Nitrogen addition and drought impose divergent effects on belowground bud banks of grassland community: a meta-analysis

Wu, Jing; Hou, Xian-zhang; Zhu, Jin-lei; Miao, Ren-hui; Adomako, Michael Opoku

doi:10.3389/fpls.2024.1464973

SYSTEMATIC REVIEW article

Front. Plant Sci., 06 January 2025

Sec. Functional Plant Ecology

Volume 15 - 2024 | https://doi.org/10.3389/fpls.2024.1464973

Nitrogen addition and drought impose divergent effects on belowground bud banks of grassland community: a meta-analysis

Jing Wu^1,2

Xian-zhang Hou¹

Jin-lei Zhu³

Ren-hui Miao⁴

Michael Opoku Adomako^1,2*†

¹School of Life Sciences, Taizhou University, Taizhou, China
²Institute of Wetland Ecology & Clone Ecology/Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, China
³Chinese Academy of Forestry Research, Institute of Forestry, Beijing, China
⁴Dabieshan National Observation and Research Field Station of Forest Ecosystem at Henan, International Joint Research Laboratory for Global Change Ecology, School of Life Sciences, Henan University, Kaifeng, China

Introduction: Belowground bud banks (or bud-bearing organs) underlie grassland regeneration and community succession following ecosystem perturbations. Disturbances of nitrogen (N) enrichment, overgrazing, wildfire, and drought substantially affect grassland ecosystem succession and aboveground productivity.

Methods: To understand the magnitude and direction of the disturbances on the belowground bud banks, we conducted a meta-analysis on 46 peer-reviewed studies published from 1980 to 2023. The meta-analysis comprises 231 observations of bud bank density per unit area and 410 observations of bud bank density per tiller.

Results: Results indicate that N addition remarkably promotes bud banks densities and plant functional groups of grass in the belowground bud banks. While drought negatively affects bud banks densities and functional groups of grasses and forbs. We found that effects of the N addition and drought on the bud banks depend on the bud type, e.g., root sprouting buds, bulb buds, and dormant buds. However, grazing and wildfire have no significant effect on the bud banks.

Discussion: Our results suggest that the N addition and drought may significantly exert promotional and inhibitory effects, respectively, on belowground bud banks, critically altering plant regrowth, community succession, and grassland community dynamics.

Introduction

Globally, grassland communities are increasingly faced with disturbances, including nitrogen (N) addition, overgrazing, wildfire, and drought, critically underlying the loss of grassland community stability (Dawson et al., 2011; Pecl et al., 2017; Schulte to Bühne et al., 2021). Grassland ecosystems provide crucial ecosystem functions and services despite being very sensitive to the disturbances (Luo et al., 2023). This underscores the significance of belowground bud banks, serving as ecological insurance for grassland recovery and community succession following periods of environmental perturbation (Hoover et al., 2014; Ott et al., 2019; Qian et al., 2023; Wu et al., 2024). Although these environmental stressors critically impose damaging effects on individual plant species, their sensitivity and response to these effects may differ among plant functional types, including grasses and forbs (Qian et al., 2022; Song et al., 2011; Wang et al., 2019). However, it remains unclear how such disturbances – N addition, drought, grazing, and wildfire − affect belowground bud banks and the mechanisms driving such impacts.

Belowground bud banks are commonly associated with a suite of bud-bearing organs (e.g., rhizomes, tillers, and ramets) and the capacity to balance resource allocation to ensure the growth, stability, and maintenance of plant populations and communities (Klimešová et al., 2023; Qian et al., 2021; Wu and Yu, 2022). Belowground bud banks also represent a pool of carbohydrate storage structures tightly linked with their resilience and capacity to resprout under favorable environmental conditions (Klimešová et al., 2021; Ru et al., 2023). Given the frequent droughts, wildfires, and grazing in grassland ecosystems, belowground bud-bearing organs remain crucial for such ecosystems for their ultimate aboveground regrowth following the period of perturbation (Donovan et al., 2020; Twidwell et al., 2016). For example, Donovan et al. (2020) found no evidence of a persistent wildfire in North America’s grassland biome due to the rapid regrowth of all vegetation functional types, suggesting the importance of active belowground bud banks. On the contrary, Twidwell et al. (2016) observed that extreme drought following a period of wildfire significantly decreased the resprouting densities of woody shrubs and aboveground recruitment by 35−55% compared to areas that did not burn in the southern Great Plains of North America. This suggests that belowground bud-bearing organs represent a vital determining factor for aboveground recruitment and regeneration rate (Ott et al., 2019; Qian et al., 2021). However, such attributes of belowground bud banks can be constrained by serious disturbances, with cascading negative impacts on ecological restoration and community succession (Klimešová et al., 2021).

