e.g. Maljanen et al., 2003;Horvath et al., 2006). Soil water affects nitrifierand denitrifier activity, nutrient concentration,oxidation–reduction conditions and gas diffusion(Weitz et al., 2001). The changes of WFPS (waterfilled pore space) cause the shift of dominant sourcefrom nitrification to denitrification, and thus adramatic increase in N2O emission (Davidson, 1992;Dobbie and Smith, 2003a). Climate model predictsthat precipitation will increase by 30% in northern

China. Considering the sensitivity of N2O to soilwater, IP (increased precipitation) may significantlyalter N2O emission, which has further importantclimate feedback (Davidson et al., 2004). It is notknown how a 30% increase in precipitation willaffect N2O emission from this area.

A field experiment was conducted in the semi-aridgrassland and abandoned cropland under mineralfertilizer and IP in northern China. The objectives ofthis study are to (1) investigate the impacts ofagriculture abandonment and fertilization (N and P)on N2O emission from northern China and (2)examine the effect of IP on N2O fluxes and evaluatethe impact of climate change on N2O emission.

2. Materials and methods

2.1. Study sites

Two study sites (native grassland and abandonedcropland) were located in the south of DuolunCounty of Inner Mongolia, northern China(4210202700N, 11611705900E). It is a typical temperatesemi-arid climate. Mean annual precipitation is389mm, 70% falling between June and August.Mean annual temperature is 1.9 1C, ranging from�17.8 1C in January to 18.8 1C in July. The grass-land was dominated by needlegrass (Stipa krylovii)and prairie sagewort (Artemisia frigida). The aban-doned cropland had been cultivated with springbarely, benne or corn over past 30 years, thenabandoned in 2000 (Zhang, 2007). The dominantspecie in the abandoned cropland was annualArtemisia capillaris. Some other characteristics ofsites were given in Table 1.

2.2. Experiment design and treatments

Three factors were included in this study: precipita-tion, N and P fertilization. Precipitation had two levels:natural precipitation and increased precipitation(IP: natural precipitation plus a simulated precipita-tion of 15mmw�1). N fertilization had four levels: 0,5 gNm�2 y�1 (N5), 10gNm�2 y�1 (N10) and15gNm�2 y�1 (N15). P fertilization had two levels: 0and 10gPm�2 y�1 (P10). Twelve treatments wereproduced in this experiment, in which the combina-tions of two N levels (N5 and N15) and P10 wereremoved: CK (control), N5, N10, N15, P10, N10P10,IP, IPN5, IPN10, IPN15, IPP10 and IPN10P10.A split-plot design was employed to assign thesetreatments: precipitation was the main plot and the

ARTICLE IN PRESS

Table 1

The physiochemical characteristics of the grassland (NG) and abandoned cropland (AC), data are the means (n ¼ 6) from 0 to 10 cm soil

layer

Site BM (gm�2) BD (gm�3) pH Organic C (%) Total N (%) NH4+-N (mgkg�1) NO3-N (mgkg�1)

May Aug. May Aug.

NG 884.6a 1.376a 7.21a 2.45a 0.238a 1.66a 3.53a 2.23a 2.47a

AC 353.8b 1.556b 7.07a 1.89b 0.187b 1.85a 3.33a 4.32b 3.49b

BM, below-ground biomass; BD, bulk density. Different superscript letters within the same column indicate statistical difference between

two sites (Po0.05).

J. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302 293

combinations of N and P (subplots) were randomlyassigned to each main plot. All the treatments werereplicated in six blocks. Fertilizer (urea and superpho-sphate) was broadcast at half the designed rate in lateMay and in middle July. Fertilization was finishedwithin a single day. Spraying irrigation device was usedto simulate IP by spraying a known amount of water(equivalent to a precipitation of 15mmw�1) weeklyfrom 22 June to 23 August.

2.3. N2O measurements

N2O fluxes were measured monthly by using aclosed static chamber method from June to Octoberin 2005 and from April to October in 2006 (excludingMay when data was not available due to instrumentproblems). Winter fluxes data were not collected dueto limited winter accessibility. One base (10 cm height)was inserted 5 cm into the soil in each plot in May2005 and taken out in December 2005. In April 2006,bases were inserted into the soil again and left therethrough the experiment. The tin plate chamber (20 cmdiameter� 20 cm height) was used to sample gases.The sampling was carried out in mid-morning. Gassamples (40ml) were drawn with syringes fitted withthree-way stopcocks from the top of chamber at 0, 30and 60min after it was placed into the base groovefilled with water. N2O concentrations were analyzedusing a gas chromatograph (HP 5890II) equippedwith ECD (electric capture detector) within 48–60h.Gas fluxes were calculated from the linear changes inchamber gas concentration over time (Wang andWang, 2003). N2O fluxes under N5, N15, IPN5 andIPN15 treatments were not determined in 2006.

