Taking the beat of the Arctic: are lemming population cycles changing due to winter climate?

Reports of fading vole and lemming population cycles and persisting low populations in some parts of the Arctic have raised concerns about the spread of these fundamental changes to tundra food web dynamics. By compiling 24 unique time series of lemming population fluctuations across the circumpolar region, we show that virtually all populations displayed alternating periods of cyclic/non-cyclic fluctuations over the past four decades. Cyclic patterns were detected 55% of the time (n = 649 years pooled across sites) with a median periodicity of 3.7 years, and non-cyclic periods were not more frequent in recent years. Overall, there was an indication for a negative effect of warm spells occurring during the snow onset period of the preceding year on lemming abundance. However, winter duration or early winter climatic conditions did not differ on average between cyclic and non-cyclic periods. Analysis of the time series shows that there is presently no Arctic-wide collapse of lemming cycles, even though cycles have been sporadic at most sites during the last decades. Although non-stationary dynamics appears a common feature of lemming populations also in the past, continued warming in early winter may decrease the frequency of periodic irruptions with negative consequences for tundra ecosystems.

Mystery of fatal 'staggering disease' unravelled: novel rustrela virus causes severe meningoencephalomyelitis in domestic cats.

'Staggering disease' is a neurological disease entity considered a threat to European domestic cats (Felis catus) for almost five decades. However, its aetiology has remained obscure. Rustrela virus (RusV), a relative of rubella virus, has recently been shown to be associated with encephalitis in a broad range of mammalian hosts. Here, we report the detection of RusV RNA and antigen by metagenomic sequencing, RT-qPCR, in-situ hybridization and immunohistochemistry in brain tissues of 27 out of 29 cats with non-suppurative meningoencephalomyelitis and clinical signs compatible with'staggering disease' from Sweden, Austria, and Germany, but not in non-affected control cats. Screening of possible reservoir hosts in Sweden revealed RusV infection in wood mice (Apodemus sylvaticus). Our work indicates that RusV is the long-sought cause of feline 'staggering disease'. Given its reported broad host spectrum and considerable geographic range, RusV may be the aetiological agent of neuropathologies in further mammals, possibly even including humans.

Population fluctuations and synanthropy explain transmission risk in rodent-borne zoonoses.

Population fluctuations are widespread across the animal kingdom, especially in the order Rodentia, which includes many globally important reservoir species for zoonotic pathogens. The implications of these fluctuations for zoonotic spillover remain poorly understood. Here, we report a global empirical analysis of data describing the linkages between habitat use, population fluctuations and zoonotic reservoir status in rodents. Our quantitative synthesis is based on data collated from papers and databases. We show that the magnitude of population fluctuations combined with species' synanthropy and degree of human exploitation together distinguish most rodent reservoirs at a global scale, a result that was consistent across all pathogen types and pathogen transmission modes. Our spatial analyses identified hotspots of high transmission risk, including regions where reservoir species dominate the rodent community. Beyond rodents, these generalities inform our understanding of how natural and anthropogenic factors interact to increase the risk of zoonotic spillover in a rapidly changing world.

Puumala Orthohantavirus Infection Does Not Affect the Trapping Success of Its Reservoir Host.

Pathogens might affect behavior of infected reservoir hosts and hence their trappability, which could bias population estimates of pathogen prevalence. In this study, we used snap-trapping data on Puumala orthohantavirus (PUUV)-infected (n = 1619) and noninfected (n = 6940) bank voles (Myodes glareolus) from five vole cycles, normally representing increase, peak, and decline phase, to evaluate if infection status affected trapping success. If PUUV infection, as previously suggested, increases activity and/or mobility, we would expect a higher proportion of infected than noninfected specimens in the first trapping night. However, the proportion of PUUV-infected voles did not differ across the three trapping nights. We conclude that PUUV infection did not affect trapping success, confirming snap trapping as an appropriate trapping method for studies on PUUV prevalence and likely other orthohantaviruses.

