Wild Voles Research Articles

Rodent Gut Bacteria Coexisting with an Insect Gut Virus in Tapeworm Parasitic Cysts: Metagenomic Evidence of Microbial Selection in Extra-Intestinal Clinical Niches.

In medicine, parasitic cysts (e.g., brain cysticerci) are believed to be sterile, and are primarily treated with antiparasitic medications, not antibiotics, which could prevent abscess formation and localized inflammation. This study quantified the microbial composition of parasitic cysts in a wild rodent, using multi-kingdom metagenomics to comprehensively assess if parasitic cysts are sterile, and further understand gut microbial translocation and adaptation in wildlife confined environments, outside the gut. Analysis was conducted on DNA from two hepatic parasitic cysts from a feline tapeworm, Hydatigera (Taenia) taeniaeformis, affecting a wild vole mouse (Microtus pennsylvanicus), and from feces, liver and peritoneal fluid of this and two other concurrent individual wild voles trapped during pest control in one of our university research vegetable gardens. Bacterial metagenomics revealed the presence of gut commensal/opportunistic species, Parabacteroides distasonis, Bacteroides (Bacteroidota); Klebsiella variicola, E. coli (Enterobacteriaceae); Enterococcus faecium and Lactobacillus acidophilus (Bacillota) inhabiting the cysts, and peritoneal fluid. Remarkably, viral metagenomics revealed various murine viral species, and unexpectedly, a virus from the insect armyworm moth (Pseudaletia/Mythimna unipuncta), known as Mythimna unipuncta granulovirus A (MyunGV-A), in both cysts, and in one fecal and one peritoneal sample from the other non-cyst voles, indicating the survival and adaption potential of the insect virus in voles. Metagenomics also revealed a significantly lower probability of fungal detection in cysts compared to that in peritoneal fluid/feces (p < 0.05), with single taxon detection in each cyst (Malassezia and Pseudophaeomoniella oleicola). The peritoneal fluid had the highest probability for fungi. In conclusion, metagenomics revealed that bacteria/viruses/fungi coexist within parasitic cysts supporting the potential therapeutic benefits of antibiotics in cystic diseases, and in inflammatory microniches of chronic diseases, such as Crohn's disease gut wall cavitating micropathologies, from which we recently isolated similar synergistic pathogenic Bacteroidota and Enterobacteriaceae, and Bacillota.

Multiple infections of zoonotic pathogens in wild Brandt's voles (Lasiopodomys brandtii).

The frequent interactions of rodents with humans make them a common source of zoonotic infections. Brandt's vole is the dominant rodent species of the typical steppe in Inner Mongolia, and it is also an important pest in grassland. To obtain an initial unbiased measure of the microbial diversity and abundance in the blood and intestinal tracts and to detect the pathogens carried by wild Brandt's voles in Hulun Buir, Inner Mongolia. Twenty wild adult Brandt's voles were trapped using live cages, and 12 intestinal samples were collected for metagenomic analysis and 8 blood samples were collected for meta-transcriptomic analysis. We compared the sequencing data with pathogenic microbiota databases to analyse the phylogenetic characteristics of zoonotic pathogens carried by wild voles. A total of 122 phyla, 79 classes, 168 orders, 382 families and 1693 genera of bacteria and a total of 32 families of DNA and RNA viruses in Brandt's voles were characterized. We found that each sample carried more than 10 pathogens, whereas some pathogens that were low in abundance were still at risk of transmission to humans. This study improves our understanding of the viral and bacterial diversity in wild Brandt's voles and highlights the multiple viral and bacterial pathogens carried by this rodent. These findings may serve as a basis for developing strategies targeting rodent population control in Hulun Buir and provide a better approach to the surveillance of pathogenic microorganisms in wildlife.

Co-infections mask pathogen-specific associations with the gut microbiota in wild voles.

Research Highlight: Brila, I., Lavirinienko, A., Tukalenko, E., Kallio, E. R., Mappes, T. & Watts, P. C. (2022). Idiosyncratic effects of coinfection on the association between systemic pathogens and the gut microbiota of a wild rodent, the bank vole (Myodes glareolus). Journal of Animal Ecology, https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2656.13869. Interactions between pathogens and host-associated microbial communities can influence host fitness, disease progression and pathogen emergence. The vast majority of studies characterize interactions between single pathogens and bacterial commensals, yet co-infections with multiple pathogens are the norm in nature. In their paper on pathogen-microbiome interactions, Brila et al. (2022) examine how co-infections with four systemic pathogens associate with the gut microbiota in wild bank voles. Building on a series of tests, the authors show that excluding co-infection information from statistical models masks pathogen-specific patterns and confounds interpretations. This paper advances on previous studies by generating surveillance data on a phylogenetically diverse suite of vole pathogens to address the question as to whether pathogens exhibit unique or universal associations with gut commensals. They report that even bacterial pathogens with similar transmission ecology have divergent associations with gut microbes, and highlight that a mechanistic understanding of host-pathogen interactions is necessary for decoding the diverse consequences for gut microbial communities.

