The Jarman-Bell principle revisited: Gut microbiota facilitate body size-dependent nutritional strategies in herbivores

贾曼-贝尔原理再探:肠道菌群促进草食动物根据体型调整营养策略

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Abstract

Body size is a key determinant of nutritional strategies in herbivores, yet the role of gut microbiota in mediating these strategies remains insufficiently explored. To address this gap, we examined two sympatric ungulates of contrasting body sizes in an arid ecosystem-red deer (Cervus elaphus, large-bodied) and goitered gazelle (Gazella subgutturosa, small-bodied)-to test three predictions derived from the Jarman-Bell principle (JBP). We applied dietary DNA metabarcoding, plant nutritional profiling, and 16S rRNA sequencing of gut microbiota to assess how body size shapes macronutrient intake, microbial composition, and functional adaptations. Both species exhibited similar macronutrient ratios dominated by carbohydrates (∼88-90 %), supporting the nutritional balancing hypothesis. However, they differed in nutrient targets and microbial profiles: red deer consumed more non-structural carbohydrates and fats, with enriched gut microbial taxa (Paludibacter, Turicibacter) linked to energy metabolism, reflecting an energy maximization strategy. In contrast, goitered gazelles ingested more crude protein and harbored microbial taxa (Prevotella) associated with protein digestion, alongside immune-supporting microbes (Butyricicoccus, Coprococcus, and Victivallis), consistent with a protein maximization strategy. Red deer also demonstrated a greater microbial capacity for fiber degradation (Fibrobacter, Ruminococcus albus) and detoxification of plant secondary metabolites (Clostridium, Desulfovibrio, Prevotella, Variovorax). Functional pathway analysis revealed enrichment in lignocellulose and terpenoid metabolism, indicating an adaptation to low-quality forage. In contrast, goitered gazelles showed limited microbial associations with fiber or phytotoxin regulation, suggesting weaker microbial-mediated adaptation to low-quality diets. These results demonstrate that body size governs distinct nutritional strategies in sympatric herbivores, mediated through differential gut microbiota composition and function. Larger species, such as red deer, exhibit enhanced microbial capacity for fiber and toxin regulation, allowing them to utilize lower-quality forage more efficiently.

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