Pine Voles Research Articles

FREQUENT LEPTOSPIRA SPP. DETECTION BUT ABSENCE OF TULA ORTHOHANTAVIRUS IN MICROTUS SPP. VOLES, NORTHWESTERN SPAIN.

The common vole (Microtus arvalis) is a major agricultural pest in Europe and is a reservoir for several zoonotic agents, such as Leptospira spp. and Tula orthohantavirus (TULV). However, little is known about the occurrence of those pathogens in voles from Spain, where the species has largely expanded its distribution range in the past decades, causing agricultural pests and zoonotic diseases. For a molecular survey, 580 common voles and six Lusitanian pine voles (Microtus lusitanicus) were collected in 26 localities from four provinces of northwestern Spain. We assessed the presence of Leptospira spp. DNA in kidney tissue by PCR targeting the lipL32 gene, detecting a prevalence of 7.9% (95% confidence interval, 5.9-10.4) for common voles and of 33.3% (95% confidence interval, 4.3-77.7) for Lusitanian pine voles. We identified Leptospira kirschneri in 24 animals and Leptospira borgpetersenii in two animals, using secY gene-specific PCR. We analyzed environmental and demographic factors (such as age class, weight, and sex) and population dynamics data for their potential effect on the Leptospira spp. prevalence in those voles. The Leptospira spp. DNA detection rate in common voles increased significantly with maximum air temperature, vole weight, and amount of accumulated rainfall during the 90 d before capture and within the peak phase of the population cycle. We assessed the presence of TULV in lung tissue of 389 voles by reverse-transcription PCR, with no positive results. The absence of TULV might be explained by the evolutionary isolation of the common vole in Spain. The detection of two Leptospira genomospecies underlines the necessity for further typing efforts to understand the epidemiology of leptospiral infection in the common vole and the potential risk for human health in Spain.

High molecular variability in three pine vole species of the subgenus Terricola ( Microtus , Arvicolinae) and plausible source of polymorphism

High molecular variability in three pine vole species of the subgenus <i>Terricola</i> ( <i>Microtus</i> , Arvicolinae) and plausible source of polymorphism

Mediterranean Pine Vole, Microtus duodecimcostatus: A Paradigm of an Opportunistic Breeder.

Simple SummaryIn temperate zones of the Earth, some mammalian species reproduce seasonally whereas others do it continuously. Other species are summer breeders in the north and winter breeders in the south. Thus, the reproductive pattern seems not to be a species-specific but a population-specific trait. We investigated the reproduction pattern of the Mediterranean pine vole, Microtus duodecimcostatus, in the area around the city of Granada in Southern Spain, and found that individuals living in wastelands reproduce seasonally whereas those living in close poplar plantations (just 8 km apart) reproduce throughout the year, as did voles captured in wastelands and kept in captivity. These animals represent thus a paradigm of an opportunistic breeder as particular individuals stop breeding or not, depending on the environmental conditions they face at any moment. Sexually inactive male voles undergo complete testis inactivation and their sperm production is halted. The immune system in active testes is depressed, a phenomenon known as “immune privilege” that protect germ cells from autoimmune attack. We studied gene activity in active and inactive testes and our results indicate that such an immune privilege is lost in inactive testes, suggesting an important role for this process during testis regression.Most mammalian species of the temperate zones of the Earth reproduce seasonally, existing a non-breeding period in which the gonads of both sexes undergo functional regression. It is widely accepted that photoperiod is the principal environmental cue controlling these seasonal changes, although several exceptions have been described in other mammalian species in which breeding depends on cues such as food or water availability. We studied the circannual reproductive cycle in males of the Mediterranean pine vole, Microtus duodecimcostatus, in the Southeastern Iberian Peninsula. Morphological, hormonal, functional, molecular and transcriptomic analyses were performed. As reported for populations of other species from the same geographic area, male voles captured in wastelands underwent seasonal testis regression in summer whereas, surprisingly, those living either in close poplar plantations or in our animal house reproduced throughout the year, showing that it is the microenvironment of a particular vole subpopulation what determines its reproductive status and that these animals are pure opportunistic, photoperiod-independent breeders. In addition, we show that several molecular pathways, including MAPK, are deregulated and that the testicular “immune privilege” is lost in the inactive testes, providing novel mechanisms linking seasonal testosterone reduction and testis regression.

