Environmental Science and Pollution Research

https://doi.org/10.1007/s11356-019-07571-z

RESEARCH ARTICLE

Fertilizer management through coated urea to mitigate greenhouse

gas (N2O) emission and improve soil quality in agroclimatic zone
of Northeast India
Nirmali Bordoloi 1 & Kushal Kumar Baruah 2 & Barbie Hazarika 3

Received: 29 March 2019 / Accepted: 29 December 2019

# Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Agricultural soils are an important source of greenhouse gas nitrous oxide (N2O) emission. The comprehensive effects of
nitrogen fertilizer management on N2O emission from paddy fields of India have not been evaluated under field conditions. A
2-year field study was conducted to evaluate the effect of different nitrogen fertilizers, namely, conventional fertilizer (NPK),
starch-coated urea (SCU), neem-coated urea (NCU), and normal urea alone (NUA) on soil quality, grain yield, and N2O emission
from rice field. Gas samples were collected from the field at weekly intervals by static chamber technique and analyzed in a gas
chromatograph. During the crop-growing season, the application of NPK resulted in the highest cumulative N2O emission
(2.49 kg N2O–N ha−1) followed by NUA (2.34 kg N2O–N ha−1), NCU (2.20 kg N2O–N ha−1), and SCU (1.97 kg N2O–
N ha−1). As against the application of conventional fertilizer (NPK), the application of SCU and NCU reduced the total N2O
emission by 21% and 12%, respectively (p < 0.05), during the rice-growing period. The results indicate a good correlation of N2O
emissions with soil organic carbon, soil mineral nitrogen, and urease activity (p < 0.05) at different stages of crop growth.
Application of SCU significantly increased the rice grain productivity by 12%, 10%, and 3% over NPK (control), NCU, and
NUA respectively without affecting the soil quality and nutrient status. The use of SCU improved the nitrogen use efficiency
(NUE) and was the effective substitute for conventional fertilizer in terms of reducing N2O emissions from tropical rice paddy.

Keywords Nitrous oxide . Starch-coated urea . Soil urease activity . Nitrogen use efficiency

Introduction atmospheric temperature and global climate change. Among

the greenhouse gases, N2O contributes to 8% of the radiative
Nitrous oxide (N2O) is a potent greenhouse gas, responsible forcing at the global scale (Henault et al. 2012). Although
for the destruction of the stratospheric ozone (O3) layer N2O alone accounts for around 0.03% of the total GHG emis-
(Ravishankara et al. 2009). It also contributes to rising sions, it nearly has a 298-fold greater potential for global
warming effects than that of CO2 in a time horizon of
Responsible editor: Philippe Garrigues 100 years (Thomson et al. 2012; IPCC 2013). The concentra-
tion of atmospheric N2O has increased from the pre-industrial
Electronic supplementary material The online version of this article
value of 270 ppb to the pre-industrial value of 319 ppb in 2005
(https://doi.org/10.1007/s11356-019-07571-z) contains supplementary
material, which is available to authorized users. and 324 ppb in 2011(IPCC 2013).
Agricultural soils are responsible for more than one third of
* Kushal Kumar Baruah N2O emission and have contributed approximately 4.1 Tg
[email protected]; [email protected] N2O–N year−1 or 66% of total gross anthropogenic emissions
(UNEP 2013). Rice fields contribute approximately 11% of
1
Department of Environmental Sciences, Central University of global agricultural N2O emissions (Wang et al. 2011; Hussain
Jharkhand, Ranchi, Jharkhand 835205, India et al. 2015). Application of synthetic nitrogen (N) fertilizer in
2
Department of Environmental Science, Tezpur University, rice fields is a common practice of the farmers. This is likely to
Tezpur, Assam 784028, India contribute to increase global warming through enhanced emis-
3
Department of Chemical Engineering, Centre of Environment, Indian sion of N2O into the atmosphere (Trinh et al. 2016). The
Institute of Technology Guwahati, Guwahati, Assam 781039, India application of N to soils stimulates N2O production by way
 Environ Sci Pollut Res

