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Warming and altered precipitation rarely alter N addition effects on soil greenhouse gas fluxes: a meta-analysis
Ecological Processes volume 12, Article number: 56 (2023)
Abstract
Background
Changes in soil greenhouse gas (GHG) fluxes caused by nitrogen (N) addition are considered as the key factors contributing to global climate change (global warming and altered precipitation regimes), which in turn alters the feedback between N addition and soil GHG fluxes. However, the effects of N addition on soil GHG emissions under climate change are highly variable and context-dependent, so that further syntheses are required. Here, a meta-analysis of the interactive effects of N addition and climate change (warming and altered precipitation) on the fluxes of three main soil GHGs [carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O)] was conducted by synthesizing 2103 observations retrieved from 57 peer-reviewed articles on multiple terrestrial ecosystems globally.
Results
The interactive effects of N addition and climate change on GHG fluxes were generally additive. The combination of N addition and warming or altered precipitation increased N2O emissions significantly while it had minimal effects on CO2 emissions and CH4 uptake, and the effects on CH4 emissions could not be evaluated. Moreover, the magnitude of the combined effects did not differ significantly from the effects of N addition alone. Apparently, the combined effects on CO2 and CH4 varied among ecosystem types due to differences in soil moisture, which was in contrast to the soil N2O emission responses. The soil GHG flux responses to combined N addition and climate change also varied among different climatic conditions and experimental methods.
Conclusion
Overall, our findings indicate that the effects of N addition and climate change on soil GHG fluxes were relatively independent, i.e. combined effects of N addition and climate change were equal to or not significantly different from the sum of their respective individual effects. The effects of N addition on soil GHG fluxes influence the feedbacks between climate change and soil GHG fluxes.
Background
Carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O), as the three major greenhouse gases (GHGs) (World Meteorological Organization 2020), have been observed to increase over the past several decades, mainly originating from anthropogenic activities, including fossil fuel combustion, land use change, and chemical fertilizer application (IPCC 2013). Another consequence of the anthropogenic activities is increased nitrogen (N) loads in terrestrial ecosystems (Du et al. 2021; He et al. 2021). N addition can alter the biogeochemical processes of ecosystems and alter soil GHG fluxes (Li et al. 2020; Liu and Greaver 2009), further contributing to changes in both temperature and the hydrological cycle (IPCC 2022). As two key factors regulating terrestrial ecosystem processes, temperature and precipitation influence soil microclimate, microbial activity, and soil substrate availability (Harte et al. 1995; Zhang et al. 2019; Zhou et al. 2018), thus potentially influencing the effects of N addition on soil GHG fluxes (Chen et al. 2021). Therefore, understanding how climate change regulates the feedback between soil GHGs and N addition would improve our capacity to predict future soil GHG fluxes and such potential effects could be incorporated into predictive biogeochemical models.
Globally, researchers have experimentally examined the effects of N addition on soil CO2, CH4, and N2O fluxes. The main underlying mechanisms by which N addition increases soil GHG fluxes are the regulation of plant growth and microbial activities directly associated with soil GHG production and consumption processes (Chen et al. 2021; Niu et al. 2010; Quinn Thomas et al. 2010). In addition, projected shifts in temperature have been documented to enhance microbial activity thereby accelerating soil organic matter decomposition and stimulating soil GHG release (Liu et al. 2020; Zhang et al. 2020). Therefore, warming and N addition can interact to synergistically increase soil GHG fluxes (Chen et al. 2017a; Yang et al. 2022). However, warming can also negate the positive effects of N addition on soil GHGs as warming-induced soil water deficits can suppress microbial activity and plant physiological activity (Zong et al. 2018; Cheng et al. 2022). In addition, the effects of N addition on soil GHG fluxes may be suppressed under decreased precipitation due to reduced plant carbon (C) inputs and limited soluble C substrate availability (Fuchslueger et al. 2014; Aronson et al. 2019). Conversely, higher soil water availability caused by increased precipitation can increase soil labile C availability and microbial activity (Zhou et al. 2016). The findings suggested that stimulated GHG emissions by N addition may particularly occur under high precipitation regimes (Brown et al. 2012).
The effects of N addition in combination with warming or altered precipitation remain ambiguous due to differences in outcomes across ecosystem types, climatic conditions, and experimental methods (Deng et al. 2020; Gong and Wu 2021). Among individual studies, the soil CH4 fluxes’ responses to N addition in combination with warming vary from potential increase to potential decrease (Chen et al. 2017a, b; Wu et al. 2020; Liu et al. 2015). The directions of soil CH4 fluxes are highly dependent on ecosystem type and soil condition, as soil CH4 is produced by methanogens in wet anaerobic soils and consumed by methanotrophs in drier aerobic soils (Le Mer and Roger 2001; Ni and Groffman 2018). In addition, the responses of CO2 to N addition in combination with climate change are dependent on ecosystem type (Lu et al. 2011). The potential mechanisms that alter CO2 emissions are (a) transfer of nutrients that stimulate microbial growth and respiration and (b) priming effects on SOM decomposition by microorganisms (Fontaine et al. 2007; Janssens et al. 2010; Oertel et al. 2016). For example, N addition in combination with climate change can have a greater impact on soil CO2 flux in grasslands than in forests due to higher stimulation of autotrophic respiration in grasslands (Zhou et al. 2014). Climate condition is the another key determinant of differences in reported effects in empirical studies. Previous studies have reported that N addition plus increased precipitation at a dry or mesic site could stimulate GHG emissions, as opposed to a wet site, where responses are neutral or even negative (Shi et al. 2021; Wu et al. 2020). The results may be because dry regions are more sensitive to increased precipitation than moist regions. In addition, experimental methods such as the duration and magnitude of N addition, warming, and altered precipitation can drive differences in responses (Sánchez-Martín et al. 2017; Zhang et al. 2008). No overall conclusions have been reached regarding the combined effects of N addition and warming or altered precipitation, limiting our mechanistic understanding of the responses of soil GHG fluxes to global changes. A meta-analysis across multiple ecosystem types with heterogeneous climatic conditions could facilitate adequate assessment of the effects of global change on GHG emissions at the global scale.
