Environmental Pollution 269 (2021) 116143

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Combined applications of organic and synthetic nitrogen fertilizers for

improving crop yield and reducing reactive nitrogen losses from
China’s vegetable systems: A meta-analysis*
Bin Liu a, b, Xiaozhong Wang a, b, c, Lin Ma b, d, Dave Chadwick b, e, Xinping Chen a, b, c, *
a
College of Resources and Environment, Academy of Agricultural Sciences, Southwest University, Chongqing, 400716, China
b
Interdisciplinary Research Center for Agriculture Green Development in Yangtze River Basin, Southwest University, Chongqing, 400716, China
c
Chongqing Key Laboratory of Efficient Utilization of Soil and Fertilizer Resources, Southwest University, Chongqing, 400716, China
d
Key Laboratory of Agricultural Water Resources, Center for Agricultural Resources Research, Institute of Genetic and Developmental Biology, The Chinese
Academy of Sciences, 286 Huaizhong Road, Shijiazhuang, 050021, Hebei, China
e
School of Natural Sciences, Bangor University, Bangor, LL57 2UW, UK

a r t i c l e i n f o a b s t r a c t

Article history: The combined application of organic and synthetic nitrogen (N) fertilizers is being widely recommended
Received 27 April 2020 in China’s vegetable systems to reduce reliance on synthetic N fertilizer. However, the effect of
Received in revised form substituting synthetic fertilizer with organic fertilizer on vegetable productivity (yield, N uptake and
18 November 2020
nitrogen use efficiency) and reactive nitrogen (Nr) losses (N2O emission, N leaching and NH3 volatili-
Accepted 20 November 2020
Available online 23 November 2020
zation) remains unclear. A meta-analysis was performed using peer-reviewed papers published from
2000 to 2019 to comprehensively assess the effects of combined application of organic and synthetic N
fertilizers. The results indicate that overall, the vegetable yield, N2O emission and NH3 volatilization were
Keywords:
Organic fertilizer
not significantly changed, whereas N leaching was reduced by 44.6% and soil organic carbon (SOC)
Synthetic N fertilizer concentration increased by 12.5% compared to synthetic N fertilizer alone. Specifically, when synthetic N
Substitution rate substitution rates (SRs) were
70%, vegetable yields and SOC concentration were increased by 5.5%e5.6%
Vegetable systems and 13.1e18.0%, and N leaching was reduced by 41.6%e48.1%. At the high substitution rate (SR>70%),
Yield vegetable yield was reduced by 13.6%, N2O emission was reduced by 14.3%, and SOC concentration
Reactive nitrogen losses increased by 16.4%. Mixed animal-plant sources of organic N preferentially increased vegetable yield and
SOC concentration, and reduced N2O emission and N leaching compared with single sources of organic-
N. Greenhouse gas (GHG) emission was decreased by 28.4%e34.9% by combined applications of organic
and synthetic N sources, relative to synthetic N fertilizer alone. We conclude that appropriate rates
(SR
70%) of combined applications of organic and synthetic N fertilizers could improve vegetable
yields, decrease Nr and GHG emission, and facilitate sustainable development of coupled vegetable-
livestock systems.
© 2020 Elsevier Ltd. All rights reserved.

1. Introduction

Inappropriate timing and excessive application of synthetic ni-

Abbreviations: N, nitrogen; Nr, reactive nitrogen; NUE, N use efficiency; N2O,
nitrous oxide; NH3, ammonia; SOC, soil organic carbon; GHG, greenhouse gas; EFs,
emission factors; RDA, Redundancy analysis; SOM, soil organic matter; STN, soil
total nitrogen; ON, organic N; SN, synthetic N; SR, synthetic N substitution rate;
GWP, global warming potential.
*
This paper has been recommended for acceptance by Markus Hauck.
* Corresponding author. College of Resources and Environment, Academy of
Agricultural Sciences, Southwest University, Chongqing, 400716, China.
E-mail address: chenxp2017@swu.edu.cn (X. Chen).
trogen (N) fertilizer to intensive vegetable systems has resulted in
large losses of reactive nitrogen (Nr) and severe pollution of air and
water (Rashti et al., 2015; Ti et al., 2015), especially in China where
more than 95% of synthetic N fertilizers are urea and ammonium-N
(Huang et al., 2013). At present, China has the largest cultivated area
and production of vegetables in the world (FAOSTAT, 2019). How-
ever, with the rapid development of vegetable production, there
has been a greater intensity of Nr losses from intensive vegetable
production systems (Ti et al., 2015; Wang et al., 2018a, b). This is