of biochemical processes such as nitrification (aerobic) and country’s food security and is a key source of livelihood and
denitrification (anaerobic) (Akiyama et al. 2010). The impact employment. Cultivation of rice contributes to a substantial
of increasing levels of N2O on future global climate change amount of N2O production and emission to the atmosphere
has made it necessary to mitigate agricultural N2O emissions. (Pathak 2015). Several reports claim that application of neem
Changes in N fertilizer management practices like fertilizer products and neem-coated urea in agricultural fields can re-
form, amount, and fertilization method (Lin et al. 2010; Ma duce N2O emission (Kiran and Patra 2003; Malla et al. 2005).
et al. 2010) may influence and reduce N2O emissions from However, there are variations in results across the sites due to
agricultural soil. differences in environmental factors. To the best of our knowl-
In order to decrease the N2O emission by increasing the edge, literature on the use of starch as a carrier in a controlled-
nitrogen use efficiency (NUE), controlled-release fertilizers release system from the Indian subcontinent is inadequate. It is
(CRF) or slow-release fertilizers (SRF) can be used as effec- therefore imperative to take measures to reduce the N2O emis-
tive mitigation options having minimum environmental im- sion from rice fields of different regions of India. N2O emis-
pact (Shoji et al. 2001; Akiyama et al. 2010; Li et al. 2015). sions from rice fields may be reduced by applying slow-
CRFs or SRFs are often used to increase NUE and to allow N release urea fertilizers while maintaining soil health and crop
assimilation over extended periods of time. As compared to productivity. The objective of the present study was to study
normal or conventional fertilizers, CRFs and SRFs ensure the effect of slow-release urea-based fertilizers on N2O emis-
adequate nutrition during the entire crop-growing period and sions from tropical rice field. In addition, the impact of differ-
reduce the quantity of N loss to the environment (Oliet et al. ent forms of nitrogenous fertilizers on soil quality and rice
2004). Both natural and synthetic polymers are used for grain productivity was evaluated. Attempts were also made
controlled-release application. Starch is one type of encapsu- to determine the appropriate method of increasing grain pro-
lating polymers used to encapsulate the fertilizer granules to ductivity and to mitigate N2O emissions in tropical rice fields.
slow down the rate of fertilizer release. It is easily available,
less expensive, and renewable and its degradation products are
nontoxic (Lu et al. 2009). Therefore, it is ideal to use starch as Materials and methods
a carrier in a controlled-release system. The release of the
active agent, i.e., urea, can be controlled by cross-linking of Study site and soil properties
starch to provide a network structure. The intensity of the
network structure or cross-linking density depends on various A field experiment was conducted for two consecutive sea-
cross-linking agents like calcium chloride, glutaraldehyde, sons (2013 and 2014) at the north bank plain agroclimatic
and citric acid, which in turn may control the release of en- zone of Assam, India, inside the Tezpur University campus
capsulated material from starch matrix. Crosslinking agents (26° 42′ N, 92° 499′ E). The soil is characterized as recent and
form bridges among the polymer chains (of starch) and thus old alluvium soil (Typic Endoaquepts) with sandy to sandy-
make it water resistant, solvent resistant, and thermal resistant. loam texture and slightly acidic to moderately acidic soil pH
Many reports (Kumbar et al. 2001; Han et al. 2009) have been (5.5). The basic soil physicochemical properties of the site
cited in the literature regarding the use of cross-linked starch before the start of the experiment (0–15-cm depth) are as
in agriculture. follows: sand, 55.38%; silt, 17.5%; clay, 27.12%; soil organic
Besides starch, neem (Azadirachta indica) leaves are used (carbon) C, 10.4 g kg −1 ; mineralizable (nitrogen) N,
for urea coating to improve and maintain the fertility of soil 155.15 kg ha−1; available (phosphorous) P, 30.66 kg ha−1;
(Lokanadhan et al. 2012). Neem is a medicinal plant grown available (potassium) K, 255.79 kg ha−1; soil bulk density,
widely in India and is known for its herbicidal use and is 1.24 Mg m−3; and water holding capacity, 47.20%.
utilized in rice cultivation (Lokanadhan et al. 2012). In addi-
tion to various insecticidal properties, neem products are Field management and experimental design
known to have an inhibitory effect on nitrification
(Majumdar et al. 2002; Datta and Adhya 2014). Neem urea The experimental field was plowed, puddled thoroughly to
coating agents retard the activity of bacteria like Nitrobacter 15-cm depth and leveled properly before transplanting rice.
and Nitrosomonas. Neem triterpenes inhibit the activity of Twenty plots (size; 4 m × 4 m) were prepared, keeping a gap
nitrifying bacteria resulting in the delayed conversion of of 0.5 m between plots. Seeds of a high-yielding rice variety,
ammoniacal-N into nitrite-N (Kiran and Patra 2003). Lachit, recommended by the Department of Agriculture,
Rice is one of the major staple foods and consumed widely Government of Assam, India, were sown in a separate nursery
across the globe. Globally, 80% of rice is grown by small bed in the month of March 2013 and 2014. Thirty-day-old
farmers in developing nations, and in India rice is grown seedlings were transplanted (2 seedlings per hill) into the ex-
widely in an area of more than 42.7 million hectares (DAC perimental plots in April 2013 and 2014 with a spacing of
2014). In India, rice production is intimately linked to the 20 cm between rows and 15 cm between plants. Four
Environ Sci Pollut Res

