Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens

Abstract

Background Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. Methods We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. Results Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. Conclusions The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern. Graphic abstract

Prevalence and predictors of vector-borne pathogens in Dutch roe deer

“…This relatively high prevalence supports a primary role of roe deer in the maintenance of A. phagocytophilum in the Netherlands [ 58 ]. However, this is presumably the commonly detected non-zoonotic ecotype II [ 16 , 18 , 19 , 59 , 60 ]. Anaplasma phagocytophilum causes disease by infecting phagocytic cells, mainly neutrophils, in which it replicates and spreads to tissues [ 20 ].…”

The circulation of Anaplasma phagocytophilum ecotypes is associated with community composition of vertebrate hosts

“…Furthermore, we identified two new species for which data were lacking, fallow deer and western European hedgehog. In recent years, some papers have been published regarding some of these species, which we either included in our meta‐analysis (Coipan et al, 2018; Jahfari et al, 2017; e.g., Mysterud et al, 2015) or which did not fulfill our selection criteria (e.g., Dziemian et al, 2015; Fabri et al, 2021; Furness & Furness, 2018; Hofmeester et al, 2018; Marsot et al, 2012; Mysterud et al, 2021). In addition, our knowledge on infection prevalence of feeding I. ricinus with A. phagocytophilum is especially limited, with only data for 19 vertebrate host species (of the 77 species included in this study).…”

“…A similar pattern might be true for fallow deer that show a similar increase in distribution and population size throughout Europe (Apollonio et al, 2010), although data on tick burdens and A. phagocytophilum infection prevalence for this species are sparse. A recent study, however, found that fallow deer likely play an important role in the transmission of A. phagocytophilum (Fabri et al, 2021). Furthermore, our results suggest an important role for fluctuations in small mammal densities in determining the prevalence of mainly A. phagocytophilum Ecotype 3, but also of Ecotype 1.…”

Is composition of vertebrates an indicator of the prevalence of tick-borne pathogens?

“…The relative importance of several vertebrates in the epidemiology of Lyme borreliosis in Europe has been addressed in literally dozens of studies: not only the key role of rodents or birds as reservoirs of some species [i.e., 16 , 41 , 42 ] but also the dual role played by some taxa like large ungulates on the amplification/dilution of the pathogen [i.e., 43 , 44 ]. In the USA, research has been partly focused on the life history traits of different vertebrates, aiming to find a correlate of their contributions to the infection rates of ticks by B. burgdorferi s.l.…”