Leaf-cutting ants employ diverse behavioral strategies for promoting the growth of fungal cultivars in a structure known as fungus garden. As a nutritionally rich resource for the ants, the fungal crop is threatened by microbial antagonists and pathogens. Strategies for protecting the garden against harmful microbes have been described in detail, although the process of microbial threat recognition is not fully understood. Here, we review the literature on leaf-cutting ants' social immunity traits, in search of possibilities by which workers recognize harmful microbes in their system. Based on current data, we suggest mechanisms regarding (1) chemical recognition, where discrimination could be related to chemical cues from the antagonistic microbe or semiochemicals released by the fungus garden during harmful interactions, or (2) through associative learning when workers would connect the microbe cues with a damage in the fungus garden, developing a "colony-level memory" toward this threat. We also discuss evidence supporting ant-fungus communication as key for maintaining the health of the fungus garden, as well as experimental setups for future evaluation of threat detection and recognition by leaf-cutting ants.
Health and disease emerge from intricate interactions between genotypes, phenotypes, and environmental features. The outcomes of such interactions are context-dependent, existing as a dynamic continuum ranging from benefits to damage. In host-microbial interactions, both the host and environmental conditions modulate the pathogenic potential of a microorganism. Microbial interactions are the core of the agricultural systems of ants in the subtribe Attina, which cultivate basidiomycete fungi for food. The fungiculture environment harbors a diverse microbial community, including fungi in the genus Escovopsis that has been studied as damage-causing agent. Here, we consider the ant colony as a host and investigate to what extent its health impacts the dynamics and outcomes of host-Escovopsis interactions. We found that different ant fungal cultivars vary in susceptibility to the same Escovopsis strains in plate-assays interactions. In subcolony-Escovopsis interactions, while healthy subcolonies gradually recover from infection with different concentrations of Escovopsis conidia, insecticide-treated subcolonies evidenced traits of infection and died within 7 days. The opportunistic nature of Escovopsis infections indicates that diseases in attine fungiculture are a consequence of host susceptibility, rather than the effect of a single microbial agent. By addressing the host susceptibility as a major modulator of Escovopsis pathogenesis, our findings expand the understanding of disease dynamics within attine colonies.
Leaf‐cutting ants and their fungal crops are a textbook example of a long‐term obligatory mutualism. Many microbes continuously enter their nest containing the fungal cultivars, destabilizing the symbiosis and, in some cases, outcompeting the mutualistic partners. Preferably, the ant workers should distinguish between different microorganisms to respond according to their threat level and recurrence in the colony. To address these assumptions, we investigated how workers of Atta sexdens sanitize their fungal crop toward five different fungi commonly isolated from the fungus gardens: Escovopsis sp., Fusarium oxysporum , Metarhizium anisopliae , Trichoderma spirale , and Syncephalastrum sp. Also, to investigate the plasticity of these responses toward recurrences of these fungi, we exposed the colonies with each fungus three times fourteen days apart. As expected, intensities in sanitization differed according to the fungal species. Ants significantly groom their fungal crop more toward F. oxysporum , M. anisopliae , and Syncephalastrum sp. than toward Escovopsis sp. and T. spirale . Weeding, self‐, and allogrooming were observed in less frequency than fungus grooming in all cases. Moreover, we detected a significant increase in the overall responses after repeated exposures for each fungus, except for Escovopsis sp. Our results indicate that A. sexdens workers are able to distinguish between different fungi and apply distinct responses to remove these from the fungus gardens. Our findings also suggest that successive exposures to the same antagonist increase hygiene, indicating plasticity of ant colonies' defenses to previously encountered pathogens.
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