Indeed, serious disturbances negatively affect grasslands via a decrease in the density and regeneration capacity of belowground bud banks (Fischer and Knutti, 2014; Ru et al., 2023). Such impacts on grassland ecosystems have been reported at regional and global scales (Ciais et al., 2005; Leys et al., 2018; Zhao and Running, 2010). In Europe, for instance, an intense drought-induced decline in net primary productivity in 2003 has been reported (Ciais et al., 2005), while a global-level decrease in terrestrial primary productivity caused by drought between 2000 and 2009 has been documented (Zhao and Running, 2010). Prolonged impacts of these disturbances have caused the degradation of many temperate grasslands in Asia and North America and tropical grasslands in South America and Africa (Bardgett et al., 2021; Stevens et al., 2004). It is worth noting that these disturbances complement each other, thereby maximizing their gross impacts on ecosystems. For instance, chronic N additions have been found to exacerbate drought effects on grassland productivity (Meng et al., 2021). Across many field and controlled studies, variation in individual plant vulnerability has been implicated as the key limiting factor for ecosystem recovery after these disturbances (Debinski et al., 2010; Qian et al., 2023; Wang et al., 2012; Xu et al., 2021). One reason for such variation could relate to the differential responses among plant functional types, especially grasses and forbs (Qian et al., 2023; Xu et al., 2017). As a confirmation, Qian et al. (2023) have reported a consistent decrease in the density of the belowground bud bank of forbs but not grasses in response to drought. Besides the individual differences, however, mechanisms underlying such variation in plant functional type responses to disturbances, including N addition, drought, grazing, and wildfire, remain inadequate.

Understanding such disparities in bud bank responses among plant functional types is crucial for predicting future climate and human-derived impacts on grassland communities. Belowground bud banks of different plant functional types may vary in their responses to environmental stress (Carter et al., 2012; Dalgleish and Hartnett, 2009; Klimešová and Klimeš, 2007; Zhao et al., 2019). Therefore, plant functional types well-adapted to a given disturbance may exhibit a more pronounced regrowth after periods of disturbance (Hoover et al., 2014; Mackie et al., 2019). Most previous studies have demonstrated that grasses often show higher resistance to intense drought and grazing owing to their resource-use strategies compared to forbs (Carter et al., 2012; Xu et al., 2021, 2017). In an experimental study, forbs exhibit less resistance to long-term drought than grasses. However, the belowground organs of forbs had the quickest recovery rate in that study (Carter et al., 2012). While an annual wildfire least affected the belowground bud bank of grasses, it remarkably decreased that of forbs by 125% (Dalgleish and Hartnett, 2009). These differential responses of plant functional types are relevant for understanding ecosystem-level consequences of plant communities, especially those ecosystems that are dominated by a peculiar functional type.

The duration of occurrence and intensity of a disturbance regime primarily modulate the severity of impacts driven by climate change and human activities (Tonkin et al., 2017; White and Hastings, 2020). While an extreme drought condition is tightly linked with frequent and intense wildfires (Chikamoto et al., 2017; Pontes-Lopes et al., 2021; Wragg et al., 2018), increasing N addition promotes the growth of grasses and modifies their palatability, ultimately determining grazing preference and intensity. Therefore, we hypothesize that environmental stressors, including N addition, drought, grazing, and wildfire, may impose divergent effects on belowground bud banks and that such differences may vary depending on the severity, bud types, and plant functional types.

We conducted a meta-analysis of existing studies to test these hypotheses and specifically asked whether (1) disturbances of N addition, drought, grazing, and wildfire affect belowground bud bank densities in similar ways; (2) differences in plant functional types mediate belowground bud banks’ responses to the disturbances; (3) bud type differences mediate belowground bud banks’ responses to the disturbances. It was predicted that N addition and drought effects on bud banks may exhibit divergent patterns in many prominent ecosystems, e.g., grasslands.

