INTRODUCTION
Ecosystem multifunctionality, which encompasses multiple aspects of efficient above-belowground carbon and nutrient cycling processes, is crucial for delivering essential services such as food production and climate regulation (Garland et al., 2021; Manning et al., 2018). However, global change factors (GCFs) negatively affect ecosystem multifunctionality in various ways. For instance, drought decreases ecosystem functionality by restricting enzyme activities that are vital for soil nutrient cycling (Lozano et al., 2021). Furthermore, the effects of fertilization on multifunctionality vary depending on the specific nutrient limitations within an ecosystem (Chen et al., 2020; Li et al., 2023a; Ma et al., 2021). While many studies have focused on the influence of single or dual GCFs on ecosystem multifunctionality, it’s critical to recognize that multiple GCFs typically occur simultaneously in real-world scenarios (Rillig et al., 2021; Zandalinas and Mittler, 2022). For example, in agricultural ecosystems, besides warming and drought, anthropogenic activity formed stressors like overuse of mineral fertilizers and pesticides are also present (Seppelt et al., 2022). Recent studies have shown that the simultaneous occurrence of multiple GCFs result in a more pronounced negative impact on both biodiversity and ecosystem multifunctionality (Rillig et al., 2019; Speißer et al., 2022).
Biodiversity-ecosystem function (BEF) studies have demonstrated that biodiversity across multiple trophic levels, including both aboveground and belowground components, is crucial for maintaining ecosystem functions (Balvanera et al., 2006; Bardgett and van der Putten, 2014; Gamfeldt and Roger, 2017; Soliveres et al., 2016). It was believed that increased diversity might have positive effects on ecosystem multifunctionality even under multiple GCFs (Benkwitt et al., 2020). This may be because that with an increasing number of species there is a greater insurance that some species may be unaffected by particular GCF, or particularly efficient at supporting an ecosystem function under a GCF perturbation, such that the functioning of the community is maintained (Loreau and Hector, 2001). Greater species diversity may enhance ecosystem function through complementary, allowing different species to support various functions under different conditions, thus maintaining ecosystem multifunctionality (Isbell et al., 2011, Wagg et al., 2021). Such a division of labor among species can result in a ‘transgressive overyielding’ or ‘complementarity’ effect where the more diverse community results in a greater effect than the best performing individual species (Loreau and Hector, 2001; Xu et al., 2024). This means that the response of an ecosystem function when faced with GCFs could be due to either the diversity of species or the presence of a particularly important species for that function.
Recent findings suggest that the negative impacts of multiple GCFs on ecosystem multifunctionality are exacerbated in communities with high plant diversity (Xu et al., 2024). This effect is attributed to the increased abundance of soil fungal pathogens under multiple GCFs thereby eliminating the positive effects of soil biodiversity on ecosystem functions. It was indicated that an increasing number of GCFs may reduce the beneficial effects of high soil microbial diversity on ecosystem multifunctionality by decreasing fungal abundance and altering fungal community composition (Yang et al., 2022). These results suggest that soil fungi play a crucial role in determining ecosystem multifunctionality under multiple GCFs. However, it is unclear whether soil fungi can alleviate the negative impacts and regulatory mechanisms of multiple GCFs on ecosystem multifunctionality.
Arbuscular mycorrhizal fungi (AMF), one of the most important components of soil fungi, can form mycorrhizal symbiosis with 72% of flowering plants (Brundrett and Tedersoo, 2018), serving as a crucial link between plants and soil. Specifically, AMF have been found to significantly improve plant performance under various stresses, including salt, drought, warming, nitrogen deposition, and elevated CO2levels (Zhang et al., 2018; Tang et al., 2023). Previous studies have demonstrated the benefits of AMF for various ecosystem functions. For instance, AMF can reduce soil N2O emissions and partly mitigate global warming potential (Bender et al., 2014; Cui et al., 2021). AMF can also affect ecosystem functions like primary productivity, nutrient cycling, soil carbon sequestration, and soil pathogen defense (Powell and Rillig, 2018; Wang and Rengel, 2023). Additionally, the diversity of AMF plays a vital role in determining ecosystem stability and multifunctionality (van der Heijden et al., 1998; Ma et al., 2021). Higher AMF diversity leads to faster nutrient cycling and transport, which in turn improves soil health and plant growth (Zhang et al., 2024).
However, it remains unclear whether high AMF diversity could continue to benefit ecosystem multifunctionality or not under multiple GCFs. High AMF diversity could enhance ecosystem resistance and stability to GCFs (Jia et al., 2021; Yang et al., 2016, 2014), and thus the high AMF diversity treatment may exhibit a flatter slope compared to lower diversity (Figure 1a). On the other hand, functionally redundant species could become important in a changing environment (Fetzer et al., 2015). This may lead to a opposite performance of low and high diversity treatments (Figure 1b). Previous studies have also found no significant correlation between soil biodiversity and ecosystem function (Wang et al., 2022), or between AMF diversity and ecosystem function (Jing et al., 2015). In this case, the effect of GCF number could be the same for high or low diversity treatment (Figure 1c), or no effect (Figure 1d).
In this study, we conducted a microcosm experiment to address the following two questions: (1) does greater AM fungal diversity exhibit greater multifunctionality under multiple GCFs? (2) Which ecosystem functions can AM fungal diversity support under various GCFs? We grewTriticum aestivum (wheat) in a controlled glasshouse experiment. Three AMF diversity treatments based on species richness: 0 (no-AMF), 1 (low diversity), and 4 (high diversity), and three GCF treatments: no GCF control, one of six GCF, and a combination of all six GCF were included. Each treatment combination allowed us to explore the interactive effects of AMF diversity and GCFs on ecosystem functions. We measured ten functions, including net photosynthetic rate, primary productivity, soil nutrient content, soil enzyme activity, and soil greenhouse gas emission to calculate multifunctionality (Garland et al., 2021), as we focused on short-term plant and soil functions. We hypothesized that the negative effect of multiple GCFs on multifunctionality would be lower under high AMF diversity treatment (Figure 1a).