Ticks home in on body heat: A new understanding of Haller's organ and repellent action.

Ann L Carr,Vincent L Salgado,Brian Stevenson

doi:10.1371/journal.pone.0221659

Abstract

Ticks are second only to mosquitoes as vectors of disease to humans and animals. Tick host detection is mainly ascribed to Haller’s organ, a complex sensory structure on the tick foreleg that detects odors, carbon dioxide and heat, but these host detection mechanisms are not well understood. There is anecdotal evidence that ticks and other ectoparasites are attracted to heat, but it has never been demonstrated that they use radiant heat to detect hosts at a distance. In fact, previous attempts to do this have concluded that radiant heat was not used by ticks. Here we use a novel thermotaxis assay to investigate the detection range, temperature dependence and repellent sensitivity of heat perception in ticks and to identify the sensory organ responsible for this sense. We show that Amblyomma americanum and Dermacentor variabilis ticks can locate a human from several meters away by radiant heat sensed by the part of Haller’s organ known as the capsule, a covered spherical pit organ. An aperture in the capsule cover confers directionality and highly reflective interior surfaces of the capsule concentrate radiation on the sensilla to sharpen directionality and increase sensitivity. Commercial insect repellents provide an effective means of personal protection against potentially infectious tick bites by hindering host-seeking behavior. Low concentrations of the insect repellents DEET, picaridin, 2-undecanone, citronellal and nootkatone eliminate thermotaxis without affecting olfaction-stimulated host-seeking behavior. Our results demonstrate that the tick Haller’s organ capsule is a radiant heat sensor used in host-finding and that repellents disrupt this sense at concentrations that do not disrupt olfaction. We anticipate that this discovery will significantly aid insect repellent research and provide novel targets for the development of innovative integrated pest management programs and personal protection strategies for ectoparasites and vector-borne disease.

Highlights

IntroductionA. americanum and D. variabilis are non-nidiculous tick species utilizing two host-seeking strategies throughout their life cycles: active host-hunting and vantage point host-ambushing
When questing unfed virgin adult A. americanum female ticks were placed in the center of the arena, an approximately equal number moved in each direction and many ticks did not move toward either plate, when both plates were at a temperature of 22 ̊C (Fig 2, upper left and S1 Movie)
When the warm plate was at 37 ̊C, on the other hand (Fig 2, upper right and S1 Movie), most ticks began moving toward it almost immediately, and of the few that did initially move toward the cold plate, most reversed direction and headed toward the warm plate, so that after five minutes, only one of 48 female A. americanum ticks remained within 10 cm of the cold plate, while 40 were within 10 cm of the warm plate

Summary

Introduction

A. americanum and D. variabilis are non-nidiculous tick species utilizing two host-seeking strategies throughout their life cycles: active host-hunting and vantage point host-ambushing. Both strategies involve multiple sensory modalities, though olfaction is believed to be the predominant sensory modality guiding tick host-seeking [4,5,6]. Tick olfaction is ascribed mainly to Haller’s organ, a localization of chemosensory sensilla on the tarsus of the foreleg While both components of Haller’s organ, a posterior capsule and anterior pit, are thought to serve olfactory functions, there is morphological evidence that supports putative hygrosensory and/or thermosensory functions [4, 6,7,8]. The posterior capsule structure is strikingly camera-lucida-like, suggesting that it could be a very sensitive detector for thermal infrared radiation (IR), which would be of value in sensing hosts at a distance, by their radiated heat

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Conclusion