Winter wheat yield and water use efficiency response to organic fertilization in northern China: A meta-analysis

Agricultural Water Management 229 (2020) 105934

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Winter wheat yield and water use efficiency response to organic fertilization in northern China: A meta-analysis

T

Linlin Wanga,b, Qiang Lic, Jeffrey A. Coulterd, Junhong Xiea,b,*, Zhuzhu Luoa,e, Renzhi Zhanga,e, Xiping Dengf, Linglin Lia,b,* a

Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou, 730070, China College of Agronomy, Gansu Agricultural University, Lanzhou, 730070, China c College of Forestry, Henan Agricultural University, Zhengzhou, 450002, China d Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN, 55108, USA e College of Resources and Environment Science, Gansu Agricultural University, Lanzhou, 730070, China f State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, 712100, Shaanxi, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: Winter wheat Organic fertilizer Grain yield Water use efficiency Yield variability

Nitrogen (N) application is a basic practice for increasing cereal yield and efficient utilization of N sources is key to sustainable intensification. A meta-analysis was conducted to determine how organic fertilization (i.e., livestock manure) affects yield, yield variability and water use efficiency (WUE) of winter wheat (Triticum aestivum L.) in northern China, and how this is impacted by N management and growing environment. Organic fertilization significantly increased grain yield and WUE by an average of 18 and 20 % compared to without organic fertilizer, respectively, and also reduced spatial and temporal yield variability. Compared to without organic fertilizer, change in grain yield was +24, +28, and −11 % for treatments of synthetic nitrogen fertilizer plus organic fertilizer with the same level of synthetic nitrogen (NOF), decreased level of synthetic nitrogen fertilizer combined with organic fertilizer (NLOF), and a portion of synthetic nitrogen fertilizer replaced with organic nitrogen fertilizer at the same level of nitrogen (NROF), respectively. The positive effect of organic fertilizer on grain yield and WUE of winter wheat was greatest when yield levels was < 4.0 Mg ha–1. Moreover, organic fertilization was most effective at improving grain yield and WUE in North China Plain when synthetic N application was < 150 kg N ha−1 and in growing environments with SOM < 1.4 % and ET < 500 mm. These results demonstrate that applying organic fertilizer in combination with a decreased level of synthetic N fertilizer is an effective approach for advancing sustainable intensification of winter wheat in northern China, and that greatest benefits with organic fertilization may occur when local environmental factors (e.g., growing region and soil conditions) are appropriately considered.

1. Introduction

has increased markedly, improvements in crop yield have not been proportional to the increases in chemical N input (Hawkesford, 2014). Nitrogen fertilizer is a major cost in crop production (MasclauxDaubresse and Chardon, 2011) and excessive N application can have negative environmental effects, including nitrate leaching into groundwater, greenhouse gas emissions (Sainju et al., 2003; Wang et al., 2016), soil acidification (Guo et al., 2010), loss of soil organic matter (SOM) (Sainju et al., 2003; Tiessen et al., 1994), and deterioration in soil quality (Guo et al., 2010; Sainju et al., 2003; Tiessen

Increasing crop yield to meet the requirements of an ever-growing human population is a grand challenge facing society (Chen et al., 2014; Cui et al., 2018), which is exacerbated by limited and reduced resources for crop production, and variable and changing growing conditions (Pan et al., 2009). Applying nitrogen (N) fertilizer is a key approach to increase crop yield, especially for cereals (Teng et al., 2015; Wang et al., 2018a). Although N fertilizer use for crop production

Abbreviations: ET, evapotranspiration; N, nitrogen; NOF, synthetic nitrogen fertilizer plus organic fertilizer with the same level of synthetic nitrogen; NLOF, decreased level of synthetic nitrogen fertilizer combined with organic fertilizer; NROF, a portion of synthetic nitrogen fertilizer replaced with organic nitrogen fertilizer at the same level of nitrogen; SOM, soil organic matter; WUE, water use efficiency ⁎ Corresponding authors at: College of Agronomy and Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou, 730070, China. E-mail addresses: [email protected] (J. Xie), [email protected] (L. Li). https://doi.org/10.1016/j.agwat.2019.105934 Received 26 January 2019; Received in revised form 7 October 2019; Accepted 24 November 2019 Available online 10 December 2019 0378-3774/ © 2019 Elsevier B.V. All rights reserved.

