Bacteria may enhance species association in an ant–aphid mutualistic relationship

Abstract

The mutualistic relationships between certain ant and aphid species are well known, the primary benefits being protection for the aphids and carbohydrate-rich honeydew for the ants. Questions remain, however, as to the exact semiochemical factors that establish and maintain such relationships. In this study, we used a series of treatments and associated controls placed at the end of a two-way olfactometer to determine the degree of attractiveness of a complete plant-aphid-honeydew system as well as individual components of that system. Both the olfactometer branch selected by the black garden ant (Lasius niger) and the linear speed with which ants moved through the device were measured. Study results showed that ants were attracted not just to the complete plant system and the honeydew itself, but also to the microbial flora in the absence of plant or honeydew, and specifically to a bacterium from the black bean aphid (Aphis fabae) honeydew, Staphylococcus xylosus. This bacterium produces a blend of semiochemicals that attract the ant scouts. This information suggests the presence of a naturally occurring, reliable biotic cue for detection of potential aphid partners. This would have to be confirmed in natural conditions by further field experiments. Rather than being opportunistic species that coincidentally colonize a sugarrich environment, microorganisms living in aphid honeydew may be able to alter emissions of volatile organic compounds (VOCs), thus significantly mediating partner attraction. A bacterial involvement in this mutualistic relationship could alter the manner in which these and similar relationships are viewed and evaluated. Future studies into mutualism stability and function among macroscopic partners will likely need for transition from a two-partner perspective to a multiple-partner perspective, and consider the microbial component, with the potential for one or more taxa making significant contributions to the relationship.

Bacteria may contribute to distant species recognition in ant–aphid mutualistic relationships

“…However, in order to assess these criteria, ant foragers must already have found the aphid colony. Previous studies already showed ants ability to orient their search for aphid colonies using volatile cues (Verheggen et al ., ; Fischer et al ., ). The data presented here is the first evidence of distant aphid species discrimination by ants that is driven by aphid honeydew and mediated by the associated microflora through release of VOCs, in laboratory conditions.…”

“…Moreover, this tendency is supported by the relative attractiveness of honeydews and bacterial cultures issued of these 2 aphid species, confirming both ants ability to distantly discriminate between 2 aphid species, and honeydew VOCs involvement in that discrimination. Even though mVOCs emitted from honeydew have been reported to attract aphid enemies and potential ant partners (Leroy et al ., ; Fischer et al ., ), this is the first evidence of ant ability to use such volatile cues to distantly discriminate 2 aphid species. Furthermore, the attractiveness shown by Acyrthosiphon pisum when presented alone, strongly reduced when Aphis fabae is added in the possible choices, suggests that ants might adapt their response depending on available resources.…”

“…Using a methodology previously applied to highlight honeydew mVOCs effect on ant behavior (Fischer et al ., ), we observed similar ant attraction toward both myrmecophilous and nonmyrmecophilous aphid species when the aphids were presented alone. However, when given a choice between the 2 aphid species, ant showed a significant preference for the myrmecophilous Aphis fabae with an attraction level similar to the attraction observed for this aphid presented alone.…”

“…They originate mostly from bacterial degradation of diverse compounds. Potential origins and biosynthetic pathways of each compounds, as well as their involvement in different ant species communication, have been previously discussed (Fischer et al ., ). Although qualitative VOCs profiles detected are very close, even nearly identical for the 2 tested bacterial cultures, ants still shown a preference for Aphis fabae ‐related samples, suggesting recognition based on ratios between compounds instead of the attractiveness of a single molecule or group of molecules.…”

“…While aphids do not seem to actively search for ant partners, ants are known to search for their aphid partners and are able to use different volatile cues to orientate this search, namely volatile organic compounds emitted by honeydew bacteria (mVOCs) and E ‐β‐farnesene (EBF), an aphid pheromone involved in alarm and social behaviors (Verheggen et al ., ; Fischer et al ., ,b). This last molecule is a major component of the alarm pheromone of numerous aphid species, and is thus not likely to constitute alone a suitable species recognition cue (Francis et al ., ).…”