Transcriptome-wide analysis reveals different categories of response to a standardised immune challenge in a wild rodent

Individuals vary in their immune response and, as a result, some are more susceptible to infectious disease than others. Little is known about the nature of this individual variation in natural populations, or which components of immune pathways are most responsible, but defining this underlying landscape of variation is an essential first step to understanding the drivers of this variation and, ultimately, predicting the outcome of infection. We describe transcriptome-wide variation in response to a standardised immune challenge in wild field voles. We find that genes (hereafter 'markers') can be categorised into a limited number of types. For the majority of markers, the response of an individual is dependent on its baseline expression level, with significant enrichment in this category for conventional immune pathways. Another, moderately sized, category contains markers for which the responses of different individuals are also variable but independent of their baseline expression levels. This category lacks any enrichment for conventional immune pathways. We further identify markers which display particularly high individual variability in response, and could be used as markers of immune response in larger studies. Our work shows how a standardised challenge performed on a natural population can reveal the patterns of natural variation in immune response.

Conservation Implications of Shifting Gut Microbiomes in Captive-Reared Endangered Voles Intended for Reintroduction into the Wild.

The Amargosa vole is a highly endangered rodent endemic to a small stretch of the Amargosa River basin in Inyo County, California. It specializes on a single, nutritionally marginal food source in nature. As part of a conservation effort to preserve the species, a captive breeding population was established to serve as an insurance colony and a source of individuals to release into the wild as restored habitat becomes available. The colony has successfully been maintained on commercial diets for multiple generations, but there are concerns that colony animals could lose gut microbes necessary to digest a wild diet. We analyzed feces from colony-reared and recently captured wild-born voles on various diets, and foregut contents from colony and wild voles. Unexpectedly, fecal microbial composition did not greatly differ despite drastically different diets and differences observed were mostly in low-abundance microbes. In contrast, colony vole foregut microbiomes were dominated by Allobaculum sp. while wild foreguts were dominated by Lactobacillus sp. If these bacterial community differences result in beneficial functional differences in digestion, then captive-reared Amargosa voles should be prepared prior to release into the wild to minimize or eliminate those differences to maximize their chance of success.

Echinococcus multilocularis Surveillance Using Copro-DNA and Egg Examination of Shelter Dogs from an Endemic Area in Hokkaido, Japan.

Surveillance of Echinococcus multilocularis infection among 156 shelter dogs was conducted in an urban area (Sapporo city) in Hokkaido, where the parasite is endemic in Japan using copro-DNA and fecal egg examination from September 2013 to April 2017. Echinococcus infection was detected in three dogs (1.9%), including one dog that excreted eggs. The results suggested that free-roaming or stray dogs in urban area may be infected by capturing wild voles containing parasitic cysts and could be a source of human infection. Dog-to-human transmission is a significant concern, and the risk of such transmission is present even in urban areas in Hokkaido. We recommend deworming within 1 month (e.g., before egg excretion) of capture for free-roaming or stray dogs in Echinococcus-endemic area to prevent potential human infection.

Experimental infections of wild bank voles (Myodes glareolus) from nephropatia epidemica endemic and non-endemic regions revealed slight differences in Puumala virological course and immunological responses

In Europe, the occurrence of nephropathia epidemica (NE), a human disease caused by Puumala virus (PUUV), exhibits considerable geographical heterogeneity despite the continuous distribution of its reservoir, the bank vole Myodes glareolus. To better understand the causes of this heterogeneity, wild voles sampled in two adjacent NE endemic and non-endemic regions of France were infected experimentally with PUUV. The responses of bank voles to PUUV infection, based on the levels of anti-PUUV IgG and viral RNA, were compared. Slight regional differences were highlighted despite the high inter-individual variability. Voles from the NE non-endemic region showed greater immune responsiveness to PUUV infection, but lower levels of RNA in their organs than voles from the endemic region. These results suggest the existence of regional variations in the sensitivity of bank voles that could contribute to the apparent absence of PUUV circulation among voles and the absence of NE in the non-endemic region.

Methylation of avpr1a in the cortex of wild prairie voles: effects of CpG position and polymorphism.

