Science of the Total Environment 850 (2022) 158064

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Science of the Total Environment

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Responses of crop productivity and reactive nitrogen losses to the application

of animal manure to China's main crops: A meta-analysis
Fengling Ren a,b,1, Nan Sun b,1, Tom Misselbrook c, Lianhai Wu c, Minggang Xu b, Fusuo Zhang a, Wen Xu a,
⁎
a
College of Resources and Environmental Sciences, National Academy of Agriculture Green Development, Key Laboratory of Plant–Soil Interactions, Ministry of Education,
National Observation and Research Station of Agriculture Green Development (Quzhou, Hebei), China Agricultural University, Beijing 100193, China
b
Key Laboratory of Arable Land Quality Monitoring and Evaluation, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning,
Chinese Academy of Agricultural Sciences, Beijing 100081, China
c
Sustainable Agriculture Sciences, Rothamsted Research, North Wyke, Okehampton, Devon EX20 2SB, UK

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Yields decreased when substitution rate of

mineral N with manure was >70 %.
• Soil organic carbon content was nega-
tively correlated with reactive nitrogen
losses.
• Soil properties or N inputs were the main
factors affecting response in N losses.
• Substitution of mineral N with manure at
≤50 % can sustain yield and mitigate N
loss.

A R T I C L E I N F O A B S T R A C T

Editor: Elena Paoletti The effective utilization of manure in cropland systems is essential to sustain yields and reduce reactive nitrogen (Nr)
losses. However, there are still uncertainties regarding the substitution of mineral nitrogen (N) fertilizer with manure
Keywords: in terms of its effects on crop yield and Nr losses. We conducted a comprehensive meta-analysis of wheat, maize, and
Livestock manure rice applications in China and discovered that substituting mineral N fertilizer with manure increased wheat and maize
Substituting manure for fertilizer
yields by 4.9 and 5.5 %, respectively, but decreased rice yield by 1.7 %. The increase of yield is larger at low N appli-
Crop productivity
Reactive N losses
cation and low mineral N substitution rates ((SR) ≤30 %) for silt soils, warm regions, and acidic soils. High SR (>70 %)
Meta-analysis decreased rice yield as well as the N use efficiency of wheat and maize. Substitution of mineral N fertilizer with manure
resulted in lower NH3 volatilization for wheat (48.7 %), lower N2O and NH3 emissions, and N runoff for maize (12.8,
49.6, and 66.7 %, respectively), and lower total Nr losses for rice (11.3–26.5 %). The loss of Nr was significantly and
negatively correlated with soil organic carbon content. The rate of N application, soil properties, and climate were crit-
ical factors influencing N2O and NH3 emissions and N leaching, whereas climate or soil properties were the dominant
factors influencing response in N runoff. We concluded that in silt soils, warm regions, and neutral soils, a ≤ 50 % sub-
stitution of mineral N fertilizer with manure can sustain crop yields while mitigating Nr losses.

1. Introduction
⁎ Corresponding author.
E-mail addresses: xuminggang@caas.cn (M. Xu), wenxu@cau.edu.cn (W. Xu). Mineral nitrogen (N) fertilizer is a necessity for global crop production.
1
These authors contributed equally to this work. China accounts for only 7 % of the world's arable land, but it feeds nearly

