Microtus Subterraneus Research Articles

Molecular assessment of the taxonomic status of pine vole species Microtus subterraneus and Microtus majori in southeastern Europe and Turkey

Intra– and inter–specific phylogenetic relationships and the taxonomic status of pine vole populations have been controversial for years, and cryptic species are thought to exist, especially concering the species' distribution area. To clarify the taxonomic status of Turkish populations we analysed mitochondrial (cytochrome–b and cytochrome oxidase–I) and nuclear (interphotoreceptor retinoid binding protein) gene markers, adding GenBank data from Europe and Caucasia. Considering the data obtained based on mean genetic distance, genetic diversity and fixation index values, Bayesian trees and Median–joining networks, we found that M. subterraneus and M. majori are valid species which have diverged since 1.28 Mya. Findings also suggested that although Anatolian, Thracian (Turkish Thrace and Greece) and European populations of M. subterraneus and Anatolian and Caucasian populations of M. majori have been in the process of divergency since 0.528–0.337 Mya correspond to the Pleistocene glacial periods, these intrapopulations do not appear to be different species.Besides, considering the high intraspecific variation in M. subterraneus, it remains likely that new species could be identified in future studies.

Adaptive responses of the pine vole (Microtus subterraneus) population to anthropogenic environmental changes

Adaptive responses of the pine vole (Microtus subterraneus) population to anthropogenic environmental changes

Small mammals in the diet of the tawny owl Strix aluco in selected sites of the Biebrza Basin and Knyszyn Forest in north-eastern Poland.

The analysis of pellets of the tawny owl Strix aluco collected in the years 2009–2023 in 22 sites (ten in the Biebrza Basin and twelve in Knyszyn Forest) allowed for finding four species of Soricomorpha, nine species of Chiroptera and fifteen species of Rodentia (4, 5 and 12 in the Biebrza Basin and 4, 7 and 13 in Knyszyn Forest, respectively). Most common and most frequently caught by owls were: the bank vole Clethrionomys glareolus, the yellow-necked mouse Apodemus flavicollis and the common shrew Sorex araneus. Valuable species of bats included the pond bat Myotis dasycneme and the western barbastelle Barbastella barbastellus noted in Knyszyn Forest. Rare rodents found in both study areas were: the northern birch mouse Sicista betulina and the common dormouse Muscardinus avellanarius while the forest dormouse Dryomys nitedula was noted only in Knyszyn Forest. The European water vole Arvicola amphibius commonly noted in the Biebrza Basin was not found in Knyszyn Forest. On the contrary, the common pine vole Microtus subterraneus was reecorded only in Knyszyn Forest.

COI gene analyses of the Daghestan pine vole (Microtus daghestanicus Shidlovsky, 1919) population from northeastern Turkey

Daghestan pine vole (Microtus daghestanicus Shidlovsky, 1919) is spread in Caucasia, Turkey and Northwestern Iran and distribution of this species is limited to Northeastern Anatolia in Turkey. Few molecular studies on M. daghestanicus have been performed so far, and it was analysed in this study with the mitochondrial cytochrome oxidase subunit I (COI) region and compared with other Terricola species (Microtus subterraneus and Microtus majori) and other Microtus species found in its distribution area (Microtus arvalis and Microtus mystacinus). For this purpose, mean genetic distance values and fixation index values were calculated. Also, Bayesian Inference tree and Median-joining network were constructed. The acquired results showed that M. daghestanicus was clearly separated in the Pleistocene Period and was closer to M subterraneus than M. majori in the subgenus Terricola.

Distribution of Rodent Species (Mammalia: Rodentia) in Zonguldak Province, Turkey