treatments of fertilizers were applied in the field in a random- N2O sampling and measurement
ized block design with five replications. The treatments were
(i) conventional fertilizer (NPK), at a rate recommended by The fluxes were measured at 7-day intervals by using static
the Department of Agriculture, Government of Assam, India; chamber technique and gas chromatography methods (Wang
(ii) starch-coated urea (SCU); (iii) neem-coated urea (NCU); et al. 2011). The chambers of 50 cm, 30 cm, and 90 cm (length
and (iv) normal urea alone (NUA), i.e., urea without coating × width × height) made of 6-mm-thick acrylic transparent
and without phosphorous and potassium. Field management sheets were used for gas sampling. In each sampling plot, U-
practices like weeding and cleaning and plant protection mea- shaped aluminum channels (50 cm × 30 cm) were inserted
sures against insect pests were uniformly maintained during into soil to a depth of 15 cm to accommodate the chambers.
the experimental period. The chambers were placed on the channels at the time of
sampling. During gas sampling, the aluminum channel was
filled with water, which acted as air seal when the chamber
Preparation of starch-coated urea was placed on the channel. Gas samples were collected from
the chambers by airtight syringe (50-ml volume) at an interval
Starch-coated urea was prepared by following the procedure of 15 min (0, 15, 30, and 45 min) between 9.00 and 11.00 a.m.
of Chowdary and Chaithanya (2010) with little modification. on every sampling day. N2O fluxes were calculated from the
Five grams of starch was dissolved in water (25 ml) and heat- linear increase in N2O concentration inside the chamber dur-
ed at 70–75 °C until the solution became clear. Then, 95 g of ing the gas sampling period (Parashar et al. 1996). Gas sam-
urea was dissolved in 30 ml of water and the solution was ples were brought to the laboratory immediately after sam-
heated in order to obtain a clear solution. Starch solution pling and analyzed for N2O concentrations using gas chro-
was added to the urea solution under constant stirring. This matograph (Varian 3800, USA) fitted with an electron capture
was followed by addition of CaCl2 solution (1 g dissolved in detector (ECD) and a stainless steel Chromopack capillary
minimum quantity of water). This mixture was heated further column (50 cm long, 0.53 mm outside diameter, 1 μm inside
under constant stirring for 30 min in order to obtain the cross- diameter). Column, injector, and detector temperature of ECD
linked starch-urea polymer. The whole matrix was cooled, were 80, 200, and 300 °C, respectively. Carrier gas was pure
ground to a powder, and kept for subsequent application in N2 (99.999%) with a flow rate of 15 ml min−1. GC response
the experimental field. was calibrated using certified N2O standard obtained from
National Physical Laboratory, New Delhi, India.
Seasonal cumulative N2O emissions for the entire crop
Fertilization and irrigation schedule growth period were computed by the method of Ma et al.
(2009) using the following formula:
The fertilizer NPK was applied at a rate of 40:20:20 kg of
Cumulative N 2 O emission ¼ ∑ni¼1 ðRi  DiÞ
N–P2O5–K2O ha−1 in the form of urea (N), single super
phosphate (P), and muriate of potash (K) as recommended where Ri is the mean gas emission; Di is the number of days
by the Department of Agriculture, Government of Assam, between two sampling intervals, i.e., 7 days; and n is the total
India. The one third of N (as urea, 13.33 kg ha−1) was number of the measurements made during the experiment
applied as basal dose by broadcasting before last plowing (n = 19). The cumulative N2O emission obtained from the
in NPK (treatment 1) and urea alone (treatment 4). The above equation is expressed in kilograms of N2O–N ha−1.
remaining portion of N one third (13.33 kg ha−1) was
applied at 28–35 and the other one third (13.33 kg ha−1)
of N was applied during 56–70 days after transplanting Soil sampling and analysis
(DAT) of the crop as per the package of cultivation. Forty
kilograms ha−1 of SCU and NCU was applied in a way One field soil sample was collected before the start of the
similar to NPK application in three split doses as de- experiment randomly from 4 different locations of the exper-
scribed above. In the NPK-, SCU-, and NCU-treated imental field with the help of soil core and mixed thoroughly
plots, whole quantity of P2 O 5 (20 kg ha−1 ) and K 2O to prepare a composite sample. The soil sample was air-dried
(20 kg ha−1) was applied before seedling transplanting. under shade and ground, and sieved through a 2-mm sieve.
Irrigation was done before transplanting of the crop. The air-dried soil sample was tested for basic physicochemical
Consistent with local farmers’ practice, irrigation (four properties following the method of Page et al. (1982). After
times) was done up to 7 days after transplanting and then application of fertilizer, soil samples were collected from five
the crop was allowed to grow depending only on rain replications of each treatment from a depth of 0–15 cm at
water. The crop was harvested in August 2013 and different stages of crop growth. The samples were then
August 2014. brought to the laboratory in self-sealing plastic bags to retain
 Environ Sci Pollut Res