The aims of the present study were to (1) determine how warming and altered precipitation contribute to the effects of N addition on soil GHG emissions; (2) evaluate the interactions between N addition and warming or altered precipitation; and (3) explore the major drivers of the context-dependency observed in empirical studies. Accordingly, a meta-analysis of 2103 observations from published articles that reported both single-driver (N addition, warming, increased precipitation, and decreased precipitation) and corresponding two-driver effects on soil GHG fluxes was conducted. The observations were mainly collected from grassland and forest ecosystems in the Northern Hemisphere, particularly China. We hypothesized that (1) warming and increased precipitation will enhance the positive effect of N addition on soil GHG fluxes, while decreased precipitation will inhibit it and (2) these effects vary across different ecosystems and climatic conditions.
Materials and methods
Data compilation
Peer-reviewed articles published before September 2022 were searched in Web of Science (http://apps.webofknowledge.com/) and China National Knowledge Infrastructure (https://www.cnki.net/) using the following search string: (“nitrogen addition” OR “nitrogen deposition” OR “nitrogen fertilization”) AND (warming OR precipitation OR rainfall OR drought) AND (“greenhouse gas” OR CO2 OR “carbon dioxide” OR CH4 OR methane OR N2O OR “nitrous oxide”). The inclusion criteria were as follows: (1) experiments were conducted in the field and the impacts of N addition and at least one of the climate change factors (warming, increased, or decreased precipitation) were recorded, including both their single-driver and corresponding two-driver effects; (2) at least one variable among CO2 emissions, CH4 emissions, CH4 uptake, and N2O emissions was measured; (3) except for climate change factors and N addition, the conditions of the control and treatment groups were the same; and (4) the means, standard deviations (or standard errors), and sample sizes of the variables were directly provided or could be calculated.
The experiments manipulating two or more treatments, including different climate change factors or magnitudes with the same control, were divided into different control–treatment pairs. If the individual and combined effects on GHGs in a particular study were observed several times at different experimental stages, we used all observations to facilitate the evaluation of experimental duration effects. Data were directly extracted from the main text, table, or appendices, or from figures using Engauge Digitizer version 11.2 (Free Software Foundation, Boston, MA, USA). The ecosystem types (desert, cropland, wetland, forest, and grassland), experimental methods (experimental magnitude and experimental duration), climate conditions [mean annual temperature (MAT) and mean annual precipitation (MAP)], and edaphic characteristics (pH, water content, C content, and N content) were extracted from the studies to assess the impacts of moderator variables. If the MAT or MAP of the experimental sites was not provided in the studies, we extracted them from the WorldClim database (https://www.worldclim.org/).
We calculated the De Martonne (1926) aridity index for each experimental site using the MAT and MAP data as follows:
A total of 2103 paired observations were collected from 57 articles. CH4 emissions were not included owing to the small number of studies. In these articles, 2, 3, 6, 9, and 37 studies were conducted in deserts, croplands, wetlands, forests, and grasslands, respectively, accounting for 4%, 5%, 10%, 16%, and 65% of the studies, respectively (Additional file 1: Table S1). The form of N addition in 92% of the experiments was NH4NO3 and 8% were urea, CaNO3, and Ca(NO3)2. The latitude ranged from 26.32°N to 48.25°N, the altitude from 20 to 4763 m, the MAT from –5.3 °C to 19.1 °C, and the MAP from 200 to 1850 mm (Fig. 1).
Statistical analysis
Individual and combined effects
To quantify the individual and combined effects of N addition, warming, and altered precipitation on soil GHG fluxes, we calculated the response ratio (\(\mathrm{ln}RR\)) as a proxy for effect size as follows:
where \({\overline{X} }_{t}\) and \({\overline{X} }_{c}\) are the mean values of the treatment and control groups, respectively. The variance (\(v\)) of each \(\mathrm{ln}RR\) was calculated as follows:
where \({\overline{X} }_{t}\), \({S}_{t}\), and \({n}_{t}\) represent the mean, standard deviation, and sample size of the treatment group (t), respectively; and \({\overline{X} }_{c}\), \({S}_{c}\), and \({n}_{c}\) are the mean, standard deviation, and sample size of the control group (c), respectively.
To estimate the overall effect size (\(\mathrm{ln}{RR}_{++}\)), we performed linear mixed-effects models using the “lme4” package (Bates et al. 2015) in R version 4.2.0 (R Core Team 2022) with the individual \(\mathrm{ln}RR\) fitted as the response variable and the identity of the study and plots (nested inside study identity) as the random effect factors (Additional file 2). This approach explicitly accounts for the potential dependence of observations collected from a single study. To investigate whether the ecosystem type, climate (MAT and MAP), edaphic characteristics (moisture, pH, C content, and N content), and experimental methods (N addition rate, warming magnitude, and duration) influence the response of GHGs to N addition and the interaction with climate change, these factors were fitted as continuous or categorical fixed-effect factors. Data were subjected to z-score standardization prior to analysis to allow for comparisons (Ali and Faraj 2014). z-scores were determined by standardization by subtracting the mean value from the raw data and dividing the resulting number by the standard deviation of the mean. The corresponding 95% confidence interval (\(\mathrm{CI}\)) and percentage change (%) were calculated as follows:
The treatment effects were considered non-significant if the 95% \(\mathrm{CI}\) of \(\mathrm{ln}{RR}_{++}\) overlapped with zero. When the 95% \(\mathrm{CI}\) of \(\mathrm{ln}{RR}_{++}\) did not overlap with zero, the effect was identified as positive if \(\mathrm{ln}{RR}_{++}\) was greater than zero; otherwise, the effect was identified as negative if \(\mathrm{ln}{RR}_{++}\) was less than zero.