To know rodent species in an area is important in wildlife management studies, forestry applications, conservation purposes, and public health studies because of some rodent-borne diseases. To determine rodent species and their distribution in Zonguldak was aimed to supply a detailed inventory data and distribution maps for further studies in future. Samples were collected mostly by Sherman traps, and rarely conventional cage-like traps, phototraps, or visually from 33 localities that represent different habitat types, between 2009 and 2016. A total of 427 specimens from 15 species were evaluated. These species are: Sciurus anomalus, Myodes glareolus, Microtus subterraneus, M. levis, Apodemus flavicollis, A. sylvaticus, A. uralensis, A. witherbyi, A. mystacinus, Rattus rattus, R. norvegicus, Mus domesticus, M. macedonicus, Glis glis and Muscardinus avellanarius. Of them S. anomalus, M. levis, A. uralensis, M. macedonicus and M. avellanarius were recorded by primary data for the first time from Zonguldak. According to the results, Sciurus anomalus, Apodemus flavicollis and Glis glis are the most common species by being recorded from 13, 12 and 9 localities, respectively. Among the 33 localities trapped, Kurtköy and Beldibi areas have highest number of rodent species by each having 7 species. Trap Night Index (TNI) was calculated to find the most caught rodent species, the overall trap success for rodents caught and the localities where the majority of rodent samples were caught. TNI was calculated as 21.43 for seven of the localities studied. Skull and pelage morphology (pectoral spot expressions, the posterior end of the palatal bone, pterygoid process, fronto-parietal suture and upper molar crown patterns) were used to identify Apodemus species. Morphological evaluations of Apodemus specimens verified the occurrence of A. sylvaticus in Asiatic Turkey.

Здрібнення особин як стратегія популяцій в антропогенних умовах (досвід 50-річного вивчення популяцій гризунів)

Based on results of 50 years of continuous observations of populations of the pine vole (Microtus subterraneus de Selys-Longchamps, 1836) and yellow-necked wood mouse (Sylvaemus flavicollis Melchior, 1834), the phenomenon of reducing body size of individuals was revealed, particularly a significant reduction in body dimensions and body mass. The research was conducted at the Kaniv Nature Reserve covering various stages of the local ecosystem's existence under anthropogenic impact. Four cycles of density dynamics of two populations are chosen for comparison of their characteristics. The first three cycles correspond to qualitatively different periods in the existence of the protected ecosystem and populations of the studied species, whereas the last cycle reflects the current situation. It has been established that the tendency to decrease body dimensions is also characteristic for other rodent species, its manifestations are observed for 35 years, and the scale gradually increases. By fatness indexes, individuals of the pine vole on average lose 23.3% and yellow-necked wood mice lose 16.7% of the former values. It was shown that the level of reduce in exterior parameters is always greater in females than in males, and in the group of breeding adults it can reach 32%. It has been found that the phenomenon also applies to juveniles, whose fatness decreases by an average of 21%. The phenomenon occurs against the background of violations of various aspects of population dynamics, which allows it to be associated with anthropogenic changes in the environment. It is suggested that shrinking can be realized by various mechanisms. First, as a result of mortality, the largest individuals and reproductive females with their greatest energy needs fall out of the population, and, second, the growth and weight gain of young animals is slower. As a result, the decrease in external parameters of individuals reduces their specific energy needs and allows them to better survive under adverse conditions. From these points of view, reducing body dimensions can be considered as a specific population strategy to maintain ecological balance.

Helminths in Myomorph Rodents (Rodentia, Myomorpha) from the National Park “Smolny” and Its Surroundings (European Russia)

The National Park “Smolny” is a large forest area, located in the center of European Russia. The helminth fauna of myomorph rodents was studied for the first time within the National Park in 2018–2020. Rodents were examined by the method of complete helminthological dissection. A total of 30 species of parasites were recorded in 11 rodent species: 6 trematodes, 11 cestodes and 13 nematodes. The trematode Plagiorchis maculosus (Rudolphi, 1802) was found in Clethrionomys glareolus (Schreber, 1780) from the Russian fauna for the first time. Clethrionomys glareolus and Microtus arvalis (Pallas, 1779) are new hosts for P. maculosus and metacestode Versteria mustelae (Gmelin, 1790), respectively. The most widespread and eurybiont rodent species have the most diverse and rich helminth fauna, such as C/ glareolus (14 species), Apodemus agrarius (Pallas, 1771) (12) and Sylvaemus uralensis (Pallas, 1811) (10). The helminth fauna is less diverse in Sylvaemus flavicollis (Melchior, 1834), M. arvalis (7 species each), Microtus agrestis (Linnaeus, 1761) (5), Microtus subterraneus (de Selys-Longchamps, 1836) (3), Sicista betulina (Pallas, 1779) (2) and Arvicola amphibius (Linnaeus, 1758) (1). Comparative analysis the helminth fauna of small rodents from the National Park “Smolny” with micromammals from other regions of European Russia revealed that the high similarity with other areas reaches the helminth fauna of M. subterraneus, S. flavicollis, S. uralensis, S. betulina, A. amphibius and M. agrestis.

