Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics

Abstract

Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.

Fig. 1

Map of the study area, showing the 3 forests and 27 clearcut sites. The light grey area shows the extent of the forest. The darker grey area is a reservoir.

Fig. 2

Mean number of field voles caught at a site in each survey for (A) Redesdale, (B) Kielder and (C) Kershope forests. Bars are standard errors.

Fig. 3

Boxplot of the prevalences of (A) fleas; (B) Bartonella doshiae; (C) B. grahamii, (D) B. taylorii and (E) BGA at the 27 sites in each of the 7 surveys. Middle bar shows the median site prevalence. Note that no flea data are available for autumn 2001 (a01).

Fig. 4

Results of logistic regressions for flea infestation probabilities with the following clearcut field vole density estimates as explanatory variables: 12-month lag (A, B); 6 month lag (C, D) and 0 lag (E, F). Data were split by season, with A, C and E showing relationships in spring and B, D and F showing relationships in autumn. The graphs show the raw data by incorporating frequency histograms for individuals not infested with fleas (bottom histograms) and individuals infested with fleas (top histograms).