https://doi.org/10.1016/j.envpol.2020.116143
0269-7491/© 2020 Elsevier Ltd. All rights reserved.
B. Liu, X. Wang, L. Ma et al.
mainly driven by the substantial N fertilizer inputs (Ju et al., 2006).
Further, soil degradation (e.g. acidification and salinization) is also
common in vegetable fields (Guo et al., 2010). So, vegetable pro-
duction systems in China are now characterized by decreasing
productivity, environmental degradation and declines in soil
quality (Liang et al., 2013; Qiu et al., 2010). Therefore, there is an
urgent need to address these challenges and promote modern,
sustainable vegetable production systems through optimizing N
management practices.
Recycling of N from organic resources for crop growth could not
only reduce the environmental burden from organic resources, but
also reduce reliance on synthetic N fertilizer. In addition, these
organic resources supply soil with organic matter, which plays a
key role in maintaining soil fertility and soil structure (Diacono and
Montemurro, 2010; He et al., 2015; Maillard and Angers, 2014;
Naveed et al., 2014). In practice, composted animal manure (alone)
or composted manure mixed with plant straw are commonly
applied with synthetic N fertilizer, as a basal nutrient source before
sowing or at the time of transplanting vegetables. Sufficient evi-
dence has indicated that combined applications of organic and
synthetic N fertilizers can result in greater cereal yields and
improved N use efficiency (NUE) (Das and Adhya, 2014;
Efthimiadou et al., 2010; Pan et al., 2009; Wei et al., 2016). This is
the result of a better synchronization of N supply with crop N de-
mand, through the release of mineral nitrogen from organic N
sources (Chivenge et al., 2011; Liu et al., 2012). However, because of
the limited root systems of most vegetable crops (Brumm and
Schenk, 1992), the short cropping cycles, and weak nutrient ab-
sorption capacity of vegetables compared to cereal crops, crop
response to combined applications of organic and synthetic N fer-
tilizers may differ between vegetables and cereals. Recent results of
a meta-analysis have demonstrated that partial substitution of
synthetic N fertilizer with manure can significantly increase grain
crop yields, N uptake and NUE, but with no significant changes of
responses in vegetables (Xia et al., 2017). However, the effects of
substitution rate were not determined, and different cultivation
types for vegetable production were not explored. Some field
studies have indicated that productivity of vegetables (yield, N
uptake and NUE) varies with substitution rate (Zhou et al., 2019;
Zhuang et al., 2019) and organic fertilizer type (Zhang et al., 2019),
but optimal substitution rates have not been identified because of
the inconsistent and sometimes contradictory results reported in
vegetable systems.
Previous studies have shown that partial substitution of syn-
thetic N fertilizer with livestock manure tended to decrease total Nr
losses (Xia et al., 2017; Zhou et al., 2019). However, there have been
different responses for different forms of Nr (e.g. nitrous oxide
[N2O] emission, mineral N leaching, ammonia [NH3] volatilization).
For example, a meta-analysis by Xia et al. (2017) indicated NH3
volatilization and N leaching were significantly decreased while
there was little effect on N2O emission by replacing synthetic N
fertilizer with manure. Various Nr losses have been correlated with
the C/N ratio of the organic resource amendment (Akiyama and
Tsuruta, 2013; Xia et al., 2018), because microbial processes of N
cycling, e.g. mineralization, are regulated by organic matter quality
(Bhogal et al., 2016; Chadwick et al., 2000). In general, organic
fertilizers with low C/N ratios contribute to nitrification and deni-
trification, because of increases in microbial activities and N sub-
strate (Mori and Hojito, 2012), whilst higher C/N ratio could
enhance microbial N immobilization (Zhou et al., 2017). Animal
manure and plant straw are the most commonly available organic
resources in China, and single and mixed use of these organic re-
sources is common, with a wide C/N ratio. So, choice of organic
resource is critical in terms of N supply to meet crop demand and
Nr losses. In addition, studies have indicated there are differences
2
Environmental Pollution 269 (2021) 116143
in Nr losses between open-field and greenhouse vegetable systems
(Liu et al., 2013; Ti et al., 2015; Wang et al., 2018a, b), due to
different environmental conditions and management practices.
However, we lack a quantitative understanding of responses of
various Nr losses to different organic fertilizer types and cultivation
type in vegetable systems.
Furthermore, improvement of soil properties caused by appli-
cation of organic fertilizers may simulate Nr losses. For example,
some studies indicated that NH3 volatilization might be enhanced
(Tang et al., 2019; Xia et al., 2018), as the result of increases in soil
pH (Thangarajan et al., 2013; Whalen et al., 2000). In terms of N
leaching, although organic fertilizer resource application improves
soil aggregate structure (thus improving potential soil N retention),
this may lead to greater infiltration rates, increasing the risk of N
leaching (Blanco-Canqui and Lal, 2009). Zhou et al. (2017) reported
application of livestock manure significantly stimulated N2O
emissions, especially in low pH soils. Because of these contrasting
effects on potential Nr losses, there is a need to comprehensively
assess Nr losses, accounting simultaneously for N2O emission,
mineral N leaching and NH3 volatilization. Fertilizer substitution
with organic fer could directly change the available N content in the
soil, due to a reduction of mineral N application, and hence
decrease Nr losses (Hao et al., 2012a, b; Zhang et al., 2020). But, how
different rates of substitution and different N application rates will
affect Nr losses and crop yields, remains unclear.
Organic fertilizer can enhance soil C sequestration (Maillard and
Angers, 2014), with rates of soil C sequestration being largely
dependent on C application rate, organic fertilizer type and
growing environment (i.e. open-field and greenhouse). An increase
in soil organic carbon (SOC) means enhanced removal of CO2 from
the atmosphere, contributing to the mitigation of climate warming
(Lal, 2004; Powlson et al., 2011). As methane emission from soil is
rare in upland crop production systems in China (Ge et al., 2016),
N2O is the main source of non-CO2 GHG emission from vegetable
production systems. However, some studies have found that
enhanced N2O emissions can outweigh the SOC sequestration
benefits of mitigating climate warming (Pathak et al., 2005; Zhou
et al., 2017). Net global warming potential (GWP) is a useful indi-
cator to assess environmental impacts, as it considers direct and
indirect GHG emission and SOC sequestration. An understanding of
the optimal substitution rate for both crop yield and GWP is
needed.
To address these knowledge gaps, we performed a meta-
analysis of published data concerning combined applications of
organic and synthetic N fertilizers in vegetable systems in China.
The objectives of the study were to: i) determine the responses of
crop productivity (crop yield; N uptake and NUE), Nr losses (N2O
emission, N leaching and NH3 volatilization) to substitution rates, N
application rates, organic fertilizer type and cultivation type; ii)
identify critical impact factors and drivers of Nr losses; and iii)
quantitively comparing Nr losses and the GWP with different
substitution rates for vegetable systems in China.
2. Materials and methods
2.1. Data collection
Relevant peer-reviewed papers published from 2000 to 2019
were identified via systematic searches of Web of Science, China
National Knowledge Infrastructure and China Wanfang data. We
used the following key words in our search for publications:
‘organic amendment’, ‘vegetable (e.g. cabbage, amaranth, lettuce,
celery, spinach, tomato, pepper, eggplant, cucumber, radish)’, ‘ni-
trogen’, or ‘nitrous oxide’ or ‘ammonia volatilization’ or ‘N leaching’.
Studies included in the meta-analysis had to meet the following
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

criteria: i) Data were from field studies (open-field and greenhouse
cultivation, Fig. S1) conducted in China laboratory experiments
under control conditions were excluded. ii) Field studies needed to
have used synthetic N fertilizer only as the reference and included a
treatment with full or partial substitution of N fertilizer with
organic fertilizer (animal-based, plant-based, mixed animal-plant
or other organic N sources); both the synthetic N fertilizer refer-
ence and other experimental treatments were included at the same
total N application rate in the experimental design (here synthetic
N fertilizer actually means urea and ammonium-N, because they
are the most representative N fertilizer forms used in China’s
vegetable systems, >95%). iii) The N rates from synthetic fertilizer
or organic fertilizer for each treatment had to be reported, in order
to derive the substitution rate, defined by organic fertilizer N input/
total N applied. iv) Organic fertilizer type (e.g. animal-based, plant-
based, mixed animal-plant or other organic N sources) and culti-
vation type (open-field, greenhouse) needed to be reported. v) At
least one of the target variables (yield, N uptake, NUE, N2O emis-
sion, N leaching or NH3 volatilization, SOC concentration) was
quantified. vi) Observations from different literature, but cited in
more than one study were only included once, to avoid duplication
of data.
In addition, we collated another database for various Nr emis-
sion factors and SOC changes, in which studies also satisfied the
above selective criteria, except that treatments used different N
application rates. Some relevant data were only provided in figures;
where was the case we used software GetData Graph Digitizer
(version 2.22) to derive the values. Based on above selective criteria,
we collected 71 peer-reviewed studies, including 702 side-by-side
comparisons, for the meta-analysis, and 502 experimental obser-
vations from 68 experiments for the Nr emission factors and SOC
database (See the supplementary material 2).
2.2. Variables and grouping
Effects of substituting synthetic N fertilizer with organic fertil-
izer were evaluated by 3 categories with 7 variables: i) Crop pro-
ductivity: yield, N uptake and NUE; ii) Nr losses: N2O emission, N
leaching and NH3 volatilization; iii) Soil carbon sequestration: SOC
concentration. Here, N uptake refers to total aboveground N up-
take; NUE was calculated by dividing the difference in N uptake in
plots with and without fertilization by the total N rate, as N re-
covery efficiency. Emission factors (EFs) of N2O emission, N leach-
ing and NH3 volatilization were defined by dividing the difference
in Nr emission with and without fertilization by total N applied.
NUE and EF were either directly recorded from the literature or
calculated according to above descriptions. Here, the soil C
sequestration rate (topsoil) was seasonal, not annual, and was
calculated by following equation:
substitution rate was divided into 3 categories: SR
35%,
35<SR
70% and SR>70%; N application rate had 3 categories: low
rate, moderate and high rate, for leafy vegetables
150, 150e300,
>300 kg N ha1, and for fruit and pod vegetables
200, 200e400,
>400 kg N ha1, respectively, which was mainly based on published
recommended rate for vegetables in China (MARA, 2019); organic
fertilizer types were divided into animal-based, plant-based, mixed
animal-plant or ‘other’ organic N sources, e.g. sewage sludge or
biogas residue. For cultivation type, production systems were
categorized as open-field or greenhouse.
2.3. Meta-analysis
The effects of combined applications of organic and synthetic N
fertilizers on variables (X) were quantified by the natural log to
indicate the response ratio (ln RR) calculated by the following
equation (Hedges and Curtis, 1999):
ln RR ¼ lnðXt = Xc Þ (2)
where Xt and Xc represent the mean of the treatment and reference
for variable X, respectively. In order to present the results, response
ratios were transformed into percentage form by ((RR-1)  100) in
the variables. Positive percentage changes denote an increase,
whereas negative values indicate a decrease in the respective var-
iables (See Figs. 1e4).
Because some studies did not report the standard deviation (SD)
of variables (X), we assigned 6%e11% of given value as SD, which
corresponded to the respective given mean SD in the database
(Skinner et al., 2014; see the supplementary material 2). The
random-effects meta-analysis was performed in Metawin software
(version2.1), and weighted mean effect sizes and 95% confident
intervals (CIs) were generated by using a bootstrapping procedure
with 4999 interactions. Effects of combined applications of organic
and synthetic N fertilizers were considered significant if the 95% CIs
did not overlap with zero. Total heterogeneity (QT) of each variable
(X) was partitioned into within-group heterogeneity (QW) and