Climate change accelerates winter transmission of a zoonotic pathogen.

Many zoonotic diseases are weather sensitive, raising concern how their distribution and outbreaks will be affected by climate change. At northern high latitudes, the effect of global warming on especially winter conditions is strong. By using long term monitoring data (1980-1986 and 2003-2013) from Northern Europe on temperature, precipitation, an endemic zoonotic pathogen (Puumala orthohantavirus, PUUV) and its reservoir host (the bank vole, Myodes glareolus), we show that early winters have become increasingly wet, with a knock-on effect on pathogen transmission in its reservoir host population. Further, our study is the first to show a climate change effect on an endemic northern zoonosis, that is not induced by increased host abundance or distribution, demonstrating that climate change can also alter transmission intensity within host populations. Our results suggest that rainy early winters accelerate PUUV transmission in bank voles in winter, likely increasing the human zoonotic risk in the North.

Evolutionary Relationships of Ljungan Virus Variants Circulating in Multi-Host Systems across Europe.

The picornavirus named 'Ljungan virus' (LV, species Parechovirus B) has been detected in a dozen small mammal species from across Europe, but detailed information on its genetic diversity and host specificity is lacking. Here, we analyze the evolutionary relationships of LV variants circulating in free-living mammal populations by comparing the phylogenetics of the VP1 region (encoding the capsid protein and associated with LV serotype) and the 3Dpol region (encoding the RNA polymerase) from 24 LV RNA-positive animals and a fragment of the 5' untranslated region (UTR) sequence (used for defining strains) in sympatric small mammals. We define three new VP1 genotypes: two in bank voles (Myodes glareolus) (genotype 8 from Finland, Sweden, France, and Italy, and genotype 9 from France and Italy) and one in field voles (Microtus arvalis) (genotype 7 from Finland). There are several other indications that LV variants are host-specific, at least in parts of their range. Our results suggest that LV evolution is rapid, ongoing and affected by genetic drift, purifying selection, spillover and host evolutionary history. Although recent studies suggest that LV does not have zoonotic potential, its widespread geographical and host distribution in natural populations of well-characterized small mammals could make it useful as a model for studying RNA virus evolution and transmission.

Geographical Distribution and Genetic Diversity of Bank Vole Hepaciviruses in Europe.

The development of new diagnostic methods resulted in the discovery of novel hepaciviruses in wild populations of the bank vole (Myodes glareolus, syn. Clethrionomys glareolus). The naturally infected voles demonstrate signs of hepatitis similar to those induced by hepatitis C virus (HCV) in humans. The aim of the present research was to investigate the geographical distribution of bank vole-associated hepaciviruses (BvHVs) and their genetic diversity in Europe. Real-time reverse transcription polymerase chain reaction (RT-qPCR) screening revealed BvHV RNA in 442 out of 1838 (24.0%) bank voles from nine European countries and in one of seven northern red-backed voles (Myodes rutilus, syn. Clethrionomys rutilus). BvHV RNA was not found in any other small mammal species (n = 23) tested here. Phylogenetic and isolation-by-distance analyses confirmed the occurrence of both BvHV species (Hepacivirus F and Hepacivirus J) and their sympatric occurrence at several trapping sites in two countries. The broad geographical distribution of BvHVs across Europe was associated with their presence in bank voles of different evolutionary lineages. The extensive geographical distribution and high levels of genetic diversity of BvHVs, as well as the high population fluctuations of bank voles and occasional commensalism in some parts of Europe warrant future studies on the zoonotic potential of BvHVs.

Geographical Distribution of Ljungan Virus in Small Mammals in Europe.

