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How Does Recycling of Livestock Manure in Agroecosystems Affect Crop Productivity, Reactive Nitrogen Losses, and Soil...

Article in Environmental Science and Technology · June 2017 DOI: 10.1021/acs.est.6b06470

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How Does Recycling of Livestock Manure in Agroecosystems Affect Crop Productivity, Reactive Nitrogen Losses, and Soil Carbon Balance?

Longlong Xia,†,‡,§ Shu Kee Lam,‡ Xiaoyuan Yan,*,† and Deli Chen*,‡ †

State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China ‡ School of Agriculture and Food, Faculty of Veterinary and Agricultural Sciences, the University of Melbourne, Melbourne, Victoria 3010, Australia § University of Chinese Academy of Sciences, Beijing 100049, China S Supporting Information *

ABSTRACT: Recycling of livestock manure in agroecosystems to partially substitute synthetic fertilizer nitrogen (N) input is recommended to alleviate the environmental degradation associated with synthetic N fertilization, which may also affect food security and soil greenhouse gas (GHG) emissions. However, how substituting livestock manure for synthetic N fertilizer affects crop productivity (crop yield; crop N uptake; N use efficiency), reactive N (Nr) losses (ammonia (NH3) emission, N leaching and runoff), GHG (methane, CH4; and nitrous oxide, N2O; carbon dioxide) emissions and soil organic carbon (SOC) sequestration in agroecosystems is not well understood. We conducted a global meta-analysis of 141 studies and found that substituting livestock manure for synthetic N fertilizer (with equivalent N rate) significantly increased crop yield by 4.4% and significantly decreased Nr losses via NH3 emission by 26.8%, N leaching by 28.9% and N runoff by 26.2%. Moreover, annual SOC sequestration was significantly increased by 699.6 and 401.4 kg C ha−1 yr−1 in upland and paddy fields, respectively; CH4 emission from paddy field was significantly increased by 41.2%, but no significant change of that was observed from upland field; N2O emission was not significantly affected by manure substitution in upland or paddy fields. In terms of net soil carbon balance, substituting manure for fertilizer increased carbon sink in upland field, but increased carbon source in paddy field. These results suggest that recycling of livestock manure in agroecosystems improves crop productivity, reduces Nr pollution and increases SOC storage. To attenuate the enhanced carbon source in paddy field, appropriate livestock manure management practices should be adopted.

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INTRODUCTION Despite its critical role in feeding global population, the use of synthetic fertilizer N causes a cascade of adverse impacts on the environment (e.g., air pollution and freshwater eutrophication) through the release of reactive N (Nr) from agricultural soils.1−4 Synthetic N fertilization may increase soil carbon sequestration,5 but the increase in CO2 sink could be largely offset or even overweighed by N stimulation of CH4 and N2O emission from agricultural soils.6−8 Better N management in crop production is therefore critical for addressing the triple challenges of food security, environmental degradation and global warming.9−11 Globally, annual production of livestock manure N has reached nearly 100 Tg N12 and recycling of this large amount of manure N in agroecosystems to partially substitute synthetic N fertilizer (substituting manure for fertilizer, and hereafter) may help address the above-mentioned triple challenges.3,13 Substituting manure for fertilizer is beneficial for improving soil properties and subsequently crop yield.14−16 The responses of yield to substituting manure for fertilizer may vary with crop species and the proportion of manure N substitution,17−19 but © XXXX American Chemical Society

few studies have conducted a comprehensive assessment on these responses.

Substituting manure for fertilizer generally alters Nr losses through regulating crop N uptake and soil N transformation,20,21 and may result in a better synchronization of crop N demand with N supply,17,22 thereby increasing crop N uptake and likely decreasing Nr losses.23 Moreover, substituting manure for fertilizer increases the input of C substrates into soil, which may stimulate mineral N immobilization and therefore reduce N substrate that is subjected to loss as Nr.24 The effects of substituting manure for fertilizer may vary with Nr species (e.g., NH3 emission and N leaching).23 This highlights the importance of simultaneously assessing the responses of various Nr losses (NH3 emission, N leaching and runoff) to the substitution of manure for fertilizer.

Received: Revised: Accepted: Published: A

December 21, 2016 May 18, 2017 June 2, 2017 June 2, 2017 DOI: 10.1021/acs.est.6b06470 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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reviewed studies were finally selected across the world (Supporting Information (SI), Figure S1).

