How Do Leaf-Cutting Ants Recognize Antagonistic Microbes in Their Fungal Crops?

Abstract

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.

Disease management in two sympatric Apterostigma fungus‐growing ants for controlling the parasitic fungus Escovopsis

“…The ants' differential responses to different parasites suggest that the ants can discriminate between different Escovopsis strains as previously suggested (Goes et al, 2020). However, we do not know whether ants' attention to particular morphotypes can be modified by adding or removing other Escovopsis morphotypes or pathogens.…”

Fungus-Growing Ants: Models for the Integrative Analysis of Cognition and Brain Evolution

“…These tasks involve chemical signals (Schultner and Pulliainen, 2020) processed by the antennal lobes and mushroom bodies, as well as fine motor coordination of the mouthparts, mediated by subesophageal zone circuitry (Paul and Gronenberg, 2002). Minims may deposit pheromones on foraging trails (Howard, 2001;Evison et al, 2008), clean contaminants from incoming leaves and otherwise protect the fungus from microbes (Goes et al, 2020), and defend against parasitic flies (Feener and Moss, 1990).…”

Distinct and enhanced hygienic responses of a leaf‐cutting ant toward repeated fungi exposures

“…In leaf‐cutting ants (Hymenoptera: Formicidae: Myrmicinae: Attini; subtribe: Attina), studies demonstrated the wide array of hygienic defenses toward unwelcome microbes that exploit the same resources and niches as their fungal crops (Bonadies et al, 2019 ; Currie et al, 1999 ; Currie & Stuart, 2001 ; Fernández‐Marín et al, 2009 ; Rocha et al, 2014 ; Yek et al, 2012 ) (Figure 1 ). The survival of their fungal cultivars ( Basidiomycota: Agaricales , including Leucoagaricus gongylophorus ) and the microbiota found in the colony (Aylward et al, 2014 ; Barcoto et al, 2020 ; Khadempour et al, 2020 ; Suen et al, 2010 ) relies on a combination of the ants' ability to defend themselves and their partners using cleaning strategies (Goes et al, 2020 ).…”

“…Several alien fungi with distinct lifestyles were reported in Atta and Acromyrmex colonies, as generalist mycopathogens (e.g., Trichoderma and Syncephalastrum ), entomopathogens (e.g., Beauveria and Metarhizium , Rodrigues et al, Rodrigues & Pagnocca, 2005 , Rodrigues et al, 2008 ; Goffré & Folgarait, 2018 ), and mycoparasites (i.e., Escovopsis , Currie et al, 2003 ). In theory, if leaf‐cutting ants recognize the diversity of alien fungi entering their colonies, defensive responses are expected to follow their threat levels (Goes et al, 2020 ; Mighell & Van Bael, 2016 ). For instance, increased hygienic responses toward Escovopsis when compared with Trichoderma viride corroborate a possible distinction between mycelium and/or conidia of a specialist and a generalist fungal pathogen, respectively (Currie & Stuart, 2001 ).…”