2.4. The measurements of environment variables

On each gas sampling date, soil temperature at10 cm was measured with a digital thermometer. Theinitial and final air temperature was also recorded to

calculate the fluxes. One soil core was collected witha metal core of known volume from the top 10 cm ofsoil in each plot. The soil core was immediatelyplaced in a labeled airtight bag and transferred to thelab. Each soil core was weighed to obtain the freshweight and then dried for 48h at 105 1C. The driedsamples were weighed to get the dry weight. Thus,gravimetric soil moisture was available as well asbulk density. WFPS was calculated as

WFPS ¼ ðgravimetric water content� bulk densityÞ

�100

ð1� bulk density=2:65Þ

pH was determined using 1:2.5 (soil to water) extractof air-dried soil. Soil organic C was analyzed usingH2SO4–K2Cr2O7 oxidation method. Total nitrogenwas measured with an Alpkem autoanalyzer (KjektecSystem 1026 Distilling Unit, Sweden) according toKjeldahl acid-digestion method. One molar KClextract of fresh soil was used to determine NH4

+ andNO3� contents with a FIAstar 5000 Analyzer (Foss

Tecator, Denmark). pH, organic C and total N fromcontrol plots were measured at the start of theexperiment. NH4

+ and NO3� were measured twice, at

the beginning of the experiment and in the middle ofAugust 2005, respectively. All the soil cores weresampled from the top 10 cm. Below-biomass wasmeasured in middle September 2005.

2.5. Data analysis

N2O fluxes from each sampling date and cumu-lative N2O emissions were analyzed with the split-plot ANOVA to examine the effects of N, P andprecipitation. To explore the effect of time and thechanges of treatment effect with time, the split-plotANOVA with repeated measures was also employedwith time as the repeated factor. To avoid cellimbalance in 2005 dataset, we conducted thosestatistical analyses in a dataset where N5, N15,

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302294

IPN5 and IPN15 were removed. Correlation andregression analyses were used to explore therelationships of N2O with soil water and tempera-ture. The original data were log-transformed tomeet the normality before ANOVA and regressionanalysis. The split-plot ANOVAs were finished withmixed model on SPSS 13.0 for windows.

3. Results

3.1. Soil temperature and WFPS (water filled pore

space)

WFPS under natural precipitation was alwaysbelow 60% in both sites. Compared to natural

Fig. 1. N2O (a), WFPS (b) and soil temperature (c) in 10 cm in grassla

2006. These treatments were control (CK), increased precipitation (IP

(N15), P additions of 10 gNm�2 (P10), combined N and P additions

(IPN5, IPN10, IPN15, IPP10 and IPN10P10). NP: natural precipitatio

precipitation, WFPS under IP increased 0–12%(Figs. 1b and 2b) depending on the sampling date.WFPS under IP never exceeded 70%. Although soilwater content in abandoned cropland was alwayslower than the grassland, WFPS was not signifi-cantly different between them due to higher bulkdensity of abandoned cropland (Table 1, Figs. 1band 2b).

Soil temperature varied seasonally (Figs. 1c and2c). Highest soil temperature (around 26 1C in10 cm) occurred in June. Thereafter, soil temperatedecreased gradually to around 5 1C in mid-October.In mid-April, soil temperature was similar to mid-October and rose with time. Soil temperature inabandoned cropland was higher 0–3 1C than the

nd under fertilizer and precipitation treatments during 2005 and

), N additions of 5 gNm�2 (N5), 10 gNm�2 (N10), 15 gNm�2

(N10P10) and combined increased precipitation and fertilization

n.

ARTICLE IN PRESS

Fig. 2. N2O (a), WFPS (b) and soil temperature (c) in 10 cm in abandoned cropland under fertilizer and precipitation treatments during

2005 and 2006. Treatment codes as in Fig. 1.

J. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302 295

grassland depending on the sampling date (Figs. 1cand 2c).

3.2. N2O fluxes

Both grassland and abandoned cropland wereN2O sources. N2O emission from all the treatmentsshowed significant seasonal variations in both sites(Table 2, Figs. 1a and 2a). Highest N2O fluxes weremeasured in warm and wet July (2006) or August(2005). In August 2005, mean N2O emission ratesfrom the control plots of grassland and abandonedcropland were 39 and 40 mgNm�2 h�1, respectively.N2O fluxes fell nearly to zero in October or Aprilwhen soil temperature fell to around 5 1C (Figs. 1c

and 2c). N2O fluxes were considerably low in warmbut dry June. N2O seasonal variations werepositively correlated with both soil water andtemperature (Table 3).