Evaluated Variables. Effects of substituting manure for fertilizer were evaluated by the following three categories with 11 variables, including (1) crop productivity: crop yield, crop N uptake and N use efficiency (NUE); (2) Nr losses: NH3 emission, N leaching and N runoff; (3) GHG (CH4, N2O and CO2) emissions and SOC sequestration (SOC content and SOC sequestration rate). N2O is both a species of GHG and Nr, and here its responses are reported under the category of GHG. Crop N uptake refers to total aboveground N uptake for grain crop, while it denotes the total N uptake by yield, stem and leaves for vegetable crop. The NUE, referring to total N recovery efficiency, was calculated by dividing the difference in crop N uptake in plots with and without fertilization by total fertilizer N rate.

The emission of CO2 refers to soil respiration, which includes microbial and root respiration. In the studies where SOC sequestration rate (SOCSR) was not directly reported, the rate was estimated by the following equation:16,34

Substituting manure for fertilizer can also affect SOC accumulation through supplying exogenous C input to soil,25 which may also enhance soil microbial activities and stimulate soil CO2 emission.26−28 Likewise, the growth of methanogenic populations in flooded paddy field may also be stimulated by the extra C supply and consequently release more CH4.29,30 However, the response of substituting manure for fertilizer on CH4 emission from upland field remains unknown. Another knowledge gap is how substitution of manure for fertilizer affects N2O emission from agricultural soils. Through affecting the C and N availability for the processes of nitrification and denitrification, substituting manure for fertilizer can regulate N2O production and emission from soils.17,31 While a number of measurements have been reported, there has been no systematic assessment of the overall effects of substituting manure for fertilizer on CH4, N2O and CO2 emission, and SOC sequestration in agroecosystems.

Here, using a global meta-analysis of 141 studies, we evaluated the overall effects of substituting manure for fertilizer on crop productivity (crop yield; crop N uptake; N use efficiency, NUE), Nr losses (NH3 emission, N leaching and N runoff), GHG (CH4, N2O and CO2) emissions and SOC sequestration in agroecosystems. Responses of these variables to manure substitution were then evaluated against crop species, manure type, and substitution rate. Effects of substituting manure for fertilizer on the net soil carbon balance were also evaluated for upland and paddy fields. In the end, the underlying causes of different responses of variables to manure substitution, and the implications of the findings were discussed.

SOCSR(kg C ha−1yr −1) = (SOCDt − SOCD0 )/T

(1)

where SOCDt and SOCD0 refer to SOC density (kg C ha−1) in final and initial years of the experiment, respectively, which was calculated using eq 2. T refers to the experimental duration of substituting manure for fertilizer (year).

SOCD = SOC × ρ × H × 10−1

(2)

where SOC is soil organic carbon content (g C kg−1); ρ is soil bulk density (g cm−3) and H is the sampling depth. In studies where ρ was missing, it was estimated using following equation:35

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MATERIALS AND METHODS Data Collection. This meta-analysis is based on studies that evaluated the effects of substituting manure for fertilizer on crop productivity, Nr losses, GHG emissions and SOC sequestration in grain and vegetable cropping systems. Several databases were employed to search relevant peer-reviewed studies published before August 2016, including Web of Science, China National Knowledge Infrastructure database, SCOPUS, CAB Abstracts and Google Scholar. Studies included in this analysis had to meet the following criteria. First, species and amounts of applied manure, cropping system and experimental durations had to be clearly stated. Second, manure type was restricted to livestock manure and animalexcreta dominated farm yard manure. Third, the control (synthetic N fertilization) and treatment (substituting manure for fertilizer) had equal total N rate. Fourth, the substitution rate, defined by manure N input/total N applied, had to be reported.

Fifth, studies were restricted to field, lysimeter and pot studies with crop growth. Means and samples size must be provided for the control and treatment plots. Multiple observations conducted in the same experimental site over sampling years were averaged. The observation methods of various GHG emissions and Nr losses should be widely adopted. Specifically, GHG emissions should be measured by the static chamber technique,32 NH3 emission by the dynamic chamber method or micrometeorological method,23 and N leaching and runoff by lysimeter method or suction cap.24 In addition, when evaluating the response of SOC sequestration, studies with experimental durations less than 3 year were excluded to avoid a short-term noise.33 A total of 141 peer-

ρ = −0.0048 × ln SOC + 1.377

(3)

Effects of substituting manure for fertilizer were further categorized, according to crop species (grain crop and vegetable crop, SI Table S1), manure type (fresh and composted manure) and substitution rate (Rs, manure N input/total N applied) (Rs ≤ 25%, 25 < Rs ≤ 50%, 50 < Rs ≤ 75% and 75 < Rs ≤ 100%). In addition, effects of substituting manure for fertilizer on microbial biomass carbon (MBC), microbial biomass nitrogen (MBN) and soil properties were also evaluated (SI Table S2).