http://dx.doi.org/10.1016/j.scitotenv.2022.158064
Received 9 June 2022; Received in revised form 3 August 2022; Accepted 12 August 2022
Available online 15 August 2022
0048-9697/© 2022 Elsevier B.V. All rights reserved.
F. Ren et al.
20 % of the global population (Fang et al., 2018). China's N fertilizer con-
sumption nearly tripled between 1980 and 2014 to attain high crop yields
(Liu et al., 2016). While high rates of mineral N fertilizer improve crop
yields, they also increase reactive nitrogen pollution (Nr). Therefore,
China has a large N surplus and a low N use efficiency (NUE). The crop
NUE in China ranges from 25 to 36 %, much lower than the >50 % achieved
in most developed countries (Ju et al., 2009). Excessive N use results in Nr
emissions to the environment, such as N leaching and runoff to ground and
surface waters, and emissions of N2O and NH3 to the atmosphere (Xia et al.,
2017; Hou et al., 2021; Meng et al., 2022), with environmental conse-
quences including water and air pollution (Feng et al., 2022; Xu et al.,
2022), and soil acidification (Guo et al., 2010). Cropland is estimated to
account for roughly half of total Nr losses in the global food supply chain
(Bodirsky et al., 2015), with increasing occurrence in developing countries,
particularly China and India. Thus, management strategies to reduce the
use of mineral N while maintaining yields and thus mitigating environmen-
tal impacts are required.
China has a large livestock production sector, with an average annual
mean production of 23 Tg of N in the form of manure, which is close to
half of its fertilizer N consumption (Zhang et al., 2020). However, owing
to the high labor cost of transportation and spreading as well as the lack
of proper storage and processing facilities, only a small proportion of ma-
nure is applied to arable land (Niu and Ju, 2017). Substituting mineral N
fertilizer with manure increased the carbon (C) addition to the soil, which
can promote coupling of the C and N cycles, stimulating mineral N immobi-
lization and soil N transformations to reduce N losses from arable soils
(Zhou et al., 2016a). Manure is high in nutrients that are readily available
to crops, reducing the need for mineral fertilizer (Du et al., 2020). Further-
more, manure can regulate crop N uptake, improve soil fertility, and
increase soil C sequestration, resulting in higher grain yield. (Pan et al.,
2009). Chen et al. (2014) found that applying manure to over 150 field
experiments in China increased crop yields by 8.5–14.2 Mg ha−1 when
compared to mineral fertilizer. Thus, substituting mineral N fertilizer with
manure can be an effective and economical management measure strategy
for maintaining crop yields while reducing environmental damage.
Manure application on Nr losses can be influenced by management
practices, soil properties, and climatic conditions. Soil texture, for example,
determines pore size distribution and thus oxygen availability for soil
aeration and manure decomposition, which affects the dynamics of N trans-
formations associated with Nr losses in different soils (Ji et al., 2011). Typ-
ically, sandy soils are less capable of retaining water and nutrients, and the
application of manure N in conjunction with increased water infiltration
can promote the loss of Nr (Blanco-Canqui and Lal, 2009). Soil acidity
affects soil's physical and biological properties, as well as plant growth,
thereby affecting Nr losses (Thangarajan et al., 2013). Moreover, manage-
ment practices, such as flooding rice (Oryza sativa L.) fields (Zhang et al.,
2013a) and the rate of N application, as well as climatic conditions (Zhou
et al., 2017), can affect the manure decomposition and N transformation
processes and thus, affect the Nr losses. However, there are only a few stud-
ies conducted for detailed examination of the influence of these explana-
tory factors, particularly their relative importance to the loss of Nr.
Wheat (Triticum aestivum L.), maize (Zea mays L.), and rice are the
world's main food crops, accounting for 63 % of total crop production in
China, but their production consumes >50 % of the world's mineral N fer-
tilizer (Zhang et al., 2017), and >15 million t per year in China alone
(Chen et al., 2017). The NH3 emissions from these three crops account for
approximately 70 % of the mineral N-induced NH3 emissions from
China's croplands (Ma et al., 2020). In addition, the NUE of rice in China
is <30 %, and substantial quantities of N are lost to watercourses. However,
there are no systematic investigations of Nr losses from these three impor-
tant crops.
Using meta-analytical studies, there has been a significant focus on pro-
ducing guidance for farmers and parameterizing relevant C and N models
on the contribution of manure application to crop yields and losses of Nr
(Xia et al., 2017; Zhou et al., 2017; Zhang et al., 2020). The reported effect
of the manure application on crop yields is inconsistent, with some studies
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Science of the Total Environment 850 (2022) 158064
indicating an increase and others a decrease in crop yields after amendment
with manure, depending on soil and climatic conditions and crop type
(Edmeades, 2003; Chen et al., 2014; Xia et al., 2017). Similarly, there are
contradicting observations in the scientific literature regarding the effect
of manure application on N2O emissions relative to mineral N fertilizer
(Akiyama and Tsuruta, 2003; Rochette et al., 2004; Ding et al., 2013).
Responses to Nr losses vary across cropping systems, and cover crops vary
in their ability to reduce surface runoff and soil erosion (Jiao et al., 2012;
Hou et al., 2018). Significant differences in rainfall intensity, water storage
capacity, soil oxygen levels, and other soil properties between upland and
paddy rice fields can influence N leaching and runoff responses (Hou
et al., 2021). Additionally, derived average emission factors (EF) for N2O
and NH3 following manure application vary between upland and paddy
soils (Zhou et al., 2017; Zhang et al., 2020). Such EF has not yet to be
determined for wheat, maize, and rice across the major intensively man-
aged cultivation systems in China, limiting the ability to develop accurate
emission inventories. Therefore, an improved understanding of the effect
of substituting manure for mineral N fertilizers on crop yields and Nr losses
for wheat, maize, and rice is required to minimize Nr losses while maximiz-
ing crop yields across the main intensive agricultural cropping systems in
China.
Recent meta-analyses have addressed several aspects of substituting
manure for mineral N fertilizer (Du et al., 2020; Wei et al., 2020; Xia
et al., 2017; Zhang et al., 2020). Du et al. (2020) compared crop yield
and soil properties under manure and mineral fertilizer applications but
did not account for the same N input. Another recent meta-analysis focused
solely on the substitution of mineral N fertilizer with manure in crop pro-
duction on upland and paddy land (Zhang et al., 2020). Wei et al. (2020)
only evaluated the evaluated maize productivity, and N and C emissions re-
sponses. However, the high complexity of cropland Nr dynamics highlights
the importance of a comprehensive assessment on the pathways of Nr losses
rather than focusing on a single Nr loss or a particular crop. A recent meta-
analysis has evaluated the effects of the manure substitution on crop
productivity, Nr losses and identified critical impact factors and drivers of
Nr losses (Liu et al., 2021). However, the research on cereals were not de-
termined, but there are distinct Nr losses between vegetables and cereals.
Xia et al. (2017) investigated the global responses of whole grain yield in
general and Nr losses to the substitution on a global scale without consider-
ing crop types, experimental durations, N application rates and soil proper-
ties. Furthermore, the relationships between Nr losses and C sequestration
following manure application have not fully explored, although few studies
have reported a strong association between Nr losses and C sequestration in
agroecosystems (Fan et al., 2017; Liu et al., 2021). To evaluate the overall
environmental effects of manure amendments, it is crucial to account for
the interactions between Nr losses and C sequestration. Further, neither
climate conditions nor key soil physical and chemical properties were re-
ported, nor the primary determinants of Nr losses following the substitution
of mineral fertilizer N with manure were distinguished in the published
analyses, which hinders our understanding of the underlying mechanisms
of Nr losses after manure application.
In this context, we conducted a meta-analysis to integrate published re-
sults from field studies in China on the effect of substituting manure for
mineral N fertilizers on crop productivity (crop yield, N uptake, and NUE)
and Nr losses (N2O emission, NH3 volatilization, N leaching, and N runoff)
across the three major staple crops (wheat, maize, and rice). Information on
management and environmental conditions having the potential of
influencing Nr losses were also extracted to enable a predictive and mech-
anistic understanding of these losses.
2. Materials and methods
2.1. Data collection
Peer-reviewed journal papers published between 1990 and 2021 and
indexed by the Web of Science (http://apps.webofknowledge.com/) or
the China Knowledge Resource Integrated Database (http://www.cnki.
F. Ren et al. Science of the Total Environment 850 (2022) 158064

