Inorganic N fertilization reduces soil organic carbon in bamboo forests in China

Abstract

Soil organic carbon (SOC) plays a vital role in mitigating climate change. While fertilization can substantially influence SOC, its impact on SOC storage in arbuscular mycorrhizal (AM)-dominated forests remains uncertain. To address this knowledge gap, we conducted a meta-analysis of 631 observations from 28 published studies to examine SOC responses to fertilization in bamboo forests dominated by AM fungi. Contrary to numerous previous meta-analyses, our results revealed that fertilization significantly decreased SOC by 4.46%. Specifically, inorganic nitrogen (N) fertilizers negatively affected SOC by disrupting the soil N:P:K stoichiometric balance, which can contribute to soil degradation and potentially impair the role of AM fungi in regulating soil carbon dynamics. In contrast, organic and compound N fertilizers showed no significant effect on SOC due to external nutrient inputs and additional C offsetting these negative impacts. The effects of fertilization on SOC varied depending on the level and duration of fertilization, as well as soil depth. Low-level and long-term fertilization resulted in significant SOC losses, particularly in the subsoil. Furthermore, our correlation analysis indicated that MAP, soil pH, MBC, NH₄⁺-N, and AK were key drivers of SOC responses to fertilization. Our findings offer a new perspective that contrasts with previous studies, showing that N fertilization significantly reduces SOC in bamboo forests. This underscores the need for future investigation into the mechanisms by which AM fungi regulate SOC dynamics. Consequently, we recommend using organic or compound N fertilizers to maintain SOC storage and contribute to climate change mitigation efforts.

Graphical abstract

Keywords

fertilization / soil organic carbon / arbuscular mycorrhizal / fertilizer types / bamboo forests

1 Introduction

Soil organic carbon (SOC) is crucial for maintaining the health, productivity, and resilience of forest ecosystems. It supports essential processes such as nutrient cycling, improving soil structure and water retention, and promoting biodiversity. Furthermore, SOC plays a vital role in carbon (C) sequestration, significantly contributing to climate change mitigation by storing C that would otherwise be released into the atmosphere (Bai and Cotrufo, 2022; Moinet et al., 2023). Fertilization, one of the most common forest management practices, has the potential to substantially influence SOC dynamics. It affects plant growth, which in turn alters the quantity and quality of organic matter inputs to the soil. Additionally, fertilization can impact the rate of organic matter decomposition and influence microbial community composition and activity, all of which are key factors in SOC accumulation and stabilization. Despite its significance, the relationship between fertilization and SOC in forest ecosystems remains inadequately understood. This knowledge gap hinders our ability to develop fertilization strategies that optimize SOC sequestration, which is essential for enhancing ecosystem sustainability and contributing to the global C balance.

Numerous studies have investigated the responses of SOC to fertilization, yet the results remain inconclusive due to variations in fertilizer types (Xu et al., 2021; Liu et al., 2023). Previous research has examined SOC responses to fertilization using inorganic nitrogen (N) fertilizer (NH₄NO₃, often used to simulate atmospheric N deposition) (Zhang et al., 2015), organic N fertilizer (urea) (Nave et al., 2022), and compound N fertilizers (including manure, bamboo special fertilizer, composted rapeseed cake, and other fertilizers containing two or more nutrients in N, phosphorus (P), and potassium (K)) (Hammad et al., 2020; Marshall et al., 2023). Findings suggest that inorganic N fertilizer application can enhance SOC by inhibiting microbial activity and increasing C input, leading to C accumulation and sequestration (Liu and Greaver, 2010; Lu et al., 2014; Lu et al., 2021). However, recent studies have reported that inorganic N fertilizer addition may decrease SOC by altering mycorrhizal action modes and affecting plant–soil C allocation (Tian et al., 2019; Yang et al., 2023). Conversely, the application of organic and compound N fertilizers is generally believed to increase SOC stocks due to the addition of external organic matter inputs (Li et al., 2014). Furthermore, P from compound N fertilizers can enhance SOC by promoting plant and microbial C inputs (Feng et al., 2023). Fertilization methods also influence SOC response to fertilization. While moderate fertilization can increase SOC through enhanced plant growth and organic matter inputs, excessive and long-term fertilization may accelerate organic matter decomposition, disrupt microbial communities, and degrade soil structure, potentially resulting in a net loss of SOC (Liu et al., 2011; Li et al., 2018). Additionally, the effects of fertilization on SOC vary throughout the soil profile. Fertilization significantly increases SOC storage in topsoil but decreases SOC in subsoil over the long-term (Hu et al., 2024). These mixed results indicate that the impact of fertilization on forest SOC can vary significantly across different experimental settings. Our understanding of how fertilization affects SOC across various fertilizer types, levels, durations, and soil depths remains limited, constraining the ability to make large-scale extrapolations.

Approximately 94% of plant species form associations with mycorrhizal fungi, which significantly influence forest C cycling by affecting plant nutrient uptake, litter quality, and microbial community (van der Heijden et al., 2015; Lin et al., 2016; Frey, 2019; Bennett and Groten, 2022). Among these fungi, arbuscular mycorrhizal (AM) fungi are the most prevalent, establishing symbiotic relationships with over 80% of terrestrial plant species and playing a crucial role in global C cycling (Chagnon et al., 2013; Han et al., 2020). More than 20% of plant photosynthetic C is allocated to AM fungi in exchange for nutrients, some of which accumulate as SOC (Parniske, 2008; Horsch et al., 2023). Furthermore, the hypha and exudates of AM fungi can protect soil organic matter (SOM) from decomposition by promoting soil aggregate formation and stability (Zhang et al., 2015). However, in certain instances, AM fungi can also contribute to SOC loss. The C from plant photosynthesis allocated to AM fungi can enhance microbial decomposition through priming effects (Jeewani et al., 2021). The impact of AM fungi on SOC exhibits considerable variation, and fertilization further complicates this relationship, primarily due to altered nutrient availability. Fertilization provides plants with essential nutrients and may reduce the C plants use to exchange nutrients with AM fungi, potentially leading to a reduction in newly fixed SOC (Wilson et al., 2009). However, increased soil nutrients can decrease SOM decomposition and induce SOC accumulation as it becomes less necessary to stimulate microbial decomposition for nutrient absorption (Craine et al., 2007). Fertilization can also increase N availability, reducing AM fungi colonization and activity, which may weaken the fungi’s protection of soil aggregates and lead to SOC loss (Treseder, 2004; Chen et al., 2019). Conversely, imbalanced fertilization can induce greater P limitation in plants, stimulating AM fungi colonization (Ferrol et al., 2019). The overall impact of fertilization on SOC storage in AM-dominated forests remains largely unknown, necessitating further investigation as a high priority.

Bamboo forests represent a crucial forest type in subtropical and tropical regions worldwide. They cover an area of 3.70 × 10⁸ ha globally (Lobovikov et al., 2007) and are expanding rapidly, even as global forest areas decline (Zhou et al., 2011). In China, the Phyllostachys genus stands out as the most significant among bamboo genera, comprising over 50 species. Phyllostachys edulis alone accounts for approximately 63% of the bamboo forest area and generates about 5 billion US dollars in production value (Li et al., 2015; Li et al., 2017). Physiologically, Phyllostachys bamboo exhibits an exceptionally rapid growth rate, typically completing its diameter and height growth within 45−60 days (Li et al., 2017). Consequently, Phyllostachys bamboo can swiftly accumulate photosynthetic C in a short period and sequester substantial amounts of SOC (Jiang et al., 2011). Furthermore, bamboo forests are predominantly colonized by AM fungi (Qin et al., 2017). Fertilization in Phyllostachys bamboo forests may lead to more complex changes in SOC due to the combined effects of AM fungi (Averill et al., 2014).