Furthermore, publication bias was assessed to analyze whether the studies used in the present meta-analysis were representative or not using Egger’s regression tests (Egger et al. 1997). Funnel plots were generated using the response ratios (\(\mathrm{ln}RR\)) and their standard errors. All results indicated that studies used in this meta-analysis were robust against publication bias (Additional file 1: Fig. S1).
Interactive effects
To further understand the interactive effects of two drivers occurring simultaneously (combined effects), Hedges’ \(d\) was used to calculate interactive effect size (\({d}_{I}\)) as previously described (Gurevitch et al. 2000):
where \({\overline{X} }_{c}\), \({\overline{X} }_{A}\), \({\overline{X} }_{B}\), and \({\overline{X} }_{AB}\), are the means of the variables in the control group, treatment groups A and B, and their combination (A + B), respectively.
The standard deviation (\({s}\)), degrees of freedom (\(m\)), and correction term (\({J}\left(m\right)\)) were estimated using Eqs. (7–9).
where \({n}_{c}\), \({n}_{A}\), \({n}_{B}\), and \({n}_{AB}\) are the sample sizes and \({s}_{c}\), \({s}_{A}\), \({s}_{B}\), and \({s}_{AB}\) are the standard deviations in the control and treatment groups of A, B, and their combination (A + B), respectively.
The variance (\({v}_{2}\)) of \({d}_{I}\) was estimated as follows:
We performed linear mixed-effects models to calculate the weighted mean of \({d}_{I}\) (\({d}_{++}\)) with \({d}_{I}\) as the response variable and study identity and plots (nested inside study identity) as the random effect factors. All the analyses were conducted in R version 4.2.0 (R Core Team 2022) using the ‘lme4’ package (Bates et al. 2015).
The interactions between treatments were classified into three types: additive, synergistic, and antagonistic (Folt et al. 1999; Crain et al. 2008). Additive effects occurred when their combined effects were not significantly different from the sum of their individual effects; synergistic interactions were observed when the combined effect was significantly greater than the sum of their individual effects and antagonistic interactions when the combined effect was less than the sum of their individual effects. In terms of Hedges’ \(d\), interactions were considered additive if the 95% \(\mathrm{CI}\) of the weighted mean \({d}_{I}\) overlapped with zero. If the 95% \(\mathrm{CI}\) did not overlap with zero, we determined the interaction effect through their individual effects. If the individual effects of the two drivers were both negative or one negative and one positive, interaction effect sizes less than zero were considered synergistic, and those greater than zero were antagonistic. In cases where the individual effects were both positive, interaction effect sizes greater than zero were synergistic, and those less than zero were antagonistic.
Results
Overall responses of soil GHG fluxes
Overall, soil CO2 emissions did not respond significantly to N addition alone, but it increased by an average of 17.2% and 21.7% under warming alone and warming plus N addition, respectively (Fig. 2a). N addition alone or in combination with warming or altered precipitation minimally affected soil CH4 uptake, while warming alone significantly increased CH4 uptake by an average of 28.2% (Fig. 2b). In contrast, N2O emissions increased significantly by 106.2%, 112.2%, 108.2%, and 105.2% under N addition alone, warming plus N addition, increased precipitation plus N addition, and decreased precipitation plus N addition, respectively. However, individual climate change treatments did not affect soil N2O emissions, except for decreased precipitation, which significantly decreased N2O emissions by 40.6% (Fig. 2c).
Variation among ecosystem types
The effects of N addition alone on CO2 emissions were independent of ecosystem type, whereas the effects of N addition plus warming or altered precipitation were different among ecosystem types, significantly affecting grasslands but not forests (Fig. 3a). The individual and combined effects of N addition and warming positively impacted soil CH4 uptake in grasslands, but their effects were negative in croplands (Fig. 3b). The responses of soil N2O emissions to various treatments were independent of ecosystem type (Fig. 3c). Based on the results of linear mixed-effects models, the most important regulator of the differences among ecosystem types was soil moisture rather than soil pH, and initial soil C and N content (Table 1). Soil moisture had significantly negative effects on the \(\mathrm{ln}RR\) of CO2 emissions to N addition plus warming, increased precipitation alone, and N addition plus increased precipitation, and the \(\mathrm{ln}RR\) of CH4 uptake to warming alone and N addition plus warming.
Effects of climate and experimental methods
The \(\mathrm{ln}RR\) of GHG fluxes to N addition plus warming or altered precipitation was significantly influenced by climate and experimental methods (Table 1). Aridity index was the most important driver of the combined effects of N addition and increased precipitation on soil CH4 uptake, showing significant negative effects. The \(\mathrm{ln}RR\) of CO2 and N2O under warming plus N addition was positively affected by the magnitude of warming. Altered precipitation magnitude, N addition rate (Additional file 1: Fig. S2), and experimental duration had non-significant effects on the \(\mathrm{ln}RR\) of GHG fluxes.
Interactions between N addition and climate change
Across all two-driver pairs, the overall interactive effects of N addition and warming or altered precipitation on GHG fluxes were generally additive, except for the antagonistic interaction between decreased precipitation and N addition on N2O emissions (Fig. 4). Additive interactions accounted for a higher proportion than synergistic or antagonistic effects among individual pairwise observations, representing 26–54%, 60–75%, and 41–67% of the combined effects of warming plus N addition, increased precipitation plus N addition, and decreased precipitation plus N addition, respectively.
