Abstract

Interactions between leaf-cutting ants, their fungal symbiont (Leucoagaricus) and the endophytic fungi within the vegetation they carry into their colonies are still poorly understood. If endophytes antagonistic to Leucoagaricus were found in plant material being carried by these ants, then this might indicate a potential mechanism for plants to defend themselves from leaf-cutter attack. In addition, it could offer possibilities for the management of these important Neotropical pests. Here, we show that, for Atta sexdens rubropilosa, there was a significantly greater incidence of Trichoderma species in the vegetation removed from the nests—and deposited around the entrances—than in that being transported into the nests. In a no-choice test, Trichoderma-infested rice was taken into the nest, with deleterious effects on both the fungal gardens and ant survival. The endophytic ability of selected strains of Trichoderma was also confirmed, following their inoculation and subsequent reisolation from seedlings of eucalyptus. These results indicate that endophytic fungi which pose a threat to ant fungal gardens through their antagonistic traits, such as Trichoderma, have the potential to act as bodyguards of their plant hosts and thus might be employed in a Trojan-horse strategy to mitigate the negative impact of leaf-cutting ants in both agriculture and silviculture in the Neotropics. We posit that the ants would detect and evict such ‘malign’ endophytes—artificially inoculated into vulnerable crops—during the quality-control process within the nest, and, moreover, that the foraging ants may then be deterred from further harvesting of ‘Trichoderma-enriched’ plants.

Highlights

  • Symbiotic fungi play a vital role in plant communities

  • The endophytic ability of selected strains of Trichoderma was confirmed, following their inoculation and subsequent reisolation from seedlings of eucalyptus. These results indicate that endophytic fungi which pose a threat to ant fungal gardens through their antagonistic traits, such as Trichoderma, have the potential to act as bodyguards of their plant hosts and might be employed in a Trojanhorse strategy to mitigate the negative impact of leaf-cutting ants in both agriculture and silviculture in the Neotropics

  • A second example of symbiosis is that between leaf-cutting ants and the basidiomycete fungus Leucoagaricus (Agaricales: Agaricaceae), in which the ants cultivate the fungus in subterranean gardens and harvest the nutrient-rich vegetative bodies produced by the fungus: a process that has been likened to human agriculture and which evolved around 8–12 Ma [8,9]

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Summary

Introduction

Symbiotic fungi play a vital role in plant communities. This is well known from mycorrhizal associations which directly influence plant diversity, ecosystem variability and productivity [1,2], as well as plant immunity [3]. The issue of leaf-cutting ants as pests is salient as products based on the insecticides sulfluramid and fipronil are currently being phased out from certified usage [21], so there is an urgency to the need for research into understanding these insects and providing alternative means of control. In this context, microbial biological control is a possibility, requiring itself an understanding of how leaf-cutting ants interact with microorganisms

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