Soil biodiversity and soil community composition determine ecosystem multifunctionality

Abstract

Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth's biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.

Keywords: ecology; global change; microbiome; soil degradation; symbiosis.

Fig. 1.

Change in soil community characteristics in grassland communities with increasing simplification of soil communities, according to size. Soil communities were established by filtering through different meshes: 1 ≤5,000 μm, 2 ≤250 μm, 3 ≤50 μm, 4 ≤25 μm, 5 ≤10 μm, and 6 sterilized soil. These measures reflect both abundance (nematodes, mycorrhizal colonization of plant roots, and microbial biomass) and richness (bacteria and fungal richness) of various guilds of soil organisms. Means ± SEM are expressed as a ratio of the most complete soil treatment (soil community 1, dashed line), such that 0 represents no detection (raw data in SI Appendix, Figs. S1 and S2). Where no error bars are shown for mycorrhiza and nematodes they were not detected in any replicate. Lines highlight the general trend in changes in the soil community characteristics along the gradient. Soil community characteristics measured in both experiments are pooled.

Fig. 2.

Change in ecosystem functions in grassland communities along the continuum of increasingly simplified soil biotic communities. Means ± SEM of plant productivity (g), plant diversity (Shannon index), N turnover (shoot ∂¹⁵N), decomposition (%), C sequestration (soil ∂¹³C), N leaching (mg), P leaching (mg), and N₂O emissions (mg m⁻²) are expressed as a ratio of the most complete soil treatment (soil community 1, dashed line) such that values below 1 represent a reduction, and values above 1 indicate an increase in the ecosystem function (raw data in SI Appendix, Fig. S5). Lines highlight trends in the changes in ecosystem functions across the gradient. Ecosystem functions measured in both experiments are pooled (Results of the individual experiments are given in SI Appendix, Figs. S6–S8 and Table S1). Soil communities are based on organism size as described in Fig. 1.

Fig. 3.

Ecosystem multifunctionality index in relation to the soil biodiversity index. Lightly shaded points represent grassland communities in experiment 1, and darkly shaded points indicate grassland communities in experiment 2. The overall regression is shown pooled for both trials because there was no difference between trials in the overall relationship between the soil biodiversity (the combined measures shown in Fig. 1) and ecosystem multifunctionality (the combined ecosystem functions shown in Fig. 2). The relationship of individual ecosystem functions to the soil biodiversity score is shown in SI Appendix, Fig. S6, and changes in the two indices across the gradient of soil communities are shown in SI Appendix, Fig. S7.