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).