dSOC concentration ð g C per kg air  dry soilÞ

¼ ððSOCtt  SOCt0 Þ  ðSOCct SOCc0 Þ Þ=n (1)

Where SOCtt and SOCt0 refer to SOC concentration of the treatment

in final and initial seasons of the experiment, respectively, and
SOCct and SOCc0 represent SOC concentration of the reference in
final and initial seasons; n is the number of growing seasons during
the experiment duration. When the studies did not report soil C
sequestration rate, the rate was estimated by changes of SOC con-
centration introduced by Xia et al. (2017).
Effects of combined applications of organic and synthetic N
Fig. 1. Summary of the overall effects of combined applications of organic and syn-
fertilizers were evaluated according to the sub-groups (substitution thetic N fertilizers on yield, N uptake, nitrogen use efficiency (NUE), N2O emission, N
rate, N application rate, organic fertilizer type and cultivation type). leaching, NH3 volatilization and soil organic carbon (SOC) concentration. Numbers in
To satisfy maximal in-group homogenization (Jeffery et al., 2011), parentheses are experimental observations.

3
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

Fig. 2. Effects of synthetic N fertilizer substitution rate (SR), N application rate, organic fertilizer type and cultivation type on yield (a), N uptake (b) and nitrogen use efficiency (NUE)
(c), respectively. Substitution rate (SR) is defined by organic nitrogen input/total nitrogen input. The number in square brackets [ ] shows the maximum value that exceeds the given
scale. Numbers in parentheses are experimental observations. P values represent significant difference between categories within a subgroup if P < 0.05.

Fig. 3. Effects of synthetic N fertilizer substitution rate (SR), N application rate, organic fertilizer type and cultivation type on N2O emission (a), N leaching (b) and NH3 volatilization
(c), respectively. Substitution rate (SR) is defined by organic nitrogen input/total nitrogen input. The number in square brackets [ ] shows the maximum value that exceeds the given
scale. Numbers in parentheses are experimental observations. P values represent significant difference between categories within a subgroup if P < 0.05.

between-group heterogeneity (QB) using chi-square distribution. tests comprised 999 permutations to determined significances of
The means of the categorical variables within each sub-group were explanatory variables.
considered significantly different from each other if P < 0.05 (QB)
following the chi-square test (Rosenberg et al., 2000; see Table S2).
Meanwhile, a one-way analysis of variance (ANOVA) was used to 3. Results
identify differences in emission factors (EFs) of Nr losses at different
substitution rates, followed by the significant different test (LSD). 3.1. The overall effects of combined applications of organic and
All statistics were conducted using SPSS Statistics (version 12.5). synthetic N fertilizers

2.4. Redundancy analysis (RDA)
Basing on our collated emission factors and SOC database, we
selected the following impact factors as explanatory variables; soil
organic matter (SOM), total soil nitrogen (STN), soil pH, total N
application rate (TN, synthetic N application rate þ organic N fer-
tilizer application rate), synthetic N (SN) application rate, organic N
(ON) fertilizer application rate, synthetic N substitution rate (SR),
and length of crop growing season (duration). Background emis-
sions, total Nr losses (fertilizer-induced Nr losses þ background
emission losses), fertilizer-induced Nr losses, and emission factors
were the response variables. The RDA was programmed by the
‘vegan’ package in RStudio software (Dixon, 2003). Monte-Carlo
4
The effects on vegetable productivity (yield, N uptake and NUE),
Nr losses (N2O emission, N leaching, NH3 volatilization) and SOC
were considered. Overall, for vegetable productivity, N uptake was
decreased by 15.9% relative to synthetic N fertilizer alone, although
no significant effects were observed for vegetable yield and NUE
through combined applications of organic and synthetic N fertil-
izers. Combined applications of organic and synthetic N fertilizers
reduced N leaching by 44.6%, and there were no significant changes
for N2O emission and NH3 volatilization, because of the substantial
variations in these two variables (Fig. 1). In addition, combined
applications of organic and synthetic N fertilizers significantly
increased SOC concentration by 12.5% compared to synthetic N
fertilizer alone.
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

14.3% (Fig. 3 a). Meanwhile, N leaching losses were significantly

decreased at SR
70%, (Fig. 3 b). No significant changes in NH3
volatilization were seen with any of the substitution rates (Fig. 3 c).
The N2O emission was lower under moderate N application
rates, but large variations were seen at low and high N rates. At all
application rates, N leaching was significantly lower from com-
bined applications of organic and synthetic N fertilizers than syn-
thetic N fertilizer only (Fig. 3 b). Ammonia volatilization was
notably lower from combined applications of organic and synthetic
N fertilizers than synthetic N fertilizer alone, but only at the high N
application rate (Fig. 3 c). Mixed animal-plant or other organic N
sources contributed to reducing both N2O emission and N leaching,
but did not affect NH3 volatilization. Applying combined animal-
based N sources with synthetic N fertilizers generally reduced N
leaching. Due to limited available data, the effects of replacing
synthetic N fertilizer with plant-based N sources on Nr losses were
uncertain. It is worthy of note that the combined applications of
organic and synthetic N fertilizers resulted in an increase in N2O
emission (25.0%, Fig. 3 a) in greenhouse systems, but with reduced
N leaching and NH3 volatilization. Combined applications of
organic and synthetic N fertilizers increased SOC concentration
compared to synthetic N fertilizer alone, regardless of SR, N appli-
cation rate, organic fertilizer type or cultivation type. Higher SRs
and N rates tended to favor SOC sequestration (Fig. 4).

