Magnus Magnusson

Dynamics and Drivers of Hantavirus Prevalence in Rodent Populations

Human encroachment on wildlife habitats has contributed to the emergence of several zoonoses. Pathogenic hantaviruses are hosted by rodents and cause severe diseases in the Americas and Eurasia. We reviewed several factors that potentially drive prevalence (the proportion of infected rodents) in host populations. These include demography, behavior, host density, small mammal diversity, predation, and habitat and landscape characteristics. This review is the first to include a quantitative summary of the literature investigating hantavirus prevalence in rodents. Demographic structure and density were investigated the most and predation the least. Reported effects of demographic structure and small mammal diversity were consistent, whereby reproductive males were most likely to be infected and prevalence decreased with small mammal diversity. The influences of habitat and landscape properties are often complex and indirect. The relationship between density and prevalence merits more investigation. Most hantavirus hosts are habitat generalists and their control is challenging. Incorporating all potential factors and their interactions is essential to understanding and controlling infection in host populations.

The importance of bank vole density and rainy winters in predicting nephropathia epidemica incidence in Northern Sweden.

Pathogenic hantaviruses (family Bunyaviridae, genus Hantavirus) are rodent-borne viruses causing hemorrhagic fever with renal syndrome (HFRS) in Eurasia. In Europe, there are more than 10,000 yearly cases of nephropathia epidemica (NE), a mild form of HFRS caused by Puumala virus (PUUV). The common and widely distributed bank vole (Myodes glareolus) is the host of PUUV. In this study, we aim to explain and predict NE incidence in boreal Sweden using bank vole densities. We tested whether the number of rainy days in winter contributed to variation in NE incidence. We forecast NE incidence in July 2013–June 2014 using projected autumn vole density, and then considering two climatic scenarios: 1) rain-free winter and 2) winter with many rainy days. Autumn vole density was a strong explanatory variable of NE incidence in boreal Sweden in 1990–2012 (R2 = 79%, p<0.001). Adding the number of rainy winter days improved the model (R2 = 84%, p<0.05). We report for the first time that risk of NE is higher in winters with many rainy days. Rain on snow and ground icing may block vole access to subnivean space. Seeking refuge from adverse conditions and shelter from predators, voles may infest buildings, increasing infection risk. In a rainy winter scenario, we predicted 812 NE cases in boreal Sweden, triple the number of cases predicted in a rain-free winter in 2013/2014. Our model enables identification of high risk years when preparedness in the public health sector is crucial, as a rainy winter would accentuate risk.

Spatiotemporal changes in the landscape structure of forests in northern Sweden

Abstract Altered forest landscape structure has been suggested as a possible cause for the decline of some specialized forest species in Fennoscandia. Here, we present a time series of boreal landscape changes in 1954–2005 in 16 5×5 km sub-areas in Sweden, based on aerial photo interpretation. We explored how coniferous forest vegetation types, known to be important to some specialized forest species, have been fragmented and also declined in mean patch size and their proportion of the landscape. We divided the studied area into a western (inland) and eastern (coastal) part based on different timing of landscape changes. The mean patch area of forest >50 yrs declined from ~90 ha in 1954 to 10 ha in 2005 in the inland and from 30 ha to only ~5 ha patches in the coastal area. Common vegetation types, such as mesic and moist forest >50 yrs showed a similar declining trend. In our study area, the long-term decline 1971–2005 of the specialized forest species grey-sided vole (Myodes rufocanus) coincided with the decline of mean focal patch size of forest >50 yrs. The data presented here can be used in further analyses of species–landscape interactions along spatiotemporal gradients.

