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

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.

蜱作为人类与动物的疾病传播媒介，其地位仅次于蚊子。蜱的宿主探测行为主要归因于其前足上的复杂感官结构——哈氏器（Haller’s organ），该结构可感知气味、二氧化碳与热量，但目前学界对这类宿主探测机制的认知仍较为有限。有轶事性证据表明，蜱与其他外寄生物会被热量吸引，但此前从未有研究证实它们可通过辐射热远距离探测宿主。事实上，过往相关研究尝试均得出“蜱不会利用辐射热进行宿主探测”的结论。本研究采用一种新型趋热测定法（thermotaxis assay），探究蜱的热感知能力的探测范围、温度依赖性与驱避剂敏感性，并明确负责该热感知功能的感官器官。研究发现，美洲钝眼蜱（Amblyomma americanum）与变异革蜱（Dermacentor variabilis）可通过哈氏器中被称为“囊状结构”的覆被球形凹窝器官感知辐射热，从而在数米外定位人类宿主。囊状结构覆盖层上的开孔赋予其感知方向性，而囊内部高度反光的表面则可将辐射聚集于感器上，进一步强化方向性并提升感知灵敏度。商用驱虫剂可通过干扰蜱的寻宿主行为，为个人免受具有感染风险的蜱叮咬提供有效防护。低浓度的避蚊胺（DEET）、派卡瑞丁（picaridin）、2-十一酮（2-undecanone）、香茅醛（citronellal）与诺卡酮（nootkatone）即可抑制蜱的趋热行为，但不会影响嗅觉介导的寻宿主行为。本研究结果证实，蜱的哈氏器囊状结构是用于宿主搜寻的辐射热传感器，且驱虫剂可在不干扰嗅觉功能的浓度下破坏该热感知能力。我们预计，这一发现将极大推动驱虫剂相关研究，并为开发创新型有害生物综合治理方案以及外寄生物与虫媒疾病的个人防护策略提供全新靶点。