Responses of rice paddy micro-food webs to elevated CO2 are modulated by nitrogen fertilization and crop cultivars

•N fertilizer and cultivar mediated the response of soil food webs to elevated CO2.•Structural equation model showed bottom-up control via root.•Responsive cultivar with higher yield was susceptible to root herbivores.•Energy channel shifted from bacteria-based to fungi-based along growth stages.

Elevated atmospheric CO2 concentrations (eCO2) often increase plant growth but simultaneously lead to the nitrogen (N) limitation in soil. The corresponding mitigation strategy such as supplementing N fertilizer and growing high-yielding cultivars at eCO2 would further modify soil ecosystem structure and function. Little attention has, however, been directed toward assessing the responses of soil food web. We report results from a long-term free air CO2 enrichment (FACE) experiment in a rice paddy agroecosystem that examined the responses of soil micro-food webs to eCO2 and exogenous nitrogen fertilization (eN) in the rhizosphere of two rice cultivars with distinctly weak and strong responses to eCO2. Soil micro-food web parameters, including microfauna (protists and nematodes) and soil microbes (bacteria and fungi from phospholipid fatty acid (PLFA) analysis), as well as soil C and N variables, were determined at the heading and ripening stages of rice. Results showed that eCO2 effects on soil micro-food webs depended strongly on N fertilization, rice cultivar and growth stage. eCO2 stimulated the fungal energy channel at the ripening stage, as evidenced by increases in fungal biomass (32%), fungi:bacteria ratio (18%) and the abundance of fungivorous nematodes (64%), mainly due to an enhanced carbon input. The eN fueled the bacterial energy channel by increasing the abundance of flagellates and bacterivorous nematodes, likely through alleviating the N-limitation of plants and rhizosphere under eCO2. While eCO2 decreased the abundance of herbivorous nematodes under the weak-responsive cultivar by 59% and 47% with eN at the heading and ripening stage, respectively, the numbers of herbivorous nematodes almost tripled (×2.9; heading) and doubled (×1.6; ripening) under the strong-responsive cultivar with eCO2 at eN due to higher root quantity and quality. Structural equation model (SEM) showed that lower trophic-level organisms were affected by bottom-up forces of altered soil resources induced by eCO2 and eN, and effects on higher trophic level organisms were driven by bottom-up cascades with 69% of the variation being explained. Taken together, strategies to adapt climate change by growing high-yielding crop cultivars under eCO2 may face a trade-off by negative soil feedbacks through the accumulation of root-feeding crop pest species.

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