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(3) organic fertilization will reduce spatial and temporal variation in yield.

et al., 1994). Increased input of inorganic N fertilizer, combined with the neglect of organic fertilizers as a source of nutrients, contribute to low N fertilizer use efficiency (Bao et al., 2006; Hawkesford, 2014). Excessive N application reduces risk of yield loss due to N deficiency and is a common practice in China (Wang et al., 2018a). This creates opportunity for farmers to reduce synthetic N fertilizer use without reducing grain yield (Hartmann et al., 2015; Zhang et al., 2017). Thus, there is great interest in reducing synthetic N input for crop production (Rieux et al., 2013). China has a long tradition of recycling organic nutrients in agriculture, but this tradition is rapidly disappearing following intensification and specialization of agricultural production with increased use of synthetic fertilizers (Cui et al., 2018; Rieux et al., 2013; Wang et al., 2007b). China’s excessive and inefficient use of synthetic fertilizers have contributed to its current harmful state of environmental pollution (Chen et al., 2014; Cui and Shoemaker, 2018; Zhang et al., 2008). With increasing concern about environmental protection, the Chinese government issued a policy of zero growth in synthetic N fertilizer use in 2015 (Xiong and Wu, 2017). Thus, improving crop yields while reducing synthetic fertilization are major goals in China. Recent studies have evaluated alternative fertilization strategies, which utilize organic amendments such as livestock manure (Fan et al., 2005; Liu et al., 2009, 2013; Wang et al., 2017b), green manure (GarciaFranco et al., 2015), and crop residues (Fan et al., 2005; Wang et al., 2007b). Some research has shown that application of organic fertilizer (i.e., livestock manure) can be a sustainable practice for crop production due to its ability to recycle nutrients and enhance soil quality (Fan et al., 2005; He et al., 2010; Kato and Yamagishi, 2011; Liu et al., 2009, 2013; Manna et al., 2007; Tiessen et al., 1994; Wang et al., 2007a, 2011, 2017b; Xu et al., 2009) while reducing environmental pollution (Fan et al., 2005; Sainju et al., 2003; Zhai et al., 2011). Other studies indicate that organic fertilizer reduces crop yield (Annett et al., 2007; Mäder et al., 2002; Mason et al., 2007; Seufert et al., 2012). Understanding the theoretical basis by which factors contribute to the discrepancy in crop yield response to organic fertilizer is key to advise the development and adoption of sustainable cropping systems. Winter wheat (Triticum aestivum L.) is an important crop in China, where its planting area and grain production are second only to that of rice (Oryza sativa L.) (Wang et al., 2018a). Winter wheat hectarage is concentrated in northern China, often in semi-arid environments, and N is typically the most yield-limiting nutrient for its production (Deng et al., 2006; Wang et al., 2018b). Therefore, knowledge of winter wheat grain yield and water use in response to organic fertilizer in China, and how this is affected by site, growing environment, and agronomic management such as N fertilizer rate and method of organic fertilization, is paramount for sustainable intensification of wheat production. Such knowledge could serve as a basis for sustainable production of other crops and a second green agriculture revolution (Li et al., 2018; Wang et al., 2018b). However, a literature synthesis to understand the response of winter wheat yield, evapotranspiration (ET), and water use efficiency (WUE) to organic fertilizer has not been conducted. Metaanalysis provides a formal statistical method to compare and integrate the results of multiple studies to reveal underlying factors contributing to responses and make inferences on regional and global scales (Gurevitch and Hedges, 1999). The present study is a meta-analysis of field experiments on winter wheat production in northern China that seeks answers to determine: (1) how grain yield, ET, and WUE of winter wheat respond to organic fertilizer, and whether this is influenced by growing region, ET, SOM, N fertilizer rate, or yield level; (2) how the method of organic fertilization affects winter wheat grain yield; and (3) whether organic fertilizer application can reduce spatial and temporal variation in winter wheat yield. We hypothesize that: (1) organic fertilizer application will result in greater yield and WUE without affecting ET compared to without organic fertilizer; (2) organic fertilization will be most effective at improving grain yield and WUE in drier environments with lower levels of SOM, N fertilizer input, and yield level; and

2. Materials and methods 2.1. Data search and collection A search of peer-reviewed publications was performed to collect data on the effects of organic fertilization (i.e., livestock manure) on yield and WUE of sole-cropped winter wheat grown in northern China. Data published in English were collected from the ISI-Web of Science (http://apps.webofknowledge.com/) and Google Scholar (https://xs. glgoo.net/), and data published in Chinese were collected from the China National Knowledge Infrastructure (http://www.cnki.net/) and Baidu Scholar (http://xueshu.baidu.com/). The keywords used for the search were organic fertilizer and grain yield or WUE and wheat. The year of publication was not restricted, but publications after July 2018 were not included. To avoid distortions caused by publication selection, the data chosen for use had to satisfy the following criteria: (1) the field studies must include a treatment with organic fertilizer application and a without organic fertilizer control; and (2) the means, standard deviations (or standard errors), and sample sizes of the variables concerned must be directly available or amenable to being calculated from the data. Data were recorded by experimental year for publications reporting results from multi-year experiments. After scrutinizing the search results, 776 observations from 177 studies conducted at 80 sites were selected for use (Fig. 1), 776 for grain yield and 179 for ET (water use during the growing season) and WUE (kg grain mm–1 ha–1). As not all studies reported winter wheat grain yield, ET, and WUE, the number of comparisons for these variables were unequal. The collected data for grain yield, ET, and WUE came from experiments located in the provinces of Anhui, Beijing, Jiangsu, Gansu, Hebei, Henan, Ningxia,

Fig. 1. Flowchart of the process of building the database and conducting the meta-analysis. 2

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Fig. 2. Location of field experiments in northern China that were included in this meta-analysis.