Materials and methods

Data compilation

We compiled data from studies that have reported belowground bud bank responses to N addition, drought, grazing, and wildfire disturbances by conducting a literature search for peer-reviewed publications in the Web of Science (http://apps.webofknowledge.com/) and Google Scholar. We used the following search string: ‘climate change’ OR ‘global change’ OR ‘human disturbance’ OR ‘drought*’ OR ‘N addition’ OR ‘increased precipitation’ OR ‘fire’ OR ‘grazing’ OR ‘clipping’ OR ‘herbivory’ AND ‘buds’ OR ‘bud bank’ OR ‘bud density.’ All published records from 1980 to 2023 were included in the search. We then screened all the studies for publications that met the criteria: (i) the publication reported effects of manipulating at least one of the following disturbances − N addition, drought, wildfire, and grazing − as well as clipping on bud bank densities of the whole plant community and/or different plant functional types; (ii) the publications that reported mean values, sample sizes, and variances for bud bank densities. In total, 46 publications met the criteria (see Materials and Methods in S1), with 246 observations on the bud bank density per unit area, 410 observations on the bud bank density per tiller, and 174 observations for the wildfire moderator, 281 observations for the grazing moderator, 149 observations for the drought moderator, as well as 52 observations for the N addition moderator. The biomes and study sites of all 46 publications across the world covered in this dataset are shown (Figure 1). Also, detailed information on studies, including classification of disturbances, ecosystem, plant functional type, and bud type, as well as the disturbances and the subsequent effects are shown in the Supplementary Material (Supplementary Table S1).

Figure 1

Figure 1. The biomes and study sites over the world covered in the analyzed dataset.

We extracted mean values of the bud bank density and their corresponding variances (standard deviations, standard errors, or 95%-confidence intervals) and sample sizes directly from the text, tables, or figures using IMAGE J 1.47 v (Rasband, 2013). For the studies involving N addition, water addition, wildfire, grazing, and/or clipping, we considered the ambient level (i.e., no treatment) as the ‘control’ and ‘treatment’ for level(s) such as the N addition, water addition, wildfire, grazing, and/or clipping. For the studies with decreased water availability relative to the ambient level (without decreased water availability), the treatment with decreased water availability was considered as the ‘control’ and ‘treatment’ using the ambient level. When more than one factor was manipulated in an experiment, we kept the other factors at the ambient level and then extracted the data on treatments for the focal factor.

Bud bank type classification

We classified the various bud banks based on their bud-bearing organs’ morphological characteristics. Thus, rhizome buds (axillary buds and apical buds on hypogeogenous rhizomes), tiller buds (axillary buds at the shoot bases of caespitose species and rhizomatous grasses), root-sprouting buds (adventitious buds formed mainly endogenously on roots of forb or shrub), and bulb buds, i.e., buds originating from the swollen bases of bulb-type species (see Figure 2). It is worth noting that buds on rhizomes and roots could be counted directly. In contrast, shoot bases need to be dissected for tiller bud counting.

Figure 2

Figure 2. Belowground bud-bearing organ types covered in the analyzed dataset.

According to papers or publications used in this meta-analysis, we classified bud into three viability classes, i.e., those that were metabolically active, dormant, or dead. Previous-year stem base halves were incubated in colorless triphenil tetrazolium chloride [TTC, 0.6% (w/v)] at 30°C in darkness for 15 h. Bud apexes that stained either red or pink were considered metabolically active. Change from colorless to either red or pink indicates an enzymatic reduction from TTC to insoluble red formazan. Buds unstained with TTC were tested using the vital stain Evan’s Blue [0.25% (w/v)], which does not penetrate intact semi-permeable membranes. Thus, unstained or dark blue-stained tissues using the vital stain were considered dormant or dead, respectively.

The degree criteria for each moderator

We define the extent of the wildfire by the frequency (number of times). Less than 5 wildfires per year were considered low, less than 10 and more than 5 were considered moderate, and more than 10 were considered high. We defined the intensity of grazing according to the number of livestock per unit or the proportion of clipping, with less than 10 per hectare considered low, more than 10 and less than 30 considered moderate, and more than 30 considered high. A clipping ratio of less than 30% is considered low, between 30% and 50% is considered moderate, and greater than 50% is considered high. This definition follows the literature collected for the meta-analysis (see Supplementary Table S2).