Meta-Analysis. The natural log of the response ratio (ln RR) was employed to quantify the effects of substituting manure for fertilizer on the variables (X), except for CH4 emission from upland field and SOCSR, using the follow equation:36 ln RR = ln(X t /Xc)

(4)

where Xt and Xc represent the mean of the treatment and control groups for variable X, respectively. The results are reported as the percentage changes ((RR−1) × 100) under treatment effects. Negative percentage changes denote a decrease due to manure substitution, whereas positive values indicate an increase in the variables.

The values of upland CH4 emission and SOCSR can be both positive and negative. This makes eq 4 problematic. Therefore, the response of these two variables (RR′) were evaluated by following equation:37,38 RR′ = X t − Xc B

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Uncertainties of This Analysis. Some uncertainties exist during the comparison of the effects following manure substitution among different levels of variables, such as manure substitution rate. First, sample numbers may be diverse among different levels of variables, which may affect the dependence of the effects of manure substitution on the gradient of variables.

Second, environmental conditions and agricultural management practices may be also diverse among different levels of variables, which may influence the magnitude of the effects of manure substitution. We have coped with these uncertainties using the high bootstrapping (4999 iterations) to generate the 95% CI of each variable to make a reliable assessment. We also weighted the effect size by the number of replications to take into account the issue of the variation in statistical significance of different studies. This approach has been widely adopted by others meta-analysis studies.10,37−39

Effect sizes in previous meta-analyses were generally weighted by replication,10,39 the inverse of pooled variance40,41 or unweighted,42 depending on the availability of the weighting parameters (e.g., standard deviation of the variable) reported in the studies included in the meta-analysis. Most of the studies included in our analysis did not report standard deviation.

Moreover, extreme weights might be generated by variancebased weighting function.38 Therefore, in this analysis, effect sizes were weighted by the following replication-based function:43 weight = (nt × nc)/(nt + nc)

(6)

where nt and nc denote the number of replicates of the treatment and control, respectively.

Mean effect sizes and the 95% confidence intervals (CI) were generated by bootstrapping (4999 iterations) using MetaWin 2.1.44 Impacts of substituting manure for fertilizer on variables were considered significant if the 95% CI did not overlap with zero. Means of categorical variables were considered significantly different from each other if their 95% CIs did not overlap.

Net Soil Carbon Balance. Responses of CH4, N2O emissions and SOC sequestration were separated into two land types (paddy and upland field) to evaluate the net carbon balance induced by substituting manure for fertilizer.33 We calculated the manure induced changes of GHG emissions per unit manure-C added (Table 1). Taking the change of CH4

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RESULTS Crop Productivity. Substituting manure for fertilizer significantly increased the yield of grain crop by 5.2% (with an overall increase of 4.4% for all crops), but did not affect vegetable yield (Figure 1a), regardless of manure type (fresh or composted) (SI Table S3). In addition, a higher manure substitution rate (75 < Rs ≤ 100%) tended to decrease crop yield. Overall, crop N uptake and NUE was significantly increased by substituting manure for fertilizer by 8.8% and 10.4% for grain crop, respectively (Figure 1b,c), but no significant changes of these variables were observed for vegetable crop. The responses of N uptake and NUE did not vary with crop species, manure type or substitution rate (SI Table S3).

Various Nr Losses. Across all studies, substituting manure for fertilizer significantly reduced NH3 emission (26.8%), N leaching (28.9%) and N runoff (26.2%) (Figure 2). Moreover, the highest rate of manure substitution (75 < Rs ≤ 100%) tended to produce the largest reduction proportion of Nr losses. Similar responses of these Nr losses were observed for different crop species and manure types (SI Table S4). NO3− leaching and runoff were significantly reduced by 34.1% and 32.4%, respectively, while NH4+ leaching and runoff decreased by 9.5% and 44.5% following substituting manure for fertilizer, respectively (SI Table S4).