First record of helminths of the European pine vole, Microtus subterraneus (Rodentia, Cricetidae) in Russia with overview on the rodent�s range

First record of helminths of the European pine vole, Microtus subterraneus (Rodentia, Cricetidae) in Russia with overview on the rodent�s range

Rickettsia spp. in rodent-attached ticks in Estonia and first evidence of spotted fever group Rickettsia species Candidatus Rickettsia uralica in Europe

BackgroundRickettsia spp. are human pathogens that cause a number of diseases and are transmitted by arthropods, such as ixodid ticks. Estonia is one of few regions where the distribution area of two medically important tick species, Ixodes persulcatus and I. ricinus, overlaps. The nidicolous rodent-associated Ixodestrianguliceps has also recently been shown to be present in Estonia. Although no data are available on human disease(s) caused by tick-borne Rickettsia spp. in Estonia, the presence of three Rickettsia species in non-nidicolous ticks has been previously reported. The aim of this study was to detect, identify and partially characterize Rickettsia species in nidicolous and non-nidicolous ticks attached to rodents in Estonia.ResultsLarvae and nymphs of I.ricinus (n = 1004), I. persulcatus (n = 75) and I.trianguliceps (n = 117), all removed from rodents and shrews caught in different parts of Estonia, were studied for the presence of Rickettsia spp. by nested PCR. Ticks were collected from 314 small animals of five species [Myodes glareolus (bank voles), Apodemus flavicollis (yellow necked mice), A.agrarius (striped field mice), Microtus subterranius (pine voles) and Sorex araneus (common shrews)]. Rickettsial DNA was detected in 8.7% (103/1186) of the studied ticks. In addition to identifying R.helvetica, which had been previously found in questing ticks, we report here the first time that the recently described I.trianguliceps-associated Candidatus Rickettsia uralica has been identified west of the Ural Mountains.Graphical

Differentiation and Phylogenetic Relationships of Three Pine Vole Species of the Subgenus Terricola (Rodentia, Arvicolinae, Microtus): Results of Analysis of the BRCA1 and XIST Nuclear Gene Fragments

Abstract—The variability of three pine vole species, as well differences between them, and the phylogenetic relationships were determined by analysis of nucleotide sequence fragments of nuclear genes BRCA1, exon 11 (1473 bp) and XIST (415 bp). The data obtained by us demonstrate significant genetic disunity of the species and M. majori separation related to M. daghestanicus–M. subterraneus. Studying the XIST gene revealed M. majori differentiation into close North Caucasian and Trans-Caucasian population groups. Fragments of both nuclear genes exhibited unexpectedly high intraspecific variability in M. daghestanicus out of clear relations with the geographic origin of the specimens. We propose that differences in the character of genetic polymorphism between M. daghestanicus and M. majori are due to their ecological peculiarities.

Does wild boar rooting affect spatial distribution of active burrows of meadow-dwelling voles?

Soil overturn by wild boar Sus scrofa is known to affect biodiversity, from plant communities to invertebrates, reptiles and small mammals. Rooting activity has been shown to be particularly intensive in open areas and particularly on fallows and meadows located on hill or mountain tops. In these habitat types, the impact of wild boar on small mammal assemblies has never been assessed. In this work, we evaluated whether rooting activity affected the spatial distribution of the Savi’s pine vole Microtus savii in a hilly area of Central Italy, throughout four seasons. The spatial distribution of this vole has been determined through the open-hole index, i.e. by assessing the vole propensity to reopen tunnel entrances which we previously closed with soil. Rooting intensity was the highest in cold months, i.e. when drive hunting may increase wild boar occurrence within protected areas and outside wooded areas. According to our GLMM, reopening of vole burrow entrances increased with increasing distances from rooted areas and with increasing geophytic diversity. Meadow-dwelling voles living on shallow underground burrow systems seem to avoid soil overturn by wild boar and that they prefer creating their tunnels where plant diversity building up the staple of their diet is the highest. Our results furtherly emphasized the importance of wild boar monitoring also in open areas and hill grasslands, particularly when rooting intensity is the highest, i.e. in cold months.

Small-mammal characteristics affect tick communities in southwestern Tennessee (USA).