This study employs a meta-analysis to investigate the effects of fertilization on SOC in Phyllostachys bamboo forests, utilizing data from 631 observations derived from 28 field studies. Specifically, this research aims to address two key questions. (i) How does fertilization impact SOC in Phyllostachys bamboo forests? (ii) Do the effects of fertilization vary with different fertilizer types, fertilization levels, fertilization duration, and sampling soil depths? Based on previous research findings, we hypothesize that (i) fertilization will increase SOC; and (ii) different fertilization levels and sampling soil depths will have distinct impacts on SOC.

2 Materials and methods

2.1 Data selection

This study conducted a comprehensive literature review of peer-reviewed journal articles examining the response of SOC to fertilization in bamboo forests. The search utilized the Web of Science and China Knowledge Resource Integrated Database (CNKI) for papers published in Chinese, covering the period from 1998 to 2023. The literature search, performed between April and June 2023, employed specific search terms: (bamboo OR Moso bamboo OR Phyllostachys OR Phyllostachys edulis OR Phyllostachys glauca OR Phyllostachys prominens OR Phyllostachys heteroclada OR Phyllostachys praecox) AND (nitrogen addition OR deposition OR fertilize OR application) AND (soil organic carbon OR dissolved organic carbon OR microbial biomass carbon OR microbial respiration OR soil respiration OR PhytOC OR carbon content OR litter input OR fine roots input OR carbon content of organic layer OR carbon content in mineral soil layer). To assess the effect of fertilization on SOC, the selection criteria for inclusion in the study were as follows: 1) field-based fertilization experiments conducted in terrestrial ecosystems; 2) clear documentation of fertilizer types, fertilization level (calculated based on N addition level), fertilization duration, and sampling depth; 3) reported SOC values for both fertilized and control plots; and 4) identical initial climatic, soil, and habitat conditions for fertilized and control plots to minimize confounding factors. In cases where multiple measurements were available for the same experiment, the most recent sampling data were selected. The literature review yielded 631 observations derived from 28 published studies (Supplementary Materials, Fig. S1and Fig. S2).

This study primarily examined changes in SOC in response to fertilization. Additionally, we gathered supplementary data from publications, encompassing experimental locations (latitude and longitude), climatic characteristics (mean annual temperature (MAT) and mean annual precipitation (MAP)), experimental variables (fertilizer type, fertilization level (kg N•ha⁻¹•yr⁻¹; calculated based on N content), fertilization duration (yr), and soil depth (cm; the middle value of the sampling depth interval)), soil properties (soil pH, total nitrogen (TN), nitrate nitrogen (NO₃⁻-N), ammonium nitrogen (NH₄⁺-N), total phosphorus (TP), available phosphorus (AP), available potassium (AK), microbial biomass carbon (MBC), microbial biomass nitrogen (MBN), the ratio of MBC and MBN (MBC/MBN), soil respiration (Rs), and autotrophic respiration (Ra)) and enzyme activity (C-related enzyme activity (consisting of β-fructofuranosidase and cellulase), N-related enzyme activity (comprising nitrate reductase, nitrite reductase, and urease) and P-related enzyme activity (acid phosphatase)). Notably, the experimental pH data indicated that bamboo forest soils were acidic, with pre-fertilization pH ranging from 3.70 to 5.68, and post-fertilization pH from 3.20 to 5.64. For publications lacking experimental locations and climate characteristics, we obtained location information (i.e., longitude and latitude) from studies conducted at the same site. MAT and MAP data were sourced from the WorldClim 2.1 database (available at worldclim.org website). We extracted means (\stackrel{-}{\mathrm{X}}), standard deviations (SD), and sample sizes (n) from reported experiments or calculated from the context and tables presented in the papers. When necessary, we utilized WebPlotDigitizer (available at automeris.io website) to extract data from graphs. In cases where the standard error (SE) was presented, we calculated SD using the formula: \mathrm{S}\mathrm{D}=\mathrm{S}\mathrm{E}\times \mathrm{s}\mathrm{q}\mathrm{r}\mathrm{t}(\mathrm{n}). For studies not reporting SD or SE, we employed the “Bracken 1992” approach to impute it using the coefficient of variation from all complete cases (Bracken, 1992).

2.2 Data analysis

The logarithmic response ratio (lnRR) was calculated as the measure of effect size (Yang et al., 2023; Zhu et al., 2023):

(1)\mathrm{l}\mathrm{n}\mathrm{R}\mathrm{R}=\mathrm{l}\mathrm{n}\frac{X_{\mathrm{t}}}{X_{\mathrm{c}}}=\mathrm{l}\mathrm{n}\left(X_{\mathrm{t}}\right)-\mathrm{l}\mathrm{n}(X_{\mathrm{c}}),

where X_t represents the mean value of the treatment group and X_c denotes the mean value of the control group.

The variance (v_i) of RR was estimated as

(2)v_{\mathrm{i}}=\frac{S_{\mathrm{t}}^2}{{N_{\mathrm{t}}X}_{\mathrm{t}}^2}+\frac{S_{\mathrm{c}}^2}{{N_{\mathrm{c}}X}_{\mathrm{c}}^2},

where N_t and N_c represent the sample sizes of the treatment and control groups, respectively; and S_t and S_c denote the standard deviations for the treatment and control groups, respectively. When X_t = 0, and consequently SD_t = 0, a continuity correction factor (k = 0.5) was applied to the mean and SD of the treatment groups to prevent calculation errors caused by zero values (Cox and Snell, 2008). An identical process was utilized for the control groups. Multilevel mixed effects meta-analyses were conducted using the metafor package (rma.mv function) in R (4.2.2) to compute the mean effect sizes and 95% bootstrap confidence intervals (CI). The results were presented as lnRR and as fertilization-induced changes in response variables, calculated using the following formula: (exp (lnRR)－1) × 100. The effect size was deemed significant if the 95% CI did not overlap zero.

Using a multilevel random-effects model, we evaluated the SOC responses to fertilization. Single mixed-effects meta-regression models were employed to examine the relationship between variations in lnRR and several categorical moderators (fertilizer types, fertilization level, fertilization duration, and soil depth). Fertilizer types were classified as inorganic (NH₄NO₃), organic (urea), and compound N fertilizers. Fertilization levels were categorized as < 50, 50−150, and > 150 kg N•ha⁻¹•yr⁻¹, based on the previous meta-analysis (Liu and Greaver, 2010). Fertilization duration was divided into < 5 and ≥ 5 years to discuss short- and long-term effects (Lu et al., 2021). Soil depths were partitioned into 0−20 cm and > 20 cm. Inter-group and intra-group difference analyses were conducted to examine variations within different variable groups and between subgroups of the same variable group, respectively. Heterogeneity among effect sizes of the moderators was evaluated using subgroup analysis based on omnibus tests (Q_m). The mean effect size was considered different among categorical factors with a significant Q_m value. The p-values were adjusted for multiple hypothesis testing using Bonferroni corrections. A correlation analysis was performed to examine the relationships between fertilization-induced changes in SOC and climate factors, as well as changes in soil properties and enzyme activity. Due to the limited number of studies, only a simple correlation analysis was conducted.

2.3 Effect of publication bias

Publication bias was assessed using funnel plots (Nakagawa et al., 2021) and Egger’s test (Macaskill et al., 2001). The Egger’s test indicated that the overall relative risk (RR) for SOC (Z = −0.24, p = 0.81) was robust (Supplementary Materials, Fig. S3). Consequently, we conclude that our analysis was not affected by publication bias.