net/) were searched and retrieved according to defined criteria. The com- 2.3. Data analysis
bined search terms related to manure (swine, sheep, poultry, farmyard ma-
nure, cattle, horse, and livestock), crops (wheat, maize, and rice), crop A meta-analysis was conducted to analyze differences in crop productiv-
productivity (yield, NUE, and crop N uptake), and Nr losses (N2O emission, ity and Nr losses between manure-amended and mineral N-fertilized treat-
NH3 volatilization, N leaching, and N runoff). To select appropriate studies, ments. The logarithmic response ratio (RR) has been utilized extensively as
the following criteria were used in particular: 1) cropland studies on wheat, a measure of fertilization effect:
maize, or rice growth in China; 2) the number of treatment means and
samples number was reported; 3) the treatments included a control using RR ¼ ln ðxt =xc Þ (1)
only mineral N fertilizer as the reference and treatments with a full or par-
tial substitution of N fertilizer with manure; 4) a substitution rate, expressed where t and c represent the manure-amended and the control (mineral fer-
as the ratio of N input from manure to total N applied in treatment, was tilizer N only) treatment, respectively, and x is the mean for variable x.
reported or could be derived; and 5) at least one of the target variables The percentage change in a specific variable in manure-amended treat-
(yield, N uptake, NUE, N2O emissions, NH3 volatilization, N leaching, and ments compared to mineral N fertilizer-only treatments was calculated as
N runoff) was quantified, and cumulative losses over a growing period (eRR++-1) × 100 %, where RR++ is based on the weighted response
were reported. Nitrogen losses are needed to be expressed as kg N ha−1 ratio (Hedges et al., 1999):
and total aboveground crop N uptake reported for the grain crops.
m ki
A total of 334 peer-reviewed studies were extracted (Data S1, Supple- ∑ ∑ wij RRij
i¼1 j¼1
mentary Material). Geographical locations, climatic variables (mean annual RRþþ ¼ (2)
m ki
temperature [MAT] and mean annual precipitation [MAP] for each site, soil ∑ ∑ wij
i¼1 j¼1
parameters in the top 20 cm soil layer (soil texture, soil pH, soil organic car-
bon [SOC] content, soil total N [TN] content, soil clay content and soil bulk
where m represents the number of levels for a given variable; ki is the num-
density [BD]) in the treatment plots, and manure and mineral N application
ber of comparisons made between the treatments that have been amended
rates in the treatments, were all included and used to quantify statistical
with manure, and the control at the ith level; RRij is the RR for the ith level
relationships with Nr losses.
and the jth pair, and Wij is the weighting factor for the ith level and the kth
i
pair and expressed as follows:
2.2. Evaluated variables and grouping
1
The following definitions and calculations were used to standardize the wij ¼ (3)
v
target variables throughout the studies:
Nitrogen uptake can be defined as the amount of N present in the crop's where v is a variance:
aboveground biomass. The NUE can be defined as the difference in N up-
take between treatments with and without fertilization divided by the SD2t SD2c
v¼ 2 þ (4)
total N rate for the fertilization treatment. Similarly, EF for N2O emission, nt xt nc x2c
NH3 volatilization, N leaching, and N runoff was calculated as the differ-
ence in N loss between the treatments with and without fertilization di- where nt and nc are the number of samples in the manure-amended treat-
vided by the total rate of N application. The values were either reported ment and the control, respectively, and SDt and SDc are the standard devia-
by the studies or calculated as previously described. tion of the manure-amended treatment and the control, respectively.
The MAT (−1.5–19.5 °C) and MAP (127–1975 mm) varied greatly The standard error of RR++ was calculated as follows:
across the sites studied. Therefore, the cropland in China was divided into vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
u 1
three climatic regions with distinct climates and cropping systems: NTM u
SðRRþþ Þ ¼ u m ki (5)
(temperate monsoon climate with the double cropping of wheat–maize, t
∑ ∑ wij
wheat–rice, wheat–soybean, etc.,), NTC (temperate continental climate i¼1 j¼1
with mono-cropping in one year or three cropping in two years), and
STM (subtropical monsoon climate with double-or three cropping of Therefore, the 95 % confidence interval (CI) of RR++ is given as:
wheat-rape, rice-rape, rice-rice, etc.) (Wang et al., 2013). The N application
rates were grouped into three levels: into three application levels: low 95%CI ¼ RRþþ  1:96SðRRþþ Þ (6)
(〈200), middle (200−300) and high (>300 kg N ha−1). There were four
SR groups: <30 %, 30–50 %, 50–70 % and > 70 %. Soil pH was categorized If the 95 % CI for a given variable did not span 0, the treatment was con-
into three groups (acid soils, ≤6; neutral soils, 6–8; alkaline soils, ≥8) (Ren sidered to represent a significant increase (the overall mean RR > 0) or de-
et al., 2019). The soil texture categories were based on the Chinese soil tex- crease (overall mean RR < 0) compared with the mineral N fertilizer
ture classification (Xiong and Chen, 1986), with three groups: sandy (Sand treatment (P < 0.05). If the CI did span 0, the treatment was considered
content >50 %; Clay content <30 %), silt (Sand content 20–50 %; Clay con- to have no significant impact on that variable compared with the reference
tent <30 %) and clay (Sand content <20 %; Clay content >30 %). (P > 0.05).
The effects of mineral N substitution with manure on crop productivity For the analysis, the METAWIN 2.1 software (Rosenberg et al., 2000)
and reactive N losses for wheat, maize, and rice as well as the overall effects was used. The overall response ratio of all paired observations (control
of mineral N substitution with manure on soil C and nitrogen dynamics, and manure-amended treatment) was determined first. At each categorical
were evaluated in three categories: (1) Nr losses (including N2O emissions, level, the response ratio of each categorized variable was determined. In ad-
NH3 volatilization, N leaching and N loss with runoff), (2) crop productivity dition, the heterogeneity (Qb) between groups of specific variables was
(yield, NUE and crop N uptake) and (3) soil chemical properties in the top assessed using the chi-square test. Compared to the other factors included
20 cm soil layer (SOC, TN, dissolved organic carbon (DOC), dissolved or- in the analysis, a significant response (P < 0.05) and large Qb values for cat-
ganic nitrogen (DON), particulate organic carbon (POC), particulate or- egorical variables are considered to predict changes in the total response
ganic nitrogen (PON), soil microbial biomass C (SMBC), soil microbial ratio more accurately.
−
biomass nitrogen (SMBN), NH+ 4 , NO3 and soil pH). The conceptual dia- Using a Random Forest (RF) model analysis (Breiman, 2001; Liaw and
gram illustrating the investigation of the interactions between Nr losses Wiener, 2002) the key factors regulating Nr losses were determined. The
and SOC sequestration would provide a better understanding of the overall RF procedure was applied using the “RandomForest” package in R (version
effects of manure application on soil N and C cycles. 3.3.3). All the statistical analyses were carried out using SPSS v. 12.5 (SPSS,

