Contrasting Effects of Grazing in Shaping the Seasonal Trajectory of Foliar Fungal Endophyte Communities on Two Semiarid Grassland Species

Abstract

Fungal endophytes are harboured in the leaves of every individual plant host and contribute to plant health, leaf senescence, and early decomposition. In grasslands, fungal endophytes and their hosts often coexist with large herbivores. However, the influence of grazing by large herbivores on foliar fungal endophyte communities remains largely unexplored. We conducted a long-term (18 yr) grazing experiment to explore the effects of grazing on the community composition and diversity of the foliar fungal endophytes of two perennial grassland species (i.e., Artemisia capillaris and Stipa bungeana) across one growing season. Grazing significantly increased the mean fungal alpha diversity of A. capillaris in the early season. In contrast, grazing significantly reduced the mean fungal alpha diversity of endophytic fungi of S. bungeana in the late season. Grazing, growing season, and their interactions concurrently structured the community composition of the foliar fungal endophytes of both plant species. However, growing season consistently outperformed grazing and environmental factors in shaping the community composition and diversity of both plant species. Overall, our findings demonstrate that the foliar endophytic fungal community diversity and composition differed in response to grazing between A. capillaris and S. bungeana during one growing season. The focus on this difference will enhance our understanding of grazing's impact on ecological systems and improve land management practices in grazing regions. This variation in the effects of leaf nutrients and plant community characteristics on foliar endophytic fungal community diversity and composition may have a pronounced impact on plant health and plant-fungal interactions.

Keywords: foliar endophytic fungal community; grassland; grazing; plant community characteristic; plant nutrient; seasonal trajectory.

Figure 1

Effects of grazing treatment on foliar fungal endophyte diversity of Artemisia capillaris (A) and Stipa bungeana (B) in the early, middle, and late growing seasons. The large circles represent the mean values, and the error bars represent standard errors. The small circles represent raw data points (n = 6). Within each panel, different lowercase letters indicate significant differences between treatments at p < 0.05 (Tukey’s HSD).

Figure 2

Responses of community composition of foliar fungal endophyte of Artemisia capillaris (A,B) and Stipa bungeana (C,D) to grazing treatment during growing season (early, middle, and late). G, grazed; CK, control. Visualization is based on principal coordinate analysis using Bray–Curtis metrics at the ASV level. The effects of grazing treatment, growing season, and their interactions on fungal community composition were assessed using permutational multivariate analysis of variance (***, p < 0.001). Stacked bar plots indicate the relative abundance (%) of foliar fungal classes of Artemisia capillaris (B) and Stipa bungeana (D) as affected by grazing treatment during growing season. The symbols ‘+’ and ‘−’ indicate a significant (p < 0.05) increase and decrease, respectively, in response to grazing based on a linear mixed-effect model.

Figure 3

Variable importance of experimental factors, leaf nutrients, defensive chemicals, and plant community characteristics for the ENSPIE of (A) Artemisia capillaris and (B) Stipa bungeana. The importance values are derived from a model-averaged analysis including variables as moderators in the model. The asterisks (*) indicate significant (p < 0.05) moderators. Red line indicates the variable importance of 0.8.

Figure 4

Amount of the variation (R²) in fungal endophyte communities in leaves of (A) Artemisia capillaris and (B) Stipa bungeana accounted for by experimental factors, leaf nutrients, defensive chemicals, and plant community characteristics. Results are from a PERMANOVA using Bray–Curtis distance and 999 permutations of the data. R² is ranked in descending order.