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

Management Intensity and Forest Successional Stages as Significant Determinants of Small Mammal Communities in a Lowland Floodplain Forest

The conversion of forests from complex natural ecosystems to simplified commercial woodlands is one of the major causes of biodiversity loss. To maintain biodiversity, we need to understand how current management practices influence forest ecosystems. We studied the effects of forest successional stage and management intensity on the abundance, species richness, and assemblage composition of small mammals. Our results show that management intensity significantly contributes to reducing the number of species after clearcutting. We revealed that intensively managed clearings can make the dispersal or foraging activity of small mammals difficult and hence negatively influence their abundance and species richness. The significantly higher species richness of small mammal species was recorded within more extensively rather than intensively managed clearings. In contrast, we did not observe significant changes in species richness and abundance after intensive management in old-growth forests. Species Clethrionomys glareolus and Apodemus flavicollis reached the greatest abundance in old-growth forest patches. On the other hand, Microtus arvalis and Microtus subterraneus were species mainly associated with the successionally youngest forest stands. Our analysis suggests that intensive management interventions (i.e., vegetation destruction by pesticides and wood debris removal by soil milling) in clearings produce unhostile environments for majority of the small mammal species.

Ticks, fleas and rodent-hosts analyzed for the presence of Borrelia miyamotoi in Slovakia: the first record of Borrelia miyamotoi in a Haemaphysalis inermis tick

In Slovakia, little knowledge is available on the occurrence, hosts and vectors of Borrelia miyamotoi of the relapsing fever group. In the current study, 2160 questing and rodent-attached ticks of six species (Ixodes ricinus, Ixodes trianguliceps, Dermacentor marginatus, Dermacentor reticulatus, Haemaphysalis concinna and Haemaphysalis inermis), 279 fleas belonging to 9 species (Ctenophthalmus agyrtes, Ctenophthalmus solutus, Ctenophthalmus assimilis, Megabothris turbidus, Amalareus penicilliger, Hystrichopsylla orientalis, Ctenophthalmus uncinatus, Doratopsylla dasycnema and Nosopsyllus fasciatus) and skin biopsies from 245 small mammals belonging to eight species (Apodemus agrarius, Apodemus flavicollis, Apodemus uralensis, Myodes glareolus, Crocidura leucodon, Micromys minutus, Microtus arvalis, Microtus subterraneus) were screened for the presence of B. miyamotoi DNA. The overall prevalence of B. miyamotoi found in questing and rodent-attached ticks was 1.8% (23 positive/1260 examined) and 3.4% (31 positive/900 examined), respectively. Borrelia miyamotoi was detected in questing I. ricinus, rodent-attached I. ricinus and H. inermis ticks, and in one male of the common vole (M. arvalis) in different habitats (mainly rural) in eastern Slovakia. However, B. miyamotoi was not found in any of the tested fleas. Our findings indicate that rural habitats with different species of tick vectors and hosts are appropriate for the occurrence of B. miyamotoi.

Detection of Rickettsia spp. in Fleas Collected from Small Mammals in Slovakia, Central Europe

This survey is aimed at investigation of species composition of fleas removed from small terrestrial mammals captured in rural, suburban, and urban types of habitat and molecular screening of the presence and diversity of Rickettsia species in collected ectoparasites. In total, 279 fleas (Siphonaptera) belonging to 9 species of 2 families, Ceratophyllidae and Hystrichopsyllidae, were collected from 115 (46%) out of 250 trapped small mammals of eight species (Apodemus agrarius, Apodemus flavicollis, Apodemus uralensis, Myodes glareolus, Microtus arvalis, Microtus subterraneus, Crocidura leucodon, and Sorex minutus). Rickettsia spp. were found in 2.5% (7/279) of tested fleas, namely in Ctenophthalmus agyrtes, Ctenophthalmus solutus, Ctenophthalmus uncinatus, Megabothris turbidus, and Amalareus penicilliger. Rickettsia felis, Rickettsia helvetica, and unidentified Rickettsia species were detected in fleas infesting small mammals in Eastern Slovakia. The results of the study suggest that some species of rickettsiae have a different range of arthropod vectors.

