Environmental Change and Disease Dynamics: Effects of Intensive Forest Management on Puumala Hantavirus Infection in Boreal Bank Vole Populations

Abstract

Intensive management of Fennoscandian forests has led to a mosaic of woodlands in different stages of maturity. The main rodent host of the zoonotic Puumala hantavirus (PUUV) is the bank vole (Myodes glareolus), a species that can be found in all woodlands and especially mature forests. We investigated the influence of forest age structure on PUUV infection dynamics in bank voles.Over four years, we trapped small mammals twice a year in a forest network of different succession stages in Northern Finland. Our study sites represented four forest age classes from young (4 to 30 years) to mature (over 100 years) forests. We show that PUUV-infected bank voles occurred commonly in all forest age classes, but peaked in mature forests. The probability of an individual bank vole to be PUUV infected was positively related to concurrent host population density. However, when population density was controlled for, a relatively higher infection rate was observed in voles trapped in younger forests. Furthermore, we found evidence of a “dilution effect” in that the infection probability was negatively associated with the simultaneous density of other small mammals during the breeding season.Our results suggest that younger forests created by intensive management can reduce hantaviral load in the environment, but PUUV is common in woodlands of all ages. As such, the Fennoscandian forest landscape represents a significant reservoir and source of hantaviral infection in humans.

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

“…In summer, reproduction in disturbed habitats, such as clear-cuts, could be as high as in old forest or even higher (Ecke et al 2002). Voutilainen et al (2012) found that PUUV infection rate of bank voles was higher in young than in old forest habitats. However, since the population density of bank voles was highest in old forests, these habitats had higher densities of PUUV infected voles (Voutilainen et al 2012).…”

“…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 .…”

“…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.…”

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

“…Our results suggest that individual variations of immune gene expression could reinforce these differences in the epidemiological roles of particular bank vole groups within natural populations. In particular, males, through higher capacities to replicate, excrete PUUV, and to perform long-distance dispersal (Kozakiewicz et al, 2007), could have key roles in spreading PUUV within the landscape (Deter et al, 2008a;Voutilainen et al, 2012). The lower expression of Mx2 gene detected in immature voles could also have important epidemiological consequences for PUUV transmission.…”

Dampening of population cycles in voles affects small mammal community structure, decreases diversity, and increases prevalence of a zoonotic disease

“…The annual incidence of NE in humans can be explained with high degree (84% of variability) by density of M. glareolus in autumn and the number of rainy days in winter (Khalil, Olsson, et al., 2014). In contrast, the number of PUUV‐infected bank voles and PUUV prevalence (the proportion of infected bank voles) has been shown to be affected by habitat type (Magnusson, Ecke, et al., 2015; Voutilainen et al., 2012). …”