3
F. Ren et al.
Inc., Chicago, IL, USA). A one-way analysis of variance (ANOVA) with a
least significant difference test (LSD) (at P < 0.05) was used to evaluate
the influence of different fertilization treatments on the Nr losses and the
EF of losses of Nr. Using a Pearson correlation coefficient, the association
between the RR of Nr losses and other parameters was analyzed.
3. Results
3.1. Overall effects of substituting mineral N fertilizer with manure
Overall, the substitution of fertilizer N with manure increased wheat
and maize yields by 4.9 and 5.5 %, respectively, but significantly decreased
rice yield by 1.7 % (Fig. 1). However, there were no significant effects on
crop N uptake. The substitution of manure for wheat lowered NH3 emis-
sions by 48.7 % but had no significant influence on N2O, N runoff, or N
leaching. In contrast, the application of manure to maize decreased NH3
emissions by 49.6 %, N2O emissions by 12.8 %, and N runoff by 66.7 %,
while not affecting N leaching. All Nr losses were significantly reduced
for rice (NH3 volatilization: -26.1 %; N2O emission: −20.8 %; N runoff:
−26.5 %; and N leaching: −11.3 %).
3.2. Effects on crop productivity
Fig. 2 depicts the effects of the independent variables on the observed
effects of crop yield, N uptake, and NUE. At low N application rates, the ad-
dition of manure enhanced wheat and maize yields by 12.9 % and 12.6 %,
respectively, but did not affect rice yields. The yield was unaffected by the
higher N application rates. Except for maize, which had a significant de-
crease in NUE at the lowest N application rate (≤200 kg N ha−1) there
was no significant effect of N application rate on crop N uptake or NUE.
At a low SR (≤30 %), fertilizer substitution with manure increased
wheat (19.4 %) and maize (9.2 %) yields but did not affect rice yield but
the rice yield was decreased (12.8 %) at a high SR (>70 %). Similarly, at
a high SR (>70 %), N uptake and NUE responses were lower and soil texture
had a significant impact. In silt soils, replacing mineral N fertilizer with ma-
nure increased wheat, maize, and rice yields by 4.0, 5.3, and 3.4 %, respec-
tively. The responses in rice yield varied based on soil texture (P < 0.05),
with a reduction in sandy (4.9 %) and clay (2.8 %) soils. Soil texture did
not affect the effects of manure on wheat and maize yields (P > 0.05). In
contrast to the yield response to the substitution of fertilizer with manure,
there was a significant decrease in the response in NUE response in silt
soils for wheat (20.3 %) and maize (29.6 %) but an increase for that of
rice (23.6 %). Similarly, the N uptake for the rice increased in the silt soils.
The use of manure instead of fertilizer increased wheat (4.9 %) and
maize (3.9 %) yields in the NTM region while decreasing NUE by 19.9 %
and 27.0 %, respectively. There were no rice experiments in the NTM re-
gion. Except for rice, where yield was significantly reduced (6.4 %), there
was no significant effect of manure substitution on crop productivity in
the NTC region. In the STM region, substitution with manure only led to
an increase in maize yield (13.5 %) and N uptake in wheat (32.8 %).
Fig. 1. Summary of the overall effects of partial or full substitution of mineral N fertilizer by manure, compared to mineral fertilizer N only, on crop yield, N uptake, nitrogen
use efficiency (NUE), N2O emission, NH3 volatilization, N runoff and N leaching. Data presented are means with 95 % confidence intervals, with number of observations
given in parentheses.
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Science of the Total Environment 850 (2022) 158064
The substitution of fertilizer with manure in acid and neutral soils in-
creased wheat yields (21.6 % and 10.9 %, respectively) and maize yields
(7.7 % and 10.6 %, respectively) but reduced rice yield by 2.0 % in neutral
soils. In alkaline soils, it also reduced rice yield by 8.7 %. Furthermore,
manure substitution reduced the NUE for wheat and maize in alkaline
soils. Manure had a negative effect on maize N uptake only in alkaline
soils. There was insufficient data to assess any response in rice N uptake
in alkaline soil.
3.3. Impacts of substituting mineral N fertilizer with manure on the losses of Nr
Fig. 3 depicts the effects of the assessed variables on the relative re-
sponse to fertilizer substitution with manure in N2O and NH3 emissions
for the various crops. There were no significant variations in N2O emissions
with different N application rates in wheat, whereas decreased NH3 emis-
sions were observed at all N application rates (by 33.1–56.5 %). N2O and
NH3 emissions from maize were reduced when fertilizer was replaced
with manure at the highest N application rate, but there was no significant
effect at lower rates. In rice, no significant difference was observed in the
emissions of N2O and NH3 at a high application rate of N but decreased sig-
nificantly at lower rates (both rates for NH3 and the 200–300 kg ha−1 rate
for N2O). With the exception of N2O emissions from wheat, where there
was no significant effect of SR, emission reductions were greatest at the
highest SR (>70 %). There was no significant effect of soil texture on N2O
emissions response in wheat, but NH3 emissions were significantly reduced
by 43.4–48.5 % across all soil types. Silt soil had the greatest effect on N2O
emissions in maize and rice, with reductions in emissions of 29.6 and
78.2 %, respectively. Similarly, the effect on NH3 emissions in maize
(57.4 %) was significantly lower in silt soils. The response to manure substi-