Declining ecosystem health and the dilution effect

The “dilution effect” implies that where species vary in susceptibility to infection by a pathogen, higher diversity often leads to lower infection prevalence in hosts. For directly transmitted pathogens, non-host species may “dilute” infection directly (1) and indirectly (2). Competitors and predators may (1) alter host behavior to reduce pathogen transmission or (2) reduce host density. In a well-studied system, we tested the dilution of the zoonotic Puumala hantavirus (PUUV) in bank voles (Myodes glareolus) by two competitors and a predator. Our study was based on long-term PUUV infection data (2003–2013) in northern Sweden. The field vole (Microtus agrestis) and the common shrew (Sorex araneus) are bank vole competitors and Tengmalm’s owl (Aegolius funereus) is a main predator of bank voles. Infection probability in bank voles decreased when common shrew density increased, suggesting that common shrews reduced PUUV transmission. Field voles suppressed bank vole density in meadows and clear-cuts and indirectly diluted PUUV infection. Further, Tengmalm’s owl decline in 1980–2013 may have contributed to higher PUUV infection rates in bank voles in 2003–2013 compared to 1979–1986. Our study provides further evidence for dilution effect and suggests that owls may have an important role in reducing disease risk.

Evidence for different drivers behind long-term decline and depression of density in cyclic voles

Decline and long-term depression of mean densities of the grey-sided vole (Myodes rufocanus) and the field vole (Microtus agrestis) have occurred in managed forest landscapes of Sweden since the 1970s. Generally poor over-winter survival during a period with mild winters suggested a common climatic driver, but other explanations exist. Here we explore the response of the grey-sided vole, preferring forested habitats, and the field vole, preferring open habitats, to clear-cutting of old forest in Sweden. The cumulated impact from long-term clear-cutting explained local disappearances of the grey-sided vole. Maintained connectivity of old forest to stone fields was important for local population survival, since no such populations disappeared. For the grey-sided vole, it is probable that climate is not the dominating driver due to different timing of the decline in our study area. Instead, habitat loss is concluded as being a potential cause of the decline in mean density and depression of grey-sided vole densities. The long-lasting depression of field vole densities, despite favourable landscape changes, suggests action of another strong driver. A recent field vole recovery, essentially back to pre-decline densities and distribution, coincided with favourable winter/snow conditions, suggesting a climatic driver in this case.

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

Zoonoses are major contributors to emerging infectious diseases globally. Hemorrhagic fever with renal syndrome (HFRS) is a zoonosis caused by rodent-borne hantaviruses. In Europe, Puumala hantavir ...

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

Abstract Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.

Red-listed wood-inhabiting fungi in natural and managed forest landscapes adjacent to the timberline in central Sweden

Many wood-inhabiting fungi are today threatened as modern forestry practices drastically reduce the amount of dead wood available in various forest ecosystems. We investigated whether the occurrence of red-listed wood-inhabiting fungi differed between natural and managed forest landscapes adjacent to the timberline in the middle part of Sweden. We assessed whether environmental variables such as the degree of human impact, length of forest roads, dead wood volume and quality affected species richness and abundance. The effects of forestry on wood-inhabiting fungi have been assessed in several studies in lowland Swedish forests. Few studies have, however, been conducted in forest landscapes adjacent to the timberline in Sweden. This is potentially important since forests close to the Swedish mountains have been pointed out as one of few intact forest landscapes in Fennoscandia and they are subjected to increasing logging pressure. Similar to other studies, species numbers and abundances were positively correlated with larger volumes of logs in various decay stages. However, never shown previously, the length of forest roads was negatively correlated with species abundance and occurrence of red-listed species. We suggest that a low amount of forest roads can be used as a conservation indicator to localize still-intact forest landscapes.

DISTRIBUTION AND SEASONAL VARIATION OF LJUNGAN VIRUS IN BANK VOLES (MYODES GLAREOLUS) IN FENNOSCANDIA

Abstract Ljungan virus (LV) is a picornavirus originally isolated from Swedish bank voles (Myodes glareolus) in 1998. The association of LV with human disease has been debated ever since, but fundamental data on the ecology of the virus are still lacking. Here we present results of the first intensive study on the prevalence of LV in bank voles trapped in Fennoscandia (Sweden and Finland) from 2009–12 as determined by PCR. Using an LV-specific real-time reverse transcriptase PCR, LV was detected in the liver of 73 out of 452 (16.2%) individuals and in 13 out of 17 sampling sites across Sweden and Finland (mean per site prevalence 16%, SE 3%, range 0–50%). We found more infected animals in autumn compared to spring, and lighter and heavier individuals had a higher prevalence than those with intermediate body masses. The result that LV prevalence is also lower in heavier (i.e., older) animals suggests for the first time that LV infection is not persistent in rodents.