Avoiding plants unsuitable for the symbiotic fungus: learning and long-term memory in leaf-cutting ants

Leaf-cutting ants are polyphagous herbivores that, despite their catholicity, show distinct preferences in the substrate choice for their symbiotic fungus. We investigated to what extent avoidance learning and long-term memory for plant unsuitability underlie foraging responses in the field. First, the acceptability of 10 rarely harvested plant species was tested on field colonies located in two different habitats, where the tested plant species were either present or not. Colonies in the habitat where the plant species occurred avoided all species on first encounter, suggesting previous experience with them. Colonies without the plant species in their habitat, however, first accepted, but then avoided four of them when tested after 24 and 48 h. Such an avoidance response towards previously acceptable leaves could be experimentally induced by infiltrating acceptable leaves with a fungicide (cycloheximide) not detectable to the ants, but harmful to the symbiotic fungus, indicating that workers learn to reject plants that have detrimental effects on the fungus, but not on themselves. To determine how robust memory for plant unsuitability was, workers from field colonies were offered the previously avoided, yet untreated plant every 2 weeks, and its acceptance monitored in the long term. It took up to 18 weeks until foragers harvested the plant again, indicating the involvement of robust long-term avoidance learning in foragers. We argue that the harvesting pattern observed in field colonies largely depends on the workersʹ foraging experience, essential in a highly diverse environment where both leaf availability and quality vary throughout the year.