tution in wheat was consistent across all climatic regions, with a significant
reduction in NH3emissions (43.4–48.5 %) but no significant change in N2O
emissions. Substitution with manure in maize in the NTM region resulted in
significantly lower N2O (23.6 %) and NH3 (54.6 %) emissions than in other
climatic regions. Soil pH did not affect wheat N2O emissions, but NH3
emissions were significantly reduced in neutral (56.4 %) and alkaline
(36.7 %) soils.
Fig. 4 depicts the effects of the variables on the response in N losses to
water for various crops. At N application rates of 200–300 kg N ha−1, re-
placing mineral fertilizer N with manure reduced N runoff in wheat by
38.3 % (Fig. 4). There was a significant decrease in N runoff at all applica-
tion rates in rice, with no significant effect of rate, while N leaching was sig-
nificantly lower at highest application rates (>300 kg N ha−1). The high SR
(>70 %) was associated with decreased N leaching for maize (31.5 %) and
rice (56.7 %). Owing to limitations in data availability, the effects of
substituting mineral N fertilizer with manure on N runoff in the NTC region
and sandy soils could not be assessed. In clay soils and the NTM region,
wheat substitution with manure resulted in a significant decrease in N run-
off. However, manure substitution only resulted in decreased N leaching for
rice in clay soils and the STM region, with no significant effect of soil type or
region on the response in N leaching for wheat or maize.
F. Ren et al.
Fig. 2. Influence of N application rate, mineral N fertilizer substitution rate (SR), soil texture, climate type and soil pH on the response in crop yield, N uptake and nitrogen use
efficiency (NUE) of wheat, maize and rice to partial or full substitution of mineral N fertilizer with manure, compared to mineral N fertilizer only. Substitution rate is defined
by manure nitrogen input/total nitrogen input. Data presented are means with 95 % confidence intervals, with number of observations given in parentheses. P values
represent significant difference between categories within a subgroup if P < 0.05.
3.4. Influencing variables on Nr losses after substituting mineral fertilizer with
manure
With the exception of N runoff, the N losses were positively correlated
with N input, which was the most important factor (Figs. 5 and 6). Both
MAT and MAP were also important factors determining the changes in
N2O following manure treatment (Fig. 5). N application rate, followed by
SOC, TN, and soil pH, clearly illustrates the response of NH3 emissions to
manure substitution (Fig. 5). In both paddy and upland soils, there was a
significant negative linear relationship between Nr losses and SOC content
after manure application, i.e., higher SOC contents were accompanied by a
greater reduction in Nr loss (Fig. 7).
4. Discussion
4.1. Crop productivity
Overall, our meta-analysis reveals that the partial substitution of min-
eral N fertilizer with manure increased wheat and maize yields by approx-
imately 5 %, while the NUE and N uptake in wheat is dramatically
increased at lower SR. The substitution of mineral N fertilizer with manure
promoted organic C supply (Fig. 8), which can facilitate the microbial im-
mobilization of bioavailable N that is subsequently released more evenly
throughout the crop growing season, resulting in an improved N uptake
and crop yield (Edmeades, 2003). While mineral fertilizer alone offers mac-
ronutrients, the combination of manure and mineral N fertilizers gives extra
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Science of the Total Environment 850 (2022) 158064
micronutrients that are not provided by mineral fertilizer alone and change
the chemical and physical properties of soil. This results in improved avail-
ability of the nutrients to the plants and positively influenced the crop yield
(Diacono and Montemurro, 2010). However, improved plant N uptake is
not always associated with an improved NUE due to changes in N allocation
within the plant, resulting in harvest index variations (ratio of grain/total
biomass) (Duan et al., 2014). The rice yield was significantly reduced at
SR >70, which is consistent with recent studies reported by Xia et al.
(2017) and Zhang et al. (2020). This could be associated with the decreased
availability of N in manure compared to inorganic fertilizer, which inhibits
root establishment during the early stages of crop development (Zhao et al.,
2015). This difference in yield response between wheat/maize and rice is
consistent with the previous findings indicating a lower yield response to
manure treatment in paddy rice than in upland crops (Du et al., 2020;
Zhang et al., 2020). This may be due to the greater mineralization of organ-
ically bound manure N in the more aerobic soils under wheat and maize
(Dawe et al., 2003), compared with the anaerobic soils for paddy rice.
This study also examined the effect of management strategies, cli-
mate, and soil characteristics on crop productivity response to N fertil-
izer substitution with manure. Relatively higher increases in crop
yield were observed in warm/humid climate regions and silt soils.
These soil aeration, temperature, and moisture conditions promoted
manure decomposition and nutrient release and enhanced the availabil-
ity of C and N (Mandal et al., 2007). The increases in yield were also
more pronounced in acidic soils. This observation is supported by
Zhang et al. (2020) and Du et al. (2020), primarily because manure
F. Ren et al. Science of the Total Environment 850 (2022) 158064