Shaanxi, Tianjin, Inner Mongolia, Hubei, Xinjiang, Heilongjiang, Shandong, and Shanxi (Fig. 2). Geographic, climate, water regime, and cropping system information for regions with experimental sites of winter wheat that were included in this meta-analysis are in Table 1. Based on the method of organic fertilization, the organic fertilizer treatment was classified into one of three categories: (1) synthetic nitrogen fertilizer plus organic fertilizer with the same level of synthetic nitrogen (NOF); (2) decreased level of synthetic nitrogen fertilizer combined with organic fertilizer (NLOF); and (3) a portion of synthetic nitrogen fertilizer replaced with organic nitrogen fertilizer at the same level of nitrogen (NROF). To explain variation in the response of winter wheat yield and WUE to environmental and site conditions, the following were obtained for each site-year: growing region, ET, SOM content, and N fertilizer rate. Some data (i.e., SOM content) unavailable in the peer-reviewed publications were obtained from the China Soil Science Database (http://vdb3.soil.csdb.cn/). According to diversity in geography, climatic conditions, and cropping systems for winter wheat production in northern China, the study areas were grouped into five regions: (1) North China Plain, (2) northwest region, (3) central plain irrigation region, (4) rice and winter wheat growing region, and (5) cold region. Evapotranspiration was categorized as < 300, 300–400, 400–500, and > 500 mm. Soil organic matter content and synthetic N fertilizer application rate were categorized according to previous studies (Wang et al., 2018b; Yu and Shi, 2015). Soil organic matter content was categorized as < 1.0 (extremely low), 1.0–1.4 (low), 1.4–2.0 (moderate), and > 2.0 % (fertile). Synthetic N fertilizer rate was categorized as 0, 0–100 (low), 100–150 (global average), 150–200 (recommended), 200–250 (farmers’ traditional rate), 250–300 (high), and > 300 kg ha–1 (ultra high).

R=

Xt Xc

(1)

Xt lnR = ln ⎛ ⎞ = lnXt − lnXc ⎝ Xc ⎠

(2)

where Xt is the mean of winter wheat yield, ET, or WUE in the organic fertilizer treatment and Xc is the mean of winter wheat yield, WUE or ET in the without organic fertilizer control. If Xt and Xc are normally distributed and Xc is unlikely to be negative, then lnR is approximately normally distributed with a mean of approximately the true response log ratio. The variance (V) of lnR was calculated using the following equation:

V=

St 2 Sc 2 + 2 Nt Xt Nc Xc 2

(3)

where St and Sc are the standard deviations for all comparisons in the treatment and control groups, respectively, and Nt and Nc are the sample sizes for the treatment and control groups, respectively. Several studies did not report values of standard deviations or standard error. In these cases, we calculated the average coefficient of variation within each data set and then back-calculated the standard error from the average coefficient of variation. Weighted means were used since individual experiments often differ in their statistical precision (Curtis and Wang, 1998). The weighted mean log ratio (ln R ) was used, which produces the greatest precision (minimum variance), and was calculated using the following equations: k

ln R =

∑i =1 k

wi ´ lnRi

∑i =1

2.2. Statistical analysis

wi ´ = Data were analyzed using the methods of meta-analysis described by Curtis and Wang (1998), Hedges et al. (1999), and Wang et al. (2017a). The natural log (lnR) of the response ratio (R) was calculated as the effect size in this meta-analysis, representing the effect of organic fertilizer application, using the following equations:

1 Vi

wi ´

(4)

(5)

where the weighting factor wi´ is the reciprocal of the total variance of lnRi (Curtis and Wang, 1998). A mixed or random effects model was employed to determine whether organic fertilizer application significantly affected each 3

Agricultural Water Management 229 (2020) 105934 Single cropping Single and double cropping Single cropping

