Learning through the waste: olfactory cues from the colony refuse influence plant preferences in foraging leaf-cutting ants

Abstract

Leaf-cutting ants learn to avoid plants initially harvested if they prove to be harmful for their symbiotic fungus once incorporated into the nest. At this point, waste particles removed from the fungus garden are likely to contain cues originating from both the unsuitable plant and the damaged fungus. We investigated whether leaf-cutting ant foragers learn to avoid unsuitable plants solely through the colony waste. We fed subcolonies of Acromymex ambiguus privet leaves treated with a fungicide undetectable to the ants, then collected the produced waste, and placed it into the fungus chamber of naive subcolonies. In individual choice tests, naive foragers preferred privet leaves before waste was put into the fungus chamber, but avoided them afterwards. Evidence on the influence of olfactory cues from the waste on decision making by foragers was obtained by scenting and transferring waste particles from subcolonies that had been fed either fungicide-treated or untreated leaves. In choice experiments, foragers from subcolonies given scented waste originating from fungicidetreated leaves collected fewer sugared paper discs with that scent compared with foragers from subcolonies given scented waste from untreated leaves. The results indicate that foragers learn to avoid plants unsuitable for the fungus by associating plant odours and cues from the damaged fungus that are present in waste particles. It is argued that waste particles may contribute to spread information about noxious plants for the fungus within the colony.

Avoidance of plants unsuitable for the symbiotic fungus in leaf-cutting ants: Learning can take place entirely at the colony dump

“…In addition, changes in the fungus garden that induced plant avoidance can only be detected by workers for a relatively short time (1–2 days; [22], suggesting that avoidance cues learned by the ants are no longer noticeable in the fungus garden after this period. Although we could not rule out that waste particles originating from treated leaves could still have been disposed of after the exchange of the waste chambers, thus appearing in the recently-exchanged waste chamber of treated subcolonies at T2, previous evidence suggests that the disposal of waste particles in the dump is considerably reduced after 36 h [36]. At T2, decisions made by an average of 26.85 ± 1.63 foragers per subcolony were recorded.…”

“…It is reasonable to think that soon after the ants recognize that the fungus is growing on an unsuitable plant, they remove the garden as waste. We have recently demonstrated that waste particles newly removed from the garden contain cues that enable plant recognition and cues or signals that resemble the impairment of the fungus [36]. In particular, we observed that volatiles of the waste mediated the identification of unsuitable host plants.…”

“…The effect of the exchange of waste chambers on individual foraging preferences was tested 16 h later (at T2, on day 5; Fig 1). This time was chosen because recent evidence indicated that waste disposal increased between 16 h and up to 28 h after a colony is fed fungicide-treated leaves [36]. In addition, changes in the fungus garden that induced plant avoidance can only be detected by workers for a relatively short time (1–2 days; [22], suggesting that avoidance cues learned by the ants are no longer noticeable in the fungus garden after this period.…”

“…In addition, the duration of their visits was measured. We predicted a task shift from foragers to waste managers due to the increase in waste disposal after the offering of fungicide-treated leaves [36] and the resulting increase in task demands. Thus, we also scored the labeled ants that started performing waste-related tasks during their stays to calculate the proportion of foragers that switched to waste managers.…”

“…The transport, manipulation and spatial isolation of waste in a dump are thought to be adaptive responses aimed at reducing the spread of pathogens within the nest [32–35]. However, waste might also represent a source of information as it contains cues that enable recognition of the plant materials from which it originates [36]. We recently showed that naïve foragers learned to avoid plants unsuitable for the fungus even if they were not directly exposed to them or to their effects on the fungus.…”