Tripartite Interactions among Ixodiphagus hookeri, Ixodes ricinus and Deer: Differential Interference with Transmission Cycles of Tick-Borne Pathogens

Aleksandra I Krawczyk,Samiye Demir,Constantianus J M Koenraadt,Hein Sprong,Julian W Bakker,Manoj Fonville,Katsuhisa Takumi

doi:10.3390/pathogens9050339

Aleksandra I Krawczyk, Samiye Demir + Show 5 more

Open Access

https://doi.org/10.3390/pathogens9050339

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Abstract

For the development of sustainable control of tick-borne diseases, insight is needed in biological factors that affect tick populations. Here, the ecological interactions among Ixodiphagus hookeri, Ixodes ricinus, and two vertebrate species groups were investigated in relation to their effects on tick-borne disease risk. In 1129 questing ticks, I. hookeri DNA was detected more often in I. ricinus nymphs (4.4%) than in larvae (0.5%) and not in adults. Therefore, we determined the infestation rate of I. hookeri in nymphs from 19 forest sites, where vertebrate, tick, and tick-borne pathogen communities had been previously quantified. We found higher than expected co-occurrence rates of I. hookeri with deer-associated Anaplasma phagocytophilum, and lower than expected rates with rodent-associated Borrelia afzelii and Neoehrlichia mikurensis. The prevalence of I. hookeri in nymphs varied between 0% and 16% and was positively correlated with the encounter probability of ungulates and the densities of all life stages of I. ricinus. Lastly, we investigated the emergence of I. hookeri from artificially fed, field-collected nymphs. Adult wasps emerged from seven of the 172 fed nymphs. From these observations, we inferred that I. hookeri is parasitizing I. ricinus larvae that are feeding on deer, rather than on rodents or in the vegetation. Since I. hookeri populations depend on deer abundance, the main propagation host of I. ricinus, these wasps have no apparent effect on tick populations. The presence of I. hookeri may directly interfere with the transmission cycle of A. phagocytophilum, but not with that of B. afzelii or N. mikurensis.

Highlights

Lyme borreliosis poses serious health concerns in the northern hemisphere [1,2,3]
The three horizontally transmitted tick-borne pathogens, Borrelia burgdorferi s.l., Anaplasma phagocytophilum, and Neoehrlichia mikurensis, were detected in nymphs and adults (Table 1), but not in larvae, except for one larva, which was positive of B. burgdorferi s.l. (Table 1)
We investigated the ecological interactions among the parasitoid wasp I. hookeri, the tick I. ricinus, and two vertebrate species groups, and their combined effect on tick-borne disease risk

Summary

Introduction

Lyme borreliosis poses serious health concerns in the northern hemisphere [1,2,3]. Increases in incidence have been observed in several countries in Europe. These increases are partially explained by geographical spread of its vector, Ixodes ricinus [4,5]. Other tick-borne diseases (TBDs), such as anaplasmosis and neoehrlichiosis, are emerging [6,7]. Understanding which factors drive the population densities of ticks and the transmission cycles of tick-borne pathogens are important steps in assessing disease risk and formulating possible intervention strategies. In north-western Europe, TBDs are generally caused by a bite of an infected I. ricinus nymph [8].

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