Habitat Factors Associated with Bank Voles (Clethrionomys glareolus) and Concomitant Hantavirus in Northern Sweden

Abstract

Puumala virus (PUUV), genus hantavirus, causes nephropathia epidemica, a mild form of hemorrhagic fever with renal syndrome in humans. In this study, bank voles, the natural reservoir of PUUV, were captured at locations of previous human PUUV exposure and paired controls within a region of high incidence in northern Sweden. The aim of the study was to evaluate the influence of environmental factors on the abundance of bank voles and the occurrence of PUUV. The total number of voles and the number of PUUV-infected voles did not differ between locations of previous human PUUV exposure and paired controls. The number of bank voles expressing antibodies to PUUV infection increased linearly with total bank vole abundance implying density independent transmission. Using principal component and partial correlation analysis, we found that particular environmental characteristics associated with old-growth moist forests (i.e., those dominated by Alectoria spp., Picea abies, fallen wood, and Vaccinium myrtillus) were also associated with increased abundance of bank vole and hence the number of PUUV-infected bank voles, whereas there were no correlations with factors associated with dry environments (i.e., Pinus sylvestris and V. vitis-idea). This suggests that circulation and persistence of PUUV within bank vole populations was influenced by habitat factors. Future modeling of risk of exposure to hantavirus and transmission of PUUV within vole populations should include the influence of these factors.

Spatial and temporal variation of hantavirus bank vole infection in managed forest landscapes

“…1). These results regarding the importance of old forest are in line with similar findings by Olsson et al (2005) and Voutilainen et al (2012). In contrast to both of these studies, we also studied the distribution of infected voles at the landscape scale and also the occurrence on mires on the habitat scale, which represent an important habitat in our study area and boreal areas in general (Ahti et al 1968) and to our knowledge has never been studied previously with respect to PUUV distribution.…”

“…As old, often spruce-dominated forest is the main habitat of bank voles (Hansson 1978, Olsson et al 2005, the negative effect of forestry on the occurrence of PUUV antibody positive voles in spring has likely resulted from clear cutting and converting such forest into cut-over forest. As reported by Stenbacka et al (2010), young, thinned forests lack many forest structures commonly found in old forest, such as coarse downed logs, implying a decrease in shelter against predators and increasing predation risk.…”

“…Nephropathia epidemica (NE) is a milder variant of HFRS caused by the hantavirus Puumala virus (PUUV) present in many parts of Europe (Olsson et al 2010), and bank voles (Myodes glareolus) are the natural reservoir (Brummer-Korvenkontio et al 1980, Yanagihara et al 1984. The epidemiology of NE is closely linked to the temporal and spatial dynamics of the bank vole (Niklasson et al 1995, Olsson et al 2005, Voutilainen et al 2012. In Sweden, approximately 90% of all diagnosed cases are found in the northern part of the country .…”

“…Prior to the 1950s, the landscape was dominated by old forests that had never been clear-cut, but by 2005 the landscape consisted of approximately 40 % cut-over forests (Ecke et al 2013). Bank voles are affected by forestry, as high densities of bank voles are associated with dead wood providing shelter (Ecke et al 2002, Olsson et al 2005. Furthermore, the winter survival of voles is higher in old forests (Ecke et al 2002, Savola et al 2013) and in spring, voles are found in these core habitats where winter survival is best.…”

“…Because of this density-dependent factor, bank voles need large forest stands to be able to build up large local populations. As large populations usually are accompanied by a high density of infected bank voles (hereafter infection load, IL; Olsson et al 2005, Voutilainen et al 2012, we hypothesize that the occurrence of virus infected individuals may be positively related to the size of the forest patch surrounding the sampling plot (i.e., the focal patch size of old forest). Since bank voles' overwinter survival is poor in young forests (Ecke et al 2002, Savola et al 2013, and overwinter survival is lower for infected than non-infected bank voles (Kallio et al 2007), we also hypothesize that winter survival and subsequent numbers of infected voles in spring would be decreased by poor-quality landscapes with high proportions of young forest.…”