Lemongrass essential oil and DEET inhibit attractant detection in infected and non-infected Ixodes scapularis ticks

Abstract

Blacklegged tick, Ixodes scapularis Say (Arachnida: Ixodidae), is a growing health concern for humans as vectors the causative agent of Lyme disease, Borrelia burgdorferi, and many other pathogens. Given the potential health threat I. scapularis entails, and the need to find effective strategies to prevent tick bites, it is pivotal to understand the chemosensory system of ticks and their host-seeking behaviour when exposed to repellents. In this study, we investigated whether the exposure to synthetic and plant-derived repellents impairs the ability of I. scapularis to detect attractants and host volatiles (butyric acid), and ultimately how these repellents interfere with host-seeking behaviour in both wild and lab-reared ticks. Furthermore, we screened wild ticks used in electrophysiology and Y-tube behavioural assays for presence of pathogens (Borrelia, Anaplasma, and Babesia) to evaluate if the bacterial infection status would affect the detection of butyric acid under the exposure to repellents. We determined that the exposure to DEET, lemongrass essential oil, citral, and geraniol significantly inhibited the ability of both lab-reared and wild adult female I. scapularis to detect and respond to butyric acid. We found that tick infection status does not significantly impact host-seeking behaviour in adult female I. scapularis. The knowledge gained from our study contributes to advance our understanding of host-seeking behaviour in ticks and the impact that the exposure to repellent has on the tick chemosensory system. These findings will be important for elucidating the mechanism of repellence in ticks and for the development of effective tick repellent management tools.

Keywords: Chemosensory system; Essential oil; Fumigation; Inhibition; N,N-diethyl-3-methyl benzamide; Repellent.

Fig. 1

a) Adult female Ixodes scapularis mounted dorsally on a fork-electrode probe using electrode gel for electrophysiology experiments. Legs not bearing the Haller's organ were surgically removed prior mounting the tick on the fork electrode. b) Example of an electrophysiological response to 10 μg of butyric acid.

Fig. 2

Experimental set-up used to measure behavioural choice of adult female Ixodes scapularis ticks between butyric acid (i.e., test stimulus) or hexane (i.e., control stimulus), pre- and post- fumigation exposure to hexane, lemongrass essential oil, DEET, citral, geraniol, and butyric acid.

Fig. 3

Electrophysiological response of wild adult female Ixodes scapularis ticks to butyric acid (BA) (100μg) in pre- and post- fumigation exposure to hexane, lemongrass essential oil, DEET, citral, and geraniol (n = 20). In fumigation treatment, ticks were exposed to the designated compound at 1.0 mg of repellent / 1.0 mL of air for 20 minutes. The dashed line separates pre- and post- exposure experiments. Responses capped with different letters are significantly different (P < 0.05).

Fig. 4

Electrophysiological response of lab-reared adult female Ixodes scapularis ticks to butyric acid (BA) (100μg) in pre- and post- fumigation exposure to hexane, lemongrass essential oil, DEET, citral, and geraniol (n = 10). In fumigation treatment, ticks were exposed to the designated compound at 1.0 mg of repellent / 1.0 mL of air for 20 minutes. The dashed line separates pre- and post- exposure experiments. Responses capped with different letters are significantly different (P < 0.05).

Fig. 5

Percentage of wild, adult, female Ixodes scapularis ticks choosing treatment (100 μg of butyric acid) or control (hexane) after 20 minutes in Y-tube two-choice behavioural assay for pre- and post-exposure to DEET (DT) and lemongrass (LG). The dashed line indicates the null expectation of 50 %. Results do not include non-responding ticks.

Fig. 6

Percentage of lab-reared, adult, female Ixodes scapularis ticks choosing treatment (100 μg of butyric acid, BA) or control (hexane, HX) in Y-tube two-choice behavioural assay for pre- and post-fumigation exposure to hexane (HX), butyric acid (BA), lemongrass essential oil (LG), DEET (DT), citral (CIT), and geraniol (GER). Dashed lines indicate the null expectation of 50 %. Results do not include non-responding ticks.

Fig. 7

Proportion of adult female Ixodes scapularis ticks infected with various pathogens for each of the sampled areas in Nova Scotia (Canada) from May to November 2022.