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.

Exploring the influence of host community composition on the outbreak potential of Anaplasma phagocytophilum and Borrelia burgdorferi s.l.

In large parts of the northern hemisphere, multiple deer species coexist, and management actions can strongly influence wild deer communities. Such changes may also indirectly influence other species in the community, such as small mammals and birds, because deer can have strong effects on their habitats and resources. Deer, small mammals and birds play an important role in the dynamics of tick-borne zoonotic diseases. It is, however, relatively underexplored how the abundance and composition of vertebrate communities may affect the outbreak potential, maintenance and circulation of tick-borne pathogens. In this study we focus on the outbreak potential by exploring how the basic reproduction number R0 for different tick-borne pathogens depends on host community composition. We used published data on co-varying roe deer (Capreolus capreolus) and fallow deer (Dama dama) densities following a hunting ban, and different small mammal and bird densities, to investigate how the change in host community influences the R0 of four tick-borne pathogens: one non-zoonotic, namely Anaplasma phagocytophilum ecotype 2, and three zoonotic, namely A. phagocytophilum ecotype 1, Borrelia afzelii and Borrelia garinii. We calculated R0 using a next generation matrix approach, and used elasticities to quantify the contributions to R0 of the different groups of host species. The value of R0 for A. phagocytophilum ecotype 1 was higher with high fallow deer density and low roe deer density, while it was the other way round for A. phagocytophilum ecotype 2. For B. afzelii, R0 was mostly related to the density of small mammals and for B. garinii it was mostly determined by bird density. Our results show that the effect of species composition is substantial in the outbreak potential of tick-borne pathogens. This implies that also management actions that change this composition, can (indirectly and unintentionally) affect the outbreak potential of tick-borne diseases.

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.

Urban forest soils harbour distinct and more diverse communities of bacteria and fungi compared to less disturbed forest soils.

Anthropogenic changes to land use drive concomitant changes in biodiversity, including that of the soil microbiota. However, it is not clear how increasing intensity of human disturbance is reflected in the soil microbial communities. To address this issue, we used amplicon sequencing to quantify the microbiota (bacteria and fungi) in the soil of forests (n = 312) experiencing four different land uses, national parks (set aside for nature conservation), managed (for forestry purposes), suburban (on the border of an urban area) and urban (fully within a town or city), which broadly represent a gradient of anthropogenic disturbance. Alpha diversity of bacteria and fungi increased with increasing levels of anthropogenic disturbance, and was thus highest in urban forest soils and lowest in the national parks. The forest soil microbial communities were structured according to the level of anthropogenic disturbance, with a clear urban signature evident in both bacteria and fungi. Despite notable differences in community composition, there was little change in the predicted functional traits of urban bacteria. By contrast, urban soils exhibited a marked loss of ectomycorrhizal fungi. Soil pH was positively correlated with the level of disturbance, and thus was the strongest predictor of variation in alpha and beta diversity of forest soil communities, indicating a role of soil alkalinity in structuring urban soil microbial communities. Hence, our study shows how the properties of urban forest soils promote an increase in microbial diversity and a change in forest soil microbiota composition.

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.

Alphacoronavirus in a Daubenton's Myotis Bat (Myotis daubentonii) in Sweden.

The ongoing COVID-19 pandemic has stimulated a search for reservoirs and species potentially involved in back and forth transmission. Studies have postulated bats as one of the key reservoirs of coronaviruses (CoVs), and different CoVs have been detected in bats. So far, CoVs have not been found in bats in Sweden and we therefore tested whether they carry CoVs. In summer 2020, we sampled a total of 77 adult bats comprising 74 Myotis daubentonii, 2 Pipistrellus pygmaeus, and 1 M. mystacinus bats in southern Sweden. Blood, saliva and feces were sampled, processed and subjected to a virus next-generation sequencing target enrichment protocol. An Alphacoronavirus was detected and sequenced from feces of a M. daubentonii adult female bat. Phylogenetic analysis of the almost complete virus genome revealed a close relationship with Finnish and Danish strains. This was the first finding of a CoV in bats in Sweden, and bats may play a role in the transmission cycle of CoVs in Sweden. Focused and targeted surveillance of CoVs in bats is warranted, with consideration of potential conflicts between public health and nature conservation required as many bat species in Europe are threatened and protected.

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.

Low-level environmental metal pollution is associated with altered gut microbiota of a wild rodent, the bank vole (Myodes glareolus).

Mining and related industries are a major source of metal pollution. In contrast to the well-studied effects of exposure to metals on animal physiology and health, the impacts of environmental metal pollution on the gut microbiota of wild animals are virtually unknown. As the gut microbiota is a key component of host health, it is important to understand whether metal pollution can alter wild animal gut microbiota composition. Using a combination of 16S rRNA amplicon sequencing and quantification of metal levels in kidneys, we assessed whether multi-metal exposure (the sum of normalized levels of fifteen metals) was associated with changes in gut microbiota of wild bank voles (Myodes glareolus) from two locations in Finland. Exposure to increased metal load was associated with higher gut microbiota species diversity (α-diversity) and altered community composition (ß-diversity), but not dispersion. Multi-metal exposure and increased levels of several metals (Cd, Hg, Pb and Se) were associated with differences in the abundance of microbial taxa, especially those within the families Clostridiales vadinBB60 group, Desulfovibrionaceae, Lachnospiraceae, Muribaculaceae and Ruminococcaceae. Our data indicate that even low-level metal pollution can affect the diversity of microbiota and be associated with deterministic differences in composition of host gut microbiota in wild animal populations. These findings highlight the need to study a broader range of metals and their cocktails that are more representative of the types of environmental exposure experienced by wild animals.