To ensure consistency, we define the intensity of nitrogen addition by the amount and concentration added. Less than or equal to 20g per square meter was categorized as low, less than 20 mmol/L^-1 as low, more than 20 mmol/L^-1 but less than 40 mmol/L^-1 as moderate, and more than 40 mmol/L^-1 as high. We defined the intensity of drought according to the amount and proportion of rainfall intercepted as mentioned in literature. Less than 200 mm was categorized as low, greater than 200 mm and less than 500 mm was categorized as moderate, and greater than 500 mm was categorized as high. The proportion of intercepted rainfall less than 30% was considered low, greater than 30%, but less than 60% was considered moderate, and greater than 60% was considered high (see Supplementary Table S2).

Effect size and variance computation

To examine the effects of N addition, drought, grazing, and wildfire disturbance on belowground bud bank density, we calculated the log response ratio (ln R) as the effect size of bud bank density for each component of N addition, drought, grazing, and wildfire disturbances for each study (Hedges et al., 1999):

\ln R = l n (\frac{{\bar{X}}_{t}}{{\bar{X}}_{c}}) = l n ({\bar{X}}_{t}) - l n ({\bar{X}}_{c})

where ${\bar{X}}_{t}$ and ${\bar{X}}_{c}$ are the mean values of the individual bud bank density in the treatment (t) and control (c), respectively. The variance of ln R was calculated, following Hedges et al. (1999), as

v_{l n R} = \frac{{(S D_{c})}^{2}}{N_{c} {({\bar{X}}_{c})}^{2}} + \frac{{(S D_{t})}^{2}}{N_{t} {({\bar{X}}_{t})}^{2}}

where N_c and N_t are sample sizes, SD_t and SD_c are standard deviations, and X_t and X_c are mean values for the bud bank density in the treatment (t) and control (c), respectively. To avoid pseudo-replication, we pooled the multiple effect sizes (weighted by the inverse variance) and corresponding variances per study (Leimu et al., 2006). Pooling was done using the fixed-effect model (using the rma function in the R package METAFOR) because we assumed a single true underlying effect size in a study.

Data analysis

All meta-analytical calculations and analyses were performed in R 3.1.3 (R Core Team, 2015) using the package METAFOR v1.9-7 (Viechtbauer, 2010). First, to test whether the bud bank densities of different plant functional types, on average, exhibited significant positive or negative responses to N addition, drought, grazing, and wildfire, we performed a general meta-analysis using a random-effect model (Gurevitch and Hedges, 2001). We computed weighted mean effect sizes and 95% confidence intervals (CIs) for each model for the moderator levels. We considered a mean effect size estimate significantly different from zero if the 95% CI around the mean did not include zero. For each of the disturbance, we compared mean effect sizes of different bud types (i.e., rhizome bud, tiller bud, root sprouting bud, and bulb bud; active bud and dormant bud) and plant functional type (i.e., forb, grass, sedge, shrub, and total plants). We also compared mean effect sizes of bud bank densities among different treatment levels (i.e., low, moderate, and high). In these models, total heterogeneity (QT) in effect sizes can be partitioned into heterogeneity explained by the model structure (QM) and unexplained heterogeneity (QE); we used the QT test (Koricheva et al., 2013) to test for a significant difference in the mean effect size among levels or groups for the moderator.

Results

Disturbance effects on belowground bud banks

The analysis of 48 studies indicated that the effect size of N addition and drought was higher than that of wildfire and grazing disturbances. Thus, drought and N addition significantly affected bud bank density but not wildfire and grazing (P < 0.05, Table 1; Figure 3). However, as drought imposed significantly negative effects on the belowground bud bank density (Table 1; Figure 3), N addition had significantly positive impacts on the belowground bud bank density (P < 0.05, Table 1; Figure 3). Neither wildfire nor grazing had significant effect on average belowground bud bank density (P < 0.05, Table 1; Figure 3).

Table 1

Table 1. Results of meta-analysis comparing bud bank densities in responses to disturbances of wildfire, grazing, drought, and N addition.

Figure 3

Figure 3. Responses (indicated by log response ratio mean effect sizes) of belowground bud bank densities to disturbances of wildfire, grazing, drought, and N addition. Error bars represent 95%-confidence intervals around the mean effect size estimates. The asterisk (*) indicates a statistically significant effect on the belowground bud bank density (i.e., P < 0.05), while ns denotes no significant effect. Sample sizes (i.e., the number of effect sizes) are given in parentheses. The dashed vertical line indicates zero effect of the global environmental change drivers.