dependent variable using the statistical software MetaWin 2.1 (Systat Software, Inc, San Jose, CA) with a resampling of 9999 iterations (Li et al., 2018; Rosenberg et al., 2000; Shcherbak et al., 2014; Wang et al., 2017a). Inverse variance statistical methods were adopted for the metaanalysis. A random effect model was adopted in cases of high heterogeneity (a chi-square P value < 0.05). We performed a KolmogorovSmirnov test and determined that the distribution of yield, WUE, and ET is not normal (P < 0.001) (Fig. 3). Means and 95 % confidence intervals (CI) on the estimated effect size were generated using the bootstrapping test (i.e., sampling with replacement of the size equal to the initial size of the subset repeated n = 9999 times) for yield, WUE, and ET in the study, as well as subgroups of yield, WUE, and ET (Shcherbak et al., 2014; Wang et al., 2017a). Groups with fewer than two valid comparisons were excluded from the meta-analysis. To facilitate interpretation, the percentage of change in winter wheat yield, WUE, and ET were calculated as (ln R −1) × 100. If the 95 % CI for a dependent variable did not overlap zero, the effect of organic fertilizer application was considered significant. Means of the different categorical variables were considered significantly different from one another if their 95 % bootstrapping CIs did not overlap (Curtis and Wang, 1998; Wang et al., 2017a). A positive percentage change indicated an increase in the respective variable with organic fertilizer relative to without organic fertilizer, while a negative value indicated a decrease. Meta-analysis assumes that studies are independent and free from publication bias, and we considered this to be the case in the metaanalysis reported here (Curtis and Wang, 1998; Wang et al., 2017a). With meta-analysis, one can test whether categorical groups are homogeneous with respect to effect size (i.e., that observed differences in lnR among studies are due to sampling error), and whether there are significant differences in mean response between these groups. We used the homogeneity statistic Q, an estimate of the among-study variance, to test whether variances were significantly different; if P < 0.05 (tested against a chi-square distribution), then the data were considered to be heterogeneous and further analyzed by single factor categorical analysis (Curtis and Wang, 1998; Wang et al., 2017a). When conducting categorical analyses, total heterogeneity of effect size among studies (Qt) was generated and partitioned into heterogeneity within categorical variables (Qw) and heterogeneity between categorical variables (Qb), such that Qt = Qw + Qb. Comparison between categorical variables was examined by Qb. The frequency distribution of effect size was plotted and the frequency of effect size was fit to a Gaussian distribution function to assess homogeneity of observations using SigmaPlot v. 12.5 software (Jandel Scientific, Corte Maders, CA).

400–1000 400–900 50–450

3. Results 3.1. Overall response of winter wheat yield and WUE to organic fertilization The frequency distribution of effect size was fit to a Gaussian distribution function for yield, ET, and WUE of winter wheat (Li et al., 2018; Shan and Yan, 2013), the Kolmogorov-Smirnov test indicated that the distribution of yield, ET, and WUE is not normal (Fig. 3). The organic fertilizer application rate was about 30–75 Mg ha−1 for NOF and NLOF and 10–22.5 Mg ha−1 for NROF (data not shown). On average, yield with organic fertilizer and without organic fertilizer was 5.4 and 4.6 Mg ha−1, respectively, ET was 394 and 392 mm, respectively, and WUE was 9.5 and 11.4 kg mm−1 ha−1, respectively (data not shown). Yield and WUE were increased by 20 and 18 % with organic fertilizer compared to without organic fertilizer, respectively (Fig. 4). Applying organic fertilizer did not significantly affect ET.

Northwest region North China Plain Cold region

6–15 10–18 0–11

Rainfed Irrigated Irrigated

Double cropping Double cropping Irrigated and rainfed Irrigated and rainfed 500–1000 800–1600 11–19 13–22

Shandong, Henan (excluding Xinyang city), and northern Anhui Hubei, Jiangsu, Shanghai, Anhui, and southeastern Henan Shanxi, Ningxia, Shannxi, and eastern and southeastern Gansu Hebei, Beijing, and Tianjin Xinjiang, Inner Mongolia, Heilongjiang, and northwestern Gansu Central plain irrigation region Rice and wheat growing region

Annual mean precipitation (mm) Annual mean temperature (℃) Province Region

Table 1 Geographic, climate, water regime, and cropping system information for regions with experimental sites of winter wheat that were included in this meta-analysis.

Water regime

Cropping system

L. Wang, et al.

3.2. Response of winter wheat yield and WUE to organic fertilization as affected by growing region and ET Winter wheat yield and WUE response to organic fertilizer 4

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Fig. 3. Frequency distribution of effect size for winter wheat yield (a), evapotranspiration (b), and water use efficiency (c) response to organic fertilizer compared to without organic fertilizer. The frequency distribution of effect size was fit to a Gaussian distribution function. The Kolmogorov-Smirnov (KS) test was used to determine the distribution of yield, ET, and WUE.