3 Results

3.1 Effects of fertilization on soil properties and enzyme activity

In bamboo forests, fertilization significantly increased soil TN, NO₃^－-N, NH₄⁺-N, TP, AP, AK, MBC, MBN, and MBC/MBN (by 5.78%, 57.43%, 25.55%, 9.97%, 35.95%, 10.20%, 29.91%, 46.11%, and 29.45%, respectively, mean lnRR = 0.06, 0.45, 0.23, 0.10, 0.31, 0.10, 0.25, 0.38, and 0.26, respectively (all p < 0.05, Fig.1). Fertilization also decreased soil pH by 4.62% (mean lnRR: −0.05, p < 0.001). However, fertilization had non-significant impacts on Rs and Ra (all p < 0.05, Fig.1). Additionally, fertilization decreased C- and P-related enzyme activities by 10.47% and 5.23%, respectively (mean lnRR: −0.11 and −0.05, all p < 0.05, Fig.1), while showing non-significant impacts on N-related enzyme activity.

3.2 Effects of fertilization on SOC and the regulating factors

Fertilization resulted in a significant overall decrease of 4.46% in SOC (p < 0.05, Fig.2) in bamboo forests. The SOC responses to fertilization did not vary significantly among fertilizer types and fertilization levels (all p > 0.05, Tab.1, Fig.2). Inorganic N fertilizers negatively affected SOC (p < 0.05), while organic and compound N fertilizers showed no significant impact (all p > 0.05). Regarding fertilization levels, SOC was negatively affected at levels < 50 kg N·ha⁻¹·yr⁻¹ (p < 0.05) but not at levels ≥ 50 kg N·ha⁻¹·yr⁻¹ (all p > 0.05). The duration of fertilization and soil depth significantly influenced SOC responses to fertilization (all p < 0.05, Tab.1). Fertilization decreased SOC when applied for ≥ 5 years or at soil depths > 20 cm (p < 0.01, Fig.2). However, fertilization had no significant impact on SOC when applied for < 5 years or at soil depths of 0−20 cm (all p > 0.05, Fig.2). The response ratios of SOC were positively correlated with MAP, soil pH, MBC, NH₄⁺-N, and AK (all p < 0.01, Tab.2, Fig.3).

4 Discussion

4.1 Overall effects of fertilization on SOC

In contrast to numerous previous studies (e.g., Rocci et al., 2021; Rambaut et al., 2022; Tang et al., 2023), our findings indicate that fertilization significantly reduced SOC. This decrease may be closely associated with roots and root-associated fungi, which contribute approximately 50% to 70% of the stored C in forest soils, particularly in newly forming SOC (Clemmensen et al., 2013; Berhongaray et al., 2018). A long-term field study has demonstrated that root-derived SOC is approximately 2.3 times higher than SOC from above-ground litter, emphasizing the crucial role of roots in SOC accumulation (Kätterer et al., 2011). According to optimal partitioning theory, plants decrease C allocation to below-ground nutrient acquisition under fertilization, resulting in increased above-ground biomass allocation and reduced root biomass allocation (Albaugh et al., 1998). Consequently, less root C allocation leads to decreased organic matter deposition into the soil, causing a reduction in SOC. This effect may be more pronounced in bamboo forests due to their unique characteristics and functions in C sequestration and cycling (Lobovikov et al., 2011). For instance, bamboo exhibits a significantly higher growth rate compared to other forest species, and its rhizome system connects culms underground, facilitating nutrient and carbonate transport from mature to young culms (Ouyang et al., 2022). Fertilization can further increase soil nutrient concentration and enhance bamboo’s nutrient uptake efficiency (Zuo et al., 2024). As a result, under fertilization conditions, newly grown bamboo culms can store more C within the culms, potentially reducing below-ground C input for nutrient absorption (Li et al., 1998; Komatsu et al., 2012).

Furthermore, the decrease in SOC may be closely linked to AM fungi-mediated changes in SOC in bamboo forests under fertilization. These findings are consistent with previous research documenting fertilization-induced SOC loss in cropland and grassland ecosystems, where AM fungi predominantly dominate (Luo et al., 2019; Shi et al., 2023). Unlike other woody plant forests, herbaceous bamboo forests are also predominantly dominated by AM fungi (Genre et al., 2020). Fertilization often inhibits root biomass and reduces the extent of root colonization by AM fungi when N is no longer the limiting nutrient (Ericsson, 1995; Hawkins and George, 2002). This reduction in AM fungi colonization diminishes the contribution of both living and dead fungal biomass to SOC (Basiru and Hijri, 2024). Moreover, a decrease in living hyphae weakens the physical and chemical protection of SOM, exposing it to air and decomposers, which accelerates its decomposition (Rillig et al., 2001; Zhang et al., 2015; Lehmann et al., 2020). The Mycorrhizal-Associated Nutrient Economy (MANE) framework posits that AM fungi contribute to a fast-decomposing forest economy (Phillips et al., 2013). This occurs because AM trees co-evolve with AM fungi (Brundrett and Tedersoo, 2018), resulting in the production of high-quality litter that is rich in N and base cations and has low lignin: N ratio (Smith, 1976; Cornelissen et al., 2001; Staddon et al., 2003). High N concentration increases N availability, promoting microbial C utilization and, consequently, higher decomposition rates (Melillo et al., 1982). Consequently, plant-derived C and nutrients are rapidly converted from organic to inorganic forms by bacteria and fungi, leading to SOC loss. Additionally, fertilization can accelerate litter decomposition in AM fungi-dominated forests by increasing N availability (Midgley et al., 2015). This process reduces N limitations on C-degrading enzymes and decreases C use efficiency (Carreiro et al., 2000; Manzoni et al., 2012; Zhang et al., 2022).

4.2 Different responses of SOC to fertilizer types

This investigation demonstrated that various fertilizer types exert distinct influences on SOC. Notably, inorganic N fertilizers led to a decrease in SOC, whereas organic and compound N fertilizers showed no significant effect. These contrasting outcomes can be attributed to the intricate interactions among soil environment, plants, and microorganisms under different fertilization regimes. Various fertilizers introduce distinct materials and elements into the soil, affecting soil C dynamics in unique ways. For example, the external C input provided by organic and compound N fertilizers can counterbalance SOC loss by supporting SOC formation and maintenance—a benefit not afforded by inorganic N fertilizer alone (Shi et al., 2024). Labile C inputs from these fertilizers mitigate SOC loss by supplying readily available C resources for plant and microbial growth, thereby minimizing the priming effect that accelerates SOM decomposition (Yu et al., 2012; Wang et al., 2017; Wu et al., 2023).

Fertilizer types significantly influence soil properties, particularly the soil C: N ratio, which plays a crucial role in regulating SOM decomposition (Enríquez et al., 1993; Schädel et al., 2013). N is essential for microbial growth and activity, and high N availability from fertilization can accelerate SOM breakdown (Xu et al., 2016). However, the exogenous C from organic and some compound N fertilizers can substantially increase the soil C: N ratio, potentially slowing SOM decay. Conversely, the application of single inorganic N fertilizers may lead to severe nutrient imbalances, exacerbating SOC loss. P, for instance, is a critical element in soil biochemical reactions, but the unbalanced input of N and P from inorganic N fertilizers can intensify P limitation (Deng et al., 2017). To address this limitation, plants and microorganisms may increase SOM decomposition to acquire P, resulting in the release of substantial amounts of C from mineral-organic complexes (Fang et al., 2019; Wen et al., 2021). This process, combined with the release of extracellular enzymes and other small-molecule organic matter, can stimulate the priming effect, leading to further SOC losses (Keiluweit et al., 2015). In contrast, compound N fertilizers provide additional essential elements such as potassium (K), sulfur (S), and calcium (Ca), which are important for SOM formation and SOC sequestration (Feng et al., 2005; Rowley et al., 2017).