Effect of different degrees of disturbance on bud bank

Considering the level of the measured disturbance on bud banks, i.e., drought, N addition, fire, and grazing, we found that higher N addition and grazing levels negatively affected belowground bud bank densities. Both high-level and moderate-level of N addition significantly affected the belowground bud bank densities. However, moderate-level disturbances of drought, grazing, and fire had no significant effects on the belowground bud bank densities (P < 0.05, Table 2). Although both moderate and high-level of drought had no effect on the belowground bud bank density, surprisingly, low levels of drought had a minimal effect (i.e., indicated by a marginally significant effect) on it (P < 0.1, see Table 2).

Table 2

Table 2. Results of meta-analysis comparing bud bank densities in responses to disturbances of wildfire, grazing, drought, and N addition.

Disturbance effects on different bud types

Results also indicate that different bud types showed different responses to disturbances of N addition, drought, wildfire, and grazing (Table 3; Figure 4). Both rhizome buds and bulb buds showed significantly negative responses to grazing (P < 0.05, Table 3; Figure 4A). However, active and dormant bud showed significantly negative and positive responses, respectively, to wildfire (P < 0.05, Table 3; Figure 4B). Moreover, rhizome and tiller buds showed significantly positive responses to N addition, but the N addition imposed significantly negative effect on root sprouting, bulbs, and dormant buds (P < 0.05, Table 3; Figure 4). Additionally, the N addition had significantly positive effect on other buds that were not specifically grouped (i.e., ungrouped) in our dataset (P < 0.05, Table 3; Figure 4). Moreover, results showed that rhizome and tiller buds showed significantly negative responses to drought (P < 0.05, Table 3; Figure 4A). However, the drought had neither positive nor negative effect on the other buds (Table 3; Figure 4).

Table 3

Table 3. Results of meta-analysis comparing bud bank densities to disturbances of wildfire, grazing, N addition, and drought.

Figure 4

Figure 4. Responses of belowground bud bank densities of different bud types to disturbances of wildfire, grazing, drought, and N addition. Error bars represent 95%-confidence intervals around the mean effect size estimates. The asterisk (*, **, and ***) indicates a statistically significant effect on the belowground bud bank density (i.e., P < 0.05), while ns denotes no significant effect. Sample sizes (i.e., the number of effect sizes) are given in parentheses. The dashed vertical line indicates zero effect of the global environmental change drivers. (A) denotes the density of bud bank per unit area, (B) denotes the density of bud bank of per tiller, respectively.

Disturbance effects on plant functional type on bud banks

Results indicate that different plant functional types showed different responses to the disturbances of N addition, drought, wildfire, and grazing (Table 4; Figure 5). Neither wildfire nor grazing had a significant positive or negative effect on plant functional type (grasses, forbs, and shrubs) (Table 4; Figure 5). However, ungrouped plant functional types showed significantly positive response to wildfire (Table 4; Figure 5). Unlike wildfire and grazing, N addition and drought significantly affected grasses and forbs but not shrubs. Thus, grasses and forbs showed significantly negative responses to drought. However, N addition significantly promoted the bud bank density of grasses (Table 4; Figure 5).

Figure 5

Figure 5. Responses of belowground bud bank densities of different plant functional groups to disturbances of wildfire, grazing, drought, and N addition. Error bars represent 95%-confidence intervals around the mean effect size estimates. The asterisk (*) indicates a statistically significant effect on the belowground bud bank density (P < 0.05), The asterisk (***) indicates a statistically significant effect on the belowground bud bank density (P < 0.001), respectively, while ns denotes no significant effect. Sample sizes (i.e., the number of effect sizes) are given in parentheses. The dashed vertical line indicates zero effect of the global environmental change drivers.

Table 4

Table 4. Results of meta-analysis comparing bud bank densities of different plant functional groups to disturbances of wildfire, grazing, N addition, and drought.

Discussion

Results of this meta-analysis provide empirical evidence that N addition and drought impose significantly divergent effects, which depend on the degree and frequency of disturbances, plant functional types, and bud types. Overall, our results confirmed the findings of most previous studies reporting that drought (Adomako et al., 2020b; Buttler et al., 2019; Lei et al., 2020; Xu et al., 2021) and N addition (Gough et al., 2012; Ren et al., 2019, 2023; Zheng et al., 2019) affect plant growth and productivity.

