BASF Corporation, Research Triangle Park, North Carolina, United States of America.
PLoS One. 2019 Aug 23;14(8):e0221659. doi: 10.1371/journal.pone.0221659. eCollection 2019.
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.
蜱虫是仅次于蚊子的人类和动物疾病的第二大传播媒介。蜱虫宿主的检测主要归因于哈勒氏器,这是蜱虫前腿上的一种复杂的感觉结构,能够检测气味、二氧化碳和热量,但这些宿主检测机制还不是很清楚。有一些传闻证据表明,蜱虫和其他外寄生虫会被热量吸引,但从未有证据表明它们会利用辐射热来远距离探测宿主。事实上,之前的尝试已经得出结论,辐射热不是蜱虫所利用的。在这里,我们使用一种新的趋热测定法来研究蜱虫对热的感知范围、温度依赖性和驱避敏感性,并确定负责这种感觉的感觉器官。我们表明,美洲钝眼蜱和变异革蜱可以通过哈勒氏器的胶囊部分感知到的辐射热,从几米远的地方定位到人类。胶囊盖的一个开口赋予了方向性,而胶囊内部高度反光的表面将辐射聚焦在感觉器上,以提高方向性和增加敏感性。商业昆虫驱避剂通过阻碍宿主寻找行为,为防止潜在传染性蜱虫叮咬提供了一种有效的个人保护手段。低浓度的昆虫驱避剂避蚊胺、派卡瑞丁、2-十一酮、香茅醛和诺卡酮消除趋热作用而不影响嗅觉刺激的宿主寻找行为。我们的结果表明,蜱虫的哈勒氏器胶囊是一种用于寻找宿主的辐射热传感器,驱避剂在不干扰嗅觉的浓度下破坏这种感觉。我们预计,这一发现将极大地促进昆虫驱避剂的研究,并为创新的综合虫害管理计划和针对外寄生虫和媒介传播疾病的个人保护策略提供新的目标。