Periodic Cicada Mass Mortality Events Drive Microbial-Mediated Gas Pulses from Forest Soils

Mass emergence of periodic cicadas (Magicicada spp.) represents a unique ecosystem disturbance with potential impacts on forest soil biogeochemistry and greenhouse gas emissions. During the 2021 Brood X emergence in Indiana, USA, we investigated how cicada emergence and subsequent decomposition affected soil microbial communities and their production of nitrous oxide (N₂O) and ammonia (NH₃). Using a combination of field measurements and controlled laboratory experiments, we discovered that the interface between cicada carcasses and soil surfaces creates hotspots of enhanced microbial nutrient cycling, leading to significant pulses of N₂O and NH₃ after approximately 10-15 days. Our study revealed that dissimilatory nitrate reduction to ammonia (DNRA) was the primary mechanism driving these emissions, evidenced by increased abundance of DNRA taxa on cicada carcass surfaces (the necrobiome) coinciding with peak gas fluxes. Notably, the abundance of Serratia marcescens, a bacteria capable of both chitin degradation and DNRA, was significantly positively associated with N₂O pulses. Analysis of 16S rRNA amplicon sequencing data showed distinct microbial community compositions between soil and cicada necrobiome samples, with significantly higher abundances of chitinolytic and DNRA taxa in the necrobiome. Time series decomposition experiments demonstrated that soil respiration rates and nitrogen cycling were significantly enhanced in cicada-amended soils. Quantitative PCR revealed that bacterial ammonia oxidisers dominated over archaeal counterparts in soil samples, while the cicada necrobiome was characterised by high abundances of heterotrophic nitrifiers. The emergence tunnels created by cicadas also influenced soil conditions, potentially creating microsites that favour DNRA over conventional denitrification. While individual emergence events may contribute relatively small amounts of nitrogen compared to annual atmospheric deposition, the predictable nature and geographic extent of cicada emergences suggest they may represent an overlooked yet significant contributor to forest nitrogen cycling and greenhouse gas emissions. Our findings provide new insights into the complex microbiological mechanisms driving biogeochemical pulses following mass mortality events and highlight the need to consider periodic ecosystem disturbances in climate change models.