Sampling scale and season influence the observed relationship between the density of deer and questing Ixodes ricinus nymphs

Abstract

Background The relationship between environmentally transmitted tick parasites, Ixodes spp., and their main reproductive host, deer, is generally thought to be positive. However, measuring host abundance and density directly can be challenging and indirect methods are often used. The observed relationship between the parasite and host may be affected by sampling scale and season, which could lead to different inferences being made. Here, we aimed to test the effect of sampling scale and season on the relationship between density of deer and the density of questing Ixodes ricinus nymphs. Methods The density of deer (primarily Dama dama) was estimated using line transect distance sampling of deer dung quantified in different seasons (winter and summer) and measured at three different nested scales (site, transect and observation level). Questing nymph density was measured using blanket drag methods and estimates were calculated at the same scales as deer density estimates. General linear models were used to evaluate the relationship between questing nymphs, deer density and other environmental variables at each sampling scale and each season deer density was measured at. Results While a positive relationship between deer density and questing nymph density was detected at the site and transect scale, no relationship was apparent at the observation level. This was likely due to increased variation and reduced precision of deer dung counts at the finest sampling scale. Seasonal changes in deer populations were observed likely reflecting seasonal shifts in habitat usage. The summer estimates of deer density explained questing nymph density whereas winter estimates did not. Conclusions Our results show that the scale of sampling can affect the detectability of the positive association between host and vector species. Furthermore, such associations can be obscured if hosts exhibit seasonal changes in habitat use. Thus, both sampling scale and season are important to consider when investigating the relationship between host and vector species.

Using mechanistic models to highlight research priorities for tick-borne zoonotic diseases: Improving our understanding of the ecology and maintenance of Kyasanur Forest Disease in India

“…If ticks do play a significant role in maintaining KFD, cattle may play an important role by acting as widely available reproductive hosts for female adult ticks and influencing abundance and distribution of ticks. A number of other studies have highlighted similar roles of larger mammals in tick-borne disease systems in Europe, showing the important role of deer influencing abundance and distribution of I. ricinus in Europe (Dickinson et al, 2020; Gilbert et al, 2012; Hofmeester et al, 2017) and the potential for non-systemic transmission through co-feeding on sheep (a non-competent host) in maintaining B. burgdorferi (Ogden et al, 1997). The limited empirical data on the number and life stage ticks parasitising cattle in KFD-affected regions has also been largely collected in agricultural settings (Balasubramanian et al, 2019) rather than in the specific agro-forest mosaics in which spillover is occurring.…”

“…The first scaling factor was used to account for the potential influence of cattle density on tick abundance and burden. As there are no data available from India on the rate of increase in tick abundance as a result of increased cattle density, we use results from a different disease system that outlines the rate of increase in the density of questing nymphs in relation to the density of deer (0.026) (Dickinson et al, 2020). This scaling factor was applied to the number of eggs produced by adult females and to all parameters related to tick burden (Eq.2).…”

No net effect of host density on tick‐borne disease hazard due to opposing roles of vector amplification and pathogen dilution

“…The highest deer density in our study was 31 deer per km 2 , which is below the threshold predicted in that study and could explain why we did not detect this quadratic relationship. However, another study conducted in Scotland investigated the correlation between questing nymphs and deer density and observed a linear correlation, even when deer density reached 50 deer/km 2 , which implies that this threshold might be higher in Europe (Dickinson et al, 2020).…”

Using mechanistic models to highlight research priorities for tick-borne zoonotic diseases: Improving our understanding of the ecology and maintenance of Kyasanur Forest Disease in India

“…Currently, there are no data available from India on the rate of increase in tick abundance as a result of increased cattle density. This relationship has been quantified for large wild ungulates in Europe and given a lack of data we used results from a different disease system that outlines the rate of increase in the density of questing nymphs in relation to the density of deer (0.026) [ 50 ]. As above, this scaling factor was applied to the number of eggs produced by adult females and to all parameters related to tick burden ( Eq 3 ).…”