Cadmium exposure disrupts the olfactory sensitivity of fire ants to semiochemicals

Fuxiang Yang; Rui Shao; Jing Zhao; Lei Li; Manqun Wang; Aiming Zhou

doi:10.1016/j.envpol.2021.117359

Cadmium exposure disrupts the olfactory sensitivity of fire ants to semiochemicals

Environ Pollut. 2021 Oct 15:287:117359. doi: 10.1016/j.envpol.2021.117359. Epub 2021 May 13.

Authors

Fuxiang Yang¹, Rui Shao¹, Jing Zhao¹, Lei Li², Manqun Wang¹, Aiming Zhou³

Affiliations

¹ Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
² Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
³ Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China. Electronic address: zhouam@mail.hzau.edu.cn.

PMID: 34020258
DOI: 10.1016/j.envpol.2021.117359

Abstract

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.

Keywords: Cd contamination; Electrophysiological and behavioral responses; Odorant binding proteins; Olfactory sensitivity; Red imported fire ant.

MeSH terms

Animals
Ants*
Cadmium / toxicity
Humans
Insect Repellents*
Pheromones

Substances

Insect Repellents
Pheromones
Cadmium