Fig. 4. Effects of synthetic nitrogen fertilizer substitution rate (SR), N application rate,
3.3. Impact factors for Nr emissions
organic fertilizer type and cultivation type on topsoil organic carbon (SOC) concen-
tration. Substitution rate (SR) is defined by organic nitrogen input/total nitrogen input.
Numbers in parentheses are experimental observations. P values represent significant Redundancy analysis (RDA) was used to identify the critical
difference between categories within a subgroup if P < 0.05. factors and their relationships with Nr losses. RDA1 and RDA2
explained 21.75% and 5.09% of the variance in N2O emission,
respectively, but there was no significant difference of N2O emis-
3.2. Effects of substitution rate (SR), N application rate, organic
sion (total N2O emission, background emissions, fertilizer-induced
fertilizer type and cultivation type
emissions and emission factors) between open-field and green-
house systems (Fig. 5 a). Total N application rate (TN), i.e. synthetic
3.2.1. Crop productivity
N (SN) application rate plus organic N (ON) fertilizer application
Although the overall effect on vegetable yield was not signifi-
rate, and SOM were the main contributors to N2O emission. There
cant, positive responses were observed when substitution rates
was a positive relationship between fertilizer-induced N2O emis-
were no more than 70% (SR
35%, 35%<SR
70%), with yield in-
sion (total emission minus background emission) and N application
creases of 5.5e5.6%. The high substitution rate (SR>70%) tended to
rates (TN, SN and ON), and total N2O emission was negatively
decrease vegetable yield (Fig. 2 a) compared to synthetic N fertilizer
related to SOM (Fig. 5 a).
alone. Similarly, N uptake and NUE were significantly lower at the
N leaching was controlled by SR, application rates of synthetic N
high substitution rate (SR>70%, Fig. 2 b, c).
and organic N fertilizer, soil pH and length of growing season
Compared to synthetic N fertilizer alone, combined applications
(duration). Fertilizer-induced N leaching was positively related to
of organic and synthetic N fertilizers could improve yield at the
synthetic N fertilizer application rate, but negatively associated
high N application rate, but there were no significant changes in N
with organic N application rate and SR. In general, soil pH and
uptake and NUE. In contrast, there were risks of decreased vege-
length of growing season (duration) positively affected total N
table yield and N uptake at the low N application rate (Fig. 2 a, b),
leaching (Fig. 5 b). The critical impact factors to NH3 volatilization
while the responses of NUE did not vary with different N rates
were N application rates (SN fertilizer application rate, ON fertilizer
(Fig. 2 c). Although there were no significant changes in vegetable
application rate), and soil pH. There was a positive relationship
yield following application of N from plant-based N sources, N
between fertilizer-induced NH3 volatilization and total N applica-
uptake and NUE were decreased by 30.7% and 47.7%, respectively.
tion rate, and a similar relationship was seen between fertilizer-
Substituting synthetic N fertilizer with N from animal-based N
induced NH3 volatilization and synthetic N application rate.
sources barely affected vegetable yield and N uptake, but NUE was
Higher soil pH generally increased background emissions of NH3,
increased. Mixed animal-plant or other organic N sources increased
and there was a positive relationship between SR and the EF for
yield (4.0%), but tended to reduce N uptake. In the open-field sys-
NH3 volatilization (Fig. 5 c).
tems, there was an increase in vegetable yield but decreases in N
uptake and NUE compared to synthetic N fertilizer alone. However,
3.4. Emission factors of Nr emissions and changes of SOC
these changes were not detected in greenhouse production
systems.
In the open-field systems, the EFs for N leaching tended to be
lower with higher SRs, and the highest EF was seen from synthetic
3.2.2. Nr losses and SOC concentration N fertilizer only (N leaching, 9.59%). However, EFs for NH3 tended to
There were large variations in the effects of combined applica- be higher with greater SRs. EFs for N2O were not significantly
tions of organic and synthetic N fertilizers on N2O emission be- different between different fertilization categories in both open-
tween different SRs, but higher SRs tended to result in lower N2O field and greenhouse systems (Table 1). In the greenhouse sys-
emission. At the high SR (SR>70%), N2O emission was reduced by tems, higher SRs tended to reduce EFs for N leaching, but with no
5
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

Fig. 5. Redundancy analysis (RDA) of correlations between the impact factors and reactive nitrogen losses, N2O emission (a), N leaching (b) and NH3 volatilization (c), respectively.
The explanatory variables include total N application rate (TN), organic N fertilizer application rate (ON), synthetic nitrogen fertilizer application rate (SN), synthetic nitrogen
fertilizer substitution rate (SR), soil pH, soil organic matter (SOM), soil total nitrogen (STN) and length of growing season (Duration). The response variables include total emissions,
background emissions, fertilizer-induced emissions (FI) and emission factors (EF). The green dots are response variables. Different symbols refer to open-field and greenhouse
systems, respectively. P values represent explanatory variables have significant impacts on various Nr losses if P < 0.05. (For interpretation of the references to colour in this figure
legend, the reader is referred to the Web version of this article.)

Table 1
Mean emission factors of N2O emission, N leaching and NH3 volatilization and seasonal changes in soil organic carbon (SOC, 0e20 cm) at different substitution rates (SR) in
open-field, greenhouse and overall systems, respectively. 95%CI indicates 95% confidence interval; n means number of the observations. Within the same category, different
letters indicate significant difference at P < 0.05.

Item Synthetic N fertilizer 35%
SR 35%<SR
70% SR>70%

N Mean 95%CI n Mean 95%CI n Mean 95%CI n Mean 95%CI

Emission factor (%) Open-field

N2O emission 101 1.60 a 1.27e1.93 21 1.01 a 0.69e1.34 12 0.94 a 0.39e1.48 13 1.00 a 0.49e1.51
N leaching 15 9.59 a 4.35e14.8 11 7.18 ab 2.39e12.0 16 4.12 b 1.35e6.89 ND ND ND
NH3 volatilization 24 9.69 b 7.39e12.0 23 9.62 b 7.26e12.0 11 14.1 a 10.4e17.8 ND ND ND
Greenhouse
N2O emission 46 0.74 a 0.55e0.94 15 0.80 a 0.50e1.09 23 0.82 a 0.56e1.09 16 0.49 a 0.33e0.66
N leaching 20 23.8 a 14.0e33.6 32 13.3 b 9.71e16.8 11 8.66 b 4.57e12.8 11 8.03 b 3.38e12.7
NH3 volatilization 10 1.45 a 1.02e1.87 2 1.44 a ND 6 1.20 a 0.30e2.10 5 1.25 a 0.62e1.87
Overall
N2O emission 147 1.33 a 1.09e1.58 36 0.92 b 0.70e1.14 35 0.86 b 0.62e1.10 29 0.72 b 0.47e0.97
N leaching 35 17.7 a 11.4e24.0 43 11.7 b 8.77e14.7 27 5.97 b 3.63e8.32 ND ND ND
NH3 volatilization 34 7.27 a 5.19e9.34 25 8.97 a 6.61e11.3 17 9.55 a 5.56e13.5 ND ND ND
Soil organic carbon (g C kg1/Mg C ha1) Open-field
dSOC concentration 8 0.43 b 0.02e0.88 8 1.91 a 0.90e2.91 3 2.14 a 1.54e2.74 5 1.67 a 1.41e1.92
dSOC stock 8 1.18 b 0.06e2.41 8 5.20 a 2.46e7.94 3 5.84 a 4.19e7.48 5 4.54 a 3.83e5.27
Greenhouse
dSOC concentration 17 0.37 b 0.05e0.78 3 3.17 a ND 6 3.21 a 2.90e3.52 4 2.82 a 2.81e3.10
dSOC stock 17 1.01 b 0.12e2.12 3 8.64 a 8.64e8.65 6 8.75 a 8.26e9.24 4 7.67 a 7.28e8.46
Overall
dSOC concentration 25 0.39 b 0.14e0.68 11 2.25 a 1.59e2.88 9 2.85 a 2.36e3.27 9 2.18 a 1.77e2.59
dSOC stock 25 1.06 b 0.37e1.85 11 6.14 a 4.29e7.90 9 7.78 a 6.36e8.93 9 5.93 a 4.82e7.07

Note: ND indicates no data; dSOC concentration and dSOC stock are seasonal changes of SOC concentration and stock, respectively, and calculated by equation (1).