Fig. 3. Influence of N application rate, mineral N fertilizer substitution rate (SR), soil texture, climate type and soil pH on the response in N2O emission and NH3 volatilization
for wheat, maize and rice to partial or full substitution of mineral N fertilizer with manure, compared to mineral N fertilizer only. Substitution rate is defined by organic
nitrogen input/total nitrogen input. Data presented are means with 95 % confidence intervals, with number of observations given in parentheses. P values represent
significant difference between categories within a subgroup if P < 0.05.

liming protects crops from aluminium toxicity. Various studies have
demonstrated that the sole application of mineral N fertilizer can signif-
icantly reduce soil pH, inhibiting crop growth (Lungu and Dynoodt,
2008). Manure application reduces the effect of mineral fertilizer on
soil pH (Noble et al., 1996), enhancing indirect C input through
increased crop yields.
4.2. Nr losses and driving factors
The manure application in conjunction with mineral N fertilizer has
been reported to increase the absorption of fertilizer N by plants through
the biotic and abiotic retention of N, thus reducing N loss from soils
(Cui et al., 2013). The application of manure increased the SOC (by an

Fig. 4. Influence of N application rate, mineral N fertilizer substitution rate (SR), soil texture, climate type and soil pH on the responses in N runoff and N leaching for wheat,
maize and rice to partial or full substitution of mineral N fertilizer with manure, compared to mineral N fertilizer only. Substitution rate is defined by manure nitrogen input/
total nitrogen input. Data presented are means with 95 % confidence intervals, with number of observations given in parentheses. P values represent significant difference
between categories within a subgroup if P < 0.05.

6
F. Ren et al. Science of the Total Environment 850 (2022) 158064

Fig. 5. Relative importance of independent variables as influencing N2O emission, NH3 volatilization, N runoff and N leaching after full or partial substitution of mineral
fertilizer N with manure as determined using random forests (RF) models.

average of 12.8 %) (Fig. 8), thus boosting the activity of heterotrophs that
immobilize NH+ 4 (Peng et al., 2006). An increase in SOC directly improves
moisture retention, and soil structure to reduce the volume of water
leaching through the soil, and increases the soil cation exchange capacity
(CEC), all of which help to retain N in the soil (Blanco-Canqui and Lal,
2009). Hence, manure application is an effective method for increasing N
immobilization while decreasing N losses to the environment.
4.2.1. Nr losses through gaseous pathways
N2O
The literature is inconclusive on whether manure application increases
N2O emissions compared to mineral N fertilizer use, and the reported effect
range is most likely due to differences in climate, soil conditions, and land
use (Zhou et al., 2017). According to the current study, replacing N fertil-
izer with manure reduced N2O emissions in maize and rice, in contrast to

Fig. 6. Relationships between N application rate and Nr loss rate following field application of fertilizer and manure N. Different crop types are indicated by different colors:
grey = rice, blue = maize, orange = wheat; n, the number of observations; R2, the coefficient of determination. P values represent significance if P < 0.05.

7
F. Ren et al. Science of the Total Environment 850 (2022) 158064

Fig. 7. Relationships between soil organic carbon content and Nr loss rate following field application of fertilizer and manure N. Different crop types are indicated by different
colors: blue = upland, orange = paddy; n, the number of observations; R2, the coefficient of determination. P values represent significance if P < 0.05.

a previous meta-analysis that found no effect from manure substitution crops. This study estimated an average N2O EF of 0.36 ± 0.44 % for
(Xia et al., 2017). However, most of the data reported by Xia et al. (2017) mineral fertilizer and 0.35 ± 0.60 % for manure substitution in maize
are related to composted manure, and the effects were reported across all soils. However, the uncertainty in the EFs of N2O is relatively large.

Fig. 8. Effects of substitution of mineral N with manure on crop productivity and reactive N losses for wheat, maize and rice and overall effects of substitution of mineral N with
manure on soil C and nitrogen dynamics in black box. All data were derived from the results of this meta-analysis. SOC, soil organic carbon; DOC, dissolved organic carbon; POC,
particulate organic carbon; SMBC, soil microbial biomass carbon; SMBN, soil microbial biomass nitrogen; DON, dissolved organic nitrogen; PON, particulate organic nitrogen.