Life histories can influence the degree of parasite infestations on a host. Pressures exerted on hosts based on age and sex convey varying degrees of parasite prevalence due to differences in host lifestyles, but it is not known how interactions between different host traits affect tick numbers. The objective of this study was to determine if host characteristics (e.g., age, sex, weight, and their interactions) affect the mean number of ticks found on small mammals regardless of host species or habitat. Sherman live traps were placed in forest and grass/forb habitats representative of the southeastern United States. After capture, host characteristics were recorded, and hosts were then searched for ticks. A total of 281 small mammals (148 Peromyscus leucopus, 34 P. maniculatus, 76 Sigmodon hispidus, 16 Microtus pinetorum, and 7 Ochrotomys nuttalli) and 610 ticks (488 Dermacentor variabilis, 114 Ixodes scapularis, 1 Amblyomma americanum, and 7 A. maculatum) were collected in this study. Host's age, sex, and weight affected the number of ticks collected from small mammals and significant interaction effects between host traits occurred (weight by sex, weight by age, and sex by age). For instance, female subadult rodents had significantly more ticks compared to female adults, male subadults had significantly fewer ticks compared to male adults, and the number of ticks on a host increased as host body mass increased. These results support the hypothesis that the number of ticks vary on rodent hosts based on life histories and trait interactions. Therefore, understanding the behavioral mechanisms of a host can aid in the management of parasites in the environment.

Cytogenetic Characteristics of Microtus guentheri, Microtus arvalis sensu lato and Microtus majori (Mammalia: Rodentia) From Turkey: Constitutive Heterochromatin Distribution

Conventionally stained and C- banded karyotypes of Guenther’s vole (Microtus guentheri), Major's pine vole (Microtus majori) and Common vole (Microtus arvalis) were studied from Turkey. Diploid chromosome numbers of M. guentheri, M. arvalis and M. majori were found as 2n=54 and NFa=52, 2n=46 and NFa=68 and 2n=54 and NFa=56, respectively. All chromosomes of M. guentheri were pericentromeric C- band. In Microtus arvalis (obscurus cytotype) and Microtus majori karyotypes, autosomal chromosomes were heterochromatin C band positive and negative band. In M. arvalis (obscurus cytotype), sex chromosome was C band negative. In this study, heterozygote chromosome was not found in the obtained autosomal chromosome set of M. arvalis. M. majori has enlarged heterochromatin block from centromere to telomere on the long arm of X chromosome. Y chromosome was completely heterochromatin.

Первая находка Microtus subterraneus (de Sélys-Longchamps, 1836) (Rodentia, Cricetidae) в Мордовии, Россия

В 2018 и 2019 гг. проведено изучение видового состава и численности микромаммалий национального парка «Смольный» (Республика Мордовия). Отловлено 8 видов грызунов (Rodentia) и 4 вида насекомоядных (Eulipotyphla). На территории Мордовии впервые была поймана одна особь подземной полевки Microtus subterraneus. На данный момент место отлова считается самым крайним восточным обнаружением вида в ареале.

Assessment of seasonal variation of diet composition in rodents using DNA barcoding and Real-Time PCR

The study of animal diet and feeding behaviour is a fundamental tool for the illustration of the ecological role of species in the ecosystem. However, size and quality of food intake samples make it hard for researchers to describe the diet composition of many small species. In our study, we exploited genomic tools for the analysis of the diet composition of the Savi’s pine vole (Microtus savii) using DNA barcoding and qPCR techniques for the identification of ingested plant species retrieved from stomach contents. In contrast with previous studies, we found that, despite being a fossorial species, the Savi’s pine vole is a selective feeder that undergoes intense superficial activity in search for food. In addition, our study shows that with a a priori knowledge of the candidate plant species included in animal diet, qPCR is a powerful tool to assess presence/absence, frequency of occurrence and electivity of ingested species. We conclude that this approach offers new opportunities to implement the analysis of food selection in small animals, thereby revealing a detailed picture of plant-animal interactions.

Enamel microstructure and morphometric discrimination of sympatric species of Microtus (Rodentia)

Prairie (Microtus ochrogaster) and woodland (Microtus pinetorum) voles, which exhibit distinctly different ecological preferences (grassland versus forest), commonly co-occur in paleontological deposits in eastern North America. Despite their ecological differences, their molar morphology is similar. Assuming that those ecologic differences occurred in the past, differentiation of these two taxa is important for paleoenvironmental reconstruction. A sample of 51 lower first molars from living populations were viewed via scanning electron microscope to qualify and quantify schmelzmuster (enamel microstructure) to species-specific standards applicable to the fossil record. The most obvious differences between schmelzmuster of the two taxa are the relatively thicker bands of radial enamel on the leading edges of triangles of M. ochrogaster, as well as the consistent retention of tangential or primitive tangential enamel on the trailing edges and posterior enamel band of the posterior loop of M. pinetorum. Discriminant analysis of landmark data from the same 51 specimens established morphological boundaries for these taxa and successfully separated the recent m1s of M. ochrogaster from those of M. pinetorum.To test identification confidence from previous work, and to add an independent means of identification for future work (at any site), both techniques were applied to a sample of three-closed triangle (“M. ochrogaster” type) m1s from the late Pleistocene Wapsipinicon Local Fauna of Jones County, Iowa. Identifications of the specimens from the Wapsipinicon l.f. based on schmelzmuster and morphometric analysis are consistent with those reached using traditional morphology. Such methods serve as independent “check” of traditional (qualitative) identification, highlight new species-level characters, and quantify previously described features, for discrimination of these taxa.