6
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

effect on the EFs for NH3. The overall EFs for N2O emission and N
leaching decreased at higher SRs, while EFs for NH3 did not show
significant difference between synthetic N fertilizer alone and
combined applications of organic and synthetic N fertilizers. NH3
volatilization is an important pathway of N fertilizer loss in open-
field systems, and EFs for NH3 in open-field systems were 6e12
times higher than those in greenhouse systems. However, green-
house systems had 2-3 times greater N leaching EFs, relative to
open-field (Table 1).
Regardless of cultivation type (open-field or greenhouse), both
SOC concentration and SOC stock were significantly increased
through combined applications of organic and synthetic N fertil-
izers, relative to applying synthetic N fertilizer alone. Typically, the
SOC concentration and SOC stock were greatest under 35%
<SR
70%, and decreased slightly when SR was >70%. The overall
SOC concentration and SOC stock also showed similar trends. The
SOC concentration and SOC stock in greenhouse systems were
1.5e2 times greater than those in open-field systems (Table 1).
3.5. Nr emission rates and GHG budgets
The mean N fertilizer inputs to open-field and greenhouse
vegetable systems, and the overall average for all studies in the
database were 255 kg N ha1, 480 kg N ha1 and 360 kg N ha1 per
season, respectively. Fertilizer-induced emissions via N2O and N
leaching showed similar trends in open-field systems, with lower
emission rates at higher SRs (Table 2). However, higher SRs
contributed to increases in fertilizer-induced NH3 volatilization in
open-field systems. Compared with synthetic N fertilizer alone, the
rates of total Nr losses were lower through replacing synthetic N
with organic fertilizer in open-field systems. In greenhouse sys-
tems, combined applications of organic and synthetic N fertilizers
generally decreased fertilizer-induced N leaching, while fertilizer-
induced N2O and NH3 emissions barely changed at SR
35% and
35%<SR
70%, compared to applying synthetic N fertilizer alone.
However, the lowest fertilizer-induced N2O emission was observed
at the highest SR (SR>70%, 2.35 kg N ha1). Total Nr losses were
significantly decreased following replacement of synthetic N fer-
tilizer in greenhouse systems. Overall, compared to synthetic N
fertilizer alone, substitution by organic fertilizer significantly
reduced fertilizer-induced N2O emission and N leaching, while
promoting fertilizer-induced NH3 volatilization. The total Nr losses
were decreased by 15e40 kg N ha1 per season compared to
synthetic N alone (Table 2).
Considering both direct and indirect GHG, total GHG emission
tended to be decreased as a result of combined applications of
organic and synthetic N fertilizers. The total GHG emission from
greenhouse systems barely changed relative to synthetic N fertil-
izer alone, except at high SR (SR>70%). Combined applications of
organic and synthetic N fertilizers increased SOC stock, which
largely offset total GHG emission. Consequently, net global warm-
ing potential (GWP) was much lower than that of synthetic N fer-
tilizer (Table 3). In addition, greenhouse vegetable systems had a
greater potential to decrease net GWP than open-field systems.
4. Discussion
4.1. Responses of crop productivity to combined applications of
organic and synthetic N fertilizers
Improving crop yield and mitigating environmental costs are
great challenges for agricultural development. Overall, the results
of this meta-analysis have demonstrated that combined applica-
tions of organic and synthetic N fertilizers did not significantly
improve vegetable yield relative to synthetic N fertilizer alone, and
this is consistent with previous results (Xia et al., 2017). This main
reasons were attributed to the reduced proportion of available N
supply with slow organic N mineralization (Zhou et al., 2016) and
stimulation of microbial N immobilization (Choi et al., 2001; Said-
Pullicino et al., 2014). In addition, this meta-analysis indicated
high substitution rates (SR>70%) resulted in the negative response
of yield, whereas vegetable yield was increased by 5.5e5.6% on
average relative to synthetic N fertilizer alone when SR were
70%
(Fig. 2 a). These rates of increased crop yield are similar to those
previously reported, e.g. a 6.6% increase for upland crops in China
(Zhang et al., 2020). The increase of vegetable yield through
appropriate substitution of synthetic N with N from organic re-
sources is mainly attributed to improved synchrony of nutrient
supply and improvement in soil properties. First, slow release of N
from organic fertilizer can maintain long-term N supply to better
match the N demand by the vegetable crop (Liu et al., 2012). Sec-
ond, organic fertilizer increases soil organic C sequestration (Fig. 3)
and improves soil microbial biomass, abundance and activity
(Watts et al., 2010), thus promoting nutrient cycling in soil. Third,
the organic resources provide additional essential micronutrients,
such as copper and zinc (Gil et al., 2008). Additionally, organic

Table 2
Fertilizer-induced N2O emission, N leaching and NH3 volatilization per season at different substitution rates (SR) in open-field and greenhouse systems, respectively, calculated
by mean N application rate and emission factors. Reactive nitrogen (Nr) losses are the sum of fertilizer-induced N2O emission, N leaching and NH3 volatilization. All data are in
kg N ha-1.

Item Synthetic N fertilizer 35%
SR 35%<SR
70% SR>70%

1 a
Open-field (255 kg N kg )
Fertilizer-induced N2O emission 4.08 2.58 2.40 2.55
Fertilizer-induced N leaching 24.4 18.3 10.5 ND
Fertilizer-induced NH3 volatilization 24.7 24.5 36.0 ND
Total Nr losses 53.2 45.4 48.8 ND
Greenhouse (480 kg N kg1)a
Fertilizer-induced N2O emission 3.55 3.84 3.94 2.35
Fertilizer-induced N leaching 114 63.8 41.6 38.5
Fertilizer-induced NH3 volatilization 6.96 6.91 5.76 6.00
Total Nr losses 125 74.6 51.3 46.9
Overall (360 kg N kg1)a
Fertilizer-induced N2O emission 4.79 3.31 3.10 2.59
Fertilizer-induced N leaching 63.7 42.1 21.5 ND
Fertilizer-induced NH3 volatilization 26.2 32.3 34.4 ND
Total Nr losses 94.7 77.7 59.0 ND

Note: ND indicates no data.

a
The values in parentheses are mean N rate in experimental observations.