Moreover, the cumulative nitrogen input from inorganic N fertilization can induce soil acidification (Haworth et al., 2007; Bowman et al., 2008; Tian and Niu, 2015), with bamboo forests being particularly susceptible to long-term acidification (Terefe et al., 2020; Zhang et al., 2020). This process results in the leaching and depletion of base cations (e.g., Ca²⁺, Al³⁺, and Fe³⁺), potentially increasing the mobilization and release of free Al³⁺ into the soil solution (Yu et al., 2020). Such changes may adversely affect plant and microbial growth, subsequently reducing both above-ground and below-ground C inputs (Johnson et al., 2018; Shi et al., 2021). In contrast, organic and compound N fertilizers help maintain base cation levels and buffer against soil acidification, mitigating its negative effects in bamboo forests (Zhang et al., 2017; Shi et al., 2019). Consequently, these fertilizers prove more effective in preserving SOC content. Our findings demonstrate that fertilization generally decreases SOC stocks in bamboo forests, with significant variations depending on the fertilizer type employed. These results emphasize the importance of organic and compound N fertilizers in maintaining SOC levels, offering valuable insights for guiding sustainable production practices in bamboo forestry.

4.3 Fertilization effects varied with fertilization level, duration, and soil depth

The results indicate that SOC tends to decrease when N fertilization levels are below 50 kg·ha⁻¹·yr⁻¹, while higher N fertilization levels show no significant effect. This discrepancy may be attributed to the varying impacts of N inputs on bamboo forest ecosystems. Low N fertilization levels may enhance SOM decomposition through several mechanisms. First, low N levels (< 50 kg N·ha⁻¹·yr⁻¹) may accelerate microbial growth and activity, promoting SOC decomposition (Zhou et al., 2017). Secondly, N fertilization alters soil N concentration and C: N ratio (Eastman et al., 2021), with lower C: N ratios potentially enhancing litter decomposition. Thirdly, insufficient N from low-level fertilization may not meet the demands of plants and AM fungi, potentially stimulating AM fungi to enhance organic material decomposition to acquire N (Hodge et al., 2001; Wu et al., 2024), as AM fungi have a higher N requirement due to their greater N concentration compared to plants (Hodge and Fitter, 2010). Conversely, higher N fertilization levels typically inhibit SOM decomposition by impairing microbial and AM fungi activity (Riggs and Hobbie, 2016; Wang et al., 2018). Excessive N input can lead to soil acidification, inhibiting microbial activity (Liu et al., 2023). Soil acidification also causes adverse effects, such as heavy metal toxicity and reduced soil buffering capacity, further hindering microbial decomposition of SOM (Holland et al., 2018; Desie et al., 2019; Anza et al., 2021). Moreover, microorganisms require a balanced C: N ratio for optimal growth, and high N fertilization can disrupt this balance, affecting their ability to decompose SOM (Yuan et al., 2019).

Our findings indicate that long-term fertilization significantly decreased SOC. This reduction may be attributed to the cumulative effects of prolonged fertilization on soil physicochemical properties, microbial communities, and mycorrhizal symbiosis. Initially, during short-term fertilization, plants rapidly absorb most of the N to support growth. However, long-term fertilization results in substantial N accumulation in the soil (Silver et al., 2005), elevating soil N concentration and lowering the C: N ratio, potentially enhancing microbial activity and accelerating SOM decomposition (Chen et al., 2021). Furthermore, prolonged fertilization can lead to continuous soil acidification, inhibiting plant growth and reducing litter input (Shi et al., 2021). Additionally, the negative impact of fertilization on microbes and AM fungi intensifies over time, accelerating the decomposition of labile C by increasing specific microbial populations and the abundance of C-utilization genes in the soil (Bragazza et al., 2006; Zhang et al., 2018). Lastly, long-term fertilization can disrupt plant-mycorrhizal symbiosis, diminishing the physical protection of SOC provided by AM fungi networks associated with host plant roots (Huang et al., 2022).

Our findings indicate that fertilization decreased SOC storage in the subsoil while having no significant impact on SOC in the topsoil. The reduction in subsoil SOC may be attributed to decreased root biomass resulting from upward C allocation and a decline in root-associated AM fungi, which play a protective role in preventing SOC decomposition. Conversely, the absence of significant changes in topsoil SOC can be explained by several factors. First, increased above-ground biomass leads to higher input of fast-decomposing litter, potentially offsetting SOC losses caused by reduced root growth (Quartucci et al., 2023). Secondly, roots and AM fungi remaining in the topsoil continue to offer effective protection for SOC, preventing its depletion (Huang et al., 2021). Thirdly, direct exposure to fertilizers can cause significant soil acidification in the topsoil, inhibiting microbial activity and slowing SOM decomposition (Zhang et al., 2018). In practice, optimizing fertilization levels and controlling application duration are crucial for maintaining SOC storage. Furthermore, fertilization plans should be tailored to specific forest types to ensure sustainable management.

4.4 Factors regulating SOC response to fertilization

The study identified MAP, soil pH, MBC, AK, and NH₄⁺-N as dominant regulators of SOC dynamics under fertilization, influencing C input and SOC stability. A favorable environment significantly enhances plant and microbial growth. Bamboo, characterized by high water requirements throughout its growth cycle (Li et al., 2019), benefits from increased precipitation, resulting in higher litter input and subsequent SOC increase (Eclesia et al., 2012; Song et al., 2016; Luo et al., 2017). Adequate soil moisture also promotes microbial growth, leading to higher MBC content, which, as an active fraction of SOM, plays a crucial role in SOC formation (Zhang et al., 2021; Su et al., 2023; Anthony et al., 2024). While fertilization typically decreases soil pH, causing direct toxicity and growth inhibition in plants and microorganisms (Yadav et al., 2020), increasing soil pH mitigates these negative effects (Zong et al., 2023). Additionally, the study observed positive correlations between changes in AK and NH₄⁺-N and changes in SOC, as these nutrients are essential for plant growth and can directly enhance biomass production (Li et al., 2024).

Environmental factors significantly influence SOC stability by affecting root-mycorrhizal symbiosis. As precipitation increases, bamboo tends to expand, extending its rhizomes throughout the forest (Shi et al., 2020). This expansion enhances mycorrhizal symbiosis, promoting soil aggregate formation and SOC sequestration (Basiru and Hijri, 2024; Lin et al., 2024). Precipitation and soil pH act synergistically to facilitate SOC accumulation, as elevated soil moisture and increased pH levels enhance the content of Fe oxides, which improve soil aggregate stability (Shen et al., 2024). Our meta-analysis also revealed a positive correlation between changes in MBC and SOC, aligning with previous findings. Higher MBC often corresponds with increased AM fungi biomass, contributing to soil structure formation and the stabilization of soil aggregates (Grandy and Neff, 2008; Liang et al., 2010; Xu et al., 2011).

In summary, contrary to numerous previous meta-analysis findings, our meta-analysis revealed that inorganic N fertilization significantly reduces SOC in AM-dominated bamboo forests. This unexpected result carries significant implications for fertilization practices and the global C balance. Based on these findings, we recommend the utilization of organic and compound N fertilizers as more appropriate forest management strategies for maintaining SOC storage and promoting sustainable forest ecosystems. The observed SOC decrease also highlights a gap in current estimates of fertilization-induced C sequestration, which often overlooks SOC changes in bamboo forests and underestimates the role of mycorrhizal symbiosis in SOC dynamics. Future research should therefore focus on the role of AM fungi in regulating the relationship between bamboo and soil carbon, as well as investigating broader plant–soil interactions in subtropical forests, with further data needed to support our perspective.