Net Soil Carbon Balance. Substituting manure for fertilizer did not affect CH4 emission from upland field (Figure 3a), but significantly increased that from paddy field by 41.2% (Figure 3b). Compared to fresh manure substitution, the application of composted manure tended to decrease the simulated CH4 emission from paddy field. Substituting manure for fertilizer had no significant impact on N2O emission from upland and paddy fields (Figure 3c, SI Table S5), irrespective of crop species, manure type or substitution rate (SI Table S3).

Overall, substituting manure for fertilizer significantly increased CO2 emission by 26.4% (Figure 4a).

Substituting manure for fertilizer significantly increased SOC sequestration rate (SOCSR) by 699.6 and 401.4 kg C ha−1 yr−1 in upland and paddy fields (SI Table S6), respectively, with an overall increase of 481.7 kg C ha−1 yr−1 (Figure 4b).

Meanwhile, SOC content was overall significantly increased by 33.3% (Figure 4c). A significant and negative exponential relationship was found between SOCSR and the duration of continuously substituting manure for fertilizer (SI Figure S2).

When compared to fresh manure, the use of composted manure substitution further increased SOCSR in paddy and

Table 1. Effects of Substituting Manure for Fertilizer on the Net Soil Carbon Balance in Agroecosystems Manure induced changes per unit manure-C added kg C or kg N ha−1 yr−1 per kg C ha−1 yr−1 land type upland paddy field

upland paddy field

upland paddy field

CH4 emission

N2O emission

SOC sequestration

1.3 × 10−5 0.25 2.6 × 10−4 0.02 −5.9 × 10−5 0.13 GWP attributed to manure-C added (kg CO2 ha−1 yr−1 per kg C ha−1 yr−1) 8.7 × 10−3 5.9 × 10−3 0.91 0.66 −0.027 0.48 NGWP attributed to manure-C added (kg CO2 ha−1 yr−1 per kg C ha−1 yr−1)a −0.90 0.15

a

Negative value of NGWP denotes net carbon sink induced by substituting manure for fertilizer, whereas positive value denotes net carbon source.

emission (CH4‑changes, kg C ha−1 yr−1 per kg C ha−1 yr−1) as an example: CH4 − change = (X t − Xc)/manure C input

(7)

where “manure C input” denotes C input rate attributed to substituting manure for fertilizer (kg C ha−1 yr−1). The net global warming potential (NGWP, kg CO2 ha−1 yr−1 per kg C ha−1 yr−1) was evaluated by following equation:33 NGWP = CH4change × 25 × 16/12 + N2Ochange × 298 × 44/28 − SOCSR change × 44/12

(8)

where negative value of NGWP denotes net carbon sink induced by substituting manure for fertilizer, whereas positive value denotes net carbon source.

C

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Figure 1. Effects of substituting manure for fertilizer on (a) crop yield, (b) N uptake, and (c) N use efficiency (NUE). Fresh and composted denotes fresh manure and composted manure, respectively. Rs represents substitution rate, defined by manure N input/total N applied. Numbers of experimental observation are in parentheses.

Figure 2. Effects of substituting manure for fertilizer on (a) NH3 emission, (b) N leaching and (c) N runoff. Fresh and composted denotes fresh manure and composted manure, respectively. Rs represents substitution rate, defined by manure N input/total N applied. Numbers of experimental observation are in parentheses.

Figure 3. Effects of substituting manure for fertilizer on (a) CH4 emission from upland field, (b) from paddy field and (c) N2O emission. Fresh and composted denotes fresh manure and composted manure, respectively. Rs represents substitution rate, defined by manure N input/total N applied.

Numbers of experimental observation are in parentheses.

upland fields (SI Table S6). The higher increases in SOCSR and SOC content were observed when the substitution rate of manure N was 50−75% (Figure 4b,c).

As for the manure C induced changes of GHG emissions, the response of SOC sequestration to manure substitution was higher in upland (0.25 kg C per kg C ha−1 yr−1) than paddy field (0.13 kg C per kg C ha−1 yr−1) (Table 1). CH4 emission was increased by 0.02 kg C per kg C ha−1 yr−1 in paddy field.

N2O emission showed a minor positive response to manure substitution in upland field, but a minor negative response in

paddy field. In terms of NGWP, substituting manure for fertilizer increased carbon sink in upland field, but increased carbon source in paddy field (Table 1).

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DISCUSSION Feeding the increasing global population with existing farmland is one of the greatest challenges facing agriculture.45 Our metaanalysis demonstrates that substituting livestock manure for fertilizer significantly increased crop yield by 4.4% and this value would be even greater (12.7%) if the substitution rate of D

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Figure 4. Effects of substituting manure for fertilizer on (a) CO2 emission, (b) soil organic carbon (SOC) content and (c) SOC sequestration rate.