7
B. Liu, X. Wang, L. Ma et al. Environmental Pollution 269 (2021) 116143

Table 3
Budgets of greenhouse gas (GHG) emission per season at different substitution rates (SR) in open-field and greenhouse systems, respectively. Total GHG emissions are the sum
of direct GHG emission and indirect GHG emission.

Item Synthetic N fertilizer 35%
SR 35%<SR
70% SR>70%

Open-field
Direct GHG emission (Mg CO2-eq ha-1)a 1.70 1.07 1.00 1.06
Indirect GHG emission (Mg CO2-eq ha-1)b 0.17 0.15 0.18 ND
Total GHG emission (Mg CO2-eq ha-1) 1.87 1.22 1.18 ND
dSOC stock (Mg C ha-1) 1.18 5.20 5.84 4.54
Net GWP (Mg CO2-eq ha-1)c 2.46 17.8 20.2 ND
Greenhouse
Direct GHG emission (Mg CO2-eq ha-1)a 1.48 1.60 1.64 0.98
Indirect GHG emission (Mg CO2-eq ha-1)b 0.37 0.22 0.15 0.14
Total GHG emission (Mg CO2-eq ha-1) 1.85 1.82 1.79 1.12
dSOC stock (Mg C ha-1) 1.01 8.64 8.75 7.67
Net GWP (Mg CO2-eq ha-1)c 1.85 29.9 30.3 27.0
Overall
Direct GHG emission (Mg CO2-eq ha-1)a 1.99 1.38 1.29 1.08
Indirect GHG emission (Mg CO2-eq ha-1)b 0.30 0.26 0.20 ND
Total GHG emission (Mg CO2-eq ha-1) 2.29 1.64 1.49 ND
dSOC stock (Mg C ha-1) 1.06 6.14 7.78 5.93
Net GWP (Mg CO2-eq ha-1)c 1.60 20.9 27.0 ND

Note: ND indicates no data.

a
Direct GHG emission ¼ Fertilizer-induced N2O emission  44/28  265 (IPCC, 2014).
b
Indirect GHG emission ¼ (Fertilizer-induce N leaching  0.75% þ Fertilizer-induced NH3 volatilization  1.0%)  44/28  265.
c
Net GWP ¼ Total GHG emission－dSOC stock  44/12.