the soil moisture. Gravimetric soil moisture was measured by Data analysis
oven-drying of soil samples at 105 °C until the weight was
constant. Water-filled pore space (WFPS) was calculated The effects of different nitrogenous fertilizers on N2O emis-
using gravimetric soil moisture and bulk density (Peng et al. sion were evaluated by analysis of variance (ANOVA) using
2011). The remaining soil was air-dried for 7 days and sieved SPSS analytical tool (IBM SPSS 20, SPSS Inc., Chicago,
as described above and subsequently used for analysis of other USA). Significant pooled differences between treatments
chemical parameters. were performed with the Duncan’s Multiple Range test and
Soil organic carbon was analyzed by TOC analyzer (Multi Fisher’s least significant difference (LSD). The correlation
NC-2100S, Analytik Zena, Germany). Soil ammonium (Pearson correlation) coefficient of nitrous oxide fluxes with
(NH4+) was analyzed by extracting with 2 M KCl following plant and soil variables was determined using the same SPSS
the indophenol blue method (Keeney and Nelson 1982). For package. Results presented are the mean of five treatment
nitrate (NO3−) estimation, soil samples were extracted with replications.
nitrate extract solution (1 N CuSO4 and 0.6 N Ag2SO4) and
NO3− content was measured by the phenol disulfonic acid
method (Ghosh et al. 1983). Diethylenetriaminepentaacetic Results
acid (DTPA) extractable micronutrients (Fe, Mn, Zn, and
Cu) in the soil sample were analyzed according to Lindsay Soil temperature, rainfall, and water-filled pore space
and Norvell (1978) in an atomic absorption spectrophotometer
(iCE 3000). Daily soil temperature (0–5 cm) varied from 26.50 to 34.75 °C
in 2013 and 28.00 to 34.50 °C in 2014 (Supplementary Fig.
1). Soil temperature showed similar patterns for all treatments
Urease activity with no significant difference among the treatments. During
the study period (April–August), the total precipitation
The urease activity was assayed by colorimetric method. Five
(127 days of experiment) was 719.27 mm in 2013 and
grams of moist field soil were mixed in 100 ml Erlenmeyer
233.61 mm in 2014 (Supplementary Fig. 2) and the average
flasks with urea solution (1 ml), dissolved in distilled water to
precipitation during the entire crop-growing period was
make a final concentration of 1000 μg g−1 soil. The contents
5.66 mm and 1.83 mm in 2013 and 2014 respectively. Water
were mixed thoroughly on a rotary shaker for 30 min. The
field pore space (WFPS) recorded at the time of N2O sampling
suspensions were incubated for 5 h in a BOD incubator at 35
is presented in Fig. 1 and was in the range of 55 to 93% in
± 2 °C. The amount of residual urea present in the soil suspen-
2013 and 56 to 91% in 2014 (Fig. 1a, b). At the initial stage
sion upon incubation was determined by the non-buffer meth-
(0–14 DAT), the WFPS varied from 85 to 93%. The magni-
od of Zantua and Bremner (1975).
tude of N2O emissions increased at the panicle initiation peri-
od (63–70DAT) when soil WFPS was 64–75% (2013) and
Measurement of leaf photosynthesis 64–73% (2014). In the first season experiment (2013), the
field soil had a relatively high percentage of WFPS due to
The net photosynthetic rate was measured with a portable maximum precipitation (Supplementary Fig. 2). Irrespective
photosynthetic system (Model LI-6400, LICOR, USA) on of the treatments, WFPS and rainfall events contributed to
the upper most fully expanded leaves. After the panicle initi- higher N2O emission at the panicle initiation stage by stimu-
ation stage (63 DAT onwards), photosynthetic rate was mea- lating the denitrification process.
sured by taking the fully expanded flag leaf.
Variation of N2O emission
Estimation of grain yield and nitrogen use efficiency The variations of N2O flux during the rice-growing period of
2 years (2013 and 2014) are presented in Fig. 2. The emission
Grain yield was recorded by harvesting rice from 1-m2 area of N2O in response to different treatments (LSD: 0.189 for
from each replication. Nitrogen use efficiency (NUE) was 2013 and 0.215 for 2014) ranged from 20.99 to
calculated according to Lopez-Bellido and Lopez-Bellido 261.50 μg m−2 h−1 in 2013 and 18.69 to 231.04 μg m−2 h−1
(2001) as follows: in 2014. The application of NPK significantly increased
Gy (p < 0.05) N2O fluxes over other treatments. Irrespective of
NUE ðkg kg−1Þ ¼ the treatments, three distinct peaks were observed, at the til-
Nsupply
lering (35–42 DAT), panicle initiation (63–70 DAT), and
where Gy is grain yield and N supply is sum of soil N content flowering (84–91 DAT) stages of the crop growth and no
at transplanting, mineralized N, and N fertilizer applied. peaks were detected thereafter until the harvest of the crop.
Environ Sci Pollut Res

Fig. 1 Soil water-filled pore

space (WFPS) during the crop
growth period (a) 2013 and (b)
2014. Vertical bars represent
standard error of mean. NPK, ni-
trogen phosphorous potassium;
SCU, starch-coated urea; NCU,
neem-coated urea; NUA, normal
urea alone

Fig. 2 Nitrous oxide flux 300

NPK
(μg m−2 h−1) from rice field (a) a)
SCU
Panicle initiation (p<0.001)
2013 and (b) 2014. Vertical bars 250 NCU
represent standard error of mean; NUA Flowering
Tillering
µg N2O-N m-2 hr-1

arrows indicate the time of fertil- 200

izer application. LSD, least sig-
nificant difference; NPK, nitrogen 150
phosphorous potassium; SCU,
starch-coated urea; NCU, neem- Harvest
100
coated urea; NUA, normal urea
alone
50

0
0 7 14 21 28 35 42 49 56 63 70 77 84 91 98 105 112 119 126
Days after transplanting

300

b) Panicle initiation (p<0.001)

250
µg N2O-N m-2 hr-1

Tillering Flowering
200

150

100
Harvest

50

0
0 7 14 21 28 35 42 49 56 63 70 77 84 91 98 105 112 119 126
Days after transplanting
 Environ Sci Pollut Res