Precipitation had a significant effect on N2O(Table 2): IP increased N2O emission in July,August and September, about 2 weeks afterstopping watering (Po0.05, Figs. 1 and 2). Nosignificant effect was found in June 2006 whenWFPS under IP was drained to a status similar tonatural precipitation and spraying irrigation hadnot been started. According to Table 4, it can becalculated an additional growing season emissionof 0.28–0.30 kgN2O-Nha�1 y�1 by IP (subtractingcumulative N2O of the control from that of IP).

ARTICLE IN PRESS

Table 2

P-values of split-plot ANOVA with repeated measures on N2O

fluxes of grassland (NG) and abandoned cropland (AC)

Sites Variation source P-values

2005 2006

NG and AC Land use 0.834 0.961

T ��� ***

Land use�T 0.302 0.353

NG N ��� ���

P 0.890 0.844

Pr ��� ��

N�P 0.484 0.405

N�Pr 0.796 0.804

P�Pr 0.743 0.521

N�P�Pr 0.552 0.855

N�T ��� ���

P�T 0.858 0.926

Pr�T ��� ��

N�P�T 0.647 0.595

N�Pr�T 0.942 0.890

P�Pr�T 0.933 0.830

N�P�Pr�T 0.949 0.913

AC N ��� ���

P �� ��

Pr ��� ���

N�P 0.860 0.234

N�Pr 0.993 0.805

P�Pr 0.393 0.763

N�P�Pr 0.934 0.977

N�T ��� ���

P�T �� �

Pr�T �� �

N�P�T 0.745 0.809

N�Pr�T 0.959 0.849

P�Pr�T 0.431 0.941

N�P�Pr�T 0.997 0.704

Pr, precipitation; T, time.�Po0.05.��Po0.01.���Po0.001.

Table 3

Person correlation coefficients between lnN2O and soil temperature an

cropland

Grassland (lnN2O)

Control N10 IP IPN10

Tsoil�10 0.631* 0.673* 0.681** 0.731*

WFPS 0.751** 0.640* 0.806** 0.687*

N10, IP and IPN10 represents urea application of 10 gNm�2 y�1, increa

(**) indicate significant correlation at Po0.05 and Po0.01, respective

J. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302296

Neither N nor P fertilization had significantinteractions with precipitation (Table 2, P40.05).

N fertilization increased N2O emission in both sites(Table 2, Figs. 1a and 2a) and interacted with time(Po0.001, Table 2). Statistical analyses month bymonth showed the effect of N fertilization wassignificant in June, July and August (Po0.05). InSeptember 2005, 2 months after the last fertilization,the effect of N fertilization was marginally significant(P ¼ 0.057) in the grassland. But it was not significantin abandoned cropland and in both sites in September2006 (P40.05). Cumulative N2O increased linearlywith N application in both sites (Fig. 4). N2Oemission from abandoned cropland was alwayshigher than the grassland under the same N rate(Table 4). The EF (cumulative N2O differencebetween fertilized plots and non-fertilized plotsexpressed as a percentage of N-fertilizer) averaged0.35% for grassland and 0.52% for abandonedcropland, respectively (Table 4). Although Naddition induced more N2O emission in abandonedcropland than the grassland (Table 4), no significantdifference was found between their control plots(Table 2, P40.05).

Phosphorus fertilization increased N2O emissionin abandoned cropland (Table 2, Fig. 2a) during thewarm months, but had no significant effect in thegrassland (Table 2, Fig. 1a). In abandoned crop-land, cumulative N2O emission from P10 treatmentwas 48% higher than that from control (Table 4).There were no interactions between N and P in bothsites (P40.05, Table 2).

4. Discussions

4.1. The control of soil temperature and water on

N2O emission

The grassland and abandoned cropland are bothsources of N2O. N2O emission from all the treatments

d WFPS (water filled pore space) in the grassland and abandoned

Abandoned cropland (lnN2O)

Control N10 IP IPN10

0.680* 0.759** 0.536* 0.782**

0.733** 0.693* 0.670** 0.686*

sed precipitation and combined N10 and IP, respectively. (*) and

ly.

