Alteration of the tree–soil microbial system triggers a feedback loop that boosts holm oak decline

Abstract

In anthropic savanna ecosystems from the Iberian Peninsula (i.e. dehesa), complex interactions between climate change, pathogen outbreaks and human land use are presumed to be behind the observed increase in holm oak decline. These environmental disturbances alter the plant–soil microbial continuum, which can destabilize the ecological balance that sustains tree health. Yet, little is known about the underlying mechanisms, particularly the directions and nature of the causal–effect relationships between plants and soil microbial communities. In this study, we aimed to determine the role of plant–soil feedbacks in climate-induced holm oak decline in the Iberian dehesa. Using a gradient of holm oak health, we reconstructed key soil biogeochemical cycles mediated by soil microbial communities. We used quantitative microbial element cycling (QMEC), a functional gene-array-based high-throughput technique to assess microbial functional potential in carbon, nitrogen, phosphorus and sulphur cycling. The onset of holm oak decline was positively related to the increase in relative abundance of soil microbial functional genes associated with denitrification and phosphorus mineralization (i.e. nirS3, ppx and pqqC; parameter value: 0.21, 0.23 and 0.4; p < 0.05). Structural equation model (χ2 = 32.26, p-value = 0.73), moreover, showed a negative association between these functional genes and soil nutrient availability (i.e. mainly mineral nitrogen and phosphate). Particularly, the holm oak crown health was mainly determined by the abundance of phosphate (parameter value = 0.27; p-value < 0.05) and organic phosphorus (parameter value = −0.37; p-value < 0.5). Hence, we propose a potential tree–soil feedback loop, in which the decline of holm oak promotes changes in the soil environment that triggers changes in key microbial-mediated metabolic pathways related to the net loss of soil nitrogen and phosphorus mineral forms. The shortage of essential nutrients, in turn, affects the ability of the trees to withstand the environmental stressors to which they are exposed. Read the free Plain Language Summary for this article on the Journal blog. © 2023 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.