At panicle development stage, the prominent peaks of N2O different fertilizer treatments. Statistical analyses showed a
were the highest and high peaks of 261.50 μg m−2 h−1 (2013) notable variation in urease activity among the treatment
and 231.04 μg m−2 h −1 (2014) were recorded in the field with (p < 0.01, LSD, 1.94). A significant linear relationship be-
NPK treatment. tween the amount of urea hydrolyzed and the time of incuba-
The highest cumulative N2O emission was recorded at tion (up to 48 h) was observed in the present study and soil
NPK application (2.49 kg N2O–N ha−1) followed by UA urease activity showed a significant interaction with N2O
(2.34 kg N2O–N ha−1), NCU (2.20 kg N2O–N ha−1), and emission (r = 0.976, p < 0.01). The maximum urease activity
SCU (1.97 kg N2O–N ha−1) (p < 0.001, Table 1). The pooled was observed in NPK followed by normal urea alone. During
data of cumulative N2O emission showed that the application the whole incubation period, SCU treatment showed 28.29%,
of SCU, NCU, and NUA reduced N2O emission by 21%, 22.95%, and 13.41% lower urease activity compared to NPK,
12%, and 6%, respectively, as against the use of conventional NUA, and NCU respectively.
fertilizer.
Soil organic carbon and N2O emission
Effect of soil mineral nitrogen on N2O emission
Soil organic carbon (SOC) recorded at different stages of the
The concentration of mineral N (NO3− and NH4+) in the soil crop growth is shown in Fig. 4 and the treatment effects (LSD,
varied in all the treatments and the results are presented in 0.260) were found to be significant in changing the organic
Fig. 3a, b (LSD, 0.260 and 0.264). During the entire crop carbon status of soil during the period of experimentation.
growth period, soil nitrate ranged from 23.62 to SOC content ranged from 10.53 to 13.73 g kg−1 during the
75.70 kg ha−1, whereas ammonium ranged from 10.51 to 2 years of the experiment. Parallel with the increase in the root
27.78 kg ha−1 (Fig. 3a, b). The concentration of NH4+ was biomass (data not presented), the SOC content also increased
lower under the application of NPK and urea alone (p < 0.05) up to the flowering stage which might have contributed to
and SCU and NCU maintained relatively higher amount of increased N2O emission. The SOC content due to NPK appli-
soil ammonium in the rice field. The impact of nitrogen fer- cation increased by 3.34% and 1.17% over SCU and NCU
tilizer on N2O emission was clearly visible with increased soil respectively during the crop growth period. Differences
NH4+–N and NO3−–N which paralleled with increased N2O (p < 0.05) in SOC content due to NPK application and urea
emission. A good correlation (Table 2) of soil nitrate and am- alone were marginal. Irrespective of the treatments, a good
monium with N2O flux was observed during the crop-growing correlation of SOC with N2O flux (r = 0.940**, p < 0.01)
period. A significant interaction was also observed among the was observed in the present study.
treatments, year, and different critical stages of growth in the
present study (Fig. 3a, b). Effect of fertilizers on soil physicochemical properties

Urease activity Changes in soil physicochemical properties (bulk density, po-

rosity, water holding capacity, pH, and soil organic carbon)
Soil urease activity was estimated at the stage of crop harvest and bioavailability of major nutrients (N, P, and K) along with
and ranged from 152 to 952 μg g−1 soil (Table 3) under micronutrients (Fe, Cu, Mn, and Zn) at the end of cropping

Table 1 Cumulative N2O

emission, agronomic nitrogen use Treatments Cumulative N2O emission Nitrogen use Grain yield (kg ha−1)
efficiency, and grain yield of (mg N2O–N) efficiency (kg kg−1)
different treatments
1) NPK 249 ± 0.12a 9.55 ± 0.38b 2047 ± 1.8c
2) SCU 197 ± `0.07d 11.98 ± 0.79a 2302 ± 3.4a
3) NCU 220 ± 0.06c 9.75 ± 0.75b 2101 ± 3.1bc
4) NUA 234 ± 0.17b 10.04 ± 1.04b 2228 ± 5.1b
p value treatment (T) 0.000 0.045 0.004
Year (Y) 0.000 0.05 0.000
T×Y 0.000 0.066 0.001
LSD (p < 0.05) 0.583 0.833 0.629

NPK, nitrogen phosphorous potassium; SCU, starch-coated urea; NCU, neem-coated urea; NUA, normal urea
alone
Values followed by the same lowercase letter are not significantly different at p < 0.05 level by Duncan’s multiple
rang test
Environ Sci Pollut Res

Fig. 3 Results of (a) soil NO3−–N 110

and (b) soil NH4+–N at different a) NPK SCU (p<0.05)
stages of crop growth. Bars (mean NCU NUA
± standard error) tagged with the 90
same letter are not significantly a

Soil NO3- -N (kg ha-1)

different at p < 0.05 level by b b
Duncan’s Multiple Range test. c
70 a b
LSD, least significant difference; a a a
NPK, nitrogen phosphorous po- b a c
tassium; SCU, starch-coated urea; c b d
50
NCU, neem-coated urea; NUA, c
normal urea alone a b
ab c
30

10
Initial Tillering Panicle Flowering Maturation
initiation
Crop growth stages

35
b)
a (p<0.05)
30

b
Soil NH4+-N (kg ha-1)

25 a
c a ab
a a b
20 a
d c a b
b
c
15 b a
b
c
10

0
Initial Tillering Panicle Flowering Maturation
Initiation
Crop growth stages

period are arranged in Table 4. The application of slow-release did not alter the concentration of phosphorous and potassium
nitrogen fertilizer increased the water holding capacity in soil. Among the four micronutrients (Fe, Cu, Mn, and Zn) a
(WHC) and decreased bulk density (BD) at the end of the noticeable difference was observed after harvest of the crop;
cropping period (Table 4). The application of SCU and NCU however, there were no significant differences due to the

Table 2 Pearson’s correlation

coefficients (r values) for different Parameters N2O–N NO3−–N NH4+–N SOC WFPS Photosynthetic NUE
parameters rate

