Carbon dioxide sensing in an obligate insect-fungus symbiosis: CO2 preferences of leaf-cutting ants to rear their mutualistic fungus

Abstract

Defense against biotic or abiotic stresses is one of the benefits of living in symbiosis. Leaf-cutting ants, which live in an obligate mutualism with a fungus, attenuate thermal and desiccation stress of their partner through behavioral responses, by choosing suitable places for fungus-rearing across the soil profile. The underground environment also presents hypoxic (low oxygen) and hypercapnic (high carbon dioxide) conditions, which can negatively influence the symbiont. Here, we investigated whether workers of the leaf-cutting ant Acromyrmex lundii use the CO2 concentration as an orientation cue when selecting a place to locate their fungus garden, and whether they show preferences for specific CO2 concentrations. We also evaluated whether levels preferred by workers for fungus-rearing differ from those selected for themselves. In the laboratory, CO2 preferences were assessed in binary choices between chambers with different CO2 concentrations, by quantifying number of workers in each chamber and amount of relocated fungus. Leaf-cutting ants used the CO2 concentration as a spatial cue when selecting places for fungus-rearing. A. lundii preferred intermediate CO2 levels, between 1 and 3%, as they would encounter at soil depths where their nest chambers are located. In addition, workers avoided both atmospheric and high CO2 levels as they would occur outside the nest and at deeper soil layers, respectively. In order to prevent fungus desiccation, however, workers relocated fungus to high CO2 levels, which were otherwise avoided. Workers’ CO2 preferences for themselves showed no clear-cut pattern. We suggest that workers avoid both atmospheric and high CO2 concentrations not because they are detrimental for themselves, but because of their consequences for the symbiotic partner. Whether the preferred CO2 concentrations are beneficial for symbiont growth remains to be investigated, as well as whether the observed preferences for fungus-rearing influences the ants’ decisions where to excavate new chambers across the soil profile.

Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions

“…Temperature stability is required for optimal fungal growth and brood development (Aylward, Currie, & Suen, ; Bollazzi & Roces, ), in which Atta species monitor through thermosensitive receptors (Ruchty et al, ). Some leaf‐cutter ant species in the genus Acromyrmex use CO 2 concentrations to determine optimal locations for fungal gardens (Römer, Bollazzi, & Roces, ), and A. vollenweideri enhance ventilation turrets in height and number in response to increasing CO 2 levels (Halboth & Roces, ). Regulation of the nest environment creates not only conditions suitable for colony needs, but also conditions that may be optimal for other organisms important for biochemical cycling.…”

Dynamic environments of fungus‐farming termite mounds exert growth‐modulating effects on fungal crop parasites

“…The very high CO 2 may play a role in controlling the growth of the parasitic fungus as suggested by Batra and Batra (). However, in a recent study on another fungus‐growing insect, i.e., leaf‐cutter ants, workers were found to avoid high CO 2 concentrations but chose intermediate levels when selecting places for fungus‐rearing, probably because of the detrimental effect of high CO 2 on the fungi (Römer et al ., ). But the termite mutualistic fungus Termitomyces is clearly able to grow even under such hypercarbic conditions.…”

“…The negative effects include an ideal environment for pathogen growth, e.g., the stable nest microclimate of red wood ants that facilitates a specialised decomposer community might also promote the growth of opportunistic pathogenic bacteria (Christe et al ., ). Importantly, animal engineers can not only sense environmental cues, e.g., fungus‐farming ants show a preference for specific CO 2 levels for fungus‐rearing (Römer et al ., ), but also regulate them either actively or passively (Jones and Oldroyd, ). However, the effect of such environmental factors on engineers and their symbionts can be compounded by genotype and environment interactions (Thomas and Blanford, ) which may select for specific mutualists or parasites.…”

Carbon Dioxide Mediates the Response to Temperature and Water Activity Levels in Aspergillus flavus during Infection of Maize Kernels

“…Hall et al [ 21 ] reported that CO 2 serves as an intra-colony signaling molecule important for colonization and pathogenesis in the fungus Candida albicans . It has also been shown that insects, in symbiosis with fungi, demonstrate preferences for certain ranges of elevated CO 2 in which to conduct their fungal-rearing [ 22 ]. Furthermore, elevated CO 2 present in the ambient environment of soil samples containing a mixed fungal population decreases respiration activity [ 23 ] and decreases AF accumulation in A. parasiticus [ 24 ].…”