ARTICLE IN PRESS

Table 4

Cumulative N2O emission (mean, n ¼ 6) and the results of split-plot ANOVA in grassland and abandoned cropland during the measured

period in 2005 and 2006

Grassland (kgN2O-Nha�1) Abandoned cropland (kgN2O-Nha�1)

2005 (EF) 2006 (EF) 2005 (EF) 2006 (EF)

CK 0.710 0.751 0.740 0.772

P10 0.763 0.792 1.098 1.042

N5 0.855 (0.290) nd 0.964 (0.448) nd

N10 1.068 (0.358) 1.095 (0.344) 1.266 (0.526) 1.293 (0.528)

N10P10 1.053 1.088 1. 62 1.677

N15 1.324 (0.409) nd 1.579 (0.559) nd

IP 1.014 1.029 1.023 1.051

IPP10 0.988 1.039 1.328 1.339

IPN5 1.08 nd 1.234 nd

IPN10 1.330 1.422 1.563 1.619

IPN10P10 1.317 1.400 1.823 1.965

IPN15 1.572 nd 1.859 nd

P-value P-value

N ** ** ** **

P ns ns * *

Precipitation * * * *

N�P ns ns ns ns

N�Precipitation ns ns ns ns

P�Precipitation ns ns ns ns

N�P�Precipitation ns ns ns ns

Treatment codes as in Fig. 1. ‘‘EF’’ stands for emission factor (%). (*) and (**) represent statistically significant at Po0.05 and 0.01,

respectively. ‘‘ns’’ indicates not significant at 0.05. ‘‘nd’’ indicates that the corresponding value was not determined.

J. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302 297

varied seasonally (Table 2, Figs. 1a and 2a). MeanN2O emission from control plots of the grasslandranged from 0 to 39 mgNm�2 h�1, well within theranges from the semi-arid grassland by Mosier et al.(1991) and Du et al. (2006). The seasonal variationof N2O was closely correlated to soil temperatureand water (Table 3, Po0.05), indicating the controlof soil temperature and water on N2O emission inthis area.

The dependence of N2O on soil temperaturewas also reported in many other studies (e.g.Dobbie and Smith, 2003b; Wang et al., 2005;Horvath et al., 2006). This can be attributed to thesensitivity of microbial activity to temperature asN2O production was mainly from microbialmediated nitrification and denitrification. When soiltemperature fell to around 5 1C, N2O emission wasnearly to zero (Figs. 1c and 2c), which agrees wellwith the threshold of 5 1C for N2O production(Dobbie and Smith, 2003a). It is also demonstratedthat both nitrification and dentrification rates arelow when soil is at 5 1C (Schmidt, 1982; Zhu andWen, 1992).

Seasonal soil water changes affect the temporalvariation of N2O in many ecosystems (Wang et al.,2005; Horvath et al., 2006). It did in the presentsemi-arid ecosystem (Table 3, Figs. 1a and 2a): themaximum N2O fluxes were observed in the wettestmonths (July or August) over 2 years. In June,although high soil temperature was favorable forN2O production, N2O fluxes were considerably low,corresponding to low WFPS. The previous studiesindicated that denitrification rates increased rapidlywhen WFPS exceeded 60%, whereas nitrificationwas the dominant source of N2O in the range of30–70% of WFPS (Davidson, 1992). During themeasured period, WFPS under natural precipitationwas always below 60% in both sites (Figs. 1c and2c), suggesting that nitrification is the dominantsource of N2O. Furthermore, NO3

�-N was alsobelow the threshold of 5mg kg�1 (Table 1) fordenitrification in unfertilized soils (Dobbie andSmith, 2003a). N2O production from nitrificationincreases with WFPS up to 60%, below whichnitrification was limited by low water content(Schmidt, 1982; Castaldi, 2000). In Fig. 3, N2O

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302298

fluxes increased with WFPS when the data fromcool months were excluded. In addition to lowprecipitation, course soil texture in this area (Li andChen, 1999) is not favorable for water retention todevelop anaerobic environment for denitrification,which can cause a sharp increase of N2O production(Castaldi et al., 2004).

IP significantly increased N2O emission over 2years (Po0.001, Figs. 1 and 2). Elevated soil watercan account for increased N2O emission. As theabove discussed, low soil water in the semi-aridecosystem is limiting to both nitrification anddenitrification. Elevated soil water can mitigate thelimitation of water to microbial processes and thusincrease N2O emission. Davidson et al. (2004)reported that the direct effect of soil water andaeration on microbial processes was responsible foraltered N2O fluxes under decreased precipitation ina moist tropic forest. WFPS under IP did not exceedthe threshold of 70% for denitrification dominance(Davidson, 1992). Therefore, IP in future willincrease N2O emission through abating waterlimitation to nitrification. But nitrification is stillthe predominant source of N2O.