Ljungan virus (LV), which belongs to the Parechovirus genus in the Picornaviridae family, was first isolated from bank voles (Myodes glareolus) in Sweden in 1998 and proposed as a zoonotic agent. To improve knowledge of the host association and geographical distribution of LV, tissues from 1685 animals belonging to multiple rodent and insectivore species from 12 European countries were screened for LV-RNA using reverse transcriptase (RT)-PCR. In addition, we investigated how the prevalence of LV-RNA in bank voles is associated with various intrinsic and extrinsic factors. We show that LV is widespread geographically, having been detected in at least one host species in nine European countries. Twelve out of 21 species screened were LV-RNA PCR positive, including, for the first time, the red vole (Myodes rutilus) and the root or tundra vole (Alexandromys formerly Microtus oeconomus), as well as in insectivores, including the bicolored white-toothed shrew (Crocidura leucodon) and the Valais shrew (Sorex antinorii). Results indicated that bank voles are the main rodent host for this virus (overall RT-PCR prevalence: 15.2%). Linear modeling of intrinsic and extrinsic factors that could impact LV prevalence showed a concave-down relationship between body mass and LV occurrence, so that subadults had the highest LV positivity, but LV in older animals was less prevalent. Also, LV prevalence was higher in autumn and lower in spring, and the amount of precipitation recorded during the 6 months preceding the trapping date was negatively correlated with the presence of the virus. Phylogenetic analysis on the 185 base pair species-specific sequence of the 5' untranslated region identified high genetic diversity (46.5%) between 80 haplotypes, although no geographical or host-specific patterns of diversity were detected.

Selective Predation by Owls on Infected Bank Voles (Myodes glareolus) as a Possible Sentinel of Tularemia Outbreaks.

Tularemia is a widely spread zoonotic disease in the northern hemisphere, caused by the bacterium Francisella tularensis. In humans, tularemia is an acute febrile illness with incidence peaks in late summer to early autumn of outbreak years, but there is no early warning system in place that can reduce the impact of disease by providing timely risk information. In this study, we revisit previously unpublished data on F. tularensis in water, sediment, soil, and small mammals from 1984 in northern Sweden. In addition, we used human case data from the national surveillance system for tularemia in the same year. In the environmental and small mammal material, bank vole (Myodes glareolus) samples from urine and bladder were the only samples that tested positive for F. tularensis. The prevalence of F. tularensis among trapped bank voles was 13.5%, although all six bank voles that were retrieved from owl nest boxes in early May tested positive. Forty-two human tularemia cases were reported from August to December in 1984. Based on these results, we encourage investigating the potential role of tularemia-infected bank voles retrieved from owl nest boxes in spring as an early warning for outbreaks of tularemia among humans in summer and autumn of the same year.

Spatio-temporal variation of metals and organic contaminants in bank voles (Myodes glareolus).

Environmental contamination with metals and organic compounds is of increasing concern for ecosystem and human health. Still, our knowledge about spatial distribution, temporal changes and ecotoxicological fate of metals and organic contaminants in wildlife is limited. We studied concentrations of 69 elements and 50 organic compounds in 300 bank voles (Myodes glareolus), Europe's most common mammal, sampled in spring and autumn 2017-2018 in five monitoring areas, representing three biogeographic regions. In addition, we compared measured concentrations with previous results from bank voles sampled within the same areas in 1995-1997 and 2001. In general, our results show regional differences, but no consistent patterns among contaminants and study areas. The exception was for the lowest concentrations of organic contaminants (e.g. perfluorooctane sulfonate, PFOS), which were generally found in the northern Swedish mountain area. Concentrations of metals and organic contaminants in adults varied seasonally with most organic contaminants being higher in spring; likely induced by diet shifts but potentially also related to age differences. In addition, metal concentrations varied between organs (liver vs. kidney), age classes (juveniles vs. adults; generally higher in adults) as well as between males and females. Concentrations of chromium and nickel in kidney and liver in the northernmost mountain area were lower in 2017-2018 than in 1995-1997 and in three of four areas, lead concentrations were lower in 2017-2018 than in 2001. Current metal concentrations (except mercury) are not expected to negatively affect the voles. Concentrations of hexachlorobenzene displayed highest concentrations in 2001 in the mountains, while it was close to detection limit in 2017-2018. Likewise, PFOS concentrations decreased in the mountains and in south-central lowland forests between 2001 and 2017-2018. Our results suggest that season, age class and sex need to be considered when designing and interpreting results from monitoring programs targeting inorganic and organic contaminants in wildlife.

