Chemosensory and Behavioural Responses of Ixodes scapularis to Natural Products: Role of Chemosensory Organs in Volatile Detection

Simple Summary Ticks are responsible of transmitting serious disease agents of importance to human and veterinary health. Despite the importance of repellents, deterrents and acaricides in tick management, little is understood about the types of chemicals recognized and the mechanism behind chemoreception. Being almost totally blind, ticks rely on chemosensation to identify and locate hosts for a successful blood meal and to detect chemical signals in the environment. We explored the neurophysiology of tick chemosensory system in the context of behaviourally-relevant volatile stimuli, including essential oil components, to evaluate how the combination of attractants and plant volatile compounds is detected and processed. The observed inhibition (or deterrent effect) in tick electrophysiological response and behavioural activity, after the tick has been exposed to a binary mixture of attractant and volatile compound, represents an important advancement in understanding how tick olfaction works and what may be the mechanism behind detecting unpleasant odor stimuli and consequently been deterred. These information will provide more insights in developing new natural product-based deterrents for self-protection. Abstract Blacklegged ticks, Ixodes scapularis, represent a significant public health concern due to their vectoring of tick-borne disease. Despite their medical importance, there is still limited knowledge of the chemosensory system of this species, and thus a poor understanding of host-seeking behaviour and chemical ecology. We investigated the electrophysiological sensitivity of adult female blacklegged ticks to attractants and plant-derived compounds via an electrode inserted into the scutum. The response of female ticks to binary mixtures with a constant concentration of a selected attractant (butyric acid) and increasing concentration of volatile organic compounds (VOCs) (geraniol, phenethyl alcohol, β-citronellol, and citral) was recorded. A strict relationship between increasing volatile concentration and a decreasing response was observed for each VOC. Y-tube bioassays confirmed that tick attraction towards butyric acid decreased with the presence of a VOC, which exerted a deterrent effect. To determine the specific role of sensory appendages involved in the detection of attractant chemical stimuli, we tested tick electrophysiological response after removing appendages that house chemosensory sensilla (foretarsi, pedipalps, or both). The chemosensory response was related to the molecular structure of attractant odorant, and the lack of pedipalps significantly reduced olfactory responses, suggesting they play an important role in detecting attractants. This study provides new insight into the neurophysiological mechanisms underlying tick olfaction and the potential for interactions between attractant and deterrent chemical detection.