The Fecal Odor of Sick Hedgehogs (Erinaceus europaeus) Mediates Olfactory Attraction of the Tick Ixodes hexagonus

Abstract

Parasite loads of animals vary among individuals, but the underlying mechanisms have not been fully identified. Here, we investigated whether health status of hedgehogs (Erinaceus europaeus) is correlated with tick burden, and whether chemical cues linked to the health status of the host mediate attraction of the tick Ixodes hexagonus. An ecological survey conducted over 10 years, involving 226 wild hedgehogs, revealed a strong association between health status and tick burden of hedgehogs, with healthy animals being less likely to carry ticks than unhealthy ones. Behavioral choice tests demonstrated that ticks display a preference for the fecal odor from sick hedgehogs compared with healthy ones. Chemical analysis of fecal odors using gas chromatography-mass spectrometry showed differences in the odor profile between sick and healthy hedgehogs. Sick animals tended to exhibit raised levels of the volatile aromatic heterocyclic compound indole in their feces. Ticks were attracted to indole when given the choice between indole and a solvent control. However, fecal matter from healthy hosts, with the addition of indole, was not attractive to ticks, suggesting that indole interacts with other, undetected compounds in mediating attraction. This study implies that it is the attraction to fecal odor that causes higher tick burdens in sick hedgehogs. Ticks might benefit from this preference by avoiding possible repulsion mechanisms of healthy hosts. We suggest that ticks potentially choose their host based on odor linked to the host's health status.

Identification of non-host semiochemicals for the brown dog tick, Rhipicephalus sanguineus sensu lato (Acari: Ixodidae), from tick-resistant beagles, Canis lupus familiaris

“…to Culicoides impunctatus (Diptera: Ceratopogonidae) (Logan et al, 2009) and Aedes aegypti (Diptera: Culicidae) (Logan et al, 2008). On other hand, Bunnell et al (2011) correlated the high burden of Ixodes hexagonus on sick hedgehogs (Erinaceus europaeus) with the presence of an attractant substance (indole) in these animals' faeces.…”

Chemosensory behaviors of parasites

“…Other species, such as the hedgehog parasitic tick Ixodes hexagonus , rely on subtle differences in host odor profiles for host selection. I. hexagonus is more attracted to the odor of sick hedgehogs than healthy hedgehogs and is more likely to parasitize sick hedgehogs [100]. The molecular basis of olfaction in many of these ectoparasites remains largely unexplored and will be an interesting avenue for future research.…”

Kairomones - important substances in interspecific communication in vertebrates: a review

“…The faeces of sick hedgehog individuals were shown to contain raised levels of the volatile aromatic compound indole (detected in experiments using gas chromatography -mass spectrometry). Ticks were attracted by indole, but not as a unique chemical cue; there must be other undetected substances mediating the attraction, because the faeces from healthy animals with the addition of indole, were not attractive to ticks (Bunnell et al 2011). Confirming this observation, e.g., in livestock, the health status of an animal corresponds to fewer tick attacks while a higher number of ticks could indicate a sick individual.…”