Documenting lemming population change in the Arctic: Can we detect trends?

Lemmings are a key component of tundra food webs and changes in their dynamics can affect the whole ecosystem. We present a comprehensive overview of lemming monitoring and research activities, and assess recent trends in lemming abundance across the circumpolar Arctic. Since 2000, lemmings have been monitored at 49 sites of which 38 are still active. The sites were not evenly distributed with notably Russia and high Arctic Canada underrepresented. Abundance was monitored at all sites, but methods and levels of precision varied greatly. Other important attributes such as health, genetic diversity and potential drivers of population change, were often not monitored. There was no evidence that lemming populations were decreasing in general, although a negative trend was detected for low arctic populations sympatric with voles. To keep the pace of arctic change, we recommend maintaining long-term programmes while harmonizing methods, improving spatial coverage and integrating an ecosystem perspective.

Effect of spatial scale and latitude on diversity-disease relationships.

Natural ecosystems provide humans with different types of ecosystem services, often linked to biodiversity. The dilution effect (DE) predicts a negative relationship between biodiversity and risk of infectious diseases of humans, other animals, and plants. We hypothesized that a stronger DE would be observed in studies conducted at smaller spatial scales, where biotic drivers may predominate, compared to studies at larger spatial scales where abiotic drivers may more strongly affect disease patterns. In addition, we hypothesized a stronger DE in studies from temperate regions at mid latitudes than in those from subtropical and tropical regions, due to more diffuse species interactions at low latitudes. To explore these hypotheses, we conducted a meta-analysis of observational studies of diversity-disease relationships for animals across spatial scales and geographic regions. Negative diversity-disease relationships were significant at small (combined site and local), intermediate (combined landscape and regional), and large (combined continental and global) scales and the effect did not differ depending on size of the study areas. For the geographic region analysis, a strongly negative diversity-disease relationship was found in the temperate region while no effect was found in the subtropical and tropical regions. However, no overall effect of absolute latitude on the strength of the dilution effect was detected. Our results suggest that a negative diversity-disease relationship occurs across scales and latitudes and is especially strong in the temperate region. These findings may help guide future management efforts in lowering disease risk.

Correction to: Documenting lemming population change in the Arctic: Can we detect trends?

In the original published article, some of the symbols in figure 1A were modified incorrectly during the typesetting and publication process. The correct version of the figure is provided in this correction.

Wildfire-induced short-term changes in a small mammal community increase prevalence of a zoonotic pathogen?

Natural disturbances like droughts and fires are important determinants of wildlife community structure and are suggested to have important implications for prevalence of wildlife-borne pathogens. After a major wildfire affecting >1,600 ha of boreal forest in Sweden in 2006, we took the rare opportunity to study the short-term response (2007-2010 and 2015) of small mammal community structure, population dynamics, and prevalence of the Puumala orthohantavirus (PUUV) hosted by bank voles (Myodes glareolus). We performed snap-trapping in permanent trapping plots in clear-cuts (n = 3), unburnt reference forests (n = 7), and the fire area (n = 7) and surveyed vegetation and habitat structure. Small mammal species richness was low in all habitats (at maximum three species per trapping session), and the bank vole was the only small mammal species encountered in the fire area after the first postfire year. In autumns of years of peak rodent densities, the trapping index of bank voles was lowest in the fire area, and in two of three peak-density years, it was highest in clear-cuts. Age structure of bank voles varied among forest types with dominance of overwintered breeders in the fire area in the first postfire spring. PUUV infection probability in bank voles was positively related to vole age. Infection probability was highest in the fire area due to low habitat complexity in burnt forests, which possibly increased encounter rate among bank voles. Our results suggest that forest fires induce cascading effects, including fast recovery/recolonization of fire areas by generalists like bank voles, impoverished species richness of small mammals, and altered prevalence of a rodent-borne zoonotic pathogen. Our pilot study suggests high human infection risk upon encountering a bank vole in the fire area, however, with even higher overall risk in unburnt forests due to their higher vole numbers. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://osf.io/6fsy3/.

