In response to the escalating challenges presented by climate change, specifically the increased intermittency of river flows, this study suggests the impact on benthic communities. This investigation commenced with a multidimensional biodiversity analysis of biofilms and assessments of ecosystem multifunctionality. Employing partial least squares path modelling, the research explored the intrinsic relationships between biodiversity, ecosystem stability, community assembly, and ecosystem multifunctionality (BE-Mf and CA-Mf relationship). The results provide evidence regarding the relationship between biodiversity and multifunctionality in intermittent streams, considering both the non-flow period and the recovery period.
In conclusion, the observed shifts in microbial communities could precipitate substantial changes in ecosystem processes and services, accentuating the need to preserve microbial diversity and functionality to ensure ecosystem robustness amid climate variability. These findings illuminate the complex interplay between biodiversity and ecosystem functionality in intermittent streams across both drying and recovery phases.
4.1 Thecritical period for rivers to dry up of biofilm biodiversity and multifunctionality
Consistent with the cluster analysis of biofilm functions and the result of the PLS-DA from multifunctionality, there was also a critical period for rivers to dry up at around 60 days for biofilm community stability and community assembly (Figs. 1–3), which may have been induced by the temporary transformation of aquatic ecosystems into terrestrial systems after 3 months of drying2. The phosphorus cycle of biofilm showed higher drought resistance than the carbon and nitrogen cycles (Fig. 2b), likely because biofilm always uses phosphorus preferentially to generate energy during the recovery phase after drying52, reflecting the importance of phosphorus as a key element of microbial metabolism during rewetting53. In contrast, the carbon and nitrogen cycles of the biofilm could not maintain the same activity with control during the rewetting period after a prolonged drought, likely because the prolonged drought led to the change of redox conditions in the biofilm habitat5. Based on the correlative nature of the individual functions54, biofilm multifunctionality was more sensitive to increasing drought than single function (Fig. 2), reflecting the similar underlying processes to increasing drought43. The significant difference in multifunctionality before and after 60 days of drought may have been caused by the temporary transformation of aquatic ecosystems into terrestrial systems, which leads to a significant change in resource availability and turnover efficiency of biofilm2.
The same critical time point of the impact of the duration of river drying on river ecosystems was also observed in the fitting result of the neutral community model (Fig. 3a), and the increasing dominance of stochasticity perhaps resulted from the stimulation from the hydrological change perturbations to stochastic factors 37,55. Although previous studies have suggested that decreasing community diversity may lead to the dominance of deterministic processes in community assembly 56, this is true only at saturated community sizes57. However, in small community sizes, such as biofilm, communities are more susceptible to stochasticity with decreasing diversity58,59, especially under the environmental stimuli of such variable hydrological conditions in IRES55 (Figure S8). Of the stochastic influence, “undominated” (meaning that dispersal and drift contribute equally to community composition)60 was the major factor for community assembly mechanisms of all components of biofilms (Fig. 3b-d), and it was especially significant for fungi. This might be due to unmeasured ecological processes, such as species competition for similar resources, that may exert a more substantial influence in a low heterogeneous environment and beta diversity (Table S2)56,61. The varied influence of dispersal limitation on different components of biofilms may be related to their different survival strategies, as the relative abundance of the microbial community could be the major factor influencing dispersal limitation62,63. The stronger influence of dispersal limitation on bacteria has also been reported by Oono, et al. 64. Prolonged droughts reduce microbial heterogeneity, diminishing ecosystem resilience by rendering microbial communities less equipped to face environmental adversities65. This homogenization disrupts the efficient cycling of key nutrients such as carbon, nitrogen, and phosphorus—elements critical for ecosystem productivity and health. Such disruptions may impair vital ecosystem services, including soil fertility, water purification, and greenhouse gas regulation66,67.
Given the important effect of diversity 68, such as beta-diversity and ecological networks, the growing theoretical and empirical evidence suggests that the mechanisms driving spatial variation in diversity to the in-depth study of the biodiversity-ecosystem functions (BEF) relationship are of high theoretical importance69. Apart from the decreased microbial alpha diversity with increasing drought (Figure S4-S6), the reduction in beta-diversity (Bray–Curtis dissimilarity between groups) with prolonged drought durations indicated that extended drought periods contributed to decreased microbial community heterogeneity (Table S2), which could substantially impact biofilm functions through the “insurance effects” of beta-diversity in varying environments (enabling the dispersal of species with different physiological responses as conditions change)70. Specifically, reduced microbial diversity could jeopardize soil carbon sequestration, potentially escalating atmospheric CO2 concentrations and impacting global climate patterns71.
Furthermore, the consistent response of the biofilm network modularity of the different components indicated different microbial communities rescaled to form a complex network of interactions following drought disturbance72. In this study, the bacterial and algal network’s response mechanism to increasing drought stress reflected a tight and complex network structure34, with a critical period of 60 days for rivers to dry up. The response of the fungal network was the opposite (Fig. 3e and f), which might be due to the higher environmental adaptation for fungi under extreme conditions73, especially under the more impaired conditions of bacterial and algal communities74,75.