4.2. The comparison of N2O emission between

grassland and abandoned cropland

The effect of agriculture conversion on N2O isrelated to the type of native ecosystem (Castaldi etal., 2004). Several investigations in the temperatesemi-arid ecosystem indicated that cultivated crop-land emitted more N2O than the grassland due toincreased N supplement from agriculture practices,

Fig. 3. Relationship between N2O fluxes and water filled pore space (W

10 gNm�2 y�1), IP (increased precipitation) and IPN10 (combined N1

tillage, the corporation of crop residual, fertilizationand fallowing, etc. (e.g. Mosier et al., 1997; Wanget al., 2001). In this study, N2O emission inabandoned cropland has returned to a level similarto the grassland over 5 years since agriculturepractices were ceased, which agrees well with theresult of the warm season in CRP (conservationreserve program) site by Mosier et al. (1997). Bycontrast, Maljanen et al. (2007) found that theending of agriculture activity did not reduce N2Oemission from croplands on boreal organic soils.This difference may be related to soil N supply oftwo ecosystems. In organic soils, N2O production isnot limited by N due to native rich N pool(Maljanen et al., 2003, 2007). Thus, increased ordecreased N with adoption or abandonment ofagriculture practices does not affect N2O emission.But in the semi-arid grassland, soil is poor in N andN2O production is limited by N (Mosier et al.,1991). When more mineral N was induced byagriculture activities, nitrification is promoted andhence increased N2O emission (Mosier et al., 1997;Wang et al., 2001). After agriculture activities stop,N2O emission will decrease due to reduced Nsupplement with agriculture abandonment.

Similar nitrification rates can account for thesimilarity in N2O between two sites. Despite ofsubstantial differences in soil properties (Table 1),nitrification rates were not significantly differentbetween the grassland and abandoned croplandaccording to the results from the same sites byZhang (2007). Compared to the grassland, formercultivation in abandoned cropland has reducedavailable organic C and N pool (Table 1), which

FPS) in 0–10 cm soil layer from control, N10 (urea application of

0 and IP) treatments in grassland and abandoned cropland.

ARTICLE IN PRESS

Fig. 4. Relationship between cumulative N2O (n ¼ 6) and N

application rate in grassland and abandon field in 2005. (*) and

ns indicate statistically significant and not significant at Po0.05,

significantly. NP and IP stand for natural precipitation and

increased precipitation, respectively.

J. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302 299

are negative for nitrification and N2O (Bouwman,1990; Li et al., 2001), while, on the other hand,higher soil temperature and less root competition(Table 1) for NH4

+ are positive for nitrification(Bowden et al., 1991). Maybe, it is the offset of thesepositive and negative impacts that led to similarnitrification rates between two sites and thus N2Oemission. Nitrification rate is a good index indicat-ing N2O variations among the sites (Bowden et al.,1991; Mosier et al., 1997). It well indicated the sitevariation of N2O in this study.

4.3. N application effect

N application generally increases N2O emissionexcept for in the N-rich ecosystems (Maljanen et al.,2003). Urea addition increased N2O emission inboth sites (Figs. 1a and 2a), implying the limitationof N to N2O production in this area. N2O emissionincreased with N application rate (Fig. 4).

The relationship between cumulative N2O and Napplication rate was linear (Fig. 4), suggesting thefeasibility of estimating N2O with N rate. However,EF, the fraction of nitrogen input released as N2Owithin the current seasonal or annual period (IPCC,2000), is highly variable, depending on climate, soiltype, land cover and management (Hellebrandet al., 2003; Zheng et al., 2004). A monthly samplingfrequency may not be sufficient for calculating EFdue to the temporal variation of N2O (Smith andDobbie, 2001; Venterea et al., 2003). But oursampling points covered the typical environmentcharacteristics (soil temperature and water) duringthe measured period and the sampling schedule ofabout a month after fertilization excluded both theimmediate peak and the latter bottom followedfertilization event (Smith and Dobbie, 2001). Thus,we followed the calculation method by Bowdenet al. (1991) and Venterea et al. (2003) to estimatethe seasonal N2O emission: each sampling date wasconsidered the midpoint of a sampling period andthe net season flux was the sum of all samplingperiods. The cumulative N2O from the control plotsof grassland was around 0.7 kgNha�1 (Table 4),comparable to the mean of the period from 2001 to2003 by Du et al. (2006). The calculated EFaveraged 0.35% for grassland and 0.52% forabandoned cropland (Table 4), respectively. TheseEFs, similar to 0.3% modeled by Li et al. (2001) and0.08–0.45% measured by Dusenbury (2006) in thesemi-arid Northern Great Plain, fell into the lowerrange of 0.001–6.8% reviewed by Bouwman (1990)

and 0.1–7.3% by Mosier and Kroeze (1999).Relatively small EFs are related to low soil waterbecause it limits the development of anaerobicenvironment and thus denitrification, which hasmuch higher magnitudes of N2O emission thannitrification. Different EFs in the grassland andabandoned cropland (Table 4) indicate the depen-dence of EF on succession stage and higher EF inthe early succession stage than the late. High EF inabandoned cropland may be related to more NH4

+

for nitirification due to less root competition formineral N (Bowden et al., 1991).