Discussion
Responses of soil CO2 emissions
The combined effects of N addition and warming or increased precipitation raised CO2 emissions more than N addition alone, partially supporting our first hypothesis. Soil CO2 emissions did not respond significantly to N addition alone, but it increased significantly under warming alone and increased precipitation alone. Therefore, the increases in CO2 emissions were mainly attributed to the effect of warming and increased precipitation, rather than N addition. These results suggested that temperature and precipitation are key drivers regulating soil CO2 emissions, which is consistent with the previous studies (Deng et al. 2020; Yang et al. 2022). Moreover, the overall interactions between N addition and warming or increased precipitation were additive, indicating that combined N addition and warming or increased precipitation on CO2 emissions were not substantially different from the sum of their respective individual effects. Therefore, the effects of N addition and climate change factors on CO2 emissions were relatively independent. The non-significant effects of N addition on CO2 emissions revealed in our meta-analysis may be attributed to the possibility that the level of N addition reached or exceeded the N critical load due to continuous N enrichment (Zong et al. 2016; Bai et al. 2019). Various studies have suggested that N addition initially stimulated soil respiration but gradually suppressed CO2 emissions (Xia et al. 2009; Yan et al. 2010). Moreover, Hui et al. (2020) have demonstrated that the absence of other nutrients, such as phosphorus, may suppress the effect of N addition. Therefore, the potential mechanisms by which N addition influenced ecosystem CO2 emission and the long-term effects of continuous N enrichment should be further explored.
Consistent with our second hypothesis, the effects of N addition in combination with warming or increased precipitation were influenced by climatic condition. Aridity index primarily regulated CO2 emissions under altered precipitation plus N addition (Table 1). Increased precipitation alleviated water shortages in arid areas and promoted soil respiration (Sierra et al. 2017), while decreased precipitation exacerbated the dry conditions, strongly affecting soil biotic processes by limiting water availability, leading to a decrease in CO2 emissions (de Dato et al. 2010). Differences in the soil moisture may explain the various responses of CO2 emissions to N addition plus increased precipitation between forests and grasslands, as forests have higher soil moisture than grasslands (Additional file 1: Fig. S3). Moreover, the combined effect of N addition plus warming on soil CO2 emissions was positively correlated with warming magnitude, indicating that these combined effects were stimulated by warming (Carey et al. 2016). Although climatic condition has been observed to be a major factor influencing differences in the soil CO2 emissions of forests and grasslands, the lack of observations from other ecosystems still contributes to our poor understanding of soil CO2 emissions among different ecosystems globally. Therefore, we propose more multifactorial experiments in various ecosystems in future work.
Responses of soil CH4 uptake
In contrast to CO2 emissions, the effects of N addition on soil CH4 uptake remained unaltered when combined with warming or altered precipitation. Additive interactions between N addition and warming or altered precipitation on soil CH4 uptake appeared to be much more common compared with synergistic and antagonistic interactions. Warming increased soil CH4 uptake significantly by increasing the biomass of methane-oxidizing and decreasing the biomass of methanogenic microorganisms (Qi et al. 2022). However, warming in combination with N addition suppressed this significantly positive effect, which may be related to the increase in soil acidity (Bowman et al. 2008; Jamil et al. 2022). Therefore, the response of soil CH4 uptake to warming plus N addition was negatively related to the N addition rate.
We found that the response of soil CH4 uptake to N addition combined with warming was negatively correlated with higher soil moisture content. Furthermore, the effect of N addition plus increased precipitation was negatively correlated with aridity index. These findings may be related to the CH4 production and consumption processes of soil microorganisms. Soil CH4 is produced by methanogens in wet anaerobic soils and consumed by methanotrophs in drier aerobic soils (Fest et al. 2017; Liu et al. 2019); therefore, warming and increased precipitation could enhance the emissions of soil CH4 by increasing the activities of methanogenic archaea and methanotrophic bacteria in humid areas (Aronson et al. 2013; Kammann et al. 2001; Zhao et al. 2017). This could also explain the significant differences in soil CH4 uptake between grasslands and croplands. Due to observational limitations, we could not analyze the effects of altered precipitation plus N addition on CH4 uptake among different ecosystem types; more experiments conducted in various ecosystems are required to predict CH4 emissions under future climate change scenarios.
Responses of soil N2O emissions
The increases in N2O emissions caused by N addition plus warming or altered precipitation did not differ from that of N addition alone, while warming and increased precipitation alone had non-significant effects. This implies that temperature and precipitation are not major factors affecting soil N2O emissions (Yang et al. 2021), which was inconsistent with the results of Zhang et al. (2021) and Huang et al. (2014). N addition was an important factor influencing soil N2O emissions because soil N2O released as an intermediate product when ammonium (NH4+) is oxidized to nitrate (NO3–) by nitrification, or during the reduction of NO3– or nitrite (NO2–) by denitrification (Snyder et al. 2009; Hube et al. 2017). Therefore, soil N2O emissions are mainly limited by soil N availability (Gao et al. 2015). Increased N supply can stimulate soil N2O emissions directly by promoting the proliferation of microbial communities involved in nitrification and denitrification (Pajares and Bohannan 2016). Similar findings were reported by Deng et al. (2020) and Du et al. (2021), they found that N addition increased soil N2O emissions by 164% and 91%, respectively, which were consistent with our result (+ 106%). In the present study, an overall antagonistic interaction between N addition and decreased precipitation on N2O emissions was observed. In this case, the negative effects of decreased precipitation on N2O emissions would be counteracted by N addition in the combined effects (Geng et al. 2017). However, overall interactions of N addition and warming or increased precipitation on N2O emissions were generally additive, indicating that the effect of N addition, warming, and increased precipitation on N2O emissions would not be changed in the combined effects. Although synergistic and antagonistic interactions were observed among the individual observations, additive interactions remained predominant. This finding may be attributed to the interactions between multiple region-dependent global change factors, where different climatic conditions and ecosystem types generate various effects (Baah-Acheamfour et al. 2016; Liu and Greaver 2009).
The responses of soil N2O emissions to individual and combined effects of N addition, warming, and altered precipitation did not vary significantly among ecosystem types. These results indicated that ecosystem type had only a minor impact on soil N2O emissions (Deng et al. 2020; Li et al. 2020). In addition, the positive effects of N addition combined with warming or altered precipitation on soil N2O emissions were hardly affected by climatic and experimental conditions. Soil N2O is consistently released rapidly at the beginning of N addition, irrespective of the experimental duration (Li et al. 2022; Xu et al. 2017; Song and Niu 2022). These observations suggested that N addition is the major driver of increased soil N2O emissions and the feedbacks between them are not altered by climate change.
