Cadmium exposure disrupts the olfactory sensitivity of fire ants to semiochemicals

Ants are eusocial insects and have evolved sensitive chemosensory systems for social communication. However, the effect of heavy metal contamination on the olfactory sensitivity of ants remains largely unknown. Here, we investigated the survival and olfactory response of Solenopsis invicta under cadmium (Cd) exposure. As a result, exposure to dietary Cd at different concentrations (100, 300 and 500 mg/L) caused higher Cd accumulation and lower survival of the ants compared with the control (0 mg/L). Cd exposure induced diverse expression patterns of odor binding protein genes (SiOBPs) in S. invicta antenna. Specifically, the expression of SiOBP4, SiOBP11, SiOBP12 and SiOBP16 was increased by 1.84-, 1.14-, 0.83- and 1.76-fold, respectively, at 300 mg/L Cd, while SiOBP7 and SiOBP9 were suppressed as Cd concentration increased. Electroantennography (EAG) and behavioral bioassays were performed to further evaluate the effect of Cd contamination on the olfactory sensitivity of S. invicta workers to 2, 4, 6-trimethylpyridine (TMP) and 2-ethyl-3,6(5)-dimethylpyrazine (EDP), the two frequent functional semiochemicals for S. invicta. The results showed that under no Cd exposure, S. invicta workers exhibited strong EAG response and apparent residing repellence to TMP and EDP, but Cd exposure suppressed EAG response and deprived the behavioral repellence to TMP and EDP of the workers, suggesting that Cd exposure decreases the olfactory sensitivity of S. invicta to these two functional semiochemicals. Further fluorescence competitive binding assay revealed that SiOBP7 had strong binding affinity to TMP and EDP, suggesting that the decrease in olfactory sensitivity may be attributed to the inhibitory effect of Cd exposure on SiOBP7. Overall, our results suggest that Cd exposure may not only directly decrease the survival of ants, but also affect their olfactory recognition.