Reviewing an eco-biogeographic question at regional scale: the unexpected absence of a ubiquitous mammal species (Microtus savii, Rodentia) in coastal Southern Tuscany (central Italy)

We reviewed the historical and recent data about the unexpected absence of a generalist ubiquitous mammal (Savi’s pine vole Microtus savii, Rodentia) from a large sub-regional coastal land reclaimed area of Tyrrhenian central Italy, trying to search for causes explaining it. We assessed the possible role of different factors for different sub-areas as, in primis, biogeographic isolation (Monte Argentario) and granulometric/geochemical soil characteristics (Maremma plain) linked to land reclaimed history. However, bioclimatic regime, and competition with other species in area of recent colonization, examined in relation to some specialized species traits could be added to explain the unexpected absence of this ubiquitous rodent. Comparing our data with other geographical areas with similar characteristics, we hypothesize that none of these factors can be considered individually determinant, but that the cause of this absence could be determined by their interaction among different causal factors. This note would stimulate future field sampling design aimed to test the different hypotheses here inductively proposed.

Winter activity rhythms of a rodent pest species in agricultural habitats

Predation risk is the main factor affecting movements of mammal prey species. Here we assessed the activity patterns of a nearly endemic fossorial rodent, the Savi’s pine vole Microtus savii, in two agroecosystems in central Italy. Direct captures were carried out in cold months (December–March) with live-traps; sex and age were recorded for each captured individual following standard methods. Savi’s pine voles were mostly active during daytime in both study sites, with no differences between sexes or age classes. Night-time movements were mainly registered during waning moon nights and were severely restricted in bright moonlight. The activity pattern of Savi’s pine voles seems to support the hypothesis of predation avoidance. The most common predators of these small rodents are mainly active during bright nights, when visibility is highest, forcing voles to be more active aboveground during daylight hours as well as in the darkest nights. Efficient monitoring and trapping programmes should therefore take place in daylight hours to increase capture success and to reduce stress levels of the captured animals.

The complete mitochondrial genome of the common pine vole Terricola subterraneus (Arvicolinae, Rodentia)

In this paper, we report the complete mitochondrial genome of the common pine vole Microtus (Terricola) subterraneus, which was sequenced for the first time using Illumina next-generation sequencing (NGS) technology. The total length of the mitogenome was 16,398 bp and contained 12S, 16S rRNAs, 22 tRNAs, 13 protein-coding genes, and a 883 bp D-loop in the characteristic arrangement of subfamily Arvicolinae, Rodentia. Overall base composition of the complete mitochondrial DNA is A (33.0%), C (26.5%), G (13.4%), and T (27.0%), respectively. Phylogenetic analysis of mitochondrial genomes showed a classic taxon pattern, identified using individual phylogenetic markers.

Vocal communication in Microtus (Terricola) schelkovnikovi and M. (T.) daghestanicus in the audible range of frequencies

Vocal communication in the audible range of sound frequencies in two species of voles from the subgenus Terricola includes two calls: squeak-type vocalizations in the context of discomfort; and courtship vocalization, although the latter is rarely used by the animals. In this study, compared with Schelkovnikov’s pine vole [Microtus (Terricola) schelkovnikovi], squeak-type vocalizations of the Daghestan pine voles [M. (T.) daghestanicus] showed higher frequency characteristics and shorter duration. The squeak-type vocalizations of the former species did not exhibit sexual dimorphism. Differences in the call characteristics of the two species could be the result of both gene drift and the effects of biotopes on the evolution of their sound signals.