Main limitations and future perspectives
We found that soil GHG fluxes could be stimulated to some extent by multiple global change factors, including N addition, warming, and altered precipitation. The responses of soil GHG fluxes to N addition were not significantly affected by warming or altered precipitation, as illustrated by the additive interaction effects. Our study provides a comprehensive analysis of soil GHG fluxes by considering the effects of N addition under joint warming or altered precipitation in multiple terrestrial ecosystems. Nevertheless, we acknowledge some limitations of our study. First, the compiled data were mainly from studies in grassland of Northern Hemisphere, particularly China (Fig. 1), with other regions of the world being poorly represented, which possibly led to a misrepresentation of global change effects on soil GHG fluxes. In addition, multiple subtypes existed in these broad categories of ecosystem types that could not be categorized due to the limited observations, which hampered our ability to draw robust and general conclusions on the effects of global change on soil GHG fluxes among different ecosystems. Second, our results showed that decreased precipitation plus N addition did not affect soil CH4 uptake, but increased N2O emissions significantly. However, the sample size of the combined effects was insufficient and only represented grassland ecosystems, which may contribute to the uncertainty of our estimations. Third, in most experiments N addition was applied in the form of NH4NO3, yet research has shown that the response of soil GHG fluxes to N addition is influenced significantly by N form (Du et al. 2021). To improve our understanding of how GHG fluxes will respond to global climate change scenarios, future multi-factor experimental studies should focus on underrepresented regions, especially the effects of altered precipitation and N addition on soil CH4 and N2O.
Conclusion
This study examined the effects of N addition combined with warming and altered precipitation on GHG fluxes at a multi-continental scale. Warming and altered precipitation rarely influenced the effects of N addition on soil GHG fluxes, both in magnitude and direction. Their overall interactions on GHG fluxes were generally additive (i.e., not differing from the sum of their individual effects) rather than synergistic or antagonistic, suggesting the relative independence of these factors. Soil CO2 emissions were mainly regulated by temperature and precipitation rather than by N addition, whereas N2O emissions were overall limited by N addition. The effects of N addition plus increased precipitation on soil CO2 emissions and the effects of N addition plus warming on soil CH4 uptake showed contrasting results among different ecosystems, which were mainly related to soil moisture. In contrast, the soil N2O emissions did not significantly differ among ecosystems. The individual and combined effects of these treatments on soil GHG fluxes were regulated by climate and experimental methods. Overall, our results not only quantitatively synthesized the patterns of N addition and climate change on soil GHG fluxes, but also showed that the effects of N addition, warming, and altered precipitation were relatively independent. These findings advance current understanding of the response of soil GHG fluxes to N addition in combination with warming and altered precipitation and provide insights into C and N cycling under global climate change.
Availability of data and materials
The data that support the findings of this study are available at https://doi.org/10.1186/s13717-023-00470-9.
Abbreviations
- GHG:
-
Greenhouse gas
- N:
-
Nitrogen
- CO2 :
-
Carbon dioxide
- CH4 :
-
Methane
- N2O:
-
Nitrous oxide
- SOM:
-
Soil organic matter
References
Ali PJM, Faraj RH (2014) Data normalization and standardization: a technical report. Mach Learn Tech Rep 1:1–6
Aronson EL, Allison SD, Helliker BR (2013) Environmental impacts on the diversity of methane-cycling microbes and their resultant function. Front Microbiol 4:225. https://doi.org/10.3389/fmicb.2013.00225
Aronson EL, Goulden ML, Allison SD (2019) Greenhouse gas fluxes under drought and nitrogen addition in a Southern California grassland. Soil Biol Biochem 131:19–27. https://doi.org/10.1016/j.soilbio.2018.12.010
Baah-Acheamfour M, Carlyle CN, Lim SS, Bork EW, Chang SX (2016) Forest and grassland cover types reduce net greenhouse gas emissions from agricultural soils. Sci Total Environ 571:1115–1127. https://doi.org/10.1016/j.scitotenv.2016.07.106
Bai W, Wang G, Xi J, Liu Y, Yin P (2019) Short-term responses of ecosystem respiration to warming and nitrogen addition in an alpine swamp meadow. Eur J Soil Biol 92:16–23. https://doi.org/10.1016/j.ejsobi.2019.04.003
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67:1–48
Bowman WD, Cleveland CC, Halada Ĺ, Hreško J, Baron JS (2008) Negative impact of nitrogen deposition on soil buffering capacity. Nat Geosci 1:767–770. https://doi.org/10.1038/ngeo339
Brown JR, Blankinship JC, Niboyet A, van Groenigen KJ, Dijkstra P, Le Roux X, Leadley PW, Hungate BA (2012) Effects of multiple global change treatments on soil N2O fluxes. Biogeochemistry 109:85–100. https://doi.org/10.1007/s10533-011-9655-2
Carey JC, Tang J, Templer PH, Kroeger KD, Crowther TW, Burton AJ, Dukes JS, Emmett B, Frey SD, Heskel MA, Jiang L, Machmuller MB, Mohan J, Panetta AM, Reich PB, Reinsch S, Wang X, Allison SD, Bamminger C, Tietema A (2016) Temperature response of soil respiration largely unaltered with experimental warming. Proc Natl Acad Sci U S A 113:13797–13802. https://doi.org/10.1073/pnas.1605365113
