Many organisms participate in symbiotic relationships with other organisms, yet studies of symbioses typically have focused on the reciprocal costs and benefits within a particular host-symbiont pair. Recent studies indicate that many ecological interactions involve alliances of symbionts acting together as mutualistic consortia against other consortia. Such interacting consortia are likely to be widespread in nature, even if the interactions often occur in a cryptic fashion. Little theory and empirical data exist concerning how these complex interactions shape ecological outcomes in nature. Here, we review recent work on fungal-fungal interactions between two consortia: (i) leaf-cutting ants and their symbiotic fungi (the latter grown as a food crop by the former) and (ii) tropical plants and their foliar endophytes (the cryptic symbiotic fungi within leaves of the former). Plant characteristics (e.g., secondary compounds or leaf physical properties of leaves) are involved in leaf-cutting ant preferences, and a synthesis of published information suggests that these plant traits could be modified by fungal presence. We discuss potential mechanisms for how fungal-fungal interactions proceed in the leaf-cutting ant agriculture and suggest themes for future research.
AbstractGrowth of the food fungus of the leaf-cutting ant Atta cephalotes (L.) on extracts of plants selected by the ants was shown to be affected by the plant species, the pH of the extract, the concentration of the sap or plant extract and pretreatment of the substrate by the ants. It was not possible to establish an unambiguous relationship between the rate of growth of the fungus on leaf extracts and the foraging preferences of the ants for the leaves. There were indications, however, that the fungus grows most rapidly on extracts of plant material preferred by A. cephalotes. Relative growth rates of the fungus on different substrates may be related to the presence of growth inhibitors rather than to nutrient availability.
Leaf-cutting ants live in mutualistic symbiosis with their garden fungus Leucoagaricus gongylophorus that can be attacked by the specialized pathogenic fungus Escovopsis. Actinomyces symbionts from Acromyrmex leaf-cutting ants contribute to protect L. gongylophorus against pathogens. The symbiont Streptomyces sp. Av25_4 exhibited strong activity against Escovopsis weberi in co-cultivation assays. Experiments physically separating E. weberi and Streptomyces sp. Av25_4 allowing only exchange of volatiles revealed that Streptomyces sp. Av25_4 produces a volatile antifungal. Volatile compounds from Streptomyces sp. Av25_4 were collected by closed loop stripping. Analysis by NMR revealed that Streptomyces sp. Av25_4 overproduces ammonia (up to 8 mM) which completely inhibited the growth of E. weberi due to its strong basic pH. Additionally, other symbionts from different Acromyrmex ants inhibited E. weberi by production of ammonia. The waste of ca. one third of Acomyrmex and Atta leaf-cutting ant colonies was strongly basic due to ammonia (up to ca. 8 mM) suggesting its role in nest hygiene. Not only complex and metabolically costly secondary metabolites, such as polyketides, but simple ammonia released by symbionts of leaf-cutting ants can contribute to control the growth of Escovopsis that is sensitive to ammonia in contrast to the garden fungus L. gongylophorus.
Fungal-Fungal Interactions in Leaf-Cutting Ant Agriculture
