Journal of Integrative Agriculture 2016, 15(12): 28652872

Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

Assessing soil nitrous oxide emission as affected by phosphorus

and nitrogen addition under two moisture levels
Bashir Ullah, Muhammad Shaaban, HU Rong-gui, ZHAO Jin-song, LIN Shan
College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, P.R.China

Abstract
Agricultural soils are deficient of phosphorus (P) worldwide. Phosphatic fertilizers are therefore applied to agricultural soils
to improve the fertility and to increase the crop yield. However, the effect of phosphorus application on soil N2O emissions
has rarely been studied. Therefore, we conducted a laboratory study to investigate the effects P addition on soil N2O emissions from P deficient alluvial soil under two levels of nitrogen (N) fertilizer and soil moisture. Treatments were arranged
as follows: P (0 and 20 mg P kg1) was applied to soil under two moisture levels of 60 and 90% water filled pore space
(WFPS). Each P and moisture treatment was further treated with two levels of N fertilizer (0 and 200 mg N kg1 as urea).
Soil variables including mineral nitrogen (NH4+-N and NO3-N), available P, dissolved organic carbon (DOC), and soil N2O
emissions were measured throughout the study period of 50 days. Results showed that addition of P increased N2O emissions either under 60% WFPS or 90% WFPS conditions. Higher N2O emissions were observed under 90% WFPS when
compared to 60% WFPS. Application of N fertilizer also enhanced N2O emissions and the highest emissions were 141
g N2O kg1 h1 in P+N treatment under 90% WFPS. The results of the present study suggest that P application markedly
increases soil N2O emissions under both low and high soil moisture levels, and either with or without N fertilizer application.
Keywords: phosphorus, N2O emission, water filled pore space, nitrogen, greenhouse gas

1. Introduction
Nitrous oxide (N2O) is a potent greenhouse gas that has the
ability to destroy ozone (O3) layer in the stratosphere. The
concentration of N2O in the atmosphere has been increasing and reached up to 120% from 270 to 324 ppb during
1750 to 2011 (Bouwman et al. 2013). Agricultural soil is the
main source of N2O emission contributing about 60% global

Received 23 October, 2015 Accepted 22 March, 2016

Correspondence HU Rong-gui, E-mail: rghu@mail.hzau.edu.cn
2016, CAAS. All rights reserved. Published by Elsevier Ltd.
doi: 10.1016/S2095-3119(16)61353-9

N2O emission (Yamulki and Jarvis 2002). Several factors

affecting N2O emissions mainly include soil type (Davidson
et al. 2000), aeration (Law et al. 2015), moisture (Dalal et al.
2003), pH (Shaaban et al. 2015b), organic matter (Shaaban
et al. 2015a), and fertilizer (Hou et al. 2000).
N2O is mainly produced by microbial nitrification and
denitrification processes. Nitrification and denitrification in
the soils are limited by various factors, such as soil moisture
and nutrients particularly N and P (Liu and Song 2009).
Contradictory reports revealing P application effects on N2O
emissions have been documented in Sundareshwar et al.
(2003) and Mori et al. (2010a). Soil N2O emissions were
increased with an increase in availability of P to nitrifiers and
denitrifiers (Mori et al. 2010, 2013a). Sundareshwar et al.
(2003) documented that P addition caused a reduction in
soil N2O emissions through stimulating N immobilization.

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Phosphorus application reduced N2O emissions during a

