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

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.

Fig 1. Thermotaxis bioassay arena with closed air circulation system.

Fig 2. Tracks of individual Amblyomma americanum ticks in thermotaxis trials.

Longitudinal position vs. time in the 1m-long arena of 48 individual female (top) or male (bottom) A. americanum ticks (six runs of eight ticks, with a different color/line type combination for each run) after placement in the center, at -50 cm, with the target plate (22, 30 and 37 °C in left, center and right panels, respectively) at 0 cm and the cold plate at -100 cm. Horizontal axis units are minutes.

Fig 3. Tracks of individual Dermacentor variabilis ticks in thermotaxis trials.

Longitudinal position vs. time as in Fig 2, but for D. variabilis ticks.

Fig 4. Average movement of ticks in thermotaxis trials.

A. Average longitudinal position vs. time in the thermotaxis arena of the indicated ticks after placement in the center at -50 cm with respect to the warm target at 0 cm. Horizontal axis units are minutes. B. Average initial speed and C. average velocity of ticks during the first 10 seconds of thermotaxis trials.

Fig 5. Thermotaxis trials scored as choice tests.

(A) Final choice of ticks at the end of a 5 min trial was scored as “warm” or “cold” if within 10 cm of the corresponding end, or “neither” if between those end areas. (B) Final warm preference index (PI), defined as (warm-cold)/(warm+cold) [20]. (C) Initial choice scores based on direction of the first movement of more than 15 cm if the tick eventually moved at least 25 cm from the origin. Ticks that failed to move at least 25 cm were scored “neither”. (D) Initial warm PI. Significance of warm/cold difference: **: p < 0.001; *: p < 0.05.

Fig 6. Sensitivity and mechanism of tick heat sensing.

A. Mean longitudinal position (± SEM) over time (s) of 88 A. americanum females (measured in 11 groups of 8) after placement adjacent to the cold end wall at -100 cm with respect to the target wall, which was set to either 22 or 40 °C. B. Distribution of initial velocities of all 88 ticks tested at 22 or 40 °C, averaged over the first 10 s, from fastest to slowest. C. Final choice scores in thermotaxis trials of A. americanum females placed in the center of the arena, with the target at 40 °C, under normal conditions, where convection and radiation from target to ticks are both possible (+C +R, normal), with an IR-transparent PVDC film barrier 5 cm from each end wall to block any possible convective air currents (-C +R, PVDC window), with both end walls clad with aluminum foil to eliminate radiant heat emission and leave only the possibility of heat transfer by convection (+C -R, Al foil), and finally in the normal arena but with both Haller’s organ capsule apertures closed with paraffin wax (+C +R, closed HOC). (** = p < 0.001 for warm/cold difference). D. Female A. americanum Haller’s organ viewed with epi-illumination shows hints of reflected light through the capsule aperture. Approximate outline of the capsule is shown by dashed oval. E. Interior surfaces of the Haller’s organ capsule and cover debris appear highly reflective after cover removal with an ultrasonic micro-etcher, but thin-walled sensilla (white arrowhead) are not reflective.

Fig 7. Disruption of thermotaxis by repellents.

(A) Mean longitudinal position (± SEM) in thermotaxis trials of unfed virgin adult A. americanum females exposed to the indicated repellent vapor concentrations (ng•cm^-3) or after 15 minutes’ recovery from the highest concentration (R). Ticks were placed into the center of the arena, at -50 cm with respect to the 40 °C target wall. (B) Final position after 5 minutes, scored as in Fig 5A. (C) Y-tube choice assays with unfed virgin adult A. americanum females under three conditions. Sham CO₂: both tubes contained pure air. Untreated: air in one tube contained 4% CO₂. DEET: air in one tube contained 4% CO₂ and all ticks were exposed to 50 ng•cm^-3 DEET. Significance of warm/cold or CO₂/air difference: **: p<0.001; *: p<0.05.

Fig 8. Proposed function of the Haller’s organ capsule as a radiant heat sensor.

When the aperture of the the Haller’s organ capsule near the tip of the foretarsus is directed at a warm target, infrared radiation within a narrow field of view passes through the aperture and warms the sensilla located deep within the capsule, whereas off-axis rays from non-target areas will be blocked by reflective pleomorphs and not influence the sensilla. The sensilla will be warmed to the average temperature within the field of view. The walls of the capsule and the pleomorphs are reflective and so will not radiate to the sensilla but instead will insulate them. Reflective cuticle is grey and normal cuticle is black. Image of female lone star tick, Amblyomma americanum, on leaf from Ticksafety.com, with permission. Differential interference contrast micrograph of the foretarsus of a larval Haemophysalis tick, from [26], with permission from W. Knee and H. Proctor.