Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity.

Mathilde Chomel,Franciska T De Vries,Elizabeth M Baggs,Mark C Emmerson,Jocelyn M Lavallee,Tancredi Caruso,Francisco De Castro,Nil Alvarez‐Segura,Richard D Bardgett,Jennifer M Rhymes,David Johnson

doi:10.1111/gcb.14754

Abstract

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below‐ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse‐labelled after the drought with 13C‐CO2 to quantify the capture of recent photosynthate and its transfer below‐ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below‐ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above‐ground–below‐ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Highlights

Drought events are a recurring phenomenon in many ecosystems and are predicted to increase in frequency and intensity in the coming decades (IPCC, 2017; Reichstein et al, 2013)
Warmer and drier conditions can affect decomposition mediated by trophic in‐ teractions (Lang, Rall, Scheu, & Brose, 2014; Thakur et al, 2018) or alter predator‐induced indirect effects on lower trophic levels (Lensing & Wise, 2006), implying that ecological effects of drought will depend on the trophic structure of the food web
Tukey comparison between trophic groups are indicated by different letters, a < b the relative amount of 13C exported from the plant shoots during these 3 days was greater under control compared to drought, with losses of 83 ± 1.19% and 75 ± 1.28% from the initial 13C amount respectively (F = 19.2, df = 1, n = 36, p < .001, Figure 3b, Table 1)

Summary

| INTRODUCTION

Drought events are a recurring phenomenon in many ecosystems and are predicted to increase in frequency and intensity in the coming decades (IPCC, 2017; Reichstein et al, 2013). Drought can have considerable effects on the composition and activity of soil microbial communities (de Vries et al, 2018; de Vries & Shade, 2013; Hawkes et al, 2011; Meisner, Deyn, Boer, & van der Putten, 2013), and structure, diversity and activity of soil arthropods (Bardgett & Wardle, 2010; Brose et al, 2012; Kardol, Reynolds, Norby, & Classen, 2011; Santonja et al, 2017; Siebert et al, 2019) These effects on soil organisms generally lead to re‐ ductions in ecosystem processes, including litter decomposition and nutrient mineralization (de Vries et al, 2013; Fuchslueger, Bahn, Fritz, Hasibeder, & Richter, 2014; Hagedorn et al, 2016; Santonja et al, 2017; Siebert et al, 2019). | 3551 decomposition due to the complementarity of organisms, leading to a higher nutrient availability in soil, and an increase of plant growth and C allocation below‐ground; (b) drought decreases plant photosynthesis and C allocation below‐ground, reducing the avail‐ ability of recently fixed plant C for soil organisms; and (c) soil food webs with fewer trophic groups will be less resistant to drought, leading to a stronger effect of the drought on soil functioning and soil fauna biomass

| MATERIALS AND METHODS

Findings

| DISCUSSION