2-year field experiment under Acacia mangium plantation
primarily due to the enhancement of root uptake of soil N and
water (Mori et al. 2013b). A study conducted on grassland
demonstrated that P addition had no significant changes
in nitrification rates and N2O emissions (Zhang and Han
2008). In another field study, Mori et al. (2014) recently
demonstrated P addition effects on N2O emissions by separating the response of microbial and plant root activities,
and documented that P addition did not have significant
effects on N2O emissions in root-excluded plots in remote
tropical forest sites. Similarly, P application did not stimulate
N2O emissions from Eucalyptus urophylla plantation, while
P applications with N together significantly decreased N2O
emission (Zhang et al. 2014). Contradictory reports regarding P addition effects on N2O emissions could be attributed
to different soil properties and environmental factors (Zhang
and Han 2008; Mori et al. 2013b).
Soil moisture is a critical factor controlling N2O emissions
(Butterbach-Bahl et al. 2013). Moisture represents the
presence of oxygen (O2) in the soil that controls nitrification
and denitrification (Simojoki and Jaakkola 2000). Nitrification is an oxic process while denitrification occurs under
anoxic conditions (Bateman and Baggs 2005). Increase in
soil moisture creates anoxic conditions providing feasible
conditions for denitrification occurrence and N2O emissions
(Ruser et al. 2006). Furthermore, application of N fertilizer
also inevitably enhances soil N2O emissions (Shaaban et al.
2015a, b). This is mainly due to increased substrates for
nitrifying and denitrifying bacteria producing N2O (Parkin
and Kaspar 2006).
The effects of phosphorus application on N2O emission
in P-deficient soils have not been well understood so far.
We hypothesized that P addition to soil will influence the
microbes activity and ultimately N2O emissions. Therefore,
we designed a laboratory study which aimed to investigate
P addition effects on soil N2O emissions. In addition,
effects of N fertilizer and moisture levels in combination
with P fertilizer were also investigated. Laboratory investigation of P addition effects on N2O emissions will be
worth enough since nutrient uptake by plant can affect
N2O emissions. Therefore, laboratory studies of P addition effects on N2O emissions can provide fundamental
scientific knowledge.

2. Materials and methods

2.1. Soil characteristic and analysis
Soil used in the present study was collected from cultivated
field of maize (Zea mays L.) from Wuhan, China (303459 N
and 1141600E; altitude 20 m above sea level). The soil

was collected from a depth of 020 cm, and is classified as

alluvial soil (Entisol) (Guan et al. 2011). Soil samples were
taken randomly from different places of the selected field.
After removing visible plant roots and stones, a composite
sample was obtained and stored in the plastic bags, and
shifted to laboratory. Soil was air-dried and passed through
a sieve (2 mm) before analysis. The characteristics of the
soil used in this study are presented in Table 1.
The soil texture was analyzed using pipette method, and
soil bulk density was measured by taking known volume
through steel core method (Shaaban et al. 2013b). Water
filled pore space (WFPS) of the soil was determined as the
method presented by Lin et al. (2013). Dissolved organic
carbon (DOC) was determined using deionized water (1:5
ratio of soil:water). Soil with deionized water was shaken
for 1 h on the mechanical shaker at 250 r min1. After that,
soil mixture was centrifuged at 8 000 r min1 for 5 min,
and the supernatant was filtered through a 0.45-m filter
membrane. The DOC contents were analyzed using a C/N
elemental analyzer (Vario Max, Germany) as described
by Lin et al. (2013). Soil ammonium (NH4+-N) and nitrate
(NO3-N) concentrations were extracted from soil using KCl
(1:5 of soil:1 mol L1 KCl solution) by shaking soil mixture
over 1 h on mechanical shaker at 250 r min1 as described
by Shaaban et al. (2015b). The soil mixture was filtered
through Whatman No. 40 filter paper and the extract was
analyzed using an ultraviolet spectrophotometer. Soil pH
was measured using a pH meter (pH electrode PB-10;
Sartorius AG, Germany) (Shaaban et al. 2013a). Available
P concentration was extracted from soil by adding 40 mL of
0.5 N NaHCO3 and shaking for 1 h on mechanical shaker at
250 r min1. The soil mixture was filtered through Whatman
No. 40 filter paper, and the extract was analyzed using an
ultraviolet spectrophotometer as described by Oilsen et al.
(1954).

2.2. Experimental design, gas sampling and analysis

Soil was pre-incubated for 7 days with 40% WFPS to initiate
the microbial activity. After pre-incubation, P was uniformly
applied to soil at the rate of 0 and 20 mg P kg1 as triple
super phosphate (TSP). Each treatment of P was treated
with 0 and 200 mg N kg1 as urea. Fertilizers of TSP and
urea were dissolved in distilled water and applied uniformly
to soil. After fertilizer application, soil moisture was raised
to 60 and 90% WFPS using distilled water.
Two separate sets of same treatments, each with three
replicates, as described above were prepared in the 1-L
glass flasks using 200 g soil (oven dry basis) for soil and gas
analysis. A polythene film was placed over the tops of flasks
and about 70 pin holes pierced for gaseous exchange, but to
prevent moisture loss. Treatment flasks were incubated in a