Fresh and composted denotes fresh manure and composted manure, respectively. Rs represents substitution rate, defined by manure N input/total N applied. Numbers of experimental observation are in parentheses.

Figure 5. Summary on the effects of substituting manure for fertilizer on crop productivity, reactive N losses and greenhouse gas emissions. All data were derived from the results of this meta-analysis. MBC, microbial biomass carbon; MBN, microbial biomass nitrogen; DOC, dissolved organic carbon; DON, dissolved organic nitrogen.

manure N was adjusted to 50−75% (Figure 1a). The increase in crop yield is largely attributed to the enhanced crop uptake of N and other mineral nutrients.22 Substituting manure for fertilizer may promote the microbial immobilization of bioavailable N (that may otherwise be lost to the environment) through increasing the supply of organic carbon,31,46 as evidenced by the increase in MBN content (36.4%) (Figure 5). The immobilized N would be released across crop growing season, thus improving N uptake and crop yield.47 The additional supplement of mineral nutrients to soil associated with substituting manure for fertilizer, such as phosphorus, potassium, copper and zinc, would also facilitate the improvement of crop yield.48 In addition, manure substitution may benefit the improvement of soil properties, such as soil structure, water holding capacity of soil and the microbial activity, and consequently promoting the improvement of crop yield.15,49 However, crop yield would be decreased when synthetic fertilizer N was substituted by more than 75% (Figure 1). This

is likely due to the insufficient N supply for early crop growth, since the N in manure requires longer time to be mineralized than urea-N.17,24 Also, vegetable crops generally grow faster than grain crops, and the delayed N supply induced by substituting manure for fertilizer may fail to satisfy their high N demand.50 Moreover, our results showed that more bioavailable N was likely immobilized during vegetable-growth period (40.5%) than grain crop-growth period (34.3%), as evidenced by the responses of MBN to substituting manure for fertilizer (SI Table S7). Consequently, neutral or even negative effect on vegetable yield was observed.50,51 Therefore, instead of manure, synthetic N fertilizer should be applied at the early stages of vegetable growth to meet the higher demand for available N. Nr loading to the environment (e.g., NH3 emission, N leaching and runoff) may increase significantly with N inputs into agricultural soils.52−54 Minimizing surplus soil mineral N is therefore critical to reduce Nr pollution in agroecosystems.55 Our study showed that substituting manure for fertilizer largely reduced various Nr losses in agroecosystems, regardless of crop E

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significantly regardless of land type (Figure 3c, SI Table S5).

Similar responses were observed for the application of other organic materials (e.g., crop straw).62 Overall, substituting manure for fertilizer increased carbon sink in upland field, but increased carbon source in paddy field owing to the stimulated CH4 emission (Table 1). To attenuate the increased CH4 emission while further enhancing the potential of SOC sequestration by manure substitution, appropriate manure management practices are needed. For example, compared to fresh manure, composted manure generally have higher contents of lignin and polyphenol.32 These compounds not only promote the formation of lignocelluloses and hemicelluloses which would enhance SOC storage, but they are also more resistant to microbial decomposition and utilization by methanogens.34 This would promote SOC sequestration but decrease the stimulated CH4 emissions in paddy field (Figures 3 and 4). Compared to fresh manure, the application of composted manure in upland field could also further increase the enhanced SOC storage (SI Table S6), without promoting CH4 and N2O emissions (Figure 2a, SI Table S5). Aerobic composting method should be adopted to decrease CH4 emission during the composting process.34 In summary, recycling of livestock manure in agroecosystems to partially substitute synthetic fertilizer N improves food production, reduces various Nr losses and increases SOC storage. Although substituting manure for fertilizer may increase carbon source in paddy field through stimulating CH4 emission (Figure 5), the increased emission may be attenuated through adopting appropriate manure management practices. Extra attention should be given to the effect of substituting manure for fertilizer on food security. Livestock manures may contain heavy metals such as lead, chromium and cadmium, and their long-term application may result in heavy metal accumulation in soils and plants,63,64 which could be a potential threat to human health65 and warrants further research. In addition, the application of livestock manure may increase the diversity and abundance of antibiotic-resistance genes in soils,66 which also deserves extra-attention.

species, manure type or substitution rates (Figure 2). This could be due to the increase in N uptake and N use efficiency induced by manure substitution, which minimized the soil mineral N pool and therefore reducing Nr losses.31,47 It has been reported that Nr losses decreased exponentially as the NUE increased.53 Therefore, the moderate increase in the NUE (10.4%) may be associated with higher reduction rate of Nr losses (26.2−28.9%) (Figures 1 and 2).