References

[1] Albaugh T J, Allen H L, Doughert P M, Kress L W, King J S (1998). Leaf area and above- and belowground growth responses of loblolly pine to nutrient and water additions.For Sci, 44(2): 317–328

[2] Anthony M A, Tedersoo L, De Vos B, Croisé L, Meesenburg H, Wagner M, Andreae H, Jacob F, Lech P, Kowalska A, Greve M, Popova G, Frey B, Gessler A, Schaub M, Ferretti M, Waldner P, Calatayud V, Canullo R, Papitto G, Marinšek A, Ingerslev M, Vesterdal L, Rautio P, Meissner H, Timmermann V, Dettwiler M, Eickenscheidt N, Schmitz A, Van Tiel N, Crowther T W, Averill C (2024). Fungal community composition predicts forest carbon storage at a continental scale.Nat Commun, 15(1): 2385

[3] Anza M, Garbisu C, Salazar O, Epelde L, Alkorta I, Martínez-Santos M (2021). Acidification alters the functionality of metal polluted soils.Appl Soil Ecol, 163: 103920

[4] Averill C, Turner B L, Finzi A C (2014). Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage.Nature, 505(7484): 543–545

[5] Bai Y F, Cotrufo M F (2022). Grassland soil carbon sequestration: current understanding, challenges, and solutions.Science, 377(6606): 603–608

[6] Basiru S, Hijri M (2024). Trade-off between soil organic carbon sequestration and plant nutrient uptake in arbuscular mycorrhizal symbiosis.Fungal Biol Rev, 49: 100381

[7] Bennett A E, Groten K (2022). The costs and benefits of plant-arbuscular mycorrhizal fungal interactions.Annu Rev Plant Biol, 73(1): 649–672

[8] Berhongaray G, Cotrufo F M, Janssens I A, Ceulemans R (2018). Below-ground carbon inputs contribute more than above-ground inputs to soil carbon accrual in a bioenergy poplar plantation.Plant Soil, 434(1−2): 363–378

[9] Bowman W D, Cleveland C C, Halada Ĺ, Hreško J, Baron J S (2008). Negative impact of nitrogen deposition on soil buffering capacity.Nat Geosci, 1(11): 767–770

[10] Bracken M B (1992). Effective care of the newborn infant.Arch Dis Child, 67: 1415

[11] Bragazza L, Freeman C, Jones T, Rydin H, Limpens J, Fenner N, Ellis T, Gerdol R, Ha’jek M, Ha’jek T, Iacumin P, Kutnar L, Tahvanainen T, Toberman H (2006). Atmospheric nitrogen deposition promotes carbon loss from peat bogs.Proc Natl Acad Sci USA, 103(51): 19386–19389

[12] Brundrett M C, Tedersoo L (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity.New Phytol, 220(4): 1108–1115

[13] Carreiro M M, Sinsabaugh R L, Repert D A, Parkhurst D F (2000). Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition.Ecology, 81(9): 2359–2365

[14] Chagnon P L, Bradley R L, Maherali H, Klironomos J N (2013). A trait-based framework to understand life history of mycorrhizal fungi.Trends Plant Sci, 18(9): 484–491

[15] Chen Q Y, Hu Y L, Niu B, Yang X Q, Jiao H Z, Ri X, Song L L, Zhang G X (2021). Shifts in the dynamic mechanisms of soil organic matter transformation with nitrogen addition: from a soil carbon/nitrogen-driven mechanism to a microbe-driven mechanism.Soil Biol Biochem, 150: 108355

[16] Chen Z J, Zhou X Y, Geng S C, Miao Y, Cao Y H, Chen Z, Zhang J H, Han S J (2019). Interactive effect of nitrogen addition and throughfall reduction decreases soil aggregate stability through reducing biological binding agents.For Ecol Manage, 445: 13–19

[17] Clemmensen K E, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay R D, Wardle D A, Lindahl B D (2013). Roots and associated fungi drive long-term carbon sequestration in boreal forest.Science, 339(6127): 1615–1618

[18] Cornelissen J, Aerts R, Cerabolini B, Werger M, van der Heijden M (2001). Carbon cycling traits of plant species are linked with mycorrhizal strategy.Oecologia, 129(4): 611–619

[19] Cox D R, Snell E J (2008). Analysis of binary data. The Concise Encyclopedia of Statistics. New York: Springer New York, 4–5

[20] Craine J M, Morrow C, Fierer N (2007). Microbial nitrogen limitation increases decomposition.Ecology, 88(8): 2105–2113

[21] Deng Q, Hui D F, Dennis S, Reddy K C (2017). Responses of terrestrial ecosystem phosphorus cycling to nitrogen addition: a meta-analysis.Glob Ecol Biogeogr, 26(6): 713–728

[22] Desie E, Vancampenhout K, Heyens K, Hlava J, Verheyen K, Muys B (2019). Forest conversion to conifers induces a regime shift in soil process domain affecting carbon stability.Soil Biol Biochem, 136: 107540

[23] Eastman B A, Adams M B, Brzostek E R, Burnham M B, Carrara J E, Kelly C, McNeil B E, Walter C A, Peterjohn W T (2021). Altered plant carbon partitioning enhanced forest ecosystem carbon storage after 25 years of nitrogen additions.New Phytol, 230(4): 1435–1448

[24] Eclesia R P, Jobbagy E G, Jackson R B, Biganzoli F, Piñeiro G (2012). Shifts in soil organic carbon for plantation and pasture establishment in native forests and grasslands of South America.Glob Change Biol, 18(10): 3237–3251

[25] Enríquez S, Duarte C M, Sand-Jensen K (1993). Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C: N: P content.Oecologia, 94: 457–471

[26] Ericsson T (1995). Growth and shoot: root ratio of seedlings in relation to nutrient availability.Plant Soil, 168: 205–214

[27] Fang X M, Zhang X L, Chen F S, Zong Y Y, Bu W S, Wan S Z, Luo Y Q, Wang H M (2019). Phosphorus addition alters the response of soil organic carbon decomposition to nitrogen deposition in a subtropical forest.Soil Biol Biochem, 133: 119–128

[28] Feng J G, Song Y J, Zhu B (2023). Ecosystem-dependent responses of soil carbon storage to phosphorus enrichment.New Phytol, 238(6): 2363–2374

[29] Feng X J, Simpson A J, Simpson M J (2005). Chemical and mineralogical controls on humic acid sorption to clay mineral surfaces.Org Geochem, 36(11): 1553–1566

[30] Ferrol N, Azcón-Aguilar C, Pérez-Tienda J (2019). Review: arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: an overview on the mechanisms involved.Plant Sci, 280: 441–447

[31] Frey S D (2019). Mycorrhizal fungi as mediators of soil organic matter dynamics.Annu Rev Ecol Evol Syst, 50(1): 237–259

[32] Genre A, Lanfranco L, Perotto S, Bonfante P (2020). Unique and common traits in mycorrhizal symbioses.Nat Rev Microbiol, 18(11): 649–660

[33] Grandy A S, Neff J C (2008). Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function.Sci Total Environ, 404(2−3): 297–307

[34] Hammad H M, Fasihuddin Nauman H M, Abbas F, Ahmad A, Bakhat H F, Saeed S, Shah G M, Ahmad A, Cerdà A (2020). Carbon sequestration potential and soil characteristics of various land use systems in arid region.J Environ Manage, 264: 110254