4.4. P application effect

P addition had no significant effect in thegrassland (Table 2, Fig. 1a), but induced N2Oemission from abandoned cropland (Table 2,Fig. 2a). In 2006, we changed the locations ofsampling base within the plot. The result was stillsimilar to 2005 (Table 2). Furthermore, N2O fluxesfrom the combinations of N10 and P10 weresignificantly higher than N10 treatment in aban-doned cropland (Fig. 2a). So we excluded thepossibility of occasional spatial heterogeneity andconcluded P addition increased N2O emission inabandoned cropland.

Enhanced N2O emissions to P addition wereobserved in aerobic soils by Minami and Fukushi(1983) and in the tropic forest by Keller et al. (1988).Furthermore, Bauhus et al. (1993) and Falkiner

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302300

et al. (1993) found that P application promotednitrification in several forest soils. In contrast,Sahrawat et al. (1985) in six acid forest soils andSteudler et al. (2002) in tropic forests and pasturesobserved no significant effects. Reviewing theprevious results, the effects of P on N2O emissionsare site specific. Different effects in the two sites alsodemonstrated this. To date, the mechanisms forincreased N2O emission to P are not clear. It isdifficult to give the reasons for different responsesbetween two sites. But these positive responsessuggested that P may play an important role inincreasing N2O due to extensive application of Pfertilizer. The mechanisms of increased N2O to Pneed to be explored further.

4.5. The potential of increased precipitation and N

fertilization for increasing N2O emission from the

semi-arid ecosystem

The impact of fertilization and IP on winter N2Ofluxes were not known due to the absence of dataduring that period. The above analysis has shownthat IP affected N2O emission mainly duringthe growing season and the effect of fertilizationdisappeared within about 2 months after N applica-tion. Thus, we assumed no significant impact of IPand fertilization on winter N2O fluxes. According toTable 4, it can be calculated an additional emissionof 0.28–0.30 kgN2O-Nha�1 y�1 by IP and averageEFs of 0.35% and 0.52% for grassland andabandoned cropland, respectively. Assuming thatinduced emission is the same across the semi-aridgrassland (2.34� 108 ha) and abandoned cropland(0.21� 108 ha) in northern China, IP and N applica-tion at 15 gNm�2 will increase 71.4–76.5 and139.23GgN2O-N emission into atmosphere an-nually. These increased emissions are about 40%and 75% of the annual emission of 186.15GgN2O-Nfrom the untreated grassland and abandoned crop-land of northern China (Du et al., 2006). Comparedto N applications of 26.6–78.2 gNm�2 y�1 from cropproduction, an application rate of 15gNm�2 y�1 isnot high, just close to the national average rate of12 gNm�2 y�1 (Zheng et al., 2004). The annualemissions, 257.55–262.65GgN2O-Ny�1 (71.4–76.5plus 186.15) under IP and 325.38GgN2O-Ny�1

(139.23 plus 186.15) under 15 gNm�2 y�1, can equaleven exceed 275GgN2O-Ny�1 from heavily ferti-lized cropland in China (Zheng et al., 2004) andbecome a very important source of the nationalemission inventory. Therefore, IP and N fertilization

in semi-arid northern China can make a substantialcontribution to the regional and national N2Oemission and their roles in N2O budget cannot beneglected.

5. Conclusions

There is a substantial seasonal variation in N2Ofluxes caused by seasonal soil temperature andwater changes in the temperate semi-arid ecosystem.Due to low precipitation and course soil texture,WFPS in the semi-arid ecosystem is always very loweven under IP (o70%), suggesting that nitrificationis the dominant source of N2O in the semi-aridecosystem.

The abandoned cropland does not constitute apotent source for increasing N2O while the effects ofnitrogen fertilization and IP cannot be neglected. IPand N application of 15 gNm�2 y�1 across thegrassland and abandoned cropland will increaseN2O emission by 40% and 75%, respectively. Theemissions under IP and 15 gNm�2 y�1 will equal orexceed the emission from croplands and become avery important part of the national inventory.

Acknowledgments

This research was funded by an InnovativeResearch Group Project of National NaturalScience Foundation of China (NSFC, No. 30521002).Thanks to researchers Xingguo Han and ShiqiangWan for the experiment design. Anonymous re-viewers and editors are much thanked for providingvaluable comments and writing improvement onearlier versions of this manuscript.

References

Bauhus, J., Khanna, P.K., Raison, R.J., 1993. The effect of fire

on carbon and nitrogen mineralization and nitrification in an

Australian forest soil. Australian Journal of Soil Research 31,

621–639.