Changes in the tawny owl Strix aluco diet along an urbanisation gradient

The aim of this study was to describe how the diet of tawny owl changed along an urbanisation gradient. The research was conducted from 2003 to 2011 in central Poland. Pellets were collected in the following zones: the center of Warsaw, capital city of Poland (inhabited by approximately 2 million people), its outskirts and rural areas beyond the city. To investigate the differences in the percentages of the main groups of prey between the three zones, a redundancy analysis (RDA) method was implemented using CANOCO software. Sparrows, rats, pine voles and striped field mice were most connected to the city center, whereas voles (all species pooled together), northern birch mice, hazel dormice and insects were more commonly found among prey items collected in rural areas. As the outskirts were transitional areas where different habitats typical for both rural areas (such as forest complexes) and urban areas (such as parks or built-up areas) were present, no prey group was strongly connected to this landscape. Mammals were dominant in the diet in winter in all habitat types. Their share ranged from 52% (in the city center) to approximately 90% in the outskirts and rural areas. Birds, amphibians, reptiles and insects were more frequent in summer. Overall, the study confirmed high plasticity of the species as an opportunistic predator and its ability to adapt to long-term changes in its main prey in most urbanized areas.

A contribution to the knowledge of diet composition of the Barn Owl Tyto alba in the area of Pisa (Italy)

Abstract We examined the pellets of the Barn Owl Tyto alba, collected in Pisa, Italy, in 2012. Altogether, 219 specimens of small mammals were found in 85 pellets. The Barn Owl diet was composed of ten species of small mammals, representing three different families (Muridae, Cricetidae, Soricidae). The main prey species was the Wood Mouse Apodemus sylvaticus, followed by the House Mouse Mus musculus and the Savi’s Pine Vole Microtus savii. While the smallest of the small mammals from the area, the Etruscan Shrew Suncus etruscus, was well represented in the pellets, some larger species of small mammals were not represented at all. The reason for such result may lie in the upper limit for our Barn Owl’s prey size. Results suggest that optimal prey weight for our Barn Owl may be between 26–75 g of body mass, however, the prey can be occasionally as heavy as almost 100 g, represented by adult Rat Rattus spp. Nevertheless, our results may not reflect the true hunting strategy of the Barn Owl, but the availability of a certain food item at one point in time.

Reproductive isolation between sister species of Iberian pine voles, Microtus duodecimcostatus and M. lusitanicus

Contact zones of recently diverged species provide the ideal opportunity to study the nature of reproductive barriers. The Mediterranean (Microtus duodecimcostatus) and Lusitanian pine voles (M. lusitanicus) are a pair of recently diverged sister species endemic to Western Europe. Recent microsatellite data raised the possibility that hybridisation events, although rare, may still occur in the area of sympatry of both species. Here we evaluated the nature and extent of reproductive isolation between M. duodecimcostatus and M. lusitanicus through a laboratory crossbreeding experiment and two-way mate preference tests on the basis of chemical cues. Crossbreeding of sympatric individuals from the two species was successful and followed Haldane’s rule, revealing hybrid male sterility and reduced fertility of hybrid females. Results from mate preference tests showed males of both pine vole species could discriminate and preferred female conspecifics to heterospecifics or hybrid females on the basis of chemical cues alone. On the contrary, females of both pine vole species did not show a clear preference for conspecific over heterospecific male chemical cues, suggesting females may need additional cues to discriminate between males of the two species. As a whole our results indicate both prezygotic (i.e. species-specific mate recognition systems) and postzygotic barriers (i.e. male hybrid sterility, female reduced fertility and behavioural sterility ― decreased ability to find or attract mates) have evolved, and should make hybridisation of the Iberian pine voles under natural conditions an unlikely event. The role of both species mating preferences and interspecific behavioural interactions in the asymmetric mitochondrial introgression pattern of the Iberian pine voles is discussed.

Detection of Rabbit Hemorrhagic Disease Virus GI.2/RHDV2/b in the Mediterranean Pine Vole ( Microtus duodecimcostatus) and White-Toothed Shrew ( Crocidura russula).

The European wild rabbit ( Oryctolagus cuniculus) is a key prey species on the Iberian Peninsula, and several predator species that are at risk of extinction are dependent on them as prey. A new rabbit hemorrhagic disease (RHD) virus genotype (GI.2/RHDV2/b) emerged in 2010 and posed a threat to wild rabbit populations. During a survey aimed at investigating RHD epidemiology in wild rabbits, GI.2/RHDV2/b was detected by duplex real-time PCR in carcasses of one Mediterranean pine vole ( Microtus duodecimcostatus) and two white-toothed shrews ( Crocidura russula). Laboratory New Zealand white rabbits that were challenged with inocula obtained from the liver of the small mammals died showing RHD lesions, confirming the infectiousness of the isolates. Phylogenetic analysis of the VP60 gene nucleotide sequences showed complete homology between the isolates from the two small mammal species and a high degree of similarity, but not complete homology, to GI.2/RHDV2/b sequences from wild rabbits. The GI.2/RHDV2/b genotype has not been reported in species outside the order Lagomorpha.