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Climate warming drives vole population collapse by amplifying flea infestation and its physiological costs

Wang, Zhenxu12; Shang, Meng1; Ji, Haoqiang1; Li, Ke3; Wang, Lu4; Guo, Chenran5; Xu, Lei6; Bai, Defeng7; Sun, Yelin1; Liu, Qiyong1

Published Nov 06, 2026 on Dryad. https://doi.org/10.5061/dryad.1rn8pk161

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Abstract

Climate warming is restructuring species interactions, yet its cascading effects through host-parasite systems to entire ecosystems are poorly understood. To predict demographic outcomes and identify responsible mechanisms, we need to establish how warming affects individual physiology and population traits, and how these scale to vegetation dynamics. Integrated, long-term studies dissecting this climate-parasite-host-vegetation pathway are therefore critical but rare.

Here, we test how climate warming affects the interaction between Brandt’s voles (Lasiopodomys brandtii) and their flea parasites, and its consequences for grassland vegetation. We relate a decade of field monitoring data on vole and flea populations to climatic variables, and combine semi-natural enclosure experiments, individual-level controlled laboratory infestation trials, and transcriptomic profiling to isolate causal mechanisms under both field and laboratory conditions.

We show that warmer temperatures significantly intensified flea infestation on voles (ecosystem scale, long-term field monitoring). This increased parasitism led to severe demographic suppression of vole populations, characterized by reduced survival and reproduction (ecosystem and population scale). This parasite-mediated suppression of the dominant herbivore indirectly enhanced grassland vegetation productivity (ecosystem scale, long-term field monitoring). Furthermore, controlled warming synergistically exacerbated the detrimental effects of flea infestation on host survival and reproduction (population scale, semi-natural enclosure experiments).

Results suggest that flea infestation impairs vole fitness through load-dependent physiological costs, including reduced growth and food intake, altered gut microbiota, and disrupted energy allocation and immune-related gene expression (e.g., in protein turnover and IgA production pathways) (individual level, controlled laboratory trials). This establishes that climate warming amplifies the burden of parasitism through interconnected ecological and molecular mechanisms, ultimately restructuring grassland ecosystems (cross-scale synthesis). Our findings highlight a complex climate-parasite-host-vegetation pathway with implications for managing ecosystem health under climate change (cross-scale synthesis).