Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany

Abstract

Identifying factors affecting individual vector burdens is essential for understanding infectious disease systems. Drawing upon data of a rodent monitoring programme conducted in nine different forest patches in southern Hesse, Germany, we developed models which predict tick (Ixodes spp. and Dermacentor spp.) burdens on two rodent species Apodemus flavicollis and Myodes glareolus. Models for the two rodent species were broadly similar but differed in some aspects. Patterns of Ixodes spp. burdens were influenced by extrinsic factors such as season, unexplained spatial variation (both species), relative humidity and vegetation cover (A. flavicollis). We found support for the ‘body mass’ (tick burdens increase with body mass/age) and for the ‘dilution’ hypothesis (tick burdens decline with increasing rodent densities) and little support for the ‘sex-bias’ hypothesis (both species). Surprisingly, roe deer densities were not correlated with larvae counts on rodents. Factors influencing the mean burden did not significantly explain the observed dispersion of tick counts. Co-feeding aggregations, which are essential for tick-borne disease transmission, were mainly found in A. flavicollis of high body mass trapped in areas with fast increase in spring temperatures. Locally, Dermacentor spp. appears to be an important parasite on A. flavicollis and M. glareolus. Dermacentor spp. was rather confined to areas with higher average temperatures during the vegetation period. Nymphs of Dermacentor spp. mainly fed on M. glareolus and were seldom found on A. flavicollis. Whereas Ixodes spp. is the dominant tick genus in woodlands of our study area, the distribution and epidemiological role of Dermacentor spp. should be monitored closely.

The wild life of tick-borne pathogens

“…Our results regarding intrinsic factors are consistent with previous studies, which showed higher tick burdens on males compared to females 215 , an increase in tick burden with increasing body mass of the host 95,215 and higher tick burdens on Apodemus mice compared to Bank voles 89,95 . These differences have been attributed both to differences in day range between host individuals 215 and differences in resistance against or tolerance for parasites between host species 13,23 .…”

“…These differences have been attributed both to differences in day range between host individuals 215 and differences in resistance against or tolerance for parasites between host species 13,23 . Our results regarding extrinsic factors (deer and predator abundance, and rodent density) are also consistent with previous studies, which Determinants of Tick Burden on Rodents | 89 found an increase in larval burden on rodents with increasing deer density 32 and a decreasing larval burden with increasing rodent density 95,227 . However, we are the first to report a decrease in tick burden with increasing relative abundance of predators.…”

“…We measured the tick burden on three rodent species, Bank vole (Myodes glareolus), Field vole (Microtus agrestis), and Wood mouse (Apodemus sylvaticus) in 20 forest plots in the Netherlands that differed strongly in their vertebrate assemblage composition, and related these to both intrinsic and extrinsic factors. The intrinsic factors were species, sex and body mass, which are known determinants of tick burden on small mammals 32,89,95,215 . The extrinsic factors were the relative abundance of deer, the relative abundance of predators and rodent density.…”

“…Evidence for these mechanisms is sparse. In Europe, where rodents are important reservoir hosts for several tick-borne pathogens 50 , two studies have linked some variation in rodent tick-burden to variation in deer density (positive correlation) 32 and rodent density (negative correlation) 95 , but left a large part of the variation unexplained. Neither study considered predators of rodents.…”

“…N. mikurensis 50 -between twenty forest plots that differed in their vertebrate assemblage composition. Based on the theoretical mechanisms of Keesing et al 31 and the empirical evidence of Cagnacci et al 32, and Kiffner et al 95 , we propose six relationships between predator, deer and rodent density, tick burden on rodents and DIN for rodent-transmitted tick-borne pathogens ( Figure 6.1): 1) tick burden on rodents increases with the density of deer, important maintenance hosts for adult female I. ricinus that can therefore increase the number of immature ticks in the environment 32,190 (vector augmentation); 2) tick burden on rodents decreases with rodent density because ticks are distributed over more individuals and because rodents decrease their spatial activity, decreasing encounter rate 95,213 (encounter reduction); 3) tick burden on rodents decreases with predator density because rodents decrease their activity in response to predation risk, decreasing encounter rate 214 (encounter reduction); 4) rodent density decreases with predator density (reservoir host regulation) 31,160 ; 5) the DIN of rodent-transmitted tick-borne pathogens increases with per-capita tick burden on rodents, because the chance of individuals becoming infected with a pathogen by feeding an infected nymph increases with tick burden, and each infected individual will infect more larvae, resulting in a higher DIN irrespective of rodent density; and 6) for a given per-capita tick burden, the DIN of rodenttransmitted tick-borne pathogens increases with rodent density 33 .…”