N2O–N 1
NO3−–N 0.954** 1
NH4+–N 0.956** 0.929** 1
SOC 0.940** 0.945** 0.821** 1
WFPS 0.370 ns 0.160 ns 0.223 ns 0.176 ns 1
Photosynthetic 0.045 ns − 0.421 ns − 0.281 ns 0.190 ns 0.282 ns 1
rate
NUE − 0.863** − 0.772** − 0.610* − 0.937** 0.679* 0.895** 1

*Correlation is significant at the 0.05 level (2-tailed); **correlation is significant at the 0.01 level (2-tailed)
SOC, soil organic carbon; WFPS, water-filled pore space; NUE, nitrogen use efficiency; ns, non-significant
 Environ Sci Pollut Res

Table 3 Urea hydrolysis

potential of soil under different Incubation time (h) NPK SCU NCU NUA
fertilizer treatments
6 192 ± 0.69 a 152 ± 1.01 a 171 ± 0.69 a 181 ± 0.88 a
24 691 ± 1.17 b 490 ± 0.69 b 574 ± 1.01 b 623 ± 2.34 b
30 762 ± 0.88 c 523 ± 1.01 c 602 ± 0.69 c 716 ± 3.78 c
36 807 ± 0.50 d 574 ± 1.01 d 661 ± 1.01 d 751 ± 1.56 d
48 952 ± 0.38 e 702 ± 0.69 e 811 ± 0.69 e 897 ± 1.35 e
LSD (p < 0.05) 1.90 2.21 2.05 2.92

NPK, nitrogen phosphorous potassium; SCU, starch-coated urea; NCU, neem-coated urea; NUA, urea alone
Values followed by the same lowercase letter are not significantly different at p < 0.05 level by Duncan’s multiple
rang test

treatments. Micronutrient of soil after harvest was in the order SCU-applied field recorded higher photosynthesis compared
of Fe > Cu > Mn > Zn. Concentration of Fe in the soil prior to to other three treatments.
transplanting and after harvest was relatively higher compared Results of the present study depicted significant variations
to other micronutrients. Irrespective of the treatments, Zn and in rice grain yield under the influence of different N fertilizer
Mn increased slightly after harvest over the base value record- management practices (Table 1). The grain yield recorded at
ed in the field prior to experimentation. However, Cu and Fe harvest ranged from 2047 to 2302 kg ha−1. Statistical analysis
remained unchanged at the end of the cropping period. revealed that the SCU treatment had a relatively greater effect
on grain production (p < 0.05, Table 1) than NPK, NCU, and
NUA treatments. SCU treatment increased the grain produc-
Nitrogen use efficiency, plant photosynthesis, tivity by 12%, 10%, and 3% compared to NPK, NCU, and
and grain yield NUA respectively coupled with low N2O emission.

The nitrogen use efficiency (NUE) in the present study varied

within a range of 9.66 to 11.98 kg kg−1. Plants grown at SCU
recorded higher NUE (Table 1) coupled with significant re- Discussion
duction in N2O emission (Table 1) over other treatments. The
net photosynthetic rate was significantly affected by the treat- There were distinct variations in N2O emission among the treat-
ments (LSD, 0.301). Rate of photosynthesis during the exper- ments due to application of different forms of nitrogenous fertil-
imental period varied from 15.33 to 46.11 μ mol CO2 m−2 s−1 izer in the rice field. The prominent N2O peaks observed at
(Fig. 5). Irrespective of the treatments, plant photosynthetic tillering (35–42 DAT) and panicle initiation (63–70 DAT) stages
rate was highest at the panicle development stage which co- were primarily due to application of nitrogenous fertilizer at these
incides with grain filling period (Fig. 5). Plants grown at the two growth stages which increased substrate availability for

Fig. 4 Soil organic carbon (SOC) 16

at different stages of crop growth. (p<0.05) NPK SCU
Bars (mean ± standard error) a
tagged with the same letter are not NCU NUA
significantly different at p < 0.05 14 b
level by Duncan’s Multiple a
a a a c
SOC (g kg-1)

Range test. LSD, least significant b

b c
difference; NPK, nitrogen phos- cd c ab a a
phorous potassium; SCU, starch- 12
b a c
coated urea; NCU, neem-coated c c
urea; NUA, normal urea alone

10

8
Initial Tillering Panicle Flowering Maturation
initiation
Crop growth stages
Environ Sci Pollut Res

20.47 ± 0.03a
20.53 ± 0.03a
20.77 ± 0.04a
20.66 ± 0.05a
nitrification and denitrification processes, resulting in more N2O

(mg kg−1)

0.944
emission (Fig. 2). Increase in N2O emissions after fertilization in
rice paddies is reported by Zhang et al. (2015) and Bordoloi et al.