DNA methylation can cause stable changes in neuronal gene expression, but we know little about its role in individual differences in the wild. In this study, we focus on the vasopressin 1a receptor (avpr1a), a gene extensively implicated in vertebrate social behaviour, and explore natural variation in DNA methylation, genetic polymorphism and neuronal gene expression among 30 wild prairie voles (Microtus ochrogaster). Examination of CpG density across 8 kb of the locus revealed two distinct CpG islands overlapping promoter and first exon, characterized by few CpG polymorphisms. We used a targeted bisulfite sequencing approach to measure DNA methylation across approximately 3 kb of avpr1a in the retrosplenial cortex, a brain region implicated in male space use and sexual fidelity. We find dramatic variation in methylation across the avrp1a locus, with pronounced diversity near the exon–intron boundary and in a genetically variable putative enhancer within the intron. Among our wild voles, differences in cortical avpr1a expression correlate with DNA methylation in this putative enhancer, but not with the methylation status of the promoter. We also find an unusually high number of polymorphic CpG sites (polyCpGs) in this focal enhancer. One polyCpG within this enhancer (polyCpG 2170) may drive variation in expression either by disrupting transcription factor binding motifs or by changing local DNA methylation and chromatin silencing. Our results contradict some assumptions made within behavioural epigenetics, but are remarkably concordant with genome-wide studies of gene regulation.

High prevalence of Babesia microti 'Munich' type in small mammals from an Ixodes persulcatus/Ixodes trianguliceps sympatric area in the Omsk region, Russia.

Babesia microti is a genetically diverse group of protozoan parasites whose life cycle is associated with both small mammals and Ixodes spp. ticks. In this study, the prevalence of different B. microti genetic groups in ticks and small rodents in an area with Ixodes persulcatus and Ixodes trianguliceps occurring in sympatry was examined. A total of 541 small mammals were captured during eight sampling periods between 2013 and 2015 at a site in the Omsk region of Russia and tested for the presence of B. microti using nested PCR with subsequent sequencing of positive samples. B. microti DNA was found in 31.6% of examined samples, and prevalence rates ranged from 5.3 to 61.6% in different sampling periods. The sequenced B. microti samples belonged to two genetic groups: enzootic B. microti 'Munich' type and zoonotic B. microti 'US' type. B. microti 'Munich' type was more common across all sampling periods, with greater than 80% prevalence in infected animals. Despite the high B. microti 'Munich'-type prevalence in voles, B. microti was not found in any of 394 adult I. persulcatus ticks collected by flagging or in the 84 I. persulcatus or 20 I. trianguliceps ticks taken from voles and molted under laboratory conditions. It was demonstrated that B. microti 'Munich'-type DNA can be detected in the blood of naturally infected voles for at least 20weeks after capture. Thus, the high prevalence of B. microti 'Munich' type in small mammals may be explained by the prolonged persistence of B. microti in the blood of wild voles.

Silicon-based plant defences, tooth wear and voles.

Plant-herbivore interactions are hypothesized to drive vole population cycles through the grazing-induced production of phytoliths in leaves. Phytoliths act as mechanical defences because they deter herbivory and lower growth rates in mammals. However, how phytoliths impair herbivore performance is still unknown. Here, we tested whether the amount of phytoliths changes tooth wear patterns. If confirmed, abrasion from phytoliths could play a role in population crashes. We applied dental microwear texture analysis (DMTA) to laboratory and wild voles. Lab voles were fed two pelleted diets with differing amounts of silicon, which produced similar dental textures. This was most probably due to the loss of food mechanical properties through pelletization and/or the small difference in silicon concentration between diets. Wild voles were trapped in Poland during spring and summer, and every year across a population cycle. In spring, voles feed on silica-rich monocotyledons, while in the summer they also include silica-depleted dicotyledons. This was reflected in the results; the amount of silica therefore leaves a traceable record in the dental microwear texture of voles. Furthermore, voles from different phases of population cycles have different microwear textures. We tentatively propose that these differences result from grazing-induced phytolith concentrations. We hypothesize that the high amount of phytoliths in response to intense grazing in peak years may result in malocclusion and other dental abnormalities, which would explain how these silicon-based plant defences help provoke population crashes. DMTA could then be used to reconstruct vole population dynamics using teeth from pellets or palaeontological material.

Leptospirosis acquisition following the reintroduction of wildlife

Potential risks posed to domestic animals and human beings by zoonotic diseases in reintroduced animals can reduce the acceptability of reintroductions. The authors investigated the role of endangered water voles,...