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Bashir Ullah et al. Journal of Integrative Agriculture 2016, 15(12): 28652872

chamber aerobically at a temperature of 25C in the dark for

50 days. Soil water content was kept constant throughout
the experiment by weighing the flask twice a week, and
distilled water was added if needed. Soil sub-samples were
destructively taken from flask on day 1, 5, 10, 15, 20, 25, 30,
35, 40, 45 and 50 for determination of DOC, NH4+-N, NO3-N,
and available phosphorus concentration was measured with
an interval of 10 days throughout the study.
For collecting gas samples, polythene film was removed
and all flasks were exposed to ambient air for 30 min before
gas sampling. After 30 min, all flasks were sealed gas tight
using three-way rubber septum lids containing a small plastic
pipe to allow for taking gas samples from the headspace of
flask. Tow gas samples were taken from the headspace of
flask, one immediately after closure and another after 2 h
closure of flasks using a 30-mL gas tight plastic syringe
(Shaaban et al. 2014).
During incubation period, gas samples were taken from
flasks on day 1, 2, 3, 4, 5, 6, 7, 9, 11, 13, 15, 17, 19, 21,
4, 27, 30, 37 and 50. N2O concentrations were analyzed
immediately after collecting gas samples using a gas chromatograph (7890-A; Agilent Technologies Santa Clara,
CA, USA) as described by Shaaban et al. (2015a) and flux
of N2O emission was calculated as described by Liu et al.
(2014). Cumulative N2O emission was calculated through
linear trapezoidal method (Mori et al. 2010).

2.3. Statistical analyses

All data were analyzed using three-way analysis of variance
(ANOVA) to analyze the main and interactive effects of three
factors, P, N and moisture, on N2O emission. Least significance difference (LSD) was used to find out differences
among individual treatments. All statistical analyses were

carried out using SPSS 16.00 (Chicago, USA).

3. Results
3.1. N2O emission
Addition of P, N fertilizer and moisture levels significantly
(P<0.05) influenced soil N2O emissions (Table 2). Application of P significantly (P<0.05) increased N2O emissions,
with higher magnitudes from 90% WFPS when compared to
60% WFPS (Fig. 1-A and B). Nitrogen fertilizer application
also significantly (P<0.05) increased N2O emissions and the
highest magnitude was 141 g kg1 h1 in P+N treatment
under 90% WFPS. Higher N2O emissions were observed at
the beginning of the study, and steadily declined afterwards
until end of the study. Cumulative N2O emissions were also
the highest in P+N treatment under 90% WFPS (Fig. 2-A).

3.2. Soil mineral nitrogen

Soil ammonium (NH4+-N) concentrations were significantly
(P<0.05) increased by P addition (Table 2). Soil NH4+-N
had also significant (P<0.05) difference between 60 and
90% WFPS (Fig. 3-A and B). Application of N fertilizer
significantly (P<0.05) increased soil NH4+-N concentrations and the highest concentration was 83 mg kg1 on
day 1 under 90% WFPS. High soil NH4+-N concentrations
were observed at the start of the incubation, while low
concentrations at later stage of the study (Fig. 3-A). Soil
nitrate (NO3-N) concentrations were significantly (P<0.05)
increased by P and N fertilizer additions, as well as with
increase in soil moisture. Addition of P significantly
(P<0.05) increased NO3-N concentration by up to 117 mg
kg1 after 1 day under 90% WFPS. Low NO3-N concentra-

Table 1 Chemical and physical properties of selected soil

pH
7.4

Total C (g kg1) Total N ( g kg1) Available P (mg kg1) Bulk density (g cm3) Sand (%)
23.7
1.5
10
1.1
12

Silt (%)
60

Clay (%)
28

Texture
Silty clay loam

Table 2 Results of analysis of variance (ANOVA) for the main and interactive effect of phosphorus, nitrogen and moisture on soil
variables
Factors1)
M
N
P
PN
MN
MP
MNP
1)
2)

N 2O
F-value
55.6
49.3
42.3
41.5
33.0
60.4
123.2

NH4+-N
P-value
0.000
0.000
0.003
0.019
0.004
0.001
0.002

F-value
35.3
65.1
71.1
60.9
71.6
46.2
87.8

M, soil moisture; N, nitrogen; P, phosphorus.

DOC, dissolved organic carbon.