Moreover, microbes constitute essential resources for various organisms, including protozoa, small invertebrates, and filter feeders. Changes in microbial community composition and functionality can alter the availability and nutritional quality of microbial biomass, affecting consumer growth, reproduction, and survival. These alterations may lead to disrupted trophic interactions and reduced biodiversity within food webs76,77. The stability and resilience of these food webs are intrinsically linked to the diversity and functional capacity of their microbial components78. Microbial communities that exhibit limited functional diversity are ill-prepared for environmental changes, which can compromise the resilience of the entire ecosystem79. This decreased adaptability may impair the ecosystem's ability to recover from disturbances, resulting in long-term shifts in community structure and function across all trophic levels, ultimately undermining ecosystem health and stability11,79,80.Considering that biofilm function sustainability depended on a relatively stable microbiome25, community stability was evaluated during rewetting after different drought times. There was also a critical time point of river drying at 60 days for eukaryotic microbial community stability, corresponding to biofilm functions and confirming the community stability's critical effect on biofilm function81. Meanwhile, bacteria were more resistant to increasing drought, likely due to its most complex network or resistant phenotypes such as spore formation 82.
4.2 The relationship between biodiversity and ecosystem functions decoupled after long-term droughts
Two possible explanations exist for the decoupling between biodiversity and ecosystem functions after prolonged drought (Fig. 4). The first facet to consider is functional plasticity, defined as the ability of microbial communities to adapt to environmental fluctuations by fine-tuning their performance75. For example, BGLU, NOS, LAP, AMO and NAR tended to adapt to environmental changes (increase followed by decrease or a decrease followed by the rise with increasing drought duration) (Fig. 2a). While analysed from the perspective of elemental metabolic cycling, the elemental metabolic cycling functions of the biofilm differed significantly before and after the critical period for rivers to dry up (60 days of drought) (Fig. 2b). This was especially true for the carbon and nitrogen element metabolic functions (Fig. 2b), indicating that functional plasticity is not the only explanation for this decoupling. So, functional redundancy might also contribute to the results that some metabolic functions of biofilms could be maintained at a certain level when the biofilm diversity had been irreversibly affected by a prolonged drought, even though they may have behaved differently for a single function83. Moreover, microbial species adapt to environmental change by generating a trade-off between environmental filtering and disposal limitation84, which could explain the strong links between biodiversity and community assembly (Fig. 4).
4.3 Community assembly is more important for ecosystem multifunctionality than biodiversity in IRES
The environment selects microbial functional traits rather than species to maintain essential ecosystem functions85, which is why community assembly contributed more to biofilm ecosystem functions than biodiversity after long-term droughts (Fig. 4 and Fig. 5). The significant effect of community assembly on biofilm ecosystem functions shifted to the phosphorus cycle from the nitrogen cycle, which could be because the phosphorus cycle was more susceptible to being filtered by environmental conditions86 (Fig. 4). Notably, the relationship between biofilm multifunctionality and different factors changed from a negative to a positive correlation following prolonged drought (Fig. 5), indicating that coexisting species, following niche partitioning based on various resources, could positively interact and further improve community functional performance14. Based on the high relativity between more minor environmental variations and higher microbial phylogenetic diversity25, there was a relatively significant positive effect between biofilm biodiversity and community stability (Fig. 5). After long-term drought, the narrow distribution of community functional groups and the depleting redundancy of biofilm functions may have weakened the relationship between biofilm biodiversity and community stability87.
4.4 Limitations and environmental implications
The results highlight that community assembly has a more significant influence on biofilm multifunctionality than biodiversity and that their relative influences vary with increasing drought. Understanding the relationship between community assembly and microbial functions is at the forefront of current ecological research88,89. Yet, this paradigm has not been broadly studied in river ecosystems. In this study, we examined the impact of different drought times on the B-EMf and CA-Mf relationship through indoor simulation experiments. Nevertheless, it is essential to acknowledge that the controlled trials conducted might potentially restrict the extensive extrapolation of our findings, considering the heterogeneous environmental composition in natural IRES. For example, the dynamics of critical variables, including light, temperature, and organic matter within natural river ecosystems, might coincide with dry-to-wet transitions and affect the extent and nature of biofilm responses47. More rigorous tests and further field experiments on the generality of this result in different ecosystems are needed for consideration as a fundamental principle of microbial ecology.
Based on this study, increasingly refined insights have been gained into the critical period for rivers to dry up of biofilm multifunctionality and the vital contribution of community assembly in driving it. Initially, the study observed the critical period for rivers to dry up in biofilm functions and community structure (network, community stability, and community assembly), while the applicability of the critical period for rivers to dry up studies for global nature conservation and policy remains somewhat limited90. Addressing the identified research gaps will progressively enhance the future policy relevance of critical periods for rivers to dry up. Implementing timely flow replenishment before reaching the critical period for rivers to dry up is likely the most essential and effective strategy. Additionally, biodiversity decoupled from ecosystem functions after long-term drought disturbances, meaning further work to identify the main drivers of ecosystem functions will be critical for ultimately predicting the response of community functions to environmental changes. More importantly, the increasing prominence of stochastic processes becomes more pronounced with longer drought durations, and community assembly is more important for ecosystem multifunctionality than biodiversity.
This study provides an inaugural demonstration of the dominant role of stochastic assembly in shaping community structure and ecosystem multifunctionality. Elucidating the intricate connections among community assembly, biodiversity, and ecosystem functioning is critical for preserving biodiversity and effectively managing ecosystems.