Drought events hamper the regeneration of belowground bud banks (Qian et al., 2023; Wang et al., 2019), profoundly affecting ecosystem succession and community composition and dynamics (Buttler et al., 2019; Lei et al., 2020; Qian et al., 2022; Wang et al., 2019). In the present analysis, drought significantly impacts forbs and grasses, key plant functional types in many grassland ecosystems worldwide (Petermann and Buzhdygan, 2021; Qian et al., 2023; Wang et al., 2019). This observation could underlie the significant losses and degradation of global grassland ecosystems, particularly in temperate grasslands of Asia and North America and tropical grasslands of South America and Africa. For instance, about 99% of North America’s aboveground regrowth of tallgrass ecosystems is recruited from the belowground bud banks (Benson and Hartnett, 2006). Moreover, a reduction of 66% of annual precipitation, indicating a severe drought, significantly reduced the bud density, consequently impacting the community’s aboveground shoot productivity (Qian et al., 2023). Although in a short term, a 90-day drought significantly reduced the net productivity (the sum of aboveground and belowground biomass) of rhizomatous grass Leymus chinensis by 69% and decreased belowground bud bank density by 56% (Wang et al., 2019). This suggests that L. chinensis, which is native to China and is dominant in the Eurasian steppe ecosystems, can easily be lost due to prolonged drought regimes (Adomako et al., 2021; Wang et al., 2019). Our results suggest that drought is critical to grassland ecosystems owing to its immediate reduction effects on net primary productivity and future productivity of grassland due to its impacts on belowground bud bank density.

However, effects of the drought largely depend on its magnitude or severity, coupled with plant functional and bud types. For example, in a grassland experimental community in Central Texas, severe drought profoundly reduced biomass productivity by 82% (Xu et al., 2017). Such negative effects on grasses were primarily attributed to reduced growth, tiller number, and rhizome buds (Zhuang et al., 2017), as well as ramets, root sprouting, and dormant buds for forbs (Saud et al., 2017). Previous studies have consistently reported that bud bank density and bud types of forbs showed the highest vulnerability to drought compared to grasses (Li et al., 2021; Qian et al., 2021, 2023). These differential responses may explain the disparities in ecosystem-level responses to the ongoing environmental disturbance (Bobbink et al., 2010; Stevens et al., 2004). Thus, ecosystems in which grasses are key dominant species may show stronger resistance than where forbs dominate (Li et al., 2016; You et al., 2017). However, in a long-term drought event, how bud banks of grasses may respond and their impact on the wider grassland vegetation require further experimental clarification.

Furthermore, results suggest that N addition significantly promoted bud bank density and aboveground growth (Qian et al., 2021). One key mechanism underpinning such observations is that N addition enhances litter quality and accumulation, promoting soil physico-chemical characteristics and their positive feedback on belowground bud banks (Hou et al., 2021; Wu et al., 2024). N enrichment and litter addition jointly enhanced bud numbers and aboveground growth, suggesting that N addition may be tightly linked with ecosystem-level growth and productivity (Li et al., 2021; Ren et al., 2024). However, N addition mostly exhibits positive effects at the plant species level under short-term conditions but cascades profound negative effects on population- and community-level diversity and dynamics (Adomako et al., 2020a; Gao et al., 2022; Li et al., 2022). Thus, increasing N addition promotes large canopy formation of species (e.g., grasses) with high nutrient use efficiency, decreasing light entry and water availability to understory plants (Wu and Yu, 2022; Xing et al., 2022), as well as decreasing soil temperature and respiration (Li et al., 2018; Yang et al., 2022). Eventually, such species dominate their ecosystems by competitively excluding weaker species (Gough et al., 2012; Liu et al., 2021). This phenomenon partly explains the loss of many species by elevated N deposition under the ongoing global environmental change (Li et al., 2022; Ren et al., 2022; Stevens et al., 2010). For example, earlier studies have attributed severe N deposition as driving the loss of species richness of grasslands across Europe and Great Britain (Stevens et al., 2004, 2010).