[35] Han Y F, Feng J G, Han M G, Zhu B (2020). Responses of arbuscular mycorrhizal fungi to nitrogen addition: a meta-analysis.Glob Change Biol, 26(12): 7229–7241

[36] Hawkins H J, George E (2002). Effect of plant nitrogen status on the contribution of arbuscular mycorrhizal hyphae to plant nitrogen uptake.Physiol Plant, 105(4): 694–700

[37] Haworth B J, Ashmore M R, Headley A D (2007). Effects of nitrogen deposition on bryophyte species composition of calcareous grasslands.Water Air Soil Pollut Focus, 7(1−3): 111–117

[38] Hodge A, Campbell C D, Fitter A H (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material.Nature, 413(6853): 297–299

[39] Hodge A, Fitter A H (2010). Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling.Proc Natl Acad Sci USA, 107(31): 13754–13759

[40] Holland J E, Bennett A E, Newton A C, White P J, McKenzie B M, George T S, Pakeman R J, Bailey J S, Fornara D A, Hayes R C (2018). Liming impacts on soils, crops and biodiversity in the UK: a review. Sci Total Environ, 610–611: 316–332

[41] Horsch C C A, Antunes P M, Fahey C, Grandy A S, Kallenbach C M (2023). Trait-based assembly of arbuscular mycorrhizal fungal communities determines soil carbon formation and retention.New Phytol, 239(1): 311–324

[42] Hu Y L, Deng Q, Kätterer T, Olesen J E, Ying S C, Ochoa-Hueso R, Mueller C W, Weintraub M N, Chen J (2024). Depth-dependent responses of soil organic carbon under nitrogen deposition.Global Change Biol, 30(3): e17247

[43] Huang B B, Yan G Y, Liu G C, Sun X Y, Wang X C, Xing Y J, Wang Q G (2022). Effects of long-term nitrogen addition and precipitation reduction on glomalin-related soil protein and soil aggregate stability in a temperate forest.Catena, 214: 106284

[44] Huang J S, Liu W X, Yang S, Yang L, Peng Z Y, Deng M F, Xu S, Zhang B B, Ahirwal J, Liu L L (2021). Plant carbon inputs through shoot, root, and mycorrhizal pathways affect soil organic carbon turnover differently.Soil Biol Biochem, 160: 108322

[45] Jeewani P H, Luo Y, Yu G H, Fu Y Y, He X H, Van Zwieten L, Liang C, Kumar A, He Y, Kuzyakov Y, Qin H, Guggenberger G, Xu J M (2021). Arbuscular mycorrhizal fungi and goethite promote carbon sequestration via hyphal-aggregate mineral interactions.Soil Biol Biochem, 162: 108417

[46] Jiang P K, Meng C F, Zhou G M, Xu Q F (2011). Comparative study of carbon storage in different forest stands in subtropical China.Bot Rev, 77(3): 242–251

[47] Johnson J, Graf Pannatier E, Carnicelli S, Cecchini G, Clarke N, Cools N, Hansen K, Meesenburg H, Nieminen T M, Pihl-Karlsson G, Titeux H, Vanguelova E, Verstraeten A, Vesterdal L, Waldner P, Jonard M (2018). The response of soil solution chemistry in European forests to decreasing acid deposition.Glob Change Biol, 24(8): 3603–3619

[48] Kätterer T, Bolinder M A, Andrén O, Kirchmann H, Menichetti L (2011). Roots contribute more to refractory soil organic matter than above-ground crop residues, as revealed by a long-term field experiment.Agric Ecosyst Environ, 141(1−2): 184–192

[49] Keiluweit M, Bougoure J J, Nico P S, Pett-Ridge J, Weber P K, Kleber M (2015). Mineral protection of soil carbon counteracted by root exudates.Nat Clim Chang, 5(6): 588–595

[50] Komatsu H, Onozawa Y, Kume T, Tsuruta K, Shinohara Y, Otsuki K (2012). Canopy conductance for a Moso bamboo (Phyllostachys pubescens) forest in western Japan.Agric Meteorol, 156: 111–120

[51] Lehmann J, Hansel C M, Kaiser C, Kleber M, Maher K, Manzoni S, Nunan N, Reichstein M, Schimel J P, Torn M S, Wieder W R, Kögel-Knabner I (2020). Persistence of soil organic carbon caused by functional complexity.Nat Geosci, 13(8): 529–534

[52] Li C, Shi Y J, Zhou G M, Zhou Y F, Xu L, Tong L, Liu X (2018). Effects of different management approaches on soil carbon dynamics in Moso bamboo forest ecosystems.Catena, 169: 59–68

[53] Li G J, Zhang L, Wu J L, Wang Z Y, Wang M, Kronzucker H J, Shi W M (2024). Plant iron status regulates ammonium-use efficiency through protein N-glycosylation.Plant Physiol, 195(2): 1712–1727

[54] Li L, Cheng Z C, Ma Y J, Bai Q S, Li X Y, Cao Z H, Wu Z N, Gao J (2017). The association of hormone signalling genes, transcription and changes in shoot anatomy during moso bamboo growth.Plant Biotechnol J, 16(1): 72–85

[55] Li P H, Zhou G M, Du H Q, Lu D S, Mo L F, Xu X J, Shi Y J, Zhou Y F (2015). Current and potential carbon stocks in Moso bamboo forests in China.J Environ Manage, 156: 89–96

[56] Li R, Werger M, During H J, Zhong Z C (1998). Carbon and nutrient dynamics in relation to growth rhythm in the giant bamboo Phyllostachys pubescens.Plant Soil, 201: 113–123

[57] Li X J, Mao F J, Du H Q, Zhou G M, Xing L Q, Liu T Y, Han N, Liu Y L, Zhu D E, Zheng J L, Dong L F, Zhang M (2019). Spatiotemporal evolution and impacts of climate change on bamboo distribution in China.J Environ Manage, 248: 109265

[58] Li Y F, Zhang J J, Chang S X, Jiang P K, Zhou G M, Shen Z M, Wu J S, Lin L, Wang Z S, Shen M C (2014). Converting native shrub forests to Chinese chestnut plantations and subsequent intensive management affected soil C and N pools.For Ecol Manage, 312: 161–169

[59] Liang B, Yang X Y, He X H, Zhou J B (2010). Effects of 17-year fertilization on soil microbial biomass C and N and soluble organic C and N in loessial soil during maize growth.Biol Fertil Soils, 47(2): 121–128

[60] Lin G G, McCormack M L, Ma C G, Guo D L (2016). Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests.New Phytol, 213(3): 1440–1451

[61] Lin Z X, Wang Q, Xu Y P, Luo S, Zhou C Y, Yu Z H, Xu C Y (2024). Soil moisture dynamics and associated rainfall-runoff processes under different land uses and land covers in a humid mountainous watershed.J Hydrol (Amst), 636: 131249

[62] Liu H Y, Huang N, Zhao C M, Li J H (2023). Responses of carbon cycling and soil organic carbon content to nitrogen addition in grasslands globally.Soil Biol Biochem, 186: 109164

[63] Liu J, Jiang P K, Wang H L, Zhou G M, Wu J S, Yang F, Qian X B (2011). Seasonal soil CO₂ efflux dynamics after land use change from a natural forest to Moso bamboo plantations in subtropical China.For Ecol Manage, 262(6): 1131–1137

[64] Liu L L, Greaver T L (2010). A global perspective on belowground carbon dynamics under nitrogen enrichment.Ecol Lett, 13(7): 819–828

[65] Lobovikov M, Paudel S, Piazza M, Ren H, Wu J Q (20072007. World Bamboo Resources. Rome: IBaR Organization