WUE came from experiments in semi-arid regions of China. In these regions, grain yield and WUE of winter wheat are primarily limited by soil water deficit during spring growth and through grain filling because of high evaporation and erratic distribution of precipitation (Wang et al., 2018a). The positive effect organic fertilizer on yield decreased as ET increased (Fig. 6a). The increase in yield with organic fertilizer was largest when ET was < 300 mm (26 %), followed by when ET was 300–500 mm (17 %), and was least when ET was > 500 mm (8 %). The positive effect of organic fertilizer on WUE was also influenced by ET. The largest increase in WUE occurred when ET was < 300 mm (21 %), followed by when ET was 300–500 mm (18–19 %), and was least when ET was > 500 mm (15 %) (Fig. 6b). 3.3. Response of winter wheat yield and WUE to organic fertilization as affected by soil organic matter Soil organic matter content significantly affected the response of winter wheat yield and WUE to organic fertilization in China (Fig. 7). The positive effect of organic fertilizer on yield decreased with increased SOM (Fig. 7a). The increase in yield with organic fertilizer was greatest when SOM was < 1.4 % (24–27 %) and least when SOM was > 1.4 % (9–11 %). Soil organic matter content did not significantly affect the response of winter wheat ET to organic fertilizer (Fig. 7b). The response of winter wheat WUE to organic fertilization varied among categories of SOM (Fig. 7c). The mean increase in WUE with organic fertilizer ranged from 17 to 19% when SOM was < 1.0 to 1.4 % or > 2.0 %, and was 11 % for sites with 1.4–2.0 % SOM.

Fig. 4. Overall response of change in winter wheat yield, evapotranspiration (ET), and water use efficiency (WUE) to organic fertilizer compared to without organic fertilizer control. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses.

application in China varied with growing region and ET during the growing season (Figs. 5 and 6). On average, yield and WUE were significantly increased with organic fertilizer compared to without organic fertilizer in different regions of northern China (Fig. 5). The increase in yield with organic fertilizer was largest in the North China Plain (33 %), followed by the northwest region (20 %), and the central plain irrigation region, rice and winter wheat growing region, and cold region (16–17 %). Organic fertilizer significantly increased ET of winter wheat in the central plain irrigation region, decreased ET in North China Plain and northwest region, and did not significantly affect ET in the rice and winter wheat growing region (Fig. 5b). Organic fertilizer significantly increased WUE by 31 % in the North China Plain, and by 16–18 % in the northwest region, central plain irrigation region, and rice and winter wheat growing region (Fig. 5c). The effect of ET on the response of winter wheat yield and WUE to organic fertilizer was evaluated in this study, since most observations of

3.4. Response of winter wheat yield and WUE to organic fertilization as affected by N fertilizer rate Yield, ET, and WUE of winter wheat in response to organic fertilization in northern China varied with N fertilizer rate (Fig. 8). The positive effect of organic fertilization on winter wheat yield was influenced by N fertilizer rate (Fig. 8a). Organic fertilizer increased wheat yield by 71 % in the absence of synthetic N fertilizer application, by 15–18 % when synthetic N fertilizer was applied up to 300 kg N ha−1, and by 10 % with synthetic N fertilization > 300 kg N ha−1. Organic fertilizer did not significantly affect ET, regardless of synthetic N fertilizer rate applied (Fig. 8b). The positive effect of organic fertilizer on WUE of winter wheat was affected by synthetic N fertilizer rate Fig. 5. Response of change in winter wheat yield (a), evapotranspiration (ET) (b), and water use efficiency (WUE) (c) to organic fertilizer compared to without organic fertilizer in different regions of northern China. NP, NW, CPI, RW, and C represent North China Plain, Northwest region, Central plain irrigation region, Rice and wheat growing region, and Cold region, respectively. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. Asterisks represent the response for a group with only one comparison.

5

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Fig. 6. Response of change in winter wheat yield (a) and water use efficiency (WUE) (b) to organic fertilizer compared to without organic fertilizer at different levels of evapotranspiration. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses.

100–150 kg N ha−1, and did not significantly affect ET in the absence of synthetic N fertilizer or when synthetic N fertilizer was applied at 200–250 kg N ha−1 (Fig. 9e). At high yield levels (> 5.5 Mg ha–1), organic fertilizer did not significantly affect ET when synthetic N fertilizer was applied at 100–250 kg N ha−1 (Fig. 9h). Water use efficiency of winter wheat in response to organic fertilizer also varied with yield level. At low yield levels (< 4.0 Mg ha–1), organic fertilizer increased WUE by an average of 16–21 % among levels of synthetic N fertilization (Fig. 9c). At medium yield levels (4.0–5.5 Mg ha–1), organic fertilizer increased WUE by 10–14 % in the absence of synthetic N fertilization or when synthetic N fertilizer was applied up to 200 kg N ha−1, but did not affect WUE when synthetic N fertilizer was applied at 200–250 kg N ha−1 (Fig. 9f). At high yield levels (> 5.5 Mg ha–1), organic fertilizer did not significantly affect WUE of winter wheat when synthetic N fertilizer was applied at 100–150 or 200–250 kg N ha−1, and increased WUE by an average of 9 % when synthetic N fertilizer was applied at 150–200 kg N ha−1 (Fig. 9i).