Effects of parasites and antigenic challenge on metabolic rates and thermoregulation in northern red-backed voles (Myodes rutilus).

Perturbations in host energetics are considered to be an essential pathway for parasite impact on host fitness. However, direct estimations of parasite-induced variations in basal metabolic rates of vertebrate hosts have so far provided contradictory results. The energy requirements of immunity and other vital functions may be compromised in energy-demanding conditions in comparison to comfortable conditions; therefore, in our study performed on the wild red-backed vole, Myodes rutilus, we compared the values of indices that reflect metabolic and thermoregulatory responses to acute cooling in individuals that had been naturally infected by gut helminths or Ixodes persulcatus taiga ticks to individuals with no signs of infestation. To consider the possible effects of an acquired immune response on host energetics, we also injected some of the tested individuals with sheep red blood cells (SRBC). Red-backed voles infected by the nematode Heligmosomum mixtum injected with SRBC showed significantly lower cold-induced maximum oxygen consumption than the saline control. Additionally, individuals infected with H. mixtum showed significantly lower oxygen consumption during the final minute of the 15-min acute cooling period and a significantly greater decline in body temperature than individuals free from helminths. In individuals concurrently infected by H. mixtum and the cestodes Arostrilepis horrida, these indices did not differ from helminth-free individuals. The number of ticks simultaneously parasitizing the voles at the moment of capture correlated positively with their SMR. Our results suggest that even natural parasites produce deleterious effects on host aerobic capacity and thermoregulatory abilities, although the effects of different parasites might not be additive.

An immunological marker of tolerance to infection in wild rodents.

Author SummaryHosts do not always resist parasites. And once infection establishes, relatively little is known of how naturally occurring hosts tolerate (mitigate for) adverse effects, or what the life history consequences of this tolerance may be. In this article we demonstrate a pattern of tolerance to parasitic worms and arthropods in wild voles and link this to increased expression of an immunological biomarker. The biomarker, Gata3, is triggered by infection, precedes significant changes in body condition, and impacts on fecundity and survival. These results point to the considerable ecological importance of tolerance in wild vertebrates and to how poorly it is understood, while at the same time giving a new perspective on the natural function of immune response pathways involving Gata3.

Identification of tannin–degrading microorganisms in the gut of plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus)

Gut microorganisms are thought to play a role in the degradation of plant secondary metabolites in herbivores. Here, we examined the presence of tannin–degrading microorganisms in the gut of two herbivores, plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). Tannase activity in the feces of wild plateau pikas and root voles increased from June to August, corresponding to the increase in condensed and hydrolyzable tannin concentrations in plants during this period. Using intragastric tannic acid infusion, we found that tannase activities were significantly higher following administration of three concentrations of tannic acid than that in the control group for root voles. In contrast, for plateau pikas, animals administered tannic acid exhibited lower tannase activity in low–dose and high–dose groups than that in the control group. Tannase activities in root voles were higher than those in plateau pikas among different months and in different tannic acid infusion groups. Three tannin–degrading anaerobic strains were isolated from the cecum of plateau pikas (termed A1, A2, and A3) and root voles (termed M1, M2, and M3). 16 s rDNA sequencing assigned isolates A1 and M1 to the genus Enterobacter, A2 and M2 to the genus Shigella, and A3 and M3 to the genus Staphylococcus. These data provided the first evidence of microorganisms with tannin–degrading activity in the gut of plateau pikas and root voles. We speculated that both animals could degrade tannins in the gut, but that root voles would have a greater ability to process tannins than plateau pikas.

Differential Susceptibility to Cadmium-Induced Liver and Kidney Injury in Wild and Laboratory-Bred Bank Voles Myodes glareolus

The objective of the study was to compare the sensitivity of wild and laboratory-bred bank voles to cadmium (Cd)-induced histopathological changes in the liver and kidneys. For 4 weeks, the male bank voles—both wild and laboratory-bred—were provided with diet containing Cd in quantities <0.1 (control), 30, and 60 μg/g dry weight. At the end of exposure period, histopathology and analyses of Cd, metallothionein (MT), glutathione (GSH), zinc (Zn), copper (Cu), iron (Fe), and lipid peroxidation—all considered to be critical factors during the development of Cd toxicity in the liver and kidneys—were carried out. Histopathological changes (focal hepatocyte swelling, vacuolation and inflammation [leukocyte infiltration] in the liver, and focal proximal tubule degeneration [including epithelial cell swelling] in the kidneys) occurred only in the wild bank voles fed a diet containing 60 μg Cd/g. There were no differences in concentrations of Cd, MT, GSH, Zn, and Cu in liver and kidney between the respective groups of wild and laboratory-bred animals. However, a decrease of hepatic Fe and lipid peroxidation was observed in the wild voles exhibiting histopathological changes. These data indicate the following: (1) wild bank voles are more susceptible to Cd-induced liver and kidney injury than those bred and raised in the laboratory; (2) the difference in sensitivity may be associated with a distinct decrease of hepatic Fe in response to Cd exposure between the two groups of bank voles; and (3) dietary Cd may produce histopathological changes indirectly through decreasing the hepatic Fe and Fe-dependent oxidative processes. These results also suggest that histopathology in the liver and kidney of wild bank voles living in a contaminated environment may occur at relatively low levels of tissue Cd.