[66] Lobovikov M, Schoene D, Lou Y P (2011). Bamboo in climate change and rural livelihoods.Mitig Adapt Strategies Glob Change, 17(3): 261–276

[67] Lu X K, Mao Q G, Gilliam F S, Luo Y Q, Mo J M (2014). Nitrogen deposition contributes to soil acidification in tropical ecosystems.Glob Change Biol, 20(12): 3790–3801

[68] Lu X K, Vitousek P M, Mao Q G, Gilliam F S, Luo Y Q, Turner B L, Zhou G Y, Mo J M (2021). Nitrogen deposition accelerates soil carbon sequestration in tropical forests.Proc Natl Acad Sci USA, 118(16): e2020790118

[69] Luo R, Fan J, Wang W, Luo J, Kuzyakov Y, He J S, Chu H, Ding W (2019). Nitrogen and phosphorus enrichment accelerates soil organic carbon loss in alpine grassland on the Qinghai-Tibetan Plateau.Sci Total Environ, 650(1): 303–312

[70] Luo Z K, Feng W T, Luo Y Q, Baldock J, Wang E L (2017). Soil organic carbon dynamics jointly controlled by climate, carbon inputs, soil properties and soil carbon fractions.Glob Change Biol, 23(10): 4430–4439

[71] Macaskill P, Walter S D, Irwig L (2001). A comparison of methods to detect publication bias in meta-analysis.Stat Med, 20(4): 641–654

[72] Manzoni S, Taylor P, Richter A, Porporato A, Ågren G I (2012). Environmental and stoichiometric controls on microbial carbon-use efficiency in soils.New Phytol, 196(1): 79–91

[73] Marshall J D, Tarvainen L, Zhao P, Lim H, Wallin G, Näsholm T, Lundmark T, Linder S, Peichl M (2023). Components explain, but do eddy fluxes constrain? Carbon budget of a nitrogen-fertilized boreal Scots pine forest.New Phytol, 239(6): 2166–2179

[74] Melillo J M, Aber J D, Muratore J F (1982). Nitrogen and lignin control of hardwood leaf litter decomposition dynamics.Ecology, 63(3): 621–626

[75] Midgley M G, Brzostek E, Phillips R P (2015). Decay rates of leaf litters from arbuscular mycorrhizal trees are more sensitive to soil effects than litters from ectomycorrhizal trees.J Ecol, 103: 1454–1463

[76] Moinet G Y K, Hijbeek R, van Vuuren D P, Giller K E (2023). Carbon for soils, not soils for carbon.Glob Change Biol, 29(9): 2384–2398

[77] Nakagawa S, Lagisz M, Jennions M D, Koricheva J, Noble D W A, Parker T H, Sánchez-Tójar A, Yang Y F, O’Dea R E (2021). Methods for testing publication bias in ecological and evolutionary meta-analyses.Methods Ecol Evol, 13(1): 4–21

[78] Nave L E, DeLyser K, Domke G M, Holub S M, Janowiak M K, Kittler B, Ontl T A, Sprague E, Sucre E B, Walters B F, Swanston C W (2022). Disturbance and management effects on forest soil organic carbon stocks in the Pacific Northwest.Ecol Appl, 32(6): e2611

[79] Ouyang M, Yang C, Tian D, Pan J M, Chen G P, Su H J, Yan Z B, Ji C J, Tang Z Y, Fang J Y (2022). A field-based estimation of moso bamboo forest biomass in China.For Ecol Manage, 505: 119885

[80] Parniske M (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses.Nat Rev Microbiol, 6(10): 763–775

[81] Phillips R P, Brzostek E, Midgley M G (2013). The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests.New Phytol, 199(1): 41–51

[82] Qin H, Chen J H, Wu Q F, Niu L M, Li Y C, Liang C F, Shen Y, Xu Q F (2017). Intensive management decreases soil aggregation and changes the abundance and community compositions of arbuscular mycorrhizal fungi in Moso bamboo (Phyllostachys pubescens) forests.For Ecol Manage, 400: 246–255

[83] Quartucci F, Gocke M, Denich M, de Moraes Gonçalves J L, Amelung W (2023). Deep soil carbon loss offsets rapid aboveground carbon accumulation after reforestation.For Ecol Manage, 548: 121403

[84] Rambaut L A E, Vayssières J, Versini A, Salgado P, Lecomte P, Tillard E (2022). 15-year fertilization increased soil organic carbon stock even in systems reputed to be saturated like permanent grassland on andosols.Geoderma, 425: 116025

[85] Riggs C E, Hobbie S E (2016). Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils.Soil Biol Biochem, 99: 54–65

[86] Rillig M C, Wright S F, Nichols K A, Schmidt W F, Torn M S (2001). Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils.Plant Soil, 233: 167–177

[87] Rocci K S, Lavallee J M, Stewart C E, Cotrufo M F (2021). Soil organic carbon response to global environmental change depends on its distribution between mineral-associated and particulate organic matter: a meta-analysis.Sci Total Environ, 793: 148569

[88] Rowley M C, Grand S, Verrecchia É P (2017). Calcium-mediated stabilisation of soil organic carbon.Biogeochemistry, 137(1−2): 27–49

[89] Schädel C, Schuur E A G, Bracho R, Elberling B, Knoblauch C, Lee H, Luo Y Q, Shaver G R, Turetsky M R (2013). Circumpolar assessment of permafrost C quality and its vulnerability over time using long-term incubation data.Glob Change Biol, 20(2): 641–652

[90] Shen Z, Han T F, Huang J, Li J W, Daba N A, Gilbert N, Khan M N, Shah A, Zhang H M (2024). Soil organic carbon regulation by pH in acidic red soil subjected to long-term liming and straw incorporation.J Environ Manage, 367: 122063

[91] Shi J C, Wang X L, Wang E T (2023). Mycorrhizal symbiosis in plant growth and stress adaptation: from genes to ecosystems.Annu Rev Plant Biol, 74(1): 569–607

[92] Shi P J, Preisler H K, Quinn B K, Zhao J, Huang W W, Röll A, Cheng X F, Li H R, Hölscher D (2020). Precipitation is the most crucial factor determining the distribution of moso bamboo in Mainland China.Glob Ecol Conserv, 22: e00924

[93] Shi R R, Liu Z D, Li Y, Jiang T M, Xu M G, Li J Y, Xu R K (2019). Mechanisms for increasing soil resistance to acidification by long-term manure application.Soil Tillage Res, 185: 77–84

[94] Shi T S, Collins S L, Yu K L, Peñuelas J, Sardans J, Li H L, Ye J S (2024). A global meta-analysis on the effects of organic and inorganic fertilization on grasslands and croplands.Nat Commun, 15(1): 3411

[95] Shi Z J, Zhang J E, Xiao Z H, Lu T T, Ren X Q, Wei H (2021). Effects of acid rain on plant growth: a meta-analysis.J Environ Manage, 297: 113213

[96] Silver W L, Thompson A W, Reich A, Ewel J J, Firestone M K (2005). Nitrogen cycling in tropical plantation forests: potential controls on nitrogen retention.Ecol Appl, 15(5): 1604–1614

[97] Smith W H (1976). Character and significance of forest tree root exudates.Ecology, 57(2): 324–331

[98] Song X Z, Peng C H, Zhou G M, Gu H H, Li Q, Zhang C (2016). Dynamic allocation and transfer of non-structural carbohydrates, a possible mechanism for the explosive growth of Moso bamboo (Phyllostachys heterocycla).Sci Rep, 6(1): srep25908

[99] Staddon P L, Ramsey C B, Ostle N, Ineson P, Fitter A H (2003). Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of ¹⁴C.Science, 300(5622): 1138–1140