(Fig. 8c). Organic fertilizer increased WUE by 41 % in the absence of synthetic N fertilizer, by 18–19 % when synthetic N fertilizer was applied up to 150 kg N ha−1 or at 250–300 kg N ha−1, and by 11–13 % when synthetic N fertilizer was applied at 150–250 kg ha−1. The effect of synthetic N fertilizer rate on the response of winter wheat yield and WUE to organic fertilizer was assessed by yield level, since the rate of synthetic N fertilization is commonly adjusted according to the expected yield of a growing environment (Wang et al., 2018a, b). On average, the positive effect organic fertilizer on yield and WUE decreased as yield level increased (Fig. 9). At low yield levels (< 4.0 Mg ha−1), organic fertilizer increased yield by 88 % in the absence of synthetic N fertilizer, by 20–27 % when synthetic N fertilizer was applied up to 300 kg ha−1, and by 7 % when the synthetic N fertilizer rate exceeded 300 kg N ha−1 (Fig. 9a). At medium yield levels (4.0–5.5 Mg ha–1), organic fertilizer increased yield by 44 % in the absence of synthetic N fertilizer, and by 15–18 % with synthetic N fertilization (Fig. 9d). At high yield levels (> 5.5 Mg ha–1); however, the positive effect organic fertilizer on yield averaged 4–11 % among levels of synthetic N fertilization (Fig. 9g). Evapotranspiration of winter wheat in response to organic fertilizer varied with yield level. At low yield levels (< 4.0 Mg ha−1), organic fertilizer significantly reduced ET in the absence of synthetic N fertilizer; however, organic fertilizer did not significantly affect ET when synthetic N fertilizer was applied (Fig. 9b). At medium yield levels (4.0–5.5 Mg ha–1), organic fertilizer reduced ET by 4–13 % when synthetic N fertilizer was applied at 0–100 or 150–200 kg N ha−1, increased ET by 8 % when synthetic N fertilizer was applied at

3.5. Response of winter wheat yield and yield variation to organic fertilization Yield of winter wheat was significantly affected by method of organic fertilization (Fig. 10). On average, yield was 5.9, 5.5, and 4.1 Mg ha−1 for NOF, NLOF, and NROF, respectively (data not shown). When organic fertilizer was applied, yield was increased by 28 and 25 % with the NLOF and NOF treatments, respectively, and was reduced by 11 % with the NROF treatment (Fig. 10). Organic fertilization significantly

Fig. 7. Response of change in winter wheat yield (a), water use efficiency (WUE) (b), and evapotranspiration (ET) (c) to organic fertilizer compared to without organic fertilizer, at different levels of soil organic matter content. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. 6

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Fig. 8. Response of change in winter wheat yield (a), water use efficiency (WUE) (b), and evapotranspiration (ET) (c) to organic fertilizer compared to without organic fertilizer control at different levels of synthetic nitrogen (N) fertilizer rate. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. Asterisks represent the response for a group with only one comparison.

Fig. 9. Response of change in winter wheat yield (a, d, g), evapotranspiration (ET) (b, e, h), and water use efficiency (WUE) (c, f, i) to organic fertilizer compared to without organic fertilizer at different levels of synthetic nitrogen (N) fertilization and at low yield (< 4.0 Mg ha–1) (a, b, c), medium yield (4.0–5.5 Mg ha–1) (d, e, f), and high yield (> 5.5 Mg ha–1) (g, h, i) levels. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. 7

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impacts of organic fertilization on the yields and WUE of winter wheat in China based on literature search. Organic fertilization was the focus of this study because of its potential to improve soil quality, reduce chemical fertilizer application, and enhance resource utilization efficiency (Xiong and Wu, 2017). 4.1. Overall response of winter wheat yield and WUE to organic fertilization This meta-analysis confirmed that organic fertilization increased grain yield of winter wheat in northern China, supporting our first hypothesis. Overall, the use of organic fertilizer increased grain yield by 20 % without affecting ET, thereby increasing WUE, as shown in previous studies (Fan et al., 2005; Liu et al., 2013; Wang et al., 2011, 2017b). This could be due to organic fertilization increasing precipitation storage efficiency (Wang et al., 2011) and alleviating soil water depletion (Liu et al., 2013). Chemical fertilization (without organic fertilizer control) can cause severe depletion of soil water in semiarid areas (Liu et al., 2013); thus, winter wheat with chemical fertilization might be insufficient to maintain high yield and WUE (Wang et al., 2011, 2013, 2018a). This can be attributed to reduced soil evaporation with organic fertilization through increased crop canopy coverage (Chen et al., 2015; Satyanarayana et al., 2002; Wang et al., 2018a; Li et al., 1993) and transpiration (Wang et al., 2018a; Zhang et al., 1998), thereby enhancing biomass accumulation and ultimately increasing yield and WUE. However, Seufert et al. (2012) found that organic fertilizer decreased wheat grain yield by 30 %. This discrepancy may be associated with differences in method of organic fertilization, since some studies have evaluated organic fertilization as part of a lowinput cropping system (i.e., a portion of N fertilizer replaced with organic fertilizer at the same level of N). This slow N release pattern of organic N sources is attributed to the dependence of organic fertilizer on microbial decomposition and subsequent mineralization of N, a process largely affected by climate (Kramer et al., 2002). Under these conditions, the N source is usually a limiting factor for adequate crop uptake of N and grain yield (Rieux et al., 2013).