resource amendments improve soil water holding capacity, po-
rosities and aggregate structure (Naveed et al., 2014). However,
high SR (SR>70%) induced a decrease in vegetable yield (Fig. 2 a),
with similar results being reported in previous studies (Zhang et al.,
2020; Zhuang et al., 2019), and may be the result of inadequate
supply of available N to meet crop demand. Substitution of syn-
thetic N with organic N fertilizer can reduce the available N supply
to the crop by two modes; i) a direct reduction in the available N
applied via the organic fertilizer, and ii) the stimulation of microbial
immobilization of soil mineral N through the addition of the
additional carbon in the organic fertilizer (Choi et al., 2001; Said-
Pullicino et al., 2014). This highlights the importance of opti-
mizing the substitution rate, and the balance of organic fertilizer
and synthetic N fertilizer applied to crops.
The low N application rate resulted in reduction of vegetable
yield, due to less plant available N in the soil following substitution
with organic N fertilizer. In the presence of sufficient N supply
levels (moderate and high N application rates), combined applica-
tions of organic and synthetic N fertilizers were capable of main-
taining and even increasing vegetable yields (Fig. 2 a), which agrees
with the study by Zhang et al. (2020). These results imply available
N rate is the main limiting factor to vegetable yield. The responses
of crop yield to organic fertilizers depend on their nutrient content
and nutrient availability. The mineralization rate of organic N to
mineral forms is controlled by C/N ratio (Bhogal et al., 2016;
Chadwick et al., 2000). Manure has a low C/N ratio relative to plant
straw, and can mineralize at faster rates (Chantigny et al., 2001;
Wang et al., 2015), thus there was no marked change of yield be-
tween animal-based N sources compared to synthetic N fertilizer
alone (Fig. 2 a). In contrast, applying N from plant-based N sources
tended to decrease vegetable yield, as a result of slow N minerali-
zation rate and high microbial N immobilization due to high C/N
ratio of the plant-based organic fertilizer input (Said-Pullicino et al.,
2014; Scotti et al., 2015). However, positive effects of applying plant
straw on vegetable yields have been shown in long-term field ex-
periments (Rong et al., 2018). Mixed animal-plant or other organic
N sources can be used to optimize the C/N ratio, to satisfy N and C
demand, favoring vegetable yields (Fig. 2 a). Our meta-analysis
indicates that combined applications of organic and synthetic N
fertilizers resulted in a better effect on yield in open-field systems
8
(4.6% increase) than in greenhouse systems. This is probably
because of the lower yield level and poor soil fertility in open-field
systems, and suggests a greater potential for improving yield in
open-field systems.
Compared to synthetic N fertilizer alone, combined applications
of organic and synthetic N fertilizers reduced N uptake by an
average of 15.9% (Fig. 1). Although vegetable yield was improved at
SR
70%, N uptake was not notably changed and was sometimes
lower than that of synthetic N fertilizer alone. We hypothesize that
this may be related to the limited root systems of vegetable crops
not being capable of accessing the reduced quantity of available N
following combined applications of organic and synthetic N fertil-
izers. However, the decrease in N uptake under positive responses
of yield may be resulted from unbalanced distribution of data.
Because of the decrease in vegetable yield, N uptake and NUE were
significantly lower at high SR (SR>70%). Similarly, N uptake
decreased with the reduction of vegetable yield at the low N
application rate and use of plant-based N sources. On the other
hand, the results of effects on N uptake and NUE were uncertain, so
more studies that would incorporate these practices will be needed
to draw more precise conclusions.
4.2. Responses of Nr losses to combined applications of organic and
synthetic N fertilizers
Overall, combined applications of organic and synthetic N fer-
tilizers markedly decreased N leaching, although there were no
significant changes in N2O emission and NH3 volatilization (Fig. 1).
Generally, minimizing the soil mineral N pool contributes to
reduced Nr losses, and this is thought to be due to increases in N
uptake and NUE (Cui et al., 2013; Yao et al., 2017). However, our
results indicated that N uptake and NUE were not increased (Fig. 1).
We believe that some N forms from the organic fertilizer remain in
the soil, as evidenced by the increase in soil total nitrogen con-
centration (Fig. S3). As a result, soil mineral N concentration might
be decreased, and thus N leaching was reduced (by 44.6%) relative
to synthetic N fertilizer alone (Figs. 1 and 3 b). Another factor
influencing decreases in N leaching is the modified soil structure
and increased SOM following repeated organic fertilizer inputs,
both of which retain moisture and reduce the volume of water
B. Liu, X. Wang, L. Ma et al.
leaching through the soil (Gao et al., 2011). Any increase in soil CEC
with higher SOM content will also help to retain N in the soil
(Blanco-Canqui and Lal, 2009). The significant effect of combined
applications on reducing N leaching in this study was greater than
the results of Xia et al. (2017), who reported a 28.9% reduction when
synthetic N was partially replaced with organic fertilizer in grain
crops. This may be due to the greater N leaching losses in vegetable
systems (with limited rooting) than cereal systems.
Our study demonstrated that N2O emissions were barely
changed as a result of combined applications of organic and syn-
thetic N fertilizers compared to synthetic N fertilizer alone, but
large variations were detected (Fig. 3 a), and similar results were
also reported by Xia et al. (2017) and Zhang et al. (2020). Never-
theless, the results of a global meta-analysis indicated manure
application significantly stimulated N2O emission, by an average of
32.7% (Zhou et al., 2017). N2O is mainly produced by microbial
nitrification or denitrification, which are dependent on multiple
factors, including the availability of C and N substrate as well as
oxygen, soil properties (texture and pH), and environmental con-
ditions (Charles et al., 2017; Zhou et al., 2017). Application of
organic fertilizer not only affects substrate availability of N and C
used by microbes to produce N2O (Chen et al., 2014; Thangarajan
et al., 2013), but it also modifies soil aeration, especially oxygen
availability (Zhou et al., 2017). Therefore, effects of organic fertilizer
application on N2O emission are variable (Charles et al., 2017; Zhou
et al., 2017). Further research is needed to improve our mechanistic
understanding of how the biotic (microbial activities, constitution)
and abiotic factors (manure characteristics, climate, soil texture,
soil moisture and soil pH) interact and control N2O production and
emission following organic fertilizer application to soil in vegetable
systems. It is worth noting that N2O emission was decreased at the
high SR (SR>70%), which is consistent with previous reports (Xia
et al., 2017; Zhang et al., 2020; Zhuang et al., 2019), suggesting
reducing excess available N in the soil is an effective way to mitigate
N2O emission. Compared with synthetic N fertilizer alone, N2O
emission increased by 24.9% following combined applications of
organic and synthetic N fertilizers in the greenhouse systems (Fig. 3
a). The higher soil temperatures in greenhouse systems may be
responsible for increased microbial N turnover and supply of
available N and C substrate, enhancing soil nitrification-
denitrification processes, and stimulating N2O production and
emission (Mori and Hojito, 2012; Zhou et al., 2017).
Although there was no significant difference in N2O emission
between the different organic fertilizer types, animal-based N
sources tended to increase N2O production relative to synthetic N
fertilizer alone, probably because they supplied greater pools of
available C and N substrates for nitrification and denitrification
(Chadwick et al., 2000; Velthof et al., 2003), whereas organic fer-
tilizers with high C/N ratios, e.g. plant-based N sources depleted
available N in the soil (via N immobilization), decreasing N2O
production (Chen et al., 2013). Also, N2O emission is controlled by
soil texture, climate and soil pH (Charles et al., 2017; Xia et al., 2018;
Zhou et al., 2017), so large variations were observed (Fig. 1; Fig. 3 a).
Further measurements are needed to provide evidence of the ef-
fects of combined applications of organic and synthetic N fertilizers
on N2O emissions in vegetable production systems.
We found no significant difference in NH3 volatilization be-
tween combined applications of organic and synthetic N fertilizers
versus applying synthetic N fertilizer (urea or ammonium-N) in this
study (Fig. 1). However, previous studies have indicated that
applying organic fertilizer significantly decreases NH3 volatilization
(Hao et al., 2012b; Xia et al., 2017). This may be due to differences in
organic fertilizer and soil properties (Bouwman et al., 2002). Im-
provements in soil CEC induced by the application of organic fer-
tilizer could increase sorption of ammonium in the soil, reducing
9
Environmental Pollution 269 (2021) 116143
NH3 emission (Duan and Xiao, 2000). At the high N application rate
and in greenhouse systems, NH3 emissions were significantly
decreased relative to synthetic N fertilizer alone, whilst no signif-
icant difference was presented in open-field systems (Fig. 3c); but
EFs for NH3 volatilization tended to be increased with SRs (Table 1).
Misselbrrok et al. (2002) showed that applying organic fertilizers
could enhance NH3 volatilization relative to synthetic N fertilizer
alone, especially in acidic soils, which may be associated with
increased soil pH through applying organic fertilizer. Besides, ef-
fects on NH3 volatilization were affected by organic fertilizers type,
because composition of nitrogen, especially ammonium, varied
widely in different organic fertilizers, which was an important N
source for NH3 volatilization. Therefore, more site-specific experi-
ments are needed to be conducted to supply data on NH3 volatili-
zation in different vegetable systems.
4.3. Emission factors for Nr losses
Overall, the effects of combined applications of organic and
synthetic N fertilizers mainly decreased EFs for N2O and leaching
but did not affect EFs for NH3 (Table 1). The study indicated mean
EFs for N2O were 1.33% and 0.72%e0.92% under synthetic N fertil-
izer and combined applications of organic and synthetic N fertil-
izers, respectively, which was greater than that previously
reported, 0.69% EF for N2O, by Wang et al. (2018a), based on a meta-
analysis in vegetable systems in China. These differences may be
caused by different criteria of data collection. Our dataset contains a
large proportion of EFs for N2O from synthetic N fertilizer only
treatments, which were included to quantitatively compare with
combined applications of organic and synthetic N fertilizers,