P-value
0.001
0.000
0.000
0.017
0.005
0.003
0.001

NO3-N
F-value
P-value
45.0
0.002
35.9
0.000
61.1
0.003
89.1
0.018
91.0
0.000
81.1
0.003
71.0
0.000

P
F-value
15.0
68.9
89.0
99.2
88.2
78.8
62.1

DOC2)
P-value
0.001
0.000
0.005
0.026
0.002
0.005
0.004

F-value
22.4
20.9
44.0
29.2
31.0
45.5
67.0

P-value
0.000
0.000
0.004
0.011
0.003
0.001
0.005

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Bashir Ullah et al. Journal of Integrative Agriculture 2016, 15(12): 28652872

CK

N+P

200

B 200

180

180

160

160

N2O emission (g kg1 h1)

N2O emission (g kg1 h1)

140
120
100
80
60
40

120
100
80
60
40
20

20
0

140

10

20

30

40

50

10

Incubation time (d)

20

30

40

50

Incubation time (d)

Fig. 1 N2O emissios from soil under different moisture levels of 60% water filled pore space (WFPS, A) and 90% WFPS (B). CK,
control; N, nitrogen fertilizer; P, phosphorus fertilizer. Vertical bars denote standard error (n=3). The same as below.

CK
A

N+P

1 200

1 200
1 000

Cumulative N2O emission

Cumulative N2O emission

1 000
800
600
400
200
0

10

20
30
40
Incubation time (d)

50

800
600
400
200
0

10

20
30
40
Incubation time (d)

50

Fig. 2 Cumulative N2O emissios from soil under different moisture levels of 60% WFPS (A) and 90% WFPS (B).

tions were observed at the start of study, while increased

after two weeks of the study (Fig. 3-B).

was at the start and steadily decreased until the end of the
study (Fig. 4-A).

3.3. Available phosphorus

3.4. Dissolved organic carbon

Addition of P and N fertilizers significantly (P<0.05) enhanced available P concentration. However, 90% WFPS
yielded higher available P concentration as compared to
60% WFPS. The highest available P concentration (42
mg kg1) was observed in P application alone treatment on
day 1 under 90% WFPS. High available P concentration

Addition of P and N fertilizers and soil moisture levels had

significant (P<0.05) effects on DOC contents (Table 2).
Addition of P significantly (P<0.05) increased DOC contents
(Fig. 4-A), and higher DOC contents were under 90% WFPS
as compared to 60% WFPS. Application of N fertilizers also
significantly (P<0.05) increased DOC contents, and the

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Bashir Ullah et al. Journal of Integrative Agriculture 2016, 15(12): 28652872

CK

NO3-N concentration (mg kg1)

N+P

60% WFPS

120
100
80
60
40
20
0

10

20
30
40
Incubation time (d)

50

60

140

60% WFPS

120
100
80
60
40
20
0

NH4+-N concentration (mg kg1)

B
140

10

20
30
40
Incubation time (d)

50

60

NO3-N concentration (mg kg1)

NH4+-N concentration (mg kg1)

P
140

90% WFPS

120
100
80
60
40
20
0

140

10

20
30
40
Incubation time (d)

50

60

20
30
40
Incubation time (d)

50

60

90% WFPS

120
100
80
60
40
20
0

10

Fig. 3 Dynamics of soil NH4+-N and NO3-N concentrations under 60% WFPS (A and C) and 90% WFPS (B and D) conditions.

highest DOC content (171 mg kg1) was observed under

90% WFPS without P addition. DOC contents gradually
decreased from start to the end of the study (Fig. 4-B).

4. Discussion
Previous research has demonstrated that soil N2O emission
is influenced by various soils properties. However, the influence of different soil nutrients, particularly soil P on N2O
emission remains unclear. The present study demonstrated
that P addition increased N2O emission in P-deficient alluvial
soil. Earlier studies have shown contrasting effects of P
addition on soil N2O emissions. A laboratory experiment
conducted by Mori et al. (2010) demonstrated that P application to soil increased N2O emissions. In another study,
P-deficient soils showed low N2O emissions due to limitation
of P to denitrifiers (Mori et al. 2013a). In contrast, reduction in N2O emissions following P addition has also been
reported (Mori et al. 2014; Wang et al. 2014). Reduction in
soil N2O emissions could be due to addition of P increased
N immobilization and, therefore, decreased denitrification
and nitrification (Sundareshwar et al. 2003). Phosphorus
application reduced N2O emissions primarily due to the enhancement of root uptake of soil N during Acacia mangium