Fig. 10. Response of change in winter wheat yield to organic fertilizer compared to without organic fertilizer for different methods of organic fertilization. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. NOF, synthetic nitrogen fertilizer plus organic fertilizer with the same level of synthetic nitrogen; NLOF, decreased level of synthetic nitrogen fertilizer combined with organic fertilizer; NROF, a portion of synthetic nitrogen fertilizer replaced with organic nitrogen fertilizer at the same level of nitrogen.

4.2. Response of winter wheat yield to method of organic fertilization In this study, the increase in yield compared to without organic fertilizer was greater with NLOF than NOF, presumably due to excessive N input with NOF (Hawkesford, 2014; Wang et al., 2018a). Winter wheat yield was reduced with NROF, likely because low available N with NROF was a limiting factor for crop uptake of N and grain yield (Wang et al., 2018a). Similar responses have been reported in wheat (Annett et al., 2007; Mason et al., 2007; Rieux et al., 2013) and legumes (Seufert et al., 2012). These results suggest that combining reduced synthetic N fertilizer input with organic fertilization as a viable option for sustainable intensification of cereal production in northern China.

Fig. 11. Response of change in coefficient of variation (CV) of winter wheat yield to organic fertilizer compared to without organic fertilizer. Error bars represent 95 % confidence intervals. The numbers of comparisons are in parentheses. Spatial variability represents yield variability across two or more locations in the same year. Temporal variability represents yield variability across two or more years in the same experiment.

4.3. Response of winter wheat yield and WUE to organic fertilization as affected by growing region and ET The effect of organic fertilization on yield and WUE of winter wheat were affected by growing region and ET. The positive effect of organic fertilization on yield and WUE of winter wheat was greatest in the North China Plain. This could be because excessive use shallow saline groundwater for irrigation in the North China Plain causes soil salinization (Ju et al., 2007; Ma et al., 2008), thereby restricting crop yield. Increased soil organic matter content is beneficial to soil desalination (Li et al., 2012; Mavi et al., 2012). We also found that the positive effect of organic fertilization on yield and WUE of winter wheat decreased as ET increased. The results of this study suggest that organic fertilizer enabled winter wheat to use water more efficiently in relatively droughty environments. Organic fertilization has been shown to increase wheat drought tolerance, leading greater WUE under drought stress (Chen et al., 2015; Wang et al., 2017b). Similar responses have

influenced spatial and temporal variation in yield (Fig. 11). On average, the coefficient of variation across locations was 28.7 and 32.9 % with organic fertilizer and without organic fertilizer, respectively, and the coefficient of variation across years was 11.8 and 14.3 % with organic fertilizer and without organic fertilizer, respectively (data not shown). Based on these values, organic fertilizer significantly reduced spatial and temporal variation in yield by an average of 11 and 23 %, respectively (Fig. 11). 4. Discussion This study provides a systematic and quantitative analysis on the 8

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4.6. Response of winter wheat yield and yield stability to organic fertilization

been reported for maize (Xie et al., 2019). The results of this study indicate that growing environments in northern China with ET < 500 mm are expected to experience the greatest improvement in WUE with organic fertilizer application.

Cereal production by most resource-poor and subsistence farmers often depends on inherent soil fertility and is thus subject to great variability (Raseduzzaman and Jensen, 2017). An analysis of the major European crops produced from 1920 to 2000 showed that crops with a higher yield level had greater yield stability than lower-yielding crops (Chloupek et al., 2004). Numerous studies have reported greater cereal productivity with organic fertilizer compared to without (Fan et al., 2005; Liu et al., 2013; Raseduzzaman and Jensen, 2017; Rieux et al., 2013; Thomsen et al., 2008; Wang et al., 2011); this productivity increase with organic fertilization could help to reduce yield variability and increase yield stability, particularly for smallholder farmers. This study shows that use of organic fertilizer contributed to greater winter wheat grain yield with less spatial and temporal variation, in agreement with previous studies (Chloupek et al., 2004; Döring et al., 2015; Fan et al., 2005; Raseduzzaman and Jensen, 2017). High grain yield with organic fertilization could be partially attributed to slower release of nutrients from organic compared to control treatment, thereby enhancing the synchrony between nutrient availability and crop nutrient uptake (Kramer et al., 2002).