Indeed, N addition effects on belowground bud banks and aboveground growth recruitments strongly correlate with the bud type and degree of N availability, as observed from our analysis. Previous studies have demonstrated that high N addition promotes vegetative growth, including rhizomes, tillers, and ramets (Adomako et al., 2022; Gough et al., 2012). Also, it has been previously indicated that rhizomatous buds are highly vulnerable to nutrient shortages and intense drought in grassland ecosystems (Qian et al., 2017). For example, a recent long- and short-term grassland study designed to test the N addition duration on clumper, stoloniferous, and rhizomatous clonal growth forms found that short-term N addition promoted the growth of the clumper clonal growth form (Zheng et al., 2019). The authors, however, reported that long-term N addition significantly suppressed stoloniferous clonal growth but remarkably favored rhizomatous clonal growth. A recent meta-analysis and some studies found that grasses and forbs responded differently to N addition (You et al., 2017). There has been a general recognition that N addition promotes the aboveground and belowground biomass of grasses but reduces that of forbs (Adomako and Yu, 2023; Cheng et al., 2023; Song et al., 2011; You et al., 2017). Our results and previous findings suggest that drought and N addition effects on bud banks and bud types depend on the magnitude of disturbances and specific plant functional type.

Although wildfire and grazing did not affect belowground bud bank densities, high grazing intensity significantly impacts bud types, particularly active, dormant, rhizome, and bulb buds. Such bud-type-specific effects can undermine ecosystems where these bud types dominate the belowground structures. In the Eurasian regions where these species dominate the ecosystem, the loss of below- and above-ground biodiversity caused by extreme grazing has resulted in grassland degradation (Liang et al., 2021). Perhaps overgrazing is among the most important disturbances driving the loss of grassland biomes worldwide (Liang et al., 2021; Osem et al., 2002; Ren et al., 2018; Zhang et al., 2023), resulting from its multifaceted damaging effects on below- and above-ground biodiversity (Cao et al., 2024; Liang et al., 2021), soil respiration and organic carbon (Li et al., 2024), and ecosystem multifunctionality (Zhang et al., 2023).

Similarly, while wildfire did not impact bud bank densities, it significantly induced negative and positive impacts on active and dormant buds. The majority of studies have documented drastic effects of wildfire on belowground processes (Clarke et al., 2022; Kong et al., 2022), nutrient availability (Kong et al., 2022), and plant aboveground productivity (Roces-Díaz et al., 2022; Wardle et al., 2003), all of which positively correlate with regeneration of active buds in ecosystems. Surprisingly, wildfire exerted promotional effects on dormant buds in the present analysis, which is consistent with few previous studies that have documented positive impacts of wildfire on grassland regrowth, especially in the semi-arid regions of Texas, USA (Fultz et al., 2016) and as management strategy of protected forest in Northeast Portugal (Fonseca et al., 2011). Our analysis indicated that N addition and drought would differentially impact specific attributes of belowground bud banks, such as plant functional types and bud types.

Conclusions

Results of our meta-analysis suggest that N addition and drought significantly impact bud bank density, potentially affecting plant populations, community-level productivity, and ecosystem stability. This analysis confirms many predictions of N deposition effects on global ecosystems in the coming decades. Results consistently replicated most previous findings, which suggest that drought adversely affects belowground bud bank densities and numbers with cascading consequences for aboveground productivity. Moreover, N addition significantly promotes belowground bud bank density, positively correlating with aboveground biomass, litter accumulation, and subsequently increased nutrient availability. The disparity effects on belowground bud banks among the measured variables may be attributed to the dependency of some factors (e.g., wildfire) on drought variables. Thus, for example, effects of wildfire on grassland ecosystems increase with drought intensity and duration. Given the importance of grassland ecosystems and the predicted increases in N deposition and drought in the coming decades, prioritizing the management of belowground bud banks will remain a critical component of maintaining the productivity and stability of grassland globally.

Data availability statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Author contributions

JW: Conceptualization, Investigation, Methodology, Validation, Writing – original draft. XH: Data curation, Formal analysis, Writing – original draft. JZ: Methodology, Writing – original draft. RM: Formal analysis, Validation, Writing – original draft. MA: Supervision, Visualization, Writing – review & editing.

Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (42477507, 31971732), the General Research Project of the Education Department of Zhejiang Province (Y202248466).

Acknowledgments

We would like to thank Shaobin Yan and Quanlai Zhou for data interpretation and English language editing.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2024.1464973/full#supplementary-material

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