[100] Su Z X, Zhong Y Q W, Zhu X Y, Wu Y, Shen Z F, Shangguan Z P (2023). Vegetation restoration altered the soil organic carbon composition and favoured its stability in a Robinia pseudoacacia plantation.Sci Total Environ, 899: 165665

[101] Tang B, Rocci K S, Lehmann A, Rillig M C (2023). Nitrogen increases soil organic carbon accrual and alters its functionality.Glob Change Biol, 29(7): 1971–1983

[102] Terefe R, Yu K Y, Deng Y B, Yao X, Wang F, Liu J (2020). Spatial variability of soil chemical properties of Moso bamboo forests of China.J For Res, 32(6): 2599–2608

[103] Tian D S, Niu S L (2015). A global analysis of soil acidification caused by nitrogen addition.Environ Res Lett, 10(2): 024019

[104] Tian J, Dungait J A J, Lu X K, Yang Y F, Hartley I P, Zhang W, Mo J M, Yu G R, Zhou J Z, Kuzyakov Y (2019). Long-term nitrogen addition modifies microbial composition and functions for slow carbon cycling and increased sequestration in tropical forest soil.Glob Change Biol, 25(10): 3267–3281

[105] Treseder K K (2004). A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO₂ in field studies.New Phytol, 164(2): 347–355

[106] van der Heijden M G A, Martin F M, Selosse M A, Sanders I R (2015). Mycorrhizal ecology and evolution: the past, the present, and the future.New Phytol, 205(4): 1406–1423

[107] Wang C, Lu X K, Mori T K, Mao Q G, Zhou K J, Zhou G Y, Nie Y X, Mo J M (2018). Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest.Soil Biol Biochem, 121: 103–112

[108] Wang Y D, Hu N, Ge T D, Kuzyakov Y, Wang Z L, Li Z F, Tang Z, Chen Y, Wu C Y, Lou Y L (2017). Soil aggregation regulates distributions of carbon, microbial community and enzyme activities after 23-year manure amendment.Appl Soil Ecol, 111: 65–72

[109] Wen Z H, White P J, Shen J B, Lambers H (2021). Linking root exudation to belowground economic traits for resource acquisition.New Phytol, 233(4): 1620–1635

[110] Wilson G W T, Rice C W, Rillig M C, Springer A, Hartnett D C (2009). Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments.Ecol Lett, 12(5): 452–461

[111] Wu L, Wang J, Xu H, Xu X L, Gao H J, Xu M G, Zhang W J (2023). Soil organic carbon priming co-regulated by labile carbon input level and long-term fertilization history.Sci Total Environ, 902: 166175

[112] Wu S L, Fu W, Rillig M C, Chen B, Zhu Y G, Huang L B (2024). Soil organic matter dynamics mediated by arbuscular mycorrhizal fungi - an updated conceptual framework.New Phytol, 242(4): 1417–1425

[113] Xu C H, Xu X, Ju C H, Chen H Y H, Wilsey B J, Luo Y Q, Fan W (2021). Long-term, amplified responses of soil organic carbon to nitrogen addition worldwide.Glob Change Biol, 27(6): 1170–1180

[114] Xu M G, Lou Y L, Sun X L, Wang W, Baniyamuddin M, Zhao K (2011). Soil organic carbon active fractions as early indicators for total carbon change under straw incorporation.Biol Fertil Soils, 47(7): 745–752

[115] Xu X, Shi Z, Li D J, Rey A, Ruan H H, Craine J M, Liang J Y, Zhou J Z, Luo Y Q (2016). Soil properties control decomposition of soil organic carbon: Results from data-assimilation analysis.Geoderma, 262: 235–242

[116] Yadav D S, Jaiswal B, Gautam M, Agrawal M (2020). Soil Acidification and its Impact on Plants. Plant Responses to Soil Pollution. Singapore: Springer

[117] Yang K, Zhang Q, Zhu J J, Wang Q Q, Gao T, Wang G G (2023). Mycorrhizal type regulates trade-offs between plant and soil carbon in forests.Nat Clim Chang, 14(1): 91–97

[118] Yu H Y, Ding W X, Luo J F, Geng R L, Cai Z C (2012). Long-term application of organic manure and mineral fertilizers on aggregation and aggregate-associated carbon in a sandy loam soil.Soil Tillage Res, 124: 170–177

[119] Yu Z P, Chen H Y H, Searle E B, Sardans J, Ciais P, Peñuelas J, Huang Z Q (2020). Whole soil acidification and base cation reduction across subtropical China.Geoderma, 361: 114107

[120] Yuan X B, Niu D C, Gherardi L A, Liu Y B, Wang Y, Elser J J, Fu H (2019). Linkages of stoichiometric imbalances to soil microbial respiration with increasing nitrogen addition: evidence from a long-term grassland experiment.Soil Biol Biochem, 138: 107580

[121] Zhang F Y, Jin Q Y, Peng H Z, Zhu T J (2020). Soil acidification in moso bamboo (Phyllostachys edulis) forests and changes of soil metal ions (Cu, Pb) concentration.Arch Agron Soil Sci, 67(13): 1799–1808

[122] Zhang J, Tang X L, He X H, Liu J X (2015). Glomalin-related soil protein responses to elevated CO₂ and nitrogen addition in a subtropical forest: Potential consequences for soil carbon accumulation.Soil Biol Biochem, 83: 142–149

[123] Zhang J F, Zhou J G, Lambers H, Li Y W, Li Y X, Qin G M, Wang M, Wang J, Li Z A, Wang F M (2022). Nitrogen and phosphorus addition exerted different influences on litter and soil carbon release in a tropical forest.Sci Total Environ, 832: 155049

[124] Zhang S, Deng Q, Wang Y P, Chen J, Yu M X, Fang X, He H B, Chen J L, Xu P P, Wang S H, Yan J H (2021). Linkage of microbial living communities and residues to soil organic carbon accumulation along a forest restoration gradient in southern China.For Ecosyst, 8(1): 57

[125] Zhang T A, Chen H Y H, Ruan H H (2018). Global negative effects of nitrogen deposition on soil microbes.ISME J, 12(7): 1817–1825

[126] Zhang Y T, de Vries W, Thomas B W, Hao X Y, Shi X J (2017). Impacts of long-term nitrogen fertilization on acid buffering rates and mechanisms of a slightly calcareous clay soil.Geoderma, 305: 92–99

[127] Zhou G M, Meng C F, Jiang P K, Xu Q F (2011). Review of carbon fixation in bamboo forests in China.Bot Rev, 77(3): 262–270

[128] Zhou Z H, Wang C K, Zheng M H, Jiang L F, Luo Y Q (2017). Patterns and mechanisms of responses by soil microbial communities to nitrogen addition.Soil Biol Biochem, 115: 433–441

[129] Zhu Y, Bian H X, Ju C H, Xu C H, Zhou Y, Zhang H G, Xu X (2023). Fertilization alters the abundance but not the diversity of soil fauna: a meta-analysis.Glob Ecol Biogeogr, 32(4): 482–494

[130] Zong Y T, Li Z C, Gui R Y, Chen D, Yuan M T, Chai Y J, Shan S D, Wong M H (2023). Manganese losses induced by severe soil acidification in the extensive Lei bamboo (Phyllostachys violascens) plantation stands in Eastern China.Chemosphere, 339: 139669

[131] Zuo K Y, Fan L L, Guo Z W, Zhang L, Duan Y Y, Zhang J R, Chen S L, Lin H, Hu R C (2024). High nutrient utilization and resorption efficiency promote bamboo expansion and invasion.J Environ Manage, 362: 121370

RIGHTS & PERMISSIONS

Higher Education Press