4.4. Response of winter wheat yield and WUE to organic fertilization as affected by soil organic matter Soil organic matter plays an important role as a pool of terrestrial carbon (Pan et al., 2009), in ecosystem productivity, in the functioning of agroecosystems (Loveland and Webb, 2003) and in cropland fertility (Tiessen et al., 1994). Previous studies consistently show that increases in SOC from applying organic fertilizers to agricultural soils improves soil quality, increases crop productivity, and alleviates global warming (Lal, 2004; Shi et al., 2016). Knowledge of site-specific factors affecting crop response to organic amendments could direct their application and result in the greatest advances in crop production (Fan et al., 2005; Liu et al., 2013). This meta-analysis shows that the positive effect of organic fertilizer on grain yield and WUE of winter wheat was greatest at sites with SOM < 1.4 %, indicating that application of organic fertilizer to infertile soils produced greater yield increases. This may be due to greater improvements in soil water storage efficiency (Fan et al., 2005; Wang et al., 2011) and soil fertility with organic fertilization in these conditions (Loveland and Webb, 2003; Pan et al., 2009), resulting in a greater increase in biomass accumulation and grain yield (Chen et al., 2015; Li et al., 2012; Mavi et al., 2012; Wang et al., 2017b).

5. Conclusions This meta-analysis, based on reported field experiments conducted across a range of soils and growing environments in northern China, shows that use of organic fertilizer increased winter wheat grain yield and WUE and reduced spatial and temporal variability in yield without affecting ET. The yield response to organic fertilizer was dependent on method of application, as NOF and NLOF substantially increased yield while NROF reduced yield. The positive effect of organic fertilizer on grain yield and WUE of winter wheat was greatest when yield levels was < 4.0 Mg ha–1. Moreover, organic fertilization was more effective at improving yield and WUE in North China Plain when synthetic N application was < 150 kg N ha−1 and in growing environments with SOM < 1.4 % and ET < 500 mm. These results highlight the potential of organic fertilizer to facilitate reduced N fertilizer input for winter wheat production while producing greater yield, mitigating spatial and temporal yield variation, and enhancing the efficiency of water resources. With rational implementation, this could serve as a cornerstone for sustainable intensification of cereal production and give rise to a second green revolution in agriculture.

4.5. Response of winter wheat yield and WUE as affected by N fertilizer rate Nitrogen fertilizers are a fundamental component of cereal production (Hawkesford, 2014), the combination of organic and inorganic fertilizer is common when organic fertilizers are used in China (Fan et al., 2005; Liu et al., 2013; Wang et al., 2011). Thus, knowledge on optimization of synthetic N fertilizer use when organic fertilizer is applied, and how this should vary based on site and growing environment, is paramount for improving resource utilization efficiency and advancing sustainable intensification of cereal production. This meta-analysis shows that increases in grain yield and WUE of winter wheat in response to organic fertilizer have not been proportional to N fertilizer input, which is in agreement with previous studies (Shi et al., 2014; Zhang et al., 2017). The positive effect of organic fertilizer on yield and WUE of winter wheat was greatest in the absence of synthetic N fertilizer, likely because organic fertilizer can supply N for wheat growth and development (Liu et al., 2009, 2013). Previous studies on winter wheat production in China without organic fertilizer show that maximum grain yield occurred with N fertilizer applied at 250 kg N ha−1 (Wang et al., 2018b; Yu and Shi, 2015). This meta-analysis shows that grain yield peaked at 100–150 kg N ha−1. The results from this study indicate that integrated use of organic fertilizer and synthetic N fertilizer has the potential to reduce synthetic N input for winter wheat production by about 150 kg N ha−1 (60 %) without affecting yield and WUE. Organic fertilizer was relatively more effective at enhancing grain yield and WUE in lower-yielding environments, consistent with the findings that these responses were greater at sites with < 1.4 % SOM. This could be partially due to greater efficiency of organic fertilizer at improving soil fertility and crop yield on low- and medium-yielding soils (Liu et al., 2013; Maeder et al., 2002; Pan et al., 2009; Tiessen et al., 1994; Wang et al., 2017b; Watson et al., 2002) as a result of improvements in soil quality (Liu et al., 2013), water storage (Fan et al., 2005; Wang et al., 2011), and soil desalination (Li et al., 2012; Mavi et al., 2012).

Declaration of Competing Interest The authors have declared that no competing interests exist. Acknowledgements This work was supported by start-up funds from Gansu Agricultural University for openly-recruited Ph.D. graduates (GAU-KYQD-2018-20), the Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University (GSCS-2019-09, GSCS-2017-4, and GSCS-2019Z04), the National Natural Science Foundation of China (31761143004, 31660373, and 31460337), the National Science and Technology Supporting Program (2015BAD22B04-03), and the Department of Education of Gansu Province (2017C-12). References Annett, L., Spaner, D., Wismer, W., 2007. Sensory profiles of bread made from paired samples of organic and conventionally grown wheat grain. J. Food Sci. 72, S254–S260. Bao, X., Watanabe, M., Wang, Q., Hayashi, S., Liu, J., 2006. Nitrogen budgets of agricultural fields of the Changjiang River basin from 1980 to 1990. Sci. Total Environ. 363, 136–148.

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