Intensive tropical land use massively shifts soil fungal communities

Abstract

Soil fungi are key players in nutrient cycles as decomposers, mutualists and pathogens, but the impact of tropical rain forest transformation into rubber or oil palm plantations on fungal community structures and their ecological functions are unknown. We hypothesized that increasing land use intensity and habitat loss due to the replacement of the hyperdiverse forest flora by nonendemic cash crops drives a drastic loss of diversity of soil fungal taxa and impairs the ecological soil functions. Unexpectedly, rain forest conversion was not associated with strong diversity loss but with massive shifts in soil fungal community composition. Fungal communities clustered according to land use system and loss of plant species. Network analysis revealed characteristic fungal genera significantly associated with different land use systems. Shifts in soil fungal community structure were particularly distinct among different trophic groups, with substantial decreases in symbiotrophic fungi and increases in saprotrophic and pathotrophic fungi in oil palm and rubber plantations in comparison with rain forests. In conclusion, conversion of rain forests and current land use systems restructure soil fungal communities towards enhanced pathogen pressure and, thus, threaten ecosystem health functions.

Figure 1

Nonmetric multidimensional scaling (NMDS) of fungal OTU communities. Three samples per plot were rarified to 1229 sequences and pooled. Significant correlations of biotic and abiotic variables with fungal communities are shown by black arrows (p ≤ 0.05). Sizes of symbols (squares and circles) correspond to the number of OTUs found in each plot, with a minimum of 172 OTUs and a maximum of 468 OTUs. Data for plant species and plant biomass were taken from Drescher et al., 2015.

Figure 2

Relative abundance of symbiotrophic, pathotrophic, saprotrophic and unknown fungi in four land use systems. Box-and-whisker plots indicate the range of the data; the horizontal lines, the median; and the dots, outliers. Generalized linear mixed effect models were fit, and post hoc (Tukey’s) tests revealed significant differences at p ≤ 0.05. Significant differences are indicated by different letters (p ≤ 0.05, n = 30).

Figure 3

Fungal community composition on order level based on relative abundances separated by landscape and land use system. Orders with lower abundance than 1% in any land use system were summarized as artificial group “Rare taxa”.

Figure 4

Association network of significantly abundant soil fungi in different land use systems (multipatt function in indicspecies package in R, de Cáceres et al., 2010). Node sizes represent the average relative abundance of OTUs in the data sets. Edges represent the association patterns of individual OTUs with the land use systems, and their lengths show the weight of the associations (edge-weighted, spring-embedded layout). The association strength of significant genera is indicated by different edge lengths varying between 0.09 and 0.79.