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, 8 (5), 764-771

Infrared Light Detection by the Haller's Organ of Adult American Dog Ticks, Dermacentor Variabilis (Ixodida: Ixodidae)

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Infrared Light Detection by the Haller's Organ of Adult American Dog Ticks, Dermacentor Variabilis (Ixodida: Ixodidae)

Robert D Mitchell 3rd et al. Ticks Tick Borne Dis.

Abstract

The Haller's organ (HO), unique to ticks and mites, is found only on the first tarsus of the front pair of legs. The organ has an unusual morphology consisting of an anterior pit (AP) with protruding sensilla and a posterior capsule (Cp). The current thinking is that the HO's main function is chemosensation analogous to the insect antennae, but the functionality of its atypical structure (exclusive to the Acari) is unexplained. We provide the first evidence that the HO allows the American dog tick, Dermacentor variabilis, to respond to infrared (IR) light. Unfed D. variabilis adults with their HOs present were positively phototactic to IR. However, when the HOs were removed, no IR response was detected. Ticks in these experiments were also attracted to white light with and without the HOs, but were only positively phototactic to white light when the ocelli (primitive eyes) were unobstructed. Covering the eyes did not prevent IR attraction. A putative TRPA1 receptor was characterized from a D. variabilis-specific HO transcriptome we constructed. This receptor was homologous to transient receptor potential cation channel, subfamily A, member 1 (TRPA1) from the pit organ of the pit viper, python, and boa families of snakes, the only receptor identified so far for IR detection. HO scanning electron microscopy (SEM) studies in the American dog tick showed the AP and Cp but also novel structures not previously described; the potential role of these structures in IR detection is discussed. The ability of ticks to use IR for host finding is consistent with their obligatory hematophagy and has practical applications in tick trapping and the development of new repellents.

Keywords: American dog tick; Dermacentor variabilis; Haller’s organ; Infrared; Light; TRPA1.

Figures

Fig. 1
Fig. 1
Scanning electron micrographs of Dermacentor variabilis Haller's organ (HO) and associated structures. (A) female, dorsal view at 25×, dotted line where tarsus I including HO was removed, (B) female, dorsal view of HO anterior pit and capsule at 500×, (C) male, dorsal view of HO anterior pit and capsule at 500×, and (D) female, dorsal view, aperture opening of capsule at 2500×. Arrows in panels B-D indicate undescribed structures resembling auricular or companiform sensilla that may serve as IR detectors or assist in this function in both male and female D. variabilis. The white star in panel A denotes the location of the HO (star just above structure). The ocellus (primitive eye) is located between the brackets in panel A. The dotted line denotes the location where the HO was ablated for the corresponding trials. Oc = ocellus, Cp = capsule, AP = anterior pit.
Fig. 2
Fig. 2
Arena calibration points and video screenshot. (A) Choice arena where two of the ports at right angles to each other were fitted with identical light sources (either visible light or infrared), and (B) high definition, IR-capable video camera capture of bioassay trial where HO and ocelli were present and unobstructed (tick moving toward IR light). At the beginning of each assay a single tick was placed at the start and a light source was illuminated (yellow bulb, lane 1). After crossing the finish line of “Direction I” the first light source was turned off (grey bulb, lane 2) and the second light source (at a right angle) was immediately illuminated (yellow bulb, lane 2). Once the tick traveled from the start to the finish of “Direction II” the assay was over. Any deviation out of the field of the light beam (and not correcting toward the light source) was considered non-responsive. Movement toward each light source was considered non-responsive if the tick took longer than 1 minute to move within 2.5 cm of the illuminated source. Yellow bulbs denote lights that were turned on while the grey bulb represents a light that was turned off.
Fig. 3
Fig. 3
Dermacentor variabilis choice assay conditions and results. (A) Response of adult ticks to visible light with Haller's organs (HOs) removed or ocelli (Oc) blocked. (B) Response of adult ticks to infrared light with Haller's organs (HOs) removed or ocelli (Oc) blocked. “+HO +Oc” means that both the HOs and Oc were intact for those trials. “+HO -Oc” means that the HOs were intact and the Oc were covered with black paint for those trials. “-HO +Oc” means that the HOs were removed and the Oc were intact for those trials. A black “X” on the illustrations above each bar graph represents where the ticks' HOs were ablated or Oc were blocked. The frequency response was analyzed using a chi-squared test of homogeneity of proportions under the null hypothesis that the expected proportion for either choice (response or no response) was 0.50. Response to either visible or infrared light was significant at P ≤ 0.001 (**), P ≤ 0.01 (*).

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