8
F. Ren et al. Science of the Total Environment 850 (2022) 158064

A reduction in N2O emissions associated with the substitution of Table 2

fertilizer N with manure is most likely due to a decrease in soil inorganic Pearson's correlation coefficients (r) between reactive nitrogen (Nr) losses and
N availability and the contrasting effects of adding easily decomposable or- controlling factors.
ganic C. Organic C substrates can increase the activity and efficiency of de- Parameters LnRR of variables
nitrification in the soil, with N2 as the main product rather than the N2O N2O emission NH3 volatilization N leaching N runoff
(intermediate product) (Ball et al., 2004). In addition, more labile organic
MAP −0.159⁎⁎ 0.076 0.100 0.113
C can increase the ability of microorganisms to assimilate mineral N, MAT −0.141⁎⁎ −0.047 0.046 0.037
thereby reducing the available substrates for nitrification or denitrification N amount −0.072⁎⁎ −0.421⁎⁎ −0.013⁎ −0.247⁎⁎
(Fontaine et al., 2003). The application of manure comparatively decreased SOC −0.146⁎⁎ −0.099⁎ −0.015 −0.189⁎
the emissions of N2O from rice soils than those in maize soils, while TN −0.114⁎ −0.106 −0.156⁎ −0.198⁎
pH 0.076 0.037 0.075 0.187⁎
exhibiting a significant increase in wheat soils (Fig. 1). Additionally, the av-
BD 0.084 −0.183⁎⁎ −0.010 −0.043
erage N2O EFs of manure applied to wheat (mean: 0.36 %) and maize soils Clay −0.193⁎⁎ −0.054 0.062 −0.033
(mean: 0.35 %) were higher than those for rice soils (mean: 0.14 %)
MAT: mean annual temperature, MAP: mean annual precipitation, N amount: N ap-
(Table 1). The results are consistent with a global meta-analysis that de-
plication rate, TN: soil total nitrogen content, SOC: soil organic carbon content car-
rived average EFs for the application of manure to upland and rice paddy
bon, pH: soil pH, BD: soil bulk density, Clay: soil clay content.
soils of 1.87 and 0.24 %, respectively (Zhou et al., 2017). Because paddy ⁎ P < 0.05.
rice soils are often highly anaerobic, a large proportion of the N2O produced ⁎⁎ P < 0.01.
is reduced to N2, especially after manure application (Zhou et al., 2015).
The mean N2O emissions in rice (Fig. S1, 0.80–0.85) were also lower than
in upland soils (Fig. S1, 1.32–1.46). Therefore, it is possible that N2O emis- reduction. Because much of the manure used in cropland in China is
sions are not a significant N-loss pathway in paddy soils. composted, the potential for NH3 emissions is relatively low, with the ma-
The response in N2O emission to the fertilizer N substitution with ma- jority of available ammonium N content being volatilized or immobilized
nure was significantly influenced by soil texture (P < 0.05), and there was during the composting process. The addition of readily decomposable C
a negative relationship between N2O emission and soil clay content to manure may also increase NH+ 4 by heterotrophs in the soil, further re-
(Table 2). Soil texture influences the soil pores size and distribution, ducing NH3 volatilization (Choi et al., 2004). Our findings indicating the
which are responsible to control the O2 availability in the soil, thereby high NH3 emissions and NH3 EF in rice soils were consistent with the previ-
influencing N2O emissions. Zhou et al. (2017) and Charles et al. (2017) ous studies for China (average 15.2 %) (Chen et al., 2014; Zhou et al.,
also found that manure substitution reduced N2O emissions more in fine- 2016b; Wang et al., 2018) and overlap with the reported 3.8–28.4 % and
textured soils than in sandy soils. This is primarily because nitrification is 7.4–18 % losses from mineral fertilizer and manure, respectively, applied
the primary process by which N2O is emitted in more aerobic sandy soils to rice soils (Zhang et al., 2020). This may be attributable to the prevalence
(Zhou et al., 2013). An increase in the soil clay content is associated with of ammonium-based fertilizers in China, as well as the imprecise surface
decreased soil aeration and oxygen availability, as well as a decrease in broadcasting technology employed in rice fields (Ju et al., 2009). In addi-
the rate of decomposition of the applied manure and the associated inor- tion, the release of NH3 is governed by the concentration of NH+ 4 –N in
ganic N release (Skiba and Ball, 2002). The lower gas diffusivity in clay floodwater, where buffering capacity is limited, and photosynthesis by
soils may also assist in the reduction of N2O to N2 via denitrification algae can also contribute to NH3 emissions from paddy soils (Sommer
(Weitz et al., 2001). et al., 2004).
The response of N2O emissions in maize was significantly affected by In silt or NTM region soils, where manure degrades relatively quickly,
climate, and MAT and MAP were identified as important influencing fac- there was a greater reduction in NH3 emissions following fertilizer substitu-
tors. Das and Adhya (2014) reported a decrease in N2O emissions under tion with manure. Ammonia emissions were found to be negatively corre-
warm and wet conditions, with increased SOC from manure application re- lated with SOC content (Fig. 6), presumably because of its effect on soil
sulting in more complete denitrification, with a higher proportion of the CEC, with lower NH3 emission in soils with higher CEC (Bouwman et al.,
gaseous end-product as N2 rather than N2O. In contrast, a global meta- 2002) due to the greater NH+ 4 adsorption and removal from the soil solu-
analysis found a 34 % increase in N2O emissions after manure application tion (Al-Kanani et al., 1991). The same effect was observed in clay soils
in warm temperate climates versus cool temperate climates (Zhou et al., owing to the presence of higher CEC. According to Rochette et al. (2013),
2017). The effect of climate on N2O emissions requires further study. NH3 emissions increase rapidly when soil pH exceeds 7, with the equilib-
NH3 rium between NH3 and NH+ 4 shifted towards the release of more NH3 at
The highest SR for all crops resulted in a significant reduction in NH3 higher pH (Roelle and Aneja, 2002).
emissions (Fig. 3). Ammonia emission is a major pathway for N loss
(Table 1), owing to the high proportion of urea fertilizer use on cereals in 4.2.2. Nr losses through hydrological pathways
China (Zhang et al., 2013b), which has a relatively high NH3 EF compared Compared with mineral fertilizer N, particularly NO−
3 -N, manure-N is
to other fertilizer types. Therefore, it has a greater potential for emission less soluble. Manure decomposes slowly and releases more available N,

Table 1
Mean emission factors for N2O emission, NH3 volatilization, N leaching and N runoff under different treatments in Chinese croplands. n is the number of observations.
Emission factor (%) Wheat maize rice

Treatment n Mean SD n Mean SD n Mean SD

N2O emission Min 60 0.39a 0.42 79 0.36a 0.44 39 0.23a 0.37

OM 115 0.36a 0.63 128 0.35a 0.60 54 0.14b 0.19
NH3 volatilization Min 30 8.17a 7.92 24 9.64a 5.45 33 10.21a 10.02
OM 73 3.71b 4.33 70 8.15a 5.85 42 9.44a 8.76
N leaching Min 22 4.41a 7.37 28 17.77a 22.14 10 4.73a 6.27
OM 24 3.04a 5.50 53 15.27b 13.54 17 4.52a 4.05
N runoff Min 14 5.90a 10.01a 11 2.71a 2.90 22 7.62a 9.60
OM 16 2.33b 3.83b 22 2.23b 1.30 44 5.16b 6.40

Note: Min: mineral N fertilizer only as the reference treatment; OM: treatments with a full or partial substitution of mineral N fertilizer with manure.
Data with different letters denote significant differences between Min and OM at P < 0.05.

