Chemical identification of an active component and putative neural mechanism for repellent effect of a native ant’s odor on invasive species

Abstract

The invasive Argentine ants (Linepithema humile) and the red imported fire ants (Solenopsis invicta) constitute a worldwide threat, causing severe disruption to ecological systems and harming human welfare. In view of the limited success of current pest control measures, we propose here to employ repellents as means to mitigate the effect of these species. We demonstrate that cuticular hydrocarbons (CHCs) used as nestmate-recognition pheromone in the Japanese carpenter ant (Camponotus japonicus), and particularly its (Z)-9-tricosene component, induced vigorous olfactory response and intense aversion in these invasive species. (Z)-9-Tricosene, when given to their antennae, caused indiscriminate glomerular activation of antennal lobe (AL) regions, creating neural disarray and leading to aversive behavior. Considering the putative massive central neural effect, we suggest that the appropriate use of certain CHCs of native ants can facilitate aversive withdrawal of invasive ants.

Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant

“…In addition, among structurally related CHCs, C. japonicus might discriminate alkenes that have a double-bond at different positions. The result correlated with C. japonicus behavior; the ants exhibit remarkable aversive behavior to alkenes with a double-bond at C9-C10, but not to those with a double-bond at C7-C8 (Uebi et al, 2022). Interestingly, C28 and C25 long-chained alkanes are mapped to a region of the receptive space that was distinct from the other CHCs, indicating that these two CHCs have specific perceptual qualities.…”

“…In contrast, salient CHCs, such as CHC pheromones, effectively activated multiple SNs via the “stronger inputs spread” filter function. This corresponds with a high concentration of 9-tricosene (9-C23) activating multiple OSNs in single basiconic sensilla and indiscriminately activating many targeted T6 glomeruli in the antennal lobe of C. japonicus ( Uebi et al, 2022 ). Thus, two peripheral sensory filters formed by sensory adaptation and gap junctions may emphasize the CHC information as the “all-or-nothing” response.…”

“…Among the 18 CHCs, seven were commercially available, but 11 needed to be synthesized ( Table 1 ). Details of CHC synthesis have been reported ( Uebi et al, 2022 ). All CHCs and C8al were diluted to 1 mM in paraffin oil, and the concentration of CHC elicited sufficient excitatory responses in SNs of basiconic sensilla ( Supplementary Figure 2 ).…”

“…To investigate the electrical coupling between dendrites of SNs in single basiconic sensilla ( Takeichi et al, 2018 ; Uebi et al, 2022 ), we used the general gap junction blocker, carbenoxolone (CBX) ( Miriyala et al, 2018 ). 3 μL of ant saline (control group) or 10 mM CBX solution (CBX group) was injected into the hemolymph of the ice-anesthetized ant.…”

“…To study CHC processing in ants, we focused on basiconic sensilla of C. japonicus as a model. In C. japonicus , gas chromatography and mass spectrometry analysis, and behavioral analysis have been identified colony-specific blends of 18 CHCs that are critical for nestmate recognition ( Ozaki et al, 2005 ), and all 18 CHCs have been synthesized ( Uebi et al, 2022 ). Furthermore, morphological features of SNs in single basiconic sensillum have been characterized in C. japonicus ; approximately 140 SNs whose dendrites connected each other via gap junctions are co-housed in single basiconic sensillum ( Nakanishi et al, 2009 ; Takeichi et al, 2018 ).…”