Temporal variation and drivers of Ixodiphagus hookeri parasitisation in Ixodes ricinus ticks in northern Europe

Abstract

Ixodiphagus hookeri (Hymenoptera: Encyrtidae) is a highly specialized koinobiont endoparasitoid of hard ticks (Acari: Ixodidae). While it is considered a prime target for biological control of ticks, longitudinal data on natural parasitisation of tick populations is scarce, consequently leading to a lack of understanding regarding the effects of global warming on wasp populations and factors impacting natural parasitisation rates of ticks. To fill in these gaps, we present a longitudinal time series on natural I. hookeri parasitisation of Ixodes ricinus from the northernmost limits of their occurrence. In total, 2,111 I. ricinus nymphs collected between 2014-2021 from Seili Island in southwestern Finland were screened for I. hookeri DNA utilizing an in-house qPCR assay. Samples had previously been screened for several tick-borne pathogens and larval blood meal sources. Generalized linear mixed models were fitted to determine factors influencing the probability of parasitisation of questing nymphs, whether parasitisation influences tick densities, and if differences in parasitisation can be identified between early (May to mid-July) and late (mid-July to October) season. Log odds ratios were calculated to assess parasitisation-pathogen and parasitisation-host associations. An artificial tick feeding system was used to feed nymphs collected from the island. An increase in I. hookeri parasitisation was observed on the island between 2014-2021. The overall parasitisation prevalence was 8.2 %, with year and study site specific values ranging from 0 to 38 %. Larvae densities, July mean temperatures and parasitisation rates at t-1 were observed to increase probability of parasitisation. Parasitisation was more likely if the nymphs had fed on deer as larvae or carried Babesia spp. protozoa, and less likely if they carried Borrelia spp. Twelve wasps emerged from an artificially fed nymph, immediately starting oviposition and expiring within seven days. We present here the longest time series of natural I. hookeri parasitisation of I. ricinus ticks. An increasing trend in parasitisation was observed, indicating increases in the wasp population likely linked to global warming. Our results regarding associations between parasitisation and tick-borne pathogens - and directly linking parasitisation events to deer - support findings from previous research, which have indicated that parasitisation of ticks is more likely to occur on large host animals than on small hosts or ticks questing on the ground. The results suggest that larvae may be more important parasitisation targets for the wasps than previously accredited.