9
F. Ren et al.
thus it is less likely to be removed by surface runoff or subsurface leaching
(Zhao et al., 2015). The manure application may influence hydrological
pathways due to its beneficial effect on crop productivity via improved
ground cover, soil structure, and soil capability to retain water (Obour
et al., 2010). According to Hou et al. (2021), the rate of N application
was the best predictor of N leaching losses, and the reduction in N leaching
and runoff was greater with the partial substitution of manure at higher ap-
plication rates. A significant management strategy for controlling N losses is
the reduction of overall fertilizer use, which has been excessive during the
1990s, as reported by Diao et al. (2020).
The intensity of rainfall is an important factor in determining losses via
hydrological pathways, with losses occurring predominantly during the
rainy season (Bouraima et al., 2016). The response of N leaching and runoff
losses to the substitution of fertilizer N with manure application showed a
positive, but no significant association with precipitation (Table 2). Losses
from leaching and runoff can be highly site-specific because they are not
only influenced by precipitation but also by soil conditions (Douglas
et al., 1998) and, more generally, by changes in climate, hydrology, fertil-
izer use, soil properties, topography and erosion (Vagstad et al., 2004;
Zhang et al., 2007). We identified only a weak association between N
leaching and runoff and the parameters examined in the present investiga-
tion (Table 2). Soil BD is a significant soil compaction parameter that influ-
ences soil-air-water interactions, microbial activity, nutrient absorption,
water content, and water retention capacity (Martınez and Zinck, 2004).
Due to its greater SOC content, soil with a high clay content typically retains
water and nutrients more effectively than other soils (Six et al., 2002). The
soil texture affects the runoff N, particularly in dryland soils that lack sur-
face water and have a plough pan, which is typically characteristic of
paddy soils to prevent water movement (Zhang et al., 2013a). When ma-
nure was applied, leaching and runoff losses were negatively correlated
with SOC content, which may be attributed to the influence of SOC on
crop production and N uptake, hence lowering N surplus and losses (Wei
et al., 2021). Furthermore, the increase in CEC is associated with higher
SOC reduces the loss of NH+ 4 and improves the ability to retain the highly
mobile NO− 3 (Blanco-Canqui and Lal, 2009).
4.3. Uncertainties of the analysis
Our analysis focused on the effects of SR, N application rates, climate
types, soil texture and soil pH on crop productivity and Nr losses in China
assuming their influence is independent. In fact, they might have interac-
tive impacts. Due to the lack of data availability we were unable to explore
this. Variations of soil properties (soil nutrient conditions and soil texture),
manure quantity and quality, irrigation amount, and irrigation method all
have a significant impact on soil N conversion, introducing some uncer-
tainty into the upscaling of national soil Nr losses. The effect of manure
application on Nr losses with different experimental durations is because
continuous manure application will increase SOC content, which may
result in improved soil structure and fertility over time. However, the exper-
imental durations are not considered in this study, which can lead to some
uncertainties. Furthermore, the driving factors of Nr losses, and the
relationship between SOC sequestration and Nr losses, may differ between
wheat, maize, and rice, necessitating separate evaluations for each crop.
4.4. Limitations and recommendations
This study performed a comprehensive meta-analysis to integrate
previously published results on the responses of crop productivity and
Nr losses to the substitution of mineral N fertilizer by manure. The sub-
stitution of mineral N fertilizer with manure could be a significant po-
tential strategy for enhancing agricultural sustainability, although
practices need to be designed according to site-specific conditions. De-
spite this comprehensive examination, further studies are needed to de-
termine the factors that affect the losses of Nr from the soils of wheat,
maize, and rice. The quantity and specific properties of manure applica-
tion, such as soluble C and N content and the C:N ratio, as well as the
10
Science of the Total Environment 850 (2022) 158064
method of application, all have an impact on Nr losses in different
crops (Charles et al., 2017; Zhou et al., 2017; Wei et al., 2021). How-
ever, these specific manure properties were rarely described in prior in-
vestigations, therefore, we did not analyze the effect of manure
properties on Nr losses. The close coupling of the C and N cycles might
result in antagonistic effects, such as an increase in SOC stock and simul-
taneous simulation of N2O or NH3 emissions. To optimize the advan-
tages across agricultural productivity and environmental losses in
wheat, maize, and rice soils, it is important to clarify the connections be-
tween the C and N cycles after substituting manure for mineral N fertil-
izer. The provided data were insufficient to analyze the changes in SOC
and draw definite conclusions regarding the effects of fertilizer substitu-
tion with manure on C sequestration and its interaction with Nr losses.
Paddy soils are an significant source of CH4 emissions, which contribute
significantly to GHG balance (Shang et al., 2011). The increase in SOC
stocks caused by manure application for rice soils could be largely coun-
tered by CH4 emissions from manure, hence the stimulation of CH 4
emissions caused by manure application should be considered.
5. Conclusions
This meta-analysis found that partial replacement of mineral N by
manure improved wheat and maize yields by about 5 %, on average,
but resulted in a slight decrease in rice yield. The partial substitution
of mineral N by manure can also minimize Nr losses, however, the size
and significance of the effect differed among crop varieties and were in-
fluenced by specific variables, such as N application rate, manure substi-
tution rate, climate, soil texture, and soil pH. The difference in Nr losses
was primarily attributable to the N application rate. In silt soil, a warm
climate, and neutral soil conditions, the highest advantage in terms of
improving crop yield and reducing Nr losses was attained at a substitu-
tion rate of about 50 %.
CRediT authorship contribution statement
Fengling Ren: Formal analysis, Writing – original draft. Nan Sun:
Writing – original draft. Tom Misselbrook: Writing – review & editing.
Lianhai Wu: Writing – review & editing. Minggang Xu: Conceptualiza-
tion, Writing – review & editing. Fusuo Zhang: Conceptualization,
Writing – review & editing. Wen Xu: Conceptualization, Funding acqui-
sition, Project administration, Supervision, Writing - original draft,
Writing - review & editing.
Data availability
I have shared the source to my data in the Supplementary material
Declaration of competing interest
The authors declare that they have no known competing financial inter-
ests or personal relationships that could have appeared to influence the
work reported in this paper.
Acknowledgments
This study was supported by the National Key Research and Development
Program of China (2021YFD1700900, 2021YFD1901205), the National
Natural Science Foundation of China (42175137, 42177341), the BBSRC
(BBS/E/C/00010320), the Natural Environment Research Council (NE/
S009094/1), and the High-level Team Project of China Agricultural
University.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2022.158064.
F. Ren et al.
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