Individual heterogeneity in ixodid tick infestation and prevalence of Borrelia burgdorferi sensu lato in a northern community of small mammalian hosts

Heterogeneous aggregation of parasites between individual hosts is common and regarded as an important factor in understanding transmission dynamics of vector-borne diseases. Lyme disease is vectored by generalist tick species, yet we have a limited understanding of how individual heterogeneities within small mammal host populations affect the aggregation of ticks and likelihood of infection. Male hosts often have higher parasite and infection levels than females, but whether this is linked to sexual body size dimorphism remains uncertain. Here, we analysed how host species, sex, and body mass influenced Ixodes ricinus tick infestations and the infection prevalence of Borrelia burgdorferi sensu lato (s.l.) in three species of small mammals involved in the enzootic transmission cycle of Lyme disease in Norway from 2018 to 2022. Larval and nymphal ticks were found on 98% and 34% of all individual hosts, respectively. In bank voles and wood mice, both larval and nymphal tick infestation and infection probability increased with body mass, and it increased more with mass for males than for females. Tick infestation in the common shrew increased with body mass and was higher in males, while pathogen infection was higher in females. Sex-biases in infestation did not correspond with level of sexual body mass dimorphism across species. This study contributes to our understanding of how individual heterogeneity among small mammalian hosts influences I. ricinus tick aggregation and prevalence of B. burgdorferi s.l. at northern latitudes. Supplementary Information The online version contains supplementary material available at 10.1007/s00442-023-05476-w.


Figure S2 :
Figure S2: Predicted Ixodes nymph intensity as a function of sex and log-transformed body mass centred by species in (a) bank vole (M.glareolus) and (b) wood mouse (A.sylvaticus) captured in South-East Norway (2018-2022).The x-axis is on log-scale, and x-axis labels denote back-transformed values of body mass (g).Shaded areas denote respective 95% confidence intervals, points denote raw data observations, and dashed lines denote mean body mass.

Figure S3 :
Figure S3: Predicted prevalence of B. burgdorferi s.l. as a function of sex and if nymphs were found on the host in (a) bank vole (M.glareolus) and (b) wood mouse (A.sylvaticus) captured in South-East Norway (2018-2022).Predicted values are shown for body mass = mean logtransformed body mass of each species.Error bars denote respective 95% confidence intervals.

Table S1 :
Sequences and adjusted primer set and probe concentrations in respective multiplex real-time quantitative PCR assays for detecting B. burgdorferi s.l. and A. phagocytophilum and I. ricinus and I. trianguliceps, with respective target genes, product size (bp), sequences, and concentration (µM).Infection prevalence of A. phagocytophilum was not considered in the present study.

Table S2 :
An overview of samples sizes of captured small mammals per season between 2018 and 2022 in Son, Viken county, Norway.

Table S3 :
Overview of individual larval and nymphal ticks from captured small mammal hosts in Son, Viken county, Norway between 2018-2022, identified by species using a multiplex real-time quantitative PCR assay(2018)(2019)and by morphology (2020-2022).

Table S4 :
An overview of sample sizes of each tick species from captured small mammalian hosts between 2018 and 2022 in Son, Viken county, Norway.The table shows the number of individuals of larval and nymphal ticks per species, the total number of ticks including unidentified ticks, the percentage of Ixodes ricinus of all species identified ticks (% I. ricinus), and percentage of species-determined ticks (% SDT) by morphology and qPCR per small mammal species.

Table S5 :
Results of model selection of body mass in bank voles, wood mice, and common shrews captured inSouth-East Norway (2018-2022)as a function of season, sex, species, and their interactions.Gravid females were excluded from the analysis.The table shows the parameters included in the top five models (+), number of parameters (df), AIC, and model weight.The model used for inference is highlighted in grey.

Table S6 :
Parameter estimates from the generalized linear mixed models of larval Ixodes tick intensity and presence of Ixodes nymphs on small mammals captured in South-East Norway (2018-2022) as a function of whether the host was found alive or dead (live/dead), logtransformed body mass, and their interaction.
[1]: Corresponds to an individual of body mass = 1 g captured and found dead.

Table S7 :
Model selection results of A) number of Ixodes larvae, B) presence of Ixodes nymphs, and C) prevalence of B. burgdorferi s.l. in small mammals captured in South-East Norway(2018)(2019)(2020)(2021)(2022).The table shows the parameters included in the top five models (+), number of parameters (df), AIC, and model weight.Body mass (mass) was log-transformed and species-centred.Models used for inference are highlighted in grey.

Table S8 :
Results of model selection of A)Ixodes nymph intensity, and B) prevalence of B. burgdorferi s.l. in bank vole (M.glareolus) and wood mouse (A.sylvaticus) captured inSouth-East Norway (2018-2022).The table shows the parameters included in the top five models (+), number of parameters (df), AIC, and model weight.Body mass (mass) was logtransformed and species-centred.Models used for inference are highlighted in grey.