Population Dynamics of Bank Voles Predicts Human Puumala Hantavirus Risk.

Predicting risk of zoonotic diseases, i.e., diseases shared by humans and animals, is often complicated by the population ecology of wildlife host(s). We here demonstrate how ecological knowledge of a disease system can be used for early prediction of human risk using Puumala hantavirus (PUUV) in bank voles (Myodes glareolus), which causes Nephropathia epidemica (NE) in humans, as a model system. Bank vole populations at northern latitudes exhibit multiannual fluctuations in density and spatial distribution, a phenomenon that has been studied extensively. Nevertheless, existing studies predict NE incidence only a few months before an outbreak. We used a time series on cyclic bank vole population density (1972-2013), their PUUV infection rates (1979-1986; 2003-2013), and NE incidence in Sweden (1990-2013). Depending on the relationship between vole density and infection prevalence (proportion of infected animals), either overall density of bank voles or the density of infected bank voles may be used to predict seasonal NE incidence. The density and spatial distribution of voles at density minima of a population cycle contribute to the early warning of NE risk later at its cyclic peak. When bank voles remain relatively widespread in the landscape during cyclic minima, PUUV can spread from a high baseline during a cycle, culminating in high prevalence in bank voles and potentially high NE risk during peak densities.

Anaplasma phagocytophilum evolves in geographical and biotic niches of vertebrates and ticks.

BACKGROUND: Anaplasma phagocytophilum is currently regarded as a single species. However, molecular studies indicate that it can be subdivided into ecotypes, each with distinct but overlapping transmission cycle. Here, we evaluate the interactions between and within clusters of haplotypes of the bacterium isolated from vertebrates and ticks, using phylogenetic and network-based methods. METHODS: The presence of A. phagocytophilum DNA was determined in ticks and vertebrate tissue samples. A fragment of the groEl gene was amplified and sequenced from qPCR-positive lysates. Additional groEl sequences from ticks and vertebrate reservoirs were obtained from GenBank and through literature searches, resulting in a dataset consisting of 1623 A. phagocytophilum field isolates. Phylogenetic analyses were used to infer clusters of haplotypes and to assess phylogenetic clustering of A. phagocytophilum in vertebrates or ticks. Network-based methods were used to resolve host-vector interactions and their relative importance in the segregating communities of haplotypes. RESULTS: Phylogenetic analyses resulted in 199 haplotypes within eight network-derived clusters, which were allocated to four ecotypes. The interactions of haplotypes between ticks, vertebrates and geographical origin, were visualized and quantified from networks. A high number of haplotypes were recorded in the tick Ixodes ricinus. Communities of A. phagocytophilum recorded from Korea, Japan, Far Eastern Russia, as well as those associated with rodents had no links with the larger set of isolates associated with I. ricinus, suggesting different evolutionary pressures. Rodents appeared to have a range of haplotypes associated with either Ixodes trianguliceps or Ixodes persulcatus and Ixodes pavlovskyi. Haplotypes found in rodents in Russia had low similarities with those recorded in rodents in other regions and shaped separate communities. CONCLUSIONS: The groEl gene fragment of A. phagocytophilum provides information about spatial segregation and associations of haplotypes to particular vector-host interactions. Further research is needed to understand the circulation of this bacterium in the gap between Europe and Asia before the overview of the speciation features of this bacterium is complete. Environmental traits may also play a role in the evolution of A. phagocytophilum in ecotypes through yet unknown relationships.

Diet shift in bank voles induced by competition from grey-sided voles?