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.

Wild ungulate species differ in their contribution to the transmission of Ixodes ricinus-borne pathogens.

BACKGROUND: Several ungulate species are feeding and propagation hosts for the tick Ixodes ricinus as well as hosts to a wide range of zoonotic pathogens. Here, we focus on Anaplasma phagocytophilum and Borrelia burgdorferi (s.l.), two important pathogens for which ungulates are amplifying and dilution hosts, respectively. Ungulate management is one of the main tools to mitigate human health risks associated with these tick-borne pathogens. Across Europe, different species of ungulates are expanding their ranges and increasing in numbers. It is currently unclear if and how the relative contribution to the life-cycle of I. ricinus and the transmission cycles of tick-borne pathogens differ among these species. In this study, we aimed to identify these relative contributions for five European ungulate species. METHODS: We quantified the tick load and collected ticks and spleen samples from hunted fallow deer (Dama dama, n = 131), moose (Alces alces, n = 15), red deer (Cervus elaphus, n = 61), roe deer (Capreolus capreolus, n = 30) and wild boar (Sus scrofa, n = 87) in south-central Sweden. We investigated the presence of tick-borne pathogens in ticks and spleen samples using real-time PCR. We determined if ungulate species differed in tick load (prevalence and intensity) and in infection prevalence in their tissue as well as in the ticks feeding on them. RESULTS: Wild boar hosted fewer adult female ticks than any of the deer species, indicating that deer are more important as propagation hosts. Among the deer species, moose had the lowest number of female ticks, while there was no difference among the other deer species. Given the low number of infected nymphs, the relative contribution of all ungulate species to the transmission of B. burgdorferi (s.l.) was low. Fallow deer, red deer and roe deer contributed more to the transmission of A. phagocytophilum than wild boar. CONCLUSIONS: The ungulate species clearly differed in their role as a propagation host and in the transmission of B. burgdorferi and A. phagocytophilum. This study provides crucial information for ungulate management as a tool to mitigate zoonotic disease risk and argues for adapting management approaches to the local ungulate species composition and the pathogen(s) of concern.

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.

Prevalence of Orthohantavirus-Reactive Antibodies in Humans and Peri-Domestic Rodents in Northern Ethiopia.

In 2012, Tigray orthohantavirus was discovered in Ethiopia, but its seasonal infection in small mammals, and whether it poses a risk to humans was unknown. The occurrence of small mammals, rodents and shrews, in human inhabitations in northern Ethiopia is affected by season and presence of stone bunds. We sampled small mammals in two seasons from low- and high-density stone bund fields adjacent to houses and community-protected semi-natural habitats in Atsbi and Hagere Selam, where Tigray orthohantavirus was first discovered. We collected blood samples from both small mammals and residents using filter paper. The presence of orthohantavirus-reactive antibodies in blood was then analyzed using immunofluorescence assay (human samples) and enzyme linked immunosorbent assays (small mammal samples) with Puumala orthohantavirus as antigen. Viral RNA was detected by RT-PCR using small mammal blood samples. Total orthohantavirus prevalence (antibodies or virus RNA) in the small mammals was 3.37%. The positive animals were three Stenocephalemys albipes rats (prevalence in this species = 13.04%). The low prevalence made it impossible to determine whether season and stone bunds were associated with orthohantavirus prevalence in the small mammals. In humans, we report the first detection of orthohantavirus-reactive IgG antibodies in Ethiopia (seroprevalence = 5.26%). S. albipes lives in close proximity to humans, likely increasing the risk of zoonotic transmission.

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.

Global patterns and determinants of lake macrophyte taxonomic, functional and phylogenetic beta diversity.

Documenting the patterns of biological diversity on Earth has always been a central challenge in macroecology and biogeography. However, for the diverse group of freshwater plants, such research program is still in its infancy. Here, we examined global variation in taxonomic, functional and phylogenetic beta diversity patterns of lake macrophytes using regional data from six continents. A data set of ca. 480 lake macrophyte community observations, together with climatic, geographical and environmental variables, was compiled across 16 regions worldwide. We (a) built the very first phylogeny comprising most freshwater plant lineages; (b) exploited a wide array of functional traits that are important to macrophyte autoecology or that relate to lake ecosystem functioning; (c) assessed if different large-scale beta diversity patterns show a clear latitudinal gradient from the equator to the poles using null models; and (d) employed evolutionary and regression models to first identify the degree to which the studied functional traits show a phylogenetic signal, and then to estimate community-environment relationships at multiple spatial scales. Our results supported the notion that ecological niches evolved independently of phylogeny in macrophyte lineages worldwide. We also showed that taxonomic and phylogenetic beta diversity followed the typical global trend with higher diversity in the tropics. In addition, we were able to confirm that species, multi-trait and lineage compositions were first and foremost structured by climatic conditions at relatively broad spatial scales. Perhaps more importantly, we showed that large-scale processes along latitudinal and elevational gradients have left a strong footprint in the current diversity patterns and community-environment relationships in lake macrophytes. Overall, our results stress the need for an integrative approach to macroecology, biogeography and conservation biology, combining multiple diversity facets at different spatial scales.

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.