Fe
(2018). Higher availability of soil organic carbon (Fig. 4) and

1.95 ± 0.03a
2.00 ± 0.04a
2.04 ± 0.05a
1.95 ± 0.02a
NO3−–N (Fig. 3a) as a result of senescence of older leaves and
(mg kg−1)

0.964
decomposition of crop roots might have contributed to high
Cu

emission resulting in the prominent peaks at flowering stage of

7.22 ± 0.03a the crop, and is in agreement with the findings of Johnson et al.
7.22 ± 0.07a
7.20 ± 0.05a
7.37 ± 0.04a
(mg kg−1)

(2006). In the present study, the soil temperature during the high

0.997
emission period (panicle initiation stage) was in the range of
Mn

30.00 to 33.50 °C (Supplementary Fig. 1) which were suitable

1.80 ± 0.05a
1.52 ± 0.07a
1.26 ± 0.02a
1.24 ± 0.01a
for microbial activity which caused higher N2O emission. The
(mg kg−1)

0.743
results are well corroborated with Liu et al. (2011) where N2O
emission is reported to exponentially increase with suitable sub-
Available nitrogen Available phosphorous Available potassium Zn

strate availability at a wide range of soil temperatures (0–50 °C).

In the present study, N2O emissions from slow-release coated
fertilizers were generally lower than those from the conventional
247.52 ± 2.65b
246.40 ± 1.11b
253.12 ± 1.52a
220.86 ± 2.32c

fertilizers. The application of slow-release fertilizers, viz., SCU

(kg ha−1)

and NCU, prevents or retards the oxidation process of NH4+

0.824

because of the presence of coating and can slow down the activ-
Soil physicochemical properties, primary nutrient (N, P, K), and micronutrient status in soil after harvesting of crop

Values followed by the same lowercase letter are not significantly different at p < 0.05 level by Duncan’s multiple range test

ities of nitrifying bacteria, resulting in lower N2O emission. This

also indirectly results in inadequate substrate availability for de-
nitrification process as reported by Akiyama et al. (2010).
30.65 ± 0.50ab

Application of thermoplastic resin-coated urea is reported to re-

31.52 ± 0.48a
32.30 ± 0.19a

31.95 ± 0.58a

duce the N2O emission by 13% in rice field (Ji et al. 2013).
(kg ha−1)

NPK, nitrogen phosphorous potassium; SCU, starch-coated urea; NCU, neem-coated urea; NUA, urea alone

These findings are in good agreement with the results of the

0.824

present study. The application of SCU reduced the N2O emission

by 17% and 24% in the year 2013 and 2014 respectively. The
156.62 ± 2.45cd

significance difference between treatment and year was also ob-

161.71 ± 1.29b
169.34 ± 3.90a
159.16 ± 1.77c

0.846

served in the present study (Table 1). The slow release of nitro-
(kg ha−1)

gen from SCU might be because of the presence of hydroxyl

group on starch chains which help to release the N slowly. The
calcium chloride used as a cross-linking agent forms an ionic
5.54 ± 0.04a
5.92 ± 0.01a
5.75 ± 0.03a
5.99 ± 0.03a

cross-link bonding between the neighboring chains of starch

molecules (Miyazaki et al. 2007). Urea is entrapped inside the
0.824
Water holding pH

calcium chloride and slowly released from the network-like

structure. Although starch is mineralizable, the formation of such
45.95 ± 0.50b

45.58 ± 0.55b
46.32 ± 0.55a
46.46 ± 0.53a
capacity (%)

ionic cross-links tightens the starch matrix and reduces the re-
lease rate of the incorporated urea. In the present study, the
0.754

application of NCU was also effective in reducing the N2O

emission by 10% and 13% in the year 2013 and 2014 respec-
39.59 ± 1.32bc

39.59 ± 1.44bc
40.60 ± 0.78b
42.13 ± 0.89a
Bulk density Porosity (%)

tively over NPK. Our results of lower N2O emissions following

the use of NCU are well corroborated with the findings of Malla
0.824

et al. (2005), where neem oil–coated urea was reported to inhibit

N2O emission by 21% from rice fields relative to that of urea
1.14 ± 0.05b
1.19 ± 0.02a

1.17 ± 0.06a
1.19 ± 0.08a

alone (UA). Neem retard the activity and growth of nitrifying

(Mg m−3)

and denitrifying bacteria, which is reported to reduce the NO3−–

0.008

N concentration (Fig. 3a) in soil, leading to lower N2O emission

(Majumdar et al. 2002; Patra et al. 2009). Although both the
LSD (p < 0.05)

coated fertilizers efficiently reduced the emission over the con-

Treatments

ventional fertilizer, however, the application of SCU was more

4) NUA
3) NCU
1) NPK
2) SCU
Table 4

efficient in reducing the emission over NCU. An average SCU

reduced emission by 10.17% than that of NCU during the entire
 Environ Sci Pollut Res

Fig. 5 Plant photosynthetic rate at 60

different stages of crop growth. NPK SCU a (p<0.05)
Bars (mean ± standard error) NCU NUA
50 c b
tagged with the same letter are not

Plant Photosynthetic rate

d
significantly different at p < 0.05
level by Duncan’s Multiple 40

(µCO2m-2sec-1)
Range test. LSD, least significant
a a a
difference; NPK, nitrogen a
30 b
phosphorous potassium; SCU, b
ab
starch-coated urea; NCU, neem- C c b a b
coated urea; UA, urea alone 20