Another possible explanation is the increase in microbial immobilization of mineral N, following manure substitution, as evidenced by the greater MBN (Figure 5), and the slow release of mineral N during manure decomposition. This reduces the availability of N substrate (e.g., NO3− and NH4+) that can be released as various Nr.24,46 Also, water stable aggregates (>0.25 mm) fraction and cation exchange capacity (CEC) were significantly increased by 13.6% and 12.0% (SI Table S2), respectively, which contributed to the adsorption of soil mineral N and hence the reduction of N leaching and runoff.56 Moreover, compared to synthetic fertilizer N particularly nitrate, organic N in manure is less mobile and therefore less readily transported to water bodies.56 In addition, the increased availability of carbon source following manure substitution, may stimulate the dissimilatory NO3− reduction to NH4+ (DNRA) and therefore promoting N retention in soil and reducing NO3− leaching and runoff.31 Although reduction of Nr losses was the largest under the highest substitution rate of manure N (Rs > 75%), crop yield was decreased by 3.3% (Figures 1 and 2). This highlights the importance of adopting appropriate substitution rate for producing more yields with lower Nr pollution.

Increasing SOC sequestration in agroecosystems is crucial for offsetting anthropogenic GHG emission.57 We found that SOC sequestration rate was significantly increased by substituting manure for fertilizer irrespective of land type (SI Table S6), manure type or substitution rate (Figure 4), which was mainly attributed to the input of exogenous carbon source.28 The stimulated crop productivity by manure substitution may increase root exudates (indigenous carbon input), which is widely reported in other studies.15,32,58,59 On the other hand, the increased fraction of macro-aggregates (e.g., water stable aggregates, SI Table S2) may slow down SOC decomposition.33 The exponential relationship between SOC sequestered and the duration indicated a possible saturation of SOC levels after 35 years of continuous substitution of manure for fertilizer (SI Figure S2), which is within the range of 26−65 year estimated by Han et al.60 However, CO2 emission and CH4 emission (paddy field) were also increased by substituting manure for fertilizer (Figures 3 and 4). The increase in CO2 emission was mainly due to the enhanced microbial activities and/or microbial biomass as evidenced by the greater MBC (Figure 5, SI Table S2), and the stimulated root respiration associated with better crop growth.61 Moreover, the enhanced soil porosity (by 6.3%) (SI Table S2) may improve soil diffusivity and consequently CO2 emission.33 As for CH4 emission from paddy field, substituting manure for fertilizer stimulated the growth of methanogenic populations through the supply of carbon substrates,7,30 thereby enhancing CH4 emission (Figure 3).

However, upland CH4 emission was not affected by substituting manure for fertilizer (Figure 3). Aerobic condition of upland field would inhibit the activities of methanogenic populations despite with supply of sufficient carbon substrates.29,33 Substituting manure for fertilizer did not affect N2O emission

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.6b06470.

Detailed information on data used for the meta-analysis (XLSX) Detailed data about the effects of substituting manure for fertilizer on N2O emission and SOC sequestration rate in upland and paddy fields as well as all the studies included in the meta-analysis (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*(X.Y.) Phone: +86 25 86881530; fax: +86 25 86881000; email: yanxy@issas.ac.cn. *(D.C.) Phone: +61 3 83448148; fax: +61 3 83445037; e-mail: delichen@unimelb.edu.au.

ORCID

Shu Kee Lam: 0000-0001-7943-5004 Xiaoyuan Yan: 0000-0001-8645-4836 Notes

The authors declare no competing financial interest.

F

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ACKNOWLEDGMENTS This study was financially supported by the National Science Foundation of China (41425005 and 41571130062), the Australia-China Joint Research Centre jointly funded by Australian Government Department of Industry and Science, and the Chinese Ministry of Science and Technology, and the BIP reinvestment funds of the Faculty of Veterinary and Agriculltural Sciences of the University of Melbourne. We thank Quan Tang for helping to prepare the database. The first author also appreciates Chinese Academy of Sciences for providing funds to support his study in Australia.

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DOI: 10.1021/acs.est.6b06470 Environ. Sci. Technol. XXXX, XXX, XXX−XXX