plantation in a 2-year field study (Mori et al. 2013b). Baral

et al. (2014) recently investigated that alleviation of P limitation in the soil reduced N2O emissions. The present study
showed that P addition increased soil N2O emissions under
the controlled laboratory conditions. However, field studies
should be conducted to demonstrate P addition effects on
N2O emission under natural environments.
The main factor which attributed to the higher N2O emission was an increase in available P concentrations in soil.
High available P concentrations suggest that P fertilizer
addition eliminated P limitations in soil for nitrifiers and denitrifiers, and consequently increased soil N2O emissions.
Mori et al. (2010) noted that, after P addition, available P
concentrations increased, which increased N consumption
during nitrification and denitrification, and consequently
increased N2O emissions. Increase in soil N2O emissions
following P addition could be result of stimulated metabolism
and growth of bacteria (Wang et al. 2014), which facilitated
denitrification process and consequently N2O production
(Mori et al. 2010).
Furthermore, P addition increased decomposition
of native organic matter in the soil and further released
easily available carbon, i.e., DOC. Bradford et al. (2008)
investigated that P addition to soil increased C pool due to

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Bashir Ullah et al. Journal of Integrative Agriculture 2016, 15(12): 28652872

CK

60% WFPS

40
30
20
10
0

10

Dissloved organic carbon (mg kg1)

50

20
30
40
Incubation time (d)

50

60% WFPS

30
20
10
0

10

20
30
40
Incubation time (d)

50

N+P

200

90% WFPS

160
120
80
40
0

10

60

20

30

40

50

Incubation time (d)

40

Available phosphorus (mg kg1)

50

Dissloved organic carbon (mg kg1)

Available phosphorus (mg kg1)

90% WFPS

200
160
120
80
40
0

10

20
30
40
Incubation time (d)

50

60

Fig. 4 Dynamics of available phosphorus and dissolved organic carbon under 60% WFPS (A and C) and 90% WFPS (B and D)
conditions.

decomposition of organic matter. Therefore, higher content

of DOC enhanced N2O prodution (Shaaban et al. 2015b).
Soil moisture plays a vital role in preceding several
microbial processes such as decomposition of organic
matter. High soil moisture of 90% WFPS generated higher
DOC content as compared to 60% WFPS, and these DOC
contents activated nitrifiers and denitrifiers, and thereby
N2O emission. In the current study, 60% WFPS produced
lower magnitudes of N2O emissions, while 90% WFPS produced higher N2O emissions. This implies that increased
N2O emissions under 90% WFPS was primarily because
of increased DOC which acted as substrate for microbial
growth and activities, and subsequently high N2O emissions
(Shaaban et al. 2015b).
An alternate explanation of high N2O emissions with an
increase in soil moisture could be that increasing moisture
created anoxic conditions which are favorable for microorganism producing N2O emissions (Ruser et al. 2006).
Nitrification is an aerobic while denitrification is an anaerobic
process (Simojoki and Jaakkola 2000). Anaerobic conditions under 90% WFPS created feasible environment for
denitrifying bacteria and N2O production. Therefore, we
assumed that 90% WFPS created anaerobic conditions
which produced higher magnitudes of N2O emissions as

compared to 60% WFPS. Furthermore, addition of P to

soil under 90% WFPS released more N2O emissions when
compared with 60% WFPS.
Application of N fertilizer significantly increased N2O
emissions. This was certainly because urea hydrolysis
produced higher mineral N concentration which acted as
a substrate for bacteria responsible for N2O emission.
Increased N2O emissions following urea fertilizer are not
surprising since several earlier studies have revealed similar
results (Castro et al. 2008). However, the effect of combined
application of P and N fertilizers on N2O emissions was for
the first time, investigated in the P-deficient alluvial soil in
the present study. The combined application of P and N
pronounced N2O emissions as compared to their alone
application. This was definitely because P and N fertilizer
addition diminished the P limitation, increased N for microorganism producing N2O.

5. Conclusion
Addition of P fertilizer markedly increased soil N2O emissions. Increasing soil moisture and N fertilizer application
also enhanced N2O emissions. The combined application
of P and N pronounced N2O emissions as compared to their

Bashir Ullah et al. Journal of Integrative Agriculture 2016, 15(12): 28652872

alone application. Our results provide fundamental scientific

basis for further research to explore P effects on processes
associated with N2O production. Field studies are suggested
to reveal long-term effects of P on N2O emissions.

Acknowledgements
This research work was supported by the National Basic
Research Program of China (2012CB417106), and the
National Natural Science Foundation of China (41171212).

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(Managing editor SUN Lu-juan)