Significant interspecies differences in induction profiles of hepatic CYP enzymes by TCDD in bank and field voles

The gene expression and induction of cytochrome P450 (CYP)-enzymes following 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) peroral administration was studied in the livers of two wild vole species--the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). The dioxin-sensitive C57BL/6 mouse was used as a reference. Doses of 0.05, 0.5, 5.0, and 50 µg/kg were applied to ascertain a dose-response relationship, and the dose of 50 µg/kg was applied to the study time course for up to 96 h. The cytochrome P450 1A1 (CYP1A1) mRNA expression showed an expected dose-dependent increase equally in both vole species. Bank voles expressed notably higher CYP2A mRNA levels as compared with field voles. Both species exhibited dose-dependent increases in putative CYP1A-, CYP2B-, and CYP2A-associated activities as measured by fluorometric assays for ethoxyresorufin-O-deethylase (EROD), penthoxyresorufin-O-depenthylase (PROD), and 7-ethoxycoumarin-O-deethylase (ECOD), respectively. Putative CYP2A-associated coumarin-7-hydroxylase (COH) activity showed a slight increase at the two highest doses of TCDD in field voles but not in bank voles, and their basal COH activity was only one-fourth or less of that in field voles. Overall, however, bank voles tended to exhibit higher CYP-associated enzyme activities measured at the two largest doses of TCDD than field voles. A western blot analysis of aryl hydrocarbon receptor (AhR) revealed that the two vole species had differential band patterns, suggesting dissimilar structures for their AhRs.

Web of Parasite Interactions

We live under constant assault from a variety of pathogens. Pathogen exposure will be more or less harmful depending on host factors, including immune status, and, as Telfer et al. (p. [243][1]; see the Perspective by [Lafferty][2] ) point out, the presence of co-infecting pathogens. In a time-series study of wild voles and four pathogens, co-infection had a larger effect on disease than any other factor. For example, infection with cowpox virus increased susceptibility and prolonged bacterial co-infections. Conversely, an ongoing infection with the bacterium Anaplasma reduced the rodents' susceptibility to the protozoan Babesia . In turn, chronic infection with Babesia limited susceptibility to the bacterium Bartonella . [1]: /lookup/doi/10.1126/science.1190333 [2]: /lookup/doi/10.1126/science.1196915

Species Interactions in a Parasite Community Drive Infection Risk in a Wildlife Population

Most hosts, including humans, are simultaneously or sequentially infected with several parasites. A key question is whether patterns of coinfection arise because infection by one parasite species affects susceptibility to others or because of inherent differences between hosts. We used time-series data from individual hosts in natural populations to analyze patterns of infection risk for a microparasite community, detecting large positive and negative effects of other infections. Patterns remain once variations in host susceptibility and exposure are accounted for. Indeed, effects are typically of greater magnitude, and explain more variation in infection risk, than the effects associated with host and environmental factors more commonly considered in disease studies. We highlight the danger of mistaken inference when considering parasite species in isolation rather than parasite communities.

Family Life on the Prairie

Family Life on the Prairie

Effects of cold stress on immune function in the grey-sided vole, Clethrionomys rufocanus

ABSTRACT Effects of cold stress on immune function and energy demand were experimentally investigated in the grey-sided vole. Laboratory-born and wild voles were divided into two groups: one maintained at 5°C (low temperature) and the control at 23°C (room temperature). The voles exposed to low temperature showed a weaker immune response to the challenge antigen than the control voles. Food intake of the voles under low temperature increased in comparison with that of the control, and fat reserves reduced in the voles under low temperature. Kidney, heart and small intestine of the voles were hypertrophied by approximately 10–20% compared with the controls. These results can be interpreted as a trade-off between thermoregulation and immunity. These physiological reactions caused by low temperature may cause higher mortality of grey-sided voles during winter (the non-breeding season) in the field.