Chen X, Wang G, Zhang T, Mao T, Wei D, Hu Z, Song C (2017a) Effects of warming and nitrogen fertilization on GHG flux in the permafrost region of an alpine meadow. Atmos Environ 157:111–124
Chen X, Wang G, Zhang T, Mao T, Wei D, Song C, Hu Z, Huang K (2017b) Effects of warming and nitrogen fertilization on GHG flux in an alpine swamp meadow of a permafrost region. Sci Total Environ 601–602:1389–1399
Chen J, Feng M, Cui Y, Liu G (2021) The impacts of nitrogen addition on upland soil methane uptake: a global meta-analysis. Sci Total Environ 795:148863. https://doi.org/10.1016/j.scitotenv.2021.148863
Cheng J, Xu L, Wu J, Xu J, Jiang M, Feng W, Wang Y (2022) Responses of ecosystem respiration and methane fluxes to warming and nitrogen addition in a subtropical littoral wetland. Catena 215:106335. https://doi.org/10.1016/j.catena.2022.106335
Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315
de Dato GD, De Angelis P, Sirca C, Beier C (2010) Impact of drought and increasing temperatures on soil CO2 emissions in a Mediterranean shrubland (gariga). Plant Soil 327:153–166. https://doi.org/10.1007/s11104-009-0041-y
De Martonne E (1926) Une nouvelle fonction climatologique: l’indice d’aridité. La Météorologie 2:449–458
Deng L, Huang C, Kim D, Shangguan Z, Wang K, Song X, Peng C (2020) Soil GHG fluxes are altered by N deposition: new data indicate lower N stimulation of the N2O flux and greater stimulation of the calculated C pools. Glob Change Biol 26:2613–2629. https://doi.org/10.1111/gcb.14970
Du Y, Ke X, Li J, Wang Y, Cao G, Guo X, Chen K (2021) Nitrogen deposition increases global grassland N2O emission rates steeply: a meta-analysis. Catena 199:105105. https://doi.org/10.1016/j.catena.2020.105105
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634. https://doi.org/10.1136/bmj.315.7109.629
Fest B, Hinko-Najera N, von Fischer JC, Livesley SJ, Arndt SK (2017) Soil methane uptake increases under continuous throughfall reduction in a temperate evergreen, broadleaved eucalypt forest. Ecosystems 20:368–379. https://doi.org/10.1007/s10021-016-0030-y
Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877
Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280. https://doi.org/10.1038/nature06275
Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927
Gao W, Yang H, Kou L, Li S (2015) Effects of nitrogen deposition and fertilization on N transformations in forest soils: a review. J Soils Sediments 15:863–879. https://doi.org/10.1007/s11368-015-1064-z
Geng S, Chen Z, Han S, Wang F, Zhang J (2017) Rainfall reduction amplifies the stimulatory effect of nitrogen addition on N2O emissions from a temperate forest soil. Sci Rep 7:43329. https://doi.org/10.1038/srep43329
Gong Y, Wu J (2021) Vegetation composition modulates the interaction of climate warming and elevated nitrogen deposition on nitrous oxide flux in a boreal peatland. Glob Change Biol 27:5588–5598. https://doi.org/10.1111/gcb.15865
Gurevitch J, Morrison JA, Hedges LV (2000) The interaction between competition and predation: a meta-analysis of field experiments. Am Nat 155:435–453
Harte J, Torn MS, Chang FR, Feifarek B, Kinzig AP, Shaw R, Shen K (1995) Global warming and soil microclimate: results from a meadow-warming experiment. Ecol Appl 5:132–150. https://doi.org/10.2307/1942058
He Y, Wang X, Wang K, Tang S, Xu H, Chen A, Ciais P, Li X, Peñuelas J, Piao S (2021) Data-driven estimates of global litter production imply slower vegetation carbon turnover. Glob Change Biol 27:1678–1688
Huang H, Wang J, Hui D, Miller DR, Bhattarai S, Dennis S, Smart D, Sammis T, Reddy KC (2014) Nitrous oxide emissions from a commercial cornfield (Zea mays) measured using the eddy covariance technique. Atmos Chem Phys 14:12839–12854. https://doi.org/10.5194/acp-14-12839-2014
Hube S, Alfaro MA, Scheer C, Brunk C, Ramírez L, Rowlings D, Grace P (2017) Effect of nitrification and urease inhibitors on nitrous oxide and methane emissions from an oat crop in a volcanic ash soil. Agric Ecosyst Environ 238:46–54. https://doi.org/10.1016/j.agee.2016.06.040
Hui D, Porter W, Phillips JR, Aidar MPM, Lebreux SJ, Schadt CW, Mayes MA (2020) Phosphorus rather than nitrogen enhances CO2 emissions in tropical forest soils: evidence from a laboratory incubation study. Eur J Soil Sci 71:495–510. https://doi.org/10.1111/ejss.12885
IPCC (2013) Climate Change 2013: the physical science basis. Cambridge University Press, Cambridge
IPCC (2022) Climate Change 2022: Impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge
Jamil MA, Hussain A, Duan W, Chen L, Khan K, Abid K, Li C, Guo Q, Zarif N, Qu M, Wang Y, Khan A (2022) Effect of simulated combined N and P on soil acidity within soil aggregates in natural and planted Korean pine forest in northeast China. Forests 13:529. https://doi.org/10.3390/f13040529
Janssens IA, Dieleman W, Luyssaert S, Subke JA, Reichstein M, Ceulemans R, Ciais P, Dolman AJ, Grace J, Matteucci G, Papale D, Piao SL, Schulze ED, Tang J, Law BE (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322. https://doi.org/10.1038/ngeo844
Kammann C, Grünhage L, Jäger HJ, Wachinger G (2001) Methane fluxes from differentially managed grassland study plots: the important role of CH4 oxidation in grassland with a high potential for CH4 production. Environ Pollut 15:261–273. https://doi.org/10.1016/S0269-7491(01)00103-8