10

0
Tillering Panicle initiation Flowering Maturation
Crop growth stages

crop-growing period. The soil urease activities were also reduced the first season experiment (2013), the field soil had higher
by application of both the slow-release fertilizers as compared to percentage of WFPS due to maximum precipitation
the conventional fertilizer (Table 3). A balanced nutrient avail- (Supplementary Fig. 2), resulting in increased N2O emission.
ability and higher root exudates may promote the urease activity In the second season (2014), an average of 6.85% higher
under conventional fertilizer treatment (NPK) and resulting in emission was observed as compared to the first season
higher N2O emission (Li et al. 2016). Our results of reduced (2013) and similar results have been corroborated by Li
urease activity and N2O emission by the application of SCU et al. (2015). Alternate drying and flooding conditions of the
and NCU in the rice paddy are consistent with findings that soil field which is evident from precipitation data have stimulated
urease activity is closely related with N2O emissions from soil the N2O emission caused by nitrification of NH4+–N at < 60%
(Bai et al. 2003). WFPS. Rainfall events and WFPS increased N2O–N emission
Higher N2O emissions from NPK and normal urea applied at panicle initiation stage predominantly by the denitrification
field were presumably due to quicker availability of NH4+N pathway and the results are in conformity with the findings of
released from urea ensuring faster nitrification leading to high Dobbie and Smith (2003) and Bhatia et al. (2010).
N2O flux and our results are in conformity with the findings of During the crop growth period, changes in N2O fluxes
Kumar et al. (2000). The availability of substrate in the form seem to be influenced by SOC and this is in agreement with
of mineral nitrogen is considered to be the primary cause of the findings of Wagner et al. (2007). The observed positive
N2O flux from soil in the current study as evident from the correlation between SOC and N2O flux is due to the influence
correlation study (Table 2). The results are in good agreement of soil carbon on nitrifying and denitrifying bacteria (Wang
with some previous reports (Lin et al. 2010; Wang et al. 2011) et al. 2011). The energy required by soil microbes for nitrifi-
where authors reported significant correlation of seasonal N2O cation and denitrification process is reported to obtain by
emission with soil mineral N content in rice paddies by regres- transferring of electrons from the carbon compounds which
sion analysis. Soil nitrate and ammonium concentration in- exist in soil organic matter (Kyaw and Toyota 2007).
creased at the initial and tillering stages of crop growth due Increased SOC concentration at the active vegetative and pan-
to basal fertilization and tilling fertilization (Fig. 3a, b) and icle development stages (Fig. 4) might be the result of a large
started to decline thereafter. Decrease in N2O emission before quantity of readily available organic compounds like plant
and after harvest of the crop may be due to low availability of root exudates, decomposable organic matter, and sloughed-
mineral N in the soil, crop maturity at the end of the growing off root cap cells (Ghosh et al. 2012). Increased root growth
season, and absence of a standing green crop. The results are is reported to be responsible for the release of root-derived
well corroborated with some previous findings (Lin et al. organic compounds stimulating the denitrification process
2010; Bordoloi et al. 2016) where lower N2O emissions at (Philippot et al. 2009), thus favoring N2O emission from rice
the end of the crop growth period are reported. Soil moisture fields. Similar mechanisms might have enhanced the nitrifica-
is also reported to affect the N2O emissions by influencing tion and denitrification in the soil, resulting in greater N2O
nitrification and denitrification processes (Bateman and emission along with increased SOC in our study. No signifi-
Baggs 2005). At the initial stage of the crop growth, the water cance difference in SOC concentration between SCU and
filled pore space varied from 85 to 93% which was possibly NCU was observed during the crop-growing period. The
dictated by irrigation event during the time of transplanting SOC content increased up to the flowering stage, which might
and is one of the causes of low N2O emission at this stage. In have contributed to increased N2O emission. Our results are in
Environ Sci Pollut Res

conformity with some earlier findings of Wang et al. (2011) other forms of fertilizers (NPK and NUA). Compared with
and Bordoloi and Baruah (2017). conventional fertilizer (NPK), SCU and NCU reduced N2O
The soil treated with SCU and NCU increased the water emission (p < 0.05) by 23% and 12% respectively without
holding capacity and decreased the bulk density. The in- compromising the agronomic productivity of the crop. In ad-
creased water holding capacity and decrease in bulk density dition to improving grain productivity, SCU also increased the
in soil may enable the rice crop for higher grain production nitrogen use efficiency by 25.45% due to improved leaf pho-
(Shirani et al. 2002). The application of coated fertilizers in- tosynthesis over NPK. Further long-term studies at different
creased the soil total porosity at harvest, which have influ- locations with SCU application in rice ecosystem are neces-
enced the crop productivity by influencing water infiltration sary for evaluative recommendation in agricultural systems.
and aeration; similar results are reported by Stine and Weil Approaches to increase rice productivity through suitable N
(2002). Results of the present study revealed that bioavailabil- fertilizer management, without effecting soil quality and pro-
ity of all the micronutrients remained unchanged in spite of the ductivity, may be particularly useful in a future climate change
application of slow-release fertilizer. From the results, it is scenario.
apparent that the application of SCU and NCU did not ad-
versely affect the soil health parameters during the cropping Acknowledgements The authors acknowledge the Rajiv Gandhi
National Fellowship, Government of India (awarded to Nirmali
period.
Bordoloi). We acknowledge the help of Prof. B.K. Danta of the
Despite the low N2O emission, SCU contributed to greater Department of English and Foreign Languages, Tezpur University, in
nitrogen use efficiency (NUE) and photosynthetic rate in both editing the manuscript.
years. An average SCU increased NUE by 25.45%, 22.87%, and
19.32% over NPK, NCU, and NUA respectively. Increased
NUE at the SCU-applied field indicates better assimilation of
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