resulting in a greater overall EFs for N2O. So, the N2O EFs from the
combined applications of organic and synthetic N fertilizer in this
study (0.72%e0.92%) are more typical of common N management
in China’s vegetable production systems and this range is closer to
previously reported values (Rashti et al., 2015). The EFs for N2O in
greenhouse systems were slightly lower than those in open-field
systems, which may be related to the higher SOM in greenhouse
systems (Wang et al., 2018a; Yang et al., 2019).
Overall, average N leaching EFs were 17.7% from applying syn-
thetic N fertilizer alone, and ranged from 5.97% to 11.7% through
combined applications of organic and synthetic N fertilizers.
Similar results for N leaching were reported by Wang et al. (2018b),
with a mean N leaching EF of 14.6%. For both open-field and
greenhouse systems, N leaching EFs of combinations of organic and
synthetic N fertilizers were significantly lower than those of syn-
thetic N fertilizer alone (Fig. 1). It is noteworthy that N leaching EFs
in greenhouse systems were ca. two times higher than those in
open-field systems, which may result from frequent irrigation,
longer growing seasons and greater nitrification rate in greenhouse
systems. EFs for NH3 in greenhouse systems were much lower than
those in open-field systems, being <5% in greenhouse and ca. 10% in
open-field systems, which agrees with previous studies (Hao et al.,
2012b; Ti et al., 2015). Relatively lower partial pressure of NH3
induced by fast air diffusion is beneficial to NH3 emission to air in
open-field systems. In addition, the higher soil moisture content
may help inhibit NH3 volatilization in greenhouse systems. A
greater understanding of factors controlling NH3 volatilization from
vegetable systems is needed, especially from open-field systems.
4.4. Fertilizer-induced Nr losses and budgets of GHG under
combined applications of organic and synthetic N fertilizers
Promoting soil C sequestration is an important method to
reduce net GHG emissions into the atmosphere. Our study indi-
cated SOC sequestration was significantly increased under
B. Liu, X. Wang, L. Ma et al.
combined applications of organic and synthetic N fertilizers, irre-
spective of substitution rate, N application rate, organic fertilizer
type or cultivation type (Fig. 4). In addition, the promotion of good
aggregate structure may help in SOC occlusion and reduced
decomposition, contributing to increasing SOC content
(Thangarajan et al., 2013). To some extent, application of synthetic
N fertilizer alone can still help increase in SOC compared to soil
without fertilization (Ding et al., 2013; Blanco-Canqui and Schlegel,
2013), due to a greater input of root and aboveground residues, and
the results of our study demonstrate this too (Table 1). However,
the capacity to increase SOC content by application of synthetic N
fertilizer alone is limited (Ding et al., 2013; Pan et al., 2019). Our
study also showed that at higher substitution rates, the soil carbon
stocks increased in both open-field and greenhouse systems
(Table 1). Since, there is an equilibrium of soil C sequestration rates
with time (Minasny et al., 2017), it is important to establish long-
term monitoring systems to quantify this.
Generally, CH4 emissions are rare from soils in upland fields in
China, because the aerobic conditions inhibit the activities of
methanogens (Cai et al., 2000). In this study, there was a lack of data
on CH4 emissions from open-field and greenhouse vegetable sys-
tems, so we were unable to consider the effects of CH4 on the
overall GHG balance. Net GWP, defined as GHG emissions and C
change in soil, is used to reflect the C balance of agricultural soils
(Koga et al., 2010; Mosier et al., 2006). Because of increased SOC
stocks, soil used to produce vegetables are a net sink of GHG
(Table 3). A decrease in total GHG emissions was seen in open-field
systems as a result of synthetic N fertilizer substitution; however,
this was only seen at the high substitution rate (SR>70%) in
greenhouse systems. The difference may be attributed to the effects
of stimulation of N2O in greenhouse soils. High concentrations of
residual mineral N, frequent irrigation and tillage are also be key
controls of N2O emissions highlighting the importance of under-
standing the effect of management practices on N2O emissions in
different vegetable systems.
In the study, GHG emissions of storage, treatment and trans-
portation of manure were not considered. Zhong et al. (2013) re-
ported GHG emissions were two times greater during composting
than those of land application. Thus, the benefits of SOC seques-
tration to mitigation global warming may be largely outweighed by
GHG emissions from the other parts of the manure management
chain (Chadwick et al., 2011). In addition, GHG emissions associated
with organic and synthetic fertilizer manufacture were not
included. Life Cycle Assessment approaches would be needed to
explore the wider impacts of combining organic and synthetic
fertilizers, by expanding the boundaries to include upstream
processes.
4.5. Uncertainties of the analysis
In the current study, we focused on the effects of SR, cultivation
type, N application rate and organic fertilizer type on agronomic
and environmental indicators following combined applications of
organic and synthetic N fertilizers in different vegetable systems in
China. In practice, the effects of these factors operate in combina-
tion (i.e. not singly), but due to the lack of data we were unable to
explore the effects of interacting factors. For example, studies
included different management practices, vegetable species, crop
rotations in both open-field and greenhouse vegetable systems,
and the effects of SR, N application rate and organic fertilizer type
on crop productivity, Nr losses and SOC would have varied between
these systems. Importantly, differently treated organic fertilizers
(e.g. fresh manure, compost, anaerobic digestate) have different
properties, such as C/N ratio, N and P forms, dry matter and water
contents and pH, which result in different effects on crop
10
Environmental Pollution 269 (2021) 116143
productivity, Nr losses and SOC sequestration (Chadwick et al.,
2000; Zhang et al., 2020; Zhou et al., 2017). Unfortunately, spe-
cific organic fertilizer types were seldom reported in original pa-
pers. Additionally, our study was unable to account for the effects of
different vegetable species (e.g. leafy vegetables, fruity vegetables,
and stem vegetables) and cultivation season (e.g. winter-spring
season, autumn-winter season, winter season), so more site-
specific field experiments are needed. Furthermore, the changes
of Nr emission and SOC may not be stable in different seasons
(spring, summer or autumn), so annual and long-term assessments
are necessary.
4.6. Implications and perspectives
Our study used meta-analysis to demonstrate that combined
applications of organic and synthetic N fertilizers can achieve
“double-wins” of improved crop production with reduced envi-
ronmental losses, when synthetic N fertilizer substitution rates
were no more than 70%. Mixed animal-plant base organic fertilizers
were better options for organic-substitute strategies. For open-field
systems, further research is needed to develop strategies to reduce
N leaching and NH3 volatilization, e.g. via manure acidification
(Fangueiro et al., 2015), deep placement application of organic and
inorganic N fertilizers (Pan et al., 2016; Webb et al., 2010). However,
to reduce N2O emissions from greenhouse systems, a switch to
organic fertilizers with high C/N ratio (straw, treated manure etc.)
would be useful, due to the negative correlation between N2O
emission and C/N ratio (Chen et al., 2013; Zhou et al., 2017).
Alongside fertigation, combined applications of organic and syn-
thetic N fertilizer may make a significant contribution to agronomic
and ecological benefits. Whilst combined applications of organic
and synthetic N fertilizers have many benefits, other nutrients,
especially phosphorus (P) should not be ignored (Edmeades, 2003).
Organic fertilizers are generally rich in P, and if the soil already has a
high P status, then additional P is not needed and represents an
increased risk of polluting watercourses via leaching or runoff
(Edmeades, 2003; Liu et al., 2007). In this case, P based organic
fertilizer management (Maguire et al., 2008) should be a priority.
Quantifying the effects of combined applications of organic and
synthetic N fertilizers on crop productivity, Nr losses and SOC
changes and providing practical management strategies is helpful
for policy makers to promote the implementation of zero growth of
chemical fertilizer, further facilitating sustainable development of
whole cropping-livestock systems. Currently, because of increased
labor costs for fertilization, organic fertilizers are mainly applied to
cash crops (vegetables, tea, fruits), because the greater economic
benefits from increased yields may compensate these costs. In or-
der to promote application of organic fertilizers, governments
should increase subsidies for transportation and application of
organic fertilizers, further gaining more economic and ecological
benefits. However, further assessments of the effectiveness of
substituting synthetic fertilizers with organic fertilizers should also
consider phosphorus (Jia et al., 2015; Yan et al., 2016), heavy metals
(Qaswar et al., 2020) and antibiotic accumulation (Guo et al., 2018)
induced by long-term application of organic fertilizer.
5. Conclusion
This meta-analysis showed that vegetable yields were signifi-
cantly increased by 5.5%e5.6% with no significant changes of N
uptake and NUE, when synthetic N substitution rates (SRs) were

70%. Combined applications of organic and synthetic N fertilizers
contributed to the reduction of N leaching, although N2O emission
and NH3 volatilization were not be affected at any substitution
rates. Using mixed animal-plant sources of organic fertilizer was
B. Liu, X. Wang, L. Ma et al.
better than using single organic fertilizer types on yields and Nr
losses. Organic and synthetic N fertilizer application rates were
main contributors to various Nr losses.
Soil organic carbon was increased by 12.5% compared to syn-
thetic N fertilizer alone. Higher synthetic N substitution rates
favored higher SOC sequestration and lower GHG emissions.
Although high substitution rates provide the best strategy to reduce
Nr losses and GHG to the environment, this is at the expense of crop
yield.
Credit author statement
Bin Liu: Formal analysis, Writing - original draft. Xiaozhong
Wang: Writing - original draft. Lin Ma, Dave Chadwick, Xinping
Chen: Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgments
The authors would like to thank the National Key R&D Program
of China (No. 2017YFD0800403), and State Cultivation Base of Eco-
agriculture for Southwest Mountainous Land, Southwest
University.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.envpol.2020.116143.
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