Le Mer J, Roger P (2001) Production, oxidation, emission and consumption of methane by soils: a review. Eur J Soil Biol 37:25–50. https://doi.org/10.1016/S1164-5563(01)01067-6
Li L, Zheng Z, Wang W, Biederman JA, Xu X, Ran Q, Qian R, Xu C, Zhang B, Wang F, Zhou S, Cui L, Che R, Hao Y, Cui X, Xu Z, Wang Y (2020) Terrestrial N2O emissions and related functional genes under climate change: a global meta-analysis. Glob Change Biol 26:931–943. https://doi.org/10.1111/gcb.14847
Li B, Chen G, Lu X, Jiao H (2022) Effects of nitrogen and phosphorus additions on soil N2O emissions and CH4 uptake in a phosphorus-limited subtropical Chinese fir plantation. Forests 13:772. https://doi.org/10.3390/f13050772
Liu L, Greaver TL (2009) A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecol Lett 12:1103–1117. https://doi.org/10.1111/j.1461-0248.2009.01351.x
Liu X, Dong Y, Qi Y, Peng Q, He Y, Sun L, Jia J, Guo S, Cao C, Yan Z, Liu X (2015) Response of N2O emission to water and nitrogen addition in temperate typical steppe soil in Inner Mongolia, China. Soil Tillage Res 151:9–17. https://doi.org/10.1016/j.still.2015.01.008
Liu L, Estiarte M, Peñuelas J (2019) Soil moisture as the key factor of atmospheric CH4 uptake in forest soils under environmental change. Geoderma 355:113920. https://doi.org/10.1016/j.geoderma.2019.113920
Liu S, Zheng Y, Ma R, Yu K, Han Z, Xiao S, Li Z, Wu S, Li S, Wang J, Luo Y, Zou J (2020) Increased soil release of greenhouse gases shrinks terrestrial carbon uptake enhancement under warming. Glob Change Biol 26:4601–4613. https://doi.org/10.1111/gcb.15156
Lu M, Zhou X, Luo Y, Yang Y, Fang C, Chen J, Li B (2011) Minor stimulation of soil carbon storage by nitrogen addition: a meta-analysis. Agric Ecosyst Environ 140:234–244. https://doi.org/10.1016/j.agee.2010.12.010
Ni X, Groffman PM (2018) Declines in methane uptake in forest soils. Proc Natl Acad Sci U S A 115:8587–8590. https://doi.org/10.1073/pnas.1807377115
Niu S, Wu M, Han Y, Xia J, Zhang Z, Yang H, Wan S (2010) Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Glob Change Biol 16:144–155. https://doi.org/10.1111/j.1365-2486.2009.01894.x
Oertel C, Matschullat J, Zurba K, Zimmermann F, Erasmi S (2016) Greenhouse gas emissions from soils: a review. Geochemistry 76(3):327–352. https://doi.org/10.1016/j.chemer.2016.04.002
Pajares S, Bohannan BJM (2016) Ecology of nitrogen fixing, nitrifying, and denitrifying microorganisms in tropical forest soils. Front Microbiol 7:1045. https://doi.org/10.3389/fmicb.2016.01045
Qi Q, Zhao J, Tian R, Zeng Y, Xie C, Gao Q, Dai T, Wang H, He S, Konstantinidis KT, Yang Y, Zhou J, Guo X (2022) Microbially enhanced methane uptake under warming enlarges ecosystem carbon sink in a Tibetan alpine grassland. Glob Change Biol 28:6906–6920. https://doi.org/10.1111/gcb.16444
Quinn Thomas R, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17. https://doi.org/10.1038/ngeo721
Sanchez-Martin L, Bermejo-Bermejo V, Garcia-Torres L, Alonso R, de la Cruz A, Calvete-Sogo H, Vallejo A (2017) Nitrogen soil emissions and belowground plant processes in Mediterranean annual pastures are altered by ozone exposure and N-inputs. Atmos Environ 165:12–22. https://doi.org/10.1016/j.atmosenv.2017.06.030
Shi H, Cai S, Sun Z, Shi Y (2021) Water-use efficiency and greenhouse gas emissions of rice affected by water saving and nitrogen reduction. Agron J 113:4777–4792. https://doi.org/10.1002/agj2.20672
Sierra CA, Malghani S, Loescher HW (2017) Interactions among temperature, moisture, and oxygen concentrations in controlling decomposition rates in a boreal forest soil. Biogeosciences 14:703–710. https://doi.org/10.5194/bg-14-703-2017
Snyder CS, Bruulsema TW, Jensen TL, Fixen PE (2009) Review of greenhouse gas emissions from crop production systems and fertilizer management effects. Agric Ecosyst Environ 133:247–266. https://doi.org/10.1016/j.agee.2009.04.021
Song L, Niu S (2022) Increased soil microbial AOB amoA and narG abundances sustain long-term positive responses of nitrification and denitrification to N deposition. Soil Biol Biochem 166:108539. https://doi.org/10.1016/j.soilbio.2021.108539
World Meteorological Organization (2020) Greenhouse Gas Bulletin: the state of greenhouse gases in the atmosphere based on global observations through 2019. Switzerland, Geneva
Wu G, Chen X, Ling J, Li F, Li F, Peixoto L, Wen Y, Zhou S (2020) Effects of soil warming and increased precipitation on greenhouse gas fluxes in spring maize seasons in the North China Plain. Sci Total Environ 734:139269. https://doi.org/10.1016/j.scitotenv.2020.139269
Xia J, Niu S, Wan S (2009) Response of ecosystem carbon exchange to warming and nitrogen addition during two hydrologically contrasting growing seasons in a temperate steppe. Glob Change Biol 15:1544–1556. https://doi.org/10.1111/j.1365-2486.2008.01807.x
Xu K, Wang C, Yang X (2017) Five-year study of the effects of simulated nitrogen deposition levels and forms on soil nitrous oxide emissions from a temperate forest in northern China. PLoS ONE 12:e0189831. https://doi.org/10.1371/journal.pone.0189831
Yan L, Chen S, Huang J, Lin G (2010) Differential responses of auto- and heterotrophic soil respiration to water and nitrogen addition in a semiarid temperate steppe. Glob Change Biol 16:2345–2357. https://doi.org/10.1111/j.1365-2486.2009.02091.x
Yang Y, Xiao Y, Li C, Wang B, Gao Y, Zhou G (2021) Nitrogen addition, rather than altered precipitation, stimulates nitrous oxide emissions in an alpine steppe. Ecol Evol 11:15153–15163. https://doi.org/10.1002/ece3.8196