Bouwman, A.F., 1990. Exchange of greenhouse gases between

terrestrial ecosystems and the atmosphere. In: Bouwman,

A.F. (Ed.), Soils and the Greenhouse Effect. Wiley,

New York, pp. 249–279.

Bowden, R.D., Melillo, J.M., Steudler, P.A., 1991. Effects of

nitrogen addition on annual nitrous fluxes from temperate

forest soils in the northeastern United States. Journal of

Geophysical Research 96, 9321–9328.

Castaldi, S., 2000. Responses of nitrous oxide, dinitrogen and

carbon dioxide production and oxygen consumption to

temperature in forest and agricultural light textured soils

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302 301

determined by model experiment. Biology and Fertility of soil

32, 67–72.

Castaldi, S., De Pascale, R.A., Grace, J., Nikonov, N., Montes,

R., San Jose, J., 2004. Nitrous oxide and methane fluxes from

soils of the Orinoco savanna under different land uses. Global

Change Biology 10, 1947–1960.

Chen, M., Bao, Y., Meng, H., He, J., 2000. The study on

fertilization on artificial Grassland. Grassland of China 22,

20–25.

Davidson, E.A., 1992. Sources of nitric oxide and nitrous oxide

following wetting of dry soil. Soil Science Society of America

Journal 56, 95–102.

Davidson, E.A., Ishida, F.Y., Nepstad, D.C., 2004. Effects of an

experimental drought on soil emissions of carbon dioxide,

methane, nitrous oxide, and nitric oxide in a moist tropical

forest. Global Change Biology 10, 718–730.

Dobbie, K.E., Smith, K.A., 2003a. Impact of different forms of N

fertilizer on N2O emissions from intensive grassland. Nutrient

Cycling in Agroecosystems 67, 37–46.

Dobbie, K.E., Smith, K.A., 2003b. Nitrous oxide emission

factors for agriculture soils in Great Britain: the impact of

soil water filled pore spore space and other controlling

variables. Global Change Biology 9, 204–218.

Dowrick, D.J., Hughes, S., Freeman, C., Lock, M.A., Reynolds,

B.R., Hudson, J.A., 1999. Nitrous oxide emissions from a

gully mire in mid-Wales UK, under simulated summer

drought. Biogeochemistry 44, 151–162.

Du, R., Lu, D., Wang, G., 2006. Diurnal, seasonal, and inter-

annual variations of N2O fluxes from native semi-arid

grassland soils of inner Mongolia. Soil Biology and Biochem-

istry 38, 3474–3482.

Dusenbury, M.P., 2006. Nitrous oxide emissions from a northern

Great Plains soil as influenced by nitrogen fertilization and

cropping systems. M.S. Thesis, Montana State University,

Bozeman, MT.

Falkiner, R.A., Khanna, P.K., Raison, R.J., 1993. Effect of

superphosphate addition on nitrogen mineralization and

nitrification in several forest soils. Australian Journal of Soil

Research 31, 285–296.

Hellebrand, H.J., Kern, J., Scholz, V., 2003. Long term studies on

greenhouse gas fluxes during cultivation of energy crops on

sandy soils. Atmospheric Environment 37, 1635–1644.

Horvath, L., Fuhrer, E., Lajtha, K., 2006. Nitric oxide and

nitrous oxide emission from Hungarian forest soils; linked

with atmospheric N-deposition. Atmospheric Environment

40, 7786–7795.

IPCC, 2000. Agriculture. In: Good Practice Guidance, Uncer-

tainty Management in National Greenhouse Gas Inventories.

IPCC/IGES, Kanagawa, Japan.

IPCC, 2001. Climate Change 2001: The Scientific Basis,

Summary for Policymakers. Cambridge University Press,

Cambridge, 12pp.

Keller, M., Kaplan, W.A., Wofsy, S.C., da Costa, J.M., 1988.

Emissions of N2O from tropical forest soils: response to

fertilization with NH4+, NO3

�, and PO43�. Journal of

Geophysical Research 93, 1600–1604.

Li, S., Chen, Y., 1999. Study on the soil water dynamic and

physical characteristic of chestnut soil in Xilin River Basin.

Grassland of China 3, 71–76.

Li, C., Zhuang, Y., Cao, Y., Crill, M.P., Dai, Z., Frolking, S.,

Salas, W., Song, W., Wang, X., 2001. Comparing a process-

based agro-ecosystem model to the IPCC methodology for

developing a national inventory of N2O emissions from arable

lands in China. Nutrient Cycling in Agroecosystems 60,

159–175.

Maljanen, M., Liikanena, A., Silvolab, J., Martikainen, P.J.,

2003. Nitrous oxide emissions from boreal organic soil under

different land-use. Soil Biology and Biochemistry 35, 1–12.