Grey-sided voles (Myodes rufocanus) and bank voles (Myodes glareolus) co-exist in boreal forests in northern Scandinavia. Previous studies suggest that the 2 species interact interspecifically, the grey-sided vole being the dominant species. We tested the hypothesis that bank voles shift their diet due to competition with the dominant grey-sided vole by studying stable isotope ratios in both species. Muscle samples were taken from voles in patches of old forest occupied by only bank voles and patches of old forest occupied by both grey-sided voles and bank voles. We found that: (i) stable isotope ratios of bank voles differed in areas with and without grey-sided voles; and that (ii) the stable isotope ratios of bank voles were more similar to those of grey-sided voles in areas where grey-sided voles were absent. Our data suggests that grey-sided voles forced bank voles to change their diet due to interspecific competition.

Seasonal shift of diet in bank voles explains trophic fate of anthropogenic osmium?

Diet shifts are common in mammals and birds, but little is known about how such shifts along the food web affect contaminant exposure. Voles are staple food for many mammalian and avian predators. There is therefore a risk of transfer of contaminants accumulated in voles within the food chain. Osmium is one of the rarest earth elements with osmium tetroxide (OsO4) as the most toxic vapor-phase airborne contaminant. Anthropogenic OsO4 accumulates in fruticose lichens that are important winter food of bank voles (Myodes glareolus). Here, we test if a) anthropogenic osmium accumulates in bank voles in winter, and b) accumulation rates and concentrations are lower in autumn when the species is mainly herbivorous. Our study, performed in a boreal forest impacted by anthropogenic osmium, supported the hypotheses for all studied tissues (kidney, liver, lung, muscle and spleen) in 50 studied bank voles. In autumn, osmium concentrations in bank voles were even partly similar to those in the graminivorous field vole (Microtus agrestis; n=14). In autumn but not in late winter/early spring, osmium concentrations were generally negatively correlated with body weight and root length of the first mandible molar, i.e. proxies of bank vole age. Identified negative correlations between organ-to-body weight ratios and osmium concentrations in late winter/early spring indicate intoxication. Our results suggest unequal accumulation risk for predators feeding on different cohorts of bank voles.

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

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.

Spatial prediction and validation of zoonotic hazard through micro-habitat properties: where does Puumala hantavirus hole - up?

BACKGROUND: To predict the risk of infectious diseases originating in wildlife, it is important to identify habitats that allow the co-occurrence of pathogens and their hosts. Puumala hantavirus (PUUV) is a directly-transmitted RNA virus that causes hemorrhagic fever in humans, and is carried and transmitted by the bank vole (Myodes glareolus). In northern Sweden, bank voles undergo 3-4 year population cycles, during which their spatial distribution varies greatly. METHODS: We used boosted regression trees; a technique inspired by machine learning, on a 10 - year time-series (fall 2003-2013) to develop a spatial predictive model assessing seasonal PUUV hazard using micro-habitat variables in a landscape heavily modified by forestry. We validated the models in an independent study area approx. 200 km away by predicting seasonal presence of infected bank voles in a five-year-period (2007-2010 and 2015). RESULTS: The distribution of PUUV-infected voles varied seasonally and inter-annually. In spring, micro-habitat variables related to cover and food availability in forests predicted both bank vole and infected bank vole presence. In fall, the presence of PUUV-infected voles was generally restricted to spruce forests where cover was abundant, despite the broad landscape distribution of bank voles in general. We hypothesize that the discrepancy in distribution between infected and uninfected hosts in fall, was related to higher survival of PUUV and/or PUUV-infected voles in the environment, especially where cover is plentiful. CONCLUSIONS: Moist and mesic old spruce forests, with abundant cover such as large holes and bilberry shrubs, also providing food, were most likely to harbor infected bank voles. The models developed using long-term and spatially extensive data can be extrapolated to other areas in northern Fennoscandia. To predict the hazard of directly transmitted zoonoses in areas with unknown risk status, models based on micro-habitat variables and developed through machine learning techniques in well-studied systems, could be used.