Yang J, Jia X, Ma H, Chen X, Liu J, Shangguan Z, Yan W (2022) Effects of warming and precipitation changes on soil GHG fluxes: a meta-analysis. Sci Total Environ 827:154351. https://doi.org/10.1016/j.scitotenv.2022.154351
Zhang W, Mo J, Zhou G, Gundersen P, Fang Y, Lu X, Zhang T, Dong S (2008) Methane uptake responses to nitrogen deposition in three tropical forests in southern China. J Geophys Res 113:D11116. https://doi.org/10.1029/2007JD009195
Zhang H, Sun H, Zhou S, Bai N, Zheng X, Li S, Zhang J, Lv W (2019) Effect of straw and straw biochar on the community structure and diversity of ammonia-oxidizing bacteria and archaea in rice-wheat rotation ecosystems. Sci Rep 9:9367. https://doi.org/10.1038/s41598-019-45877-7
Zhang Y, Zhang N, Yin J, Zhao Y, Yang F, Jiang Z, Tao J, Yan X, Qiu Y, Guo H, Hu S (2020) Simulated warming enhances the responses of microbial N transformations to reactive N input in a Tibetan alpine meadow. Environ Int 141:105795. https://doi.org/10.1016/j.envint.2020.105795
Zhang H, Deng Q, Schadt CW, Mayes MA, Zhang D, Hui D (2021) Precipitation and nitrogen application stimulate soil nitrous oxide emission. Nutr Cycl Agroecosys 120:363–378. https://doi.org/10.1007/s10705-021-10155-4
Zhao Z, Dong S, Jiang X, Liu S, Ji H, Li Y, Han Y, Sha W (2017) Effects of warming and nitrogen deposition on CH4, CO2 and N2O emissions in alpine grassland ecosystems of the Qinghai-Tibetan Plateau. Sci Total Environ 592:565–572. https://doi.org/10.1016/j.scitotenv.2017.03.082
Zhou L, Zhou X, Zhang B, Lu M, Luo Y, Liu L, Li B (2014) Different responses of soil respiration and its components to nitrogen addition among biomes: a meta-analysis. Glob Change Biol 20:2332–2343. https://doi.org/10.1111/gcb.12490
Zhou X, Zhou L, Nie Y, Fu Y, Du Z, Shao J, Zheng Z, Wang X (2016) Similar responses of soil carbon storage to drought and irrigation in terrestrial ecosystems but with contrasting mechanisms: a meta-analysis. Agric Ecosyst Environ 228:70–81
Zhou Z, Wang C, Luo Y (2018) Response of soil microbial communities to altered precipitation: a global synthesis. Glob Ecol Biogeogr 27:1121–1136. https://doi.org/10.1111/geb.12761
Zong N, Shi P, Song M, Zhang X, Jiang J, Chai X (2016) Nitrogen critical loads for an alpine meadow ecosystem on the Tibetan Plateau. Environ Manag 57:531–542. https://doi.org/10.1007/s00267-015-0626-6
Zong N, Geng S, Duan C, Shi P, Chai X, Zhang X (2018) The effects of warming and nitrogen addition on ecosystem respiration in a Tibetan alpine meadow: the significance of winter warming. Ecol Evol 8:10113–10125. https://doi.org/10.1002/ece3.4484
Acknowledgements
We are grateful to the editor and two anonymous referees for their insightful comments and kind suggestions that significantly improved our manuscript. We also thank Yaoyi Zhang, Zihao Chen, and Hongrong Guo for their assistance with writing.
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This work was supported by the National Natural Science Foundation of China (No. 32171641, 32101509, and 32271633) and the Ph.D. programme grant from China Scholarship Council (202109107009).
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XW, XN, and FW conceived the study. XW and XN collected the raw data. XW, KVM, and KY performed data analyses and all authors contributed to subsequent revisions.
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Additional file 1: Fig. S1.
Assessments of publication bias. Funnel plots displaying the response ratio (\(\mathrm{ln}RR\)) of CO2 emission, CH4 uptake, and N2O emission and standard error for each data under N addition (N), warming (W), increased precipitation (IP), decreased precipitation (DP), and N addition in combined with warming (W+N), increased precipitation (IP+N), and decreased precipitation (DP+N). Results of publication bias tests using Egger's regression are given at the top of each panel (z and P values). P values > 0.05 indicate the absence of publication bias. Fig. S2. Effects of N addition rate on the response of soil CO2 emission (a), CH4 uptake (b), and N2O emission (c) to N addition (N), warming plus N addition (W+N), increased precipitation plus N addition (IP+N), and decreased precipitation plus N addition (DP+N). Data are presented as means with 95% confident intervals (CIs). Blue solid dots indicate significant positive effects, orange solid dots indicate significant negative effects, and gray solid dots indicate non-significant effects. The vertical dashed lines are zero lines. Fig. S3. Initial soil moisture in different ecosystems under combined effects of N addition and warming or altered precipitation on CO2 emission (a) and CH4 uptake (b). Mean (solid circles), median (horizontal line), interquartile range (box) and nonoutlier range (vertical line) are shown. Lowercase letters indicate differences among different ecosystems. Table S1. Overview of the experiments involving N addition, warming, and altered precipitation included in this meta-analysis as well as their interactions.
Additional file 2.
Data used in this meta-analysis.
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Wei, X., Wu, F., Van Meerbeek, K. et al. Warming and altered precipitation rarely alter N addition effects on soil greenhouse gas fluxes: a meta-analysis. Ecol Process 12, 56 (2023). https://doi.org/10.1186/s13717-023-00470-9
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DOI: https://doi.org/10.1186/s13717-023-00470-9