Shift in the seasonality of ixodid ticks after a warm winter in an urban habitat with notes on morphotypes of Ixodes ricinus and data in support of cryptic species within Ixodes frontalis

Abstract

This study was initiated to assess the seasonality and to investigate the morphology of questing ixodid ticks in an urban habitat in Central Europe, Hungary. A neglected part of a large cemetery, with sparse tree covering and dense lower vegetation, was sampled monthly from February 2019 to May 2021. All ticks were analyzed morphologically, and selected specimens by amplifying and sequencing two genetic markers. During the study 3818 ticks were collected, including Ixodes ricinus (n = 2772), Ixodes frontalis (n = 350) and Haemaphysalis concinna (n = 696). Ixodes ricinus adults and nymphs showed year-round activity, whereas H. concinna was not active during winter months and early spring. Most I. frontalis nymphs were collected in late winter and early spring, whereas the peak activity of larvae was during late autumn. Interestingly, during the spring, the peak activity of I. ricinus adults and nymphs was later (in May) when preceded by a warm winter in 2020. In contrast, the 2019 and 2021 spring activity peaks occurred in March and April after sharply rising temperatures in February. This shift in the peak activity of I. ricinus coincided with the initiation of questing activity of H. concinna. Three notably different morphotypes and four malformed specimens of I. ricinus were found. However, these were not significantly different in their mitochondrial haplotypes and phylogenetic clustering from typical specimens of this species. On the other hand, I. frontalis was represented by two remarkably different haplogroups, between which in the nymph stage there were no recognizable morphological differences, suggesting the status of these as cryptic species.