Interacting symbioses: Leaf endophyte load and fungal garden development in leaf-cutting ants

Background/Question/Methods

Plants and insects host a wide diversity of symbiotic fungi, with some symbionts being essential to host survival. Previous studies have focused largely on the reciprocal costs and benefits within a particular host-symbiont pair, but have rarely investigated the multiple interactions among pairs of symbionts and their hosts. Because most organisms participate in symbioses, such symbiont-symbiont interactions must occur often but in a cryptic fashion. Our research focuses on the fungal-fungal interactions among two symbiotic pairs: (i) leaf-cutting ants and their symbiotic fungal gardens, and (ii) tropical plants and their foliar endophytes, the cryptic symbiotic fungi within their leaf tissue.  Previous work has shown that leaf-cutting ants prefer to cut leaf material that is relatively low in fungal endophyte content. Such a preference suggests that fungal endophytes exact a cost on the ants or on the development of their colonies.  It also suggests that endophytes may play a factor in their host plants’ defense against leaf-cutting ants. To measure the cost to the ant colony of fungal endophytes in their forage material, we conducted a 20-week laboratory experiment to measure fungal garden development for colonies that foraged on leaves with low and high endophyte content.  

Results/Conclusions

We found that the colony mass and the fungal garden dry mass did not differ significantly between the low and high endophyte feeding treatments. There was, however, a marginally significant trend toward greater mass of fungal garden per ant worker in the low relative to the high endophyte treatment. This trend was driven by differences in the fungal garden mass per worker in the earliest samples, when leaf-cutting ants had been foraging on low and high endophyte leaf material for only 2 weeks. At two weeks of foraging, the mean fungal garden mass per worker was 77% greater for colonies foraging on leaves with low relative to high endophyte loads.  Our data suggest that the cost of endophyte presence in ant forage material may be greatest to fungal colony development in its earliest stages, when there are few workers available to forage and to clean leaf material. This coincides with a period of high mortality for incipient colonies in the field. We discuss how the endophyte-leaf-cutter ant interaction may parallel constitutive defenses in plants, whereby endophytes reduce the rate of colony development when its risk of morality is greatest.