Maljanen, M., Liikanena, A., Silvolab, J., Martikainen, P.J.,

2007. Greenhouse emission from cultivated and abandoned

organic cropland in Finland. Boreal Environment Research

12, 133–140.

Minami, K., Fukushi, S., 1983. Effects of phosphate and calcium

carbonate application on emission of N2O from soils under

aerobic conditions. Soil Science and Plant Nutrition 29,

517–524.

Mosier, A.R., Kroeze, C., 1999. Contribution of agroecosystems

to the global atmospheric N2O budget. In: Desjardins, R.L.,

Keng, J.C., Haugen-Kozyra, K. (Eds.), Proceedings of

International Workshop on Reducing N2O Emission from

Agroecosystems, Canada, 3–5 March 1999. Banff, Alberta,

Canada.

Mosier, A.R., Schimel, D.S., Valentine, D.W., Bronson, K.,

Parton, W.J., 1991. Methane and nitrous oxide fluxes in

native, fertilized and cultivated grasslands. Nature 350,

330–332.

Mosier, A.R., Parton, W.J., Valentine, D.W., Ojima, D.S.,

Schimel, D.S., Heinemeyer, O., 1997. CH4 and N2O fluxes

in the Colorado shortgrass steppe 2. Long-term impact of

land use change. Global Biogeochemical Cycles 11, 29–42.

Sahrawat, K.L., Keeney, D.R., Adams, S.S., 1985. Rate of

aerobic nitrogen transformations in six acid climax forest soils

and the effect of phosphorus and CaCO3. Forest Science 31,

680–684.

Schmidt, E.L., 1982. Nitrification in soil. In: Stevenson, S.J.

(Ed.), Nitrogen in Agricultural Soils. ASA, CSSA, and SSSA,

Madison, WI, pp. 253–288.

Smith, K.A., Dobbie, K.E., 2001. The impact of sampling

frequency and sampling times on chamber-based measure-

ments of N2O emissions from fertilized soils. Global Change

Biology 7, 933–945.

Steudler, P.A., Garcia-Montiel, D.C., Piccolo, M.C., Neill, C.,

Melillo, J.M., Feigl, B.J., Cerri, C.C., 2002. Trace gas

responses of tropical forest and pasture soils to N and P

fertilization. Global Biogeochemical Cycles 16, 7-1-7-12.

Venterea, R.T., Groffman, P.M., Verchot, L.V., Magill, A.H.,

Aber, J.D., Steudler, P.A., 2003. Nirogen oxide emission from

temperate forest receiving long-term nitrogen input. Global

Change Biology 9, 346–357.

Wang, Y., Wang, Y., 2003. Quick measurement of CH4, CO2 and

N2O emission from a short-plant ecosystem. Advances in

Atmospheric Sciences 20, 842–844.

Wang, Y., Ji, B., Huang, Y., Hu, Y., Wang, Y., 2001. Effects of

grazing and cultivating on emission of nitrous oxide, carbon

dioxide and uptake of methane from Grasslands. Environ-

ment Science 22, 7–13.

Wang, Y., Xue, M., Zheng, X., Ji, B., Du, R., Wang, Y., 2005.

Effects of environmental factors on N2O emission from and

CH4 uptake by the typical grasslands in the Inner Mongolia.

Chemosphere 58, 205–215.

Weitz, A.M., Linder, E., Frolking, S., Crill, P.M., Keller, M.,

2001. N2O emissions from humid tropical agricultural soils:

effects of soil moisture, texture and nitrogen availability. Soil

Biology and Biochemistry 33, 1077–1093.

ARTICLE IN PRESSJ. Zhang, X. Han / Atmospheric Environment 42 (2008) 291–302302

Yu, Z., Zeng, D., Jiang, F., Fan, Z., Chen, F., Zhao, Q.,

2006. Responses of key carbon cycling processes to the

addition of water and fertilizers to sandy grassland in

sem-arid region. Journal of Beijing Forestry University 28,

45–50.

Zhang, X., 2007. Effects of land use (management) types on soil

net nitrogen transformation in agro-pastoral ecotone. Ph.D.

Thesis, Institute of Botany, the Chinese Academy of Science,

Beijing, China.

Zheng, X., Han, S., Huang, Y., Wang, Y., Wang, M., 2004. Re-

quantifying the emission factors based on field measurements

and estimating the direct N2O emission from Chinese crop-

lands. Global Biogeochemical Cycles 18 (2), GB2018.

Zhu, Z., Wen, Q., 1992. Nitrogen in soils of China. Jiangsu

Science and Technology Publishing House, Nanjing, China.

Zhu, Y., Han, Y., Wu, J., 2004. Effect of agricultural practices on

soil organic carbon dynamics. Chinese Journal of Soil Science

35, 248–251.