Rapid climate warming is 'greening' the tundra, reflecting a higher plant biomass, particularly of deciduous shrubs and grasses. However, the consequences of these changes for herbivore nutrition are unclear. Although, the gut microbiome mediates nutrient metabolism, and hence herbivores' capacity to adapt to dietary change, few studies have investigated the effect of annual changes in the diet-gut microbiome nexus on fitness-related traits. In a model system, the Svalbard reindeer, a species experiencing the greatest rate of climate warming on Earth, we investigate how changes in diet and the gut microbiome impact reindeer body mass. Using high-resolution DNA metabarcoding, we assessed diet and gut microbiome bacterial composition in rumen samples from animals culled in October from 1998 to 2004 in four different valleys. Overall diet diversity and grass relative reads abundance (RRA) were significantly higher following warmer summers, while the RRA of the dwarf shrub Salix polaris increased with the maximum normalised difference vegetation index (NDVI), our measure of annual biomass. Autumn body mass, a strong proxy of fitness in Svalbard reindeer, was significantly, positively correlated with Salix RRA, most pronounced in females that had reproduced, and by that depleted body reserves. Multivariate analyses revealed a highly significant relationship between diet and microbiome composition at the individual level. This included a significant positive correlation between Salix and bacterial diversity. However, a structural equation model revealed that the direct path effect of Salix on reindeer body mass was stronger than the indirect path effect, mediated through the gut microbiome. Our results suggest that climate-driven Arctic greening may have implications for herbivore body mass, operating through a change in diet composition. These findings reveal some of the mechanistic underpinnings of Arctic warming on herbivore populations and highlight the importance of the diet-gut microbiome nexus in facilitating species resilience to rapid climate change.
