Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

Optimized food acquisition is challenging because foraged diet items are chemically complex and often nutritionally imbalanced. These challenges are likely magnified when foraged foods are used to provision others (e.g., offspring, nestmates, symbionts) with different nutritional requirements. We used a theoretical framework of nutritional niches to study these provisioning challenges in leafcutter ants that cultivate a fungal symbiont with nutrients derived from freshly foraged plant fragments. While the leaf-cutting behaviours of free-ranging foragers are well studied, little is known about how colonies use these plant fragments to produce their fungal crop within underground nest chambers. For instance, gardener ants are known to convert vegetation into a nutritional mulch that they plant on the fungus garden. However, it remains poorly understood how the ants use this mulch to target the specific nutritional needs of their fungal crop, and whether the cultivar signals if provisioned mulch meets its nutritional needs. Towards answers, we performed three experiments to assess the precision and specificity of nutritional regulation in farming systems of the Panamanian leafcutter ant Acromyrmex echinatior. A laboratory feeding experiment with nutritionally defined diets showed that ant farmers collect a specific intake target for protein and carbohydrates and then linked strict protein regulation by foragers to the cultivar’s fundamental niche for protein. An in vitro experiment with the fungal cultivar in isolation did not detect a signal of protein stress that could be used by the ants to regulate their provisioning behaviour, but it did identify an elevated fatty acid that may reinforce optimal nutritional provisioning if detected by gardening ants. A feeding experiment with isotopically labelled diets then revealed nutrient-specific and caste-specific allocation timelines, with nitrogen being assimilated into the cultivar’s nutritional rewards before being exclusively consumed by developing brood. In turn, these combined results help resolve the integrated behaviours that give rise to resilient leafcutter farming productivity. These results show how nutritional niches can help disentangle reciprocal provisioning dynamics between symbionts while providing a framework to explore the nutritional transactions that mediate symbiotic stability (e.g., sanctioning, screening, policing).