Analysis of complex trophic networks reveals the signature of land-use intensification on soil communities in agroecosystems

Juliette M G Bloor,Pierre Taberlet,Sara Si-Moussi,Mickaël Hedde,Pascal Carrère

doi:10.1038/s41598-021-97300-9

Abstract

Increasing evidence suggests that agricultural intensification is a threat to many groups of soil biota, but how the impacts of land-use intensity on soil organisms translate into changes in comprehensive soil interaction networks remains unclear. Here for the first time, we use environmental DNA to examine total soil multi-trophic diversity and food web structure for temperate agroecosystems along a gradient of land-use intensity. We tested for response patterns in key properties of the soil food webs in sixteen fields ranging from arable crops to grazed permanent grasslands as part of a long-term management experiment. We found that agricultural intensification drives reductions in trophic group diversity, although taxa richness remained unchanged. Intensification generally reduced the complexity and connectance of soil interaction networks and induced consistent changes in energy pathways, but the magnitude of management-induced changes depended on the variable considered. Average path length (an indicator of food web redundancy and resilience) did not respond to our management intensity gradient. Moreover, turnover of network structure showed little response to increasing management intensity. Our data demonstrates the importance of considering different facets of trophic networks for a clearer understanding of agriculture-biodiversity relationships, with implications for nature-based solutions and sustainable agriculture.

Highlights

Increasing evidence suggests that agricultural intensification is a threat to many groups of soil biota, but how the impacts of land-use intensity on soil organisms translate into changes in comprehensive soil interaction networks remains unclear
Our study of complex soil food webs generated by Environmental DNA (eDNA) metabarcoding in 16 agricultural fields along a broad land use intensity (LUI) gradient resulted in three major findings: (1) trophic interaction networks show a range of consistent qualitative responses to agricultural intensification; (2) soil network complexity is more sensitive to agricultural intensification than network size; (3) local assemblages show stronger statistical relationships with agricultural intensification than does composition turnover (β-diversity)
Our results indicate that agricultural intensification has profound impacts on trophic interactions and soil trophic network structure, driving decreases in trophic group diversity and complexity of interactions

Summary

Introduction

Increasing evidence suggests that agricultural intensification is a threat to many groups of soil biota, but how the impacts of land-use intensity on soil organisms translate into changes in comprehensive soil interaction networks remains unclear. Increased inorganic nitrogen inputs and organic matter with a low C:N ratio are commonly reported to reduce the fungal:bacteria ratio in intensively-managed agroecosystems[10,16] Such responses to agricultural intensification at the species- or functional group-level can have implications for soil food web structure and trophic networks by modifying trophic resource availability, and the potential for trophic interactions and the prevalence of highly-connected taxa. Given that loss of interactions among species may supersede the effects of species loss within trophic groups on ecosystem f unction[20], there is a pressing need for data on the responses of complex soil interaction networks to land-use intensification. EDNA metabarcoding has clear potential to provide novel insights into the drivers of changes in soil biotic communities, this methodology has rarely been tested in the context of agricultural intensification[29]

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Results

Discussion

Conclusion