Colony-level food storage and microbial predigestion shape nutrient acquisition in the termite Velocitermes heteropterus (Isoptera: Termitidae)

In social insects, nutrient acquisition can emerge from the integration of processes operating at both individual and colony levels. We hypothesize that food storage in termite mounds enables microbial predigestion of plant material, thereby enhancing nutrient acquisition at the colony level. Here, we investigate how food storage and associated microbial communities contribute to nutrient processing in the Neotropical mound-building termite Velocitermes heteropterus. We analyzed nest architecture, carbon and nitrogen content of stored food, gut contents, and the taxonomic and functional profiles of microbial communities associated with termite guts and nest substrates. The mounds exhibited a conical shape with a sponge-like internal structure in which dry grass fragments were stored. Satellite nests connected to larger mounds suggest a polydomous organization that may facilitate spatial resource allocation. Stored food displayed significantly higher C: N ratios than senescent plant material, indicating modification of nutrient stoichiometry prior to ingestion. Microbial communities differed markedly between nest substrates and termite guts. The nest-associated microbiota was enriched in Proteobacteria and Actinobacteria and showed a higher predicted abundance of functions associated with hemicellulose degradation, particularly xylanases. In contrast, the gut microbiota was associated with cellulolytic and starch-degrading functions. Microscopic analyses revealed plant fragments and fungal propagules in both workers and soldiers. Together, these findings indicate that food storage mediates a functional separation between external microbial predigestion and internal gut digestion, forming an integrated system that enhances nutrient acquisition from recalcitrant grass substrates.