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.

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.

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.