The Palaeolithic cave of Kalamakia (Mani Peninsula), Greece: new insights on the palaeoenvironment using microvertebrates and mesowear analysis of ruminant teeth

In the present study, results from the examination of mammalian teeth from the cave of Kalamakia with modern techniques, as well as a qualitative overview of the microvertebrate and lithic material, are presented together with a revision of previous related work done for the site, in order to assess the palaeoenvironmental conditions in the area and the role they played in the Neanderthal's repeated occupation of the cave. Geometric morphometrics analyses performed on the first lower molars of Microtus spp. individuals revealed persistent populations of the subgenus Terricola, in which the presence of Microtus thomasi and Microtus subterraneus are continuous through the stratigraphic units. Mesowear analyses performed on ruminant teeth showed no significant variation in toothwear through time, except for relatively elevated levels of dietary abrasion for the more recent samples. The study of the lithics revealed that Neanderthals visited the cave in alternating short and more permanent episodes of occupation, with the human occupants exhibiting special concern for raw material economy, while exploiting poor raw materials for the construction of their tools. The overview of the microvertebrate remains showed a growing trend towards the upper stratigraphic units, where taxa typical of temperate climate, open woodland and shrubland become more dominant. These results, along with observations derived from previous studies, suggest that temperate climate and open environment were the factors that mainly contributed to making the cave of Kalamakia attractive as a habitation site to the humans of the area.

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.

The prevalence of pathogenic forms of Leptospira in natural populations of small wild mammals in Serbia.

The greatest epidemiological significance of leptospirosis in Europe comes from the fact that it is the most widespread zoonosis in the world. However, epizootiological data, especially information on maintenance hosts such as small wild mammals, are largely missing. To fill this gap in data in Serbia, we used RT-PCR for the detection of pathogenic Leptospira species and analysed 107 animals belonging to six species of small wild mammals (Apodemus agrarius, Apodemus flavicollis, Microtus arvalis, Myodes glareolus, Microtus subterraneus and Sorex araneus) collected from two localities. The animals from the first locality that was situated in a tourist area, were collected for four consecutive years (2014-2017). We found persistent incidence of infection from year to year ranging from 6.67% to 78.57%. The average frequency of infected animals was 33.3% with the highest frequency in 2014, the year characterised by a very high number of flooding days. All animals proved to be infected with pathogenic Leptospira species that were collected from the second locality situated in an agricultural area in a single year, 2014. The findings show a variable but constant presence of pathogenic Leptospira species in populations of small wild mammals in the studied areas, which indicates the need for constant monitoring.

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.

Molecular evidence and diversity of the spotted-fever group Rickettsia spp. in small mammals from natural, suburban and urban areas of Eastern Slovakia

Rickettsiae of the spotted fever group are considered as emerging pathogens; ticks, fleas and mites are known to be their vectors. However, the prevalence and species diversity of rickettsiae in small mammals and the role of these hosts in the circulation of bacteria are much less studied. During 2014–2016, a total of 250 small mammals (Apodemus agrarius, Apodemus flavicollis, Apodemus uralensis, Myodes glareolus, Crocidura leucodon, Crocidura suaveolens, Micromys minutus, Microtus arvalis, Microtus subterraneus, Neomys fodiens and Sorex minutus) were captured in natural, suburban and urban habitats of eastern Slovakia. Ear biopsies of 245 individuals were examined for the presence of SFG rickettsiae by molecular methods. The overall prevalence of Rickettsia spp. in small mammals was 11%. The predominant species, Rickettsia helvetica was confirmed in the striped field mouse (A. agrarius), the yellow-necked mouse (A. flavicollis), the bank vole (M. glareolus) and the common vole (M. arvalis) in natural and suburban habitats, followed by Rickettsia sp. closely related to R. felis identified in A. flavicollis captured in a suburban habitat. Finally, R. slovaca was found in only one yellow-necked mouse (A. flavicollis) captured in a natural habitat, with the sympatric occurrence of Dermacentor marginatus and Dermacentor reticulatus ticks. We assume the presence of R. slovaca especially in sites with the occurrence of Dermacentor spp. All small mammals captured in the urban habitat tested were negative for the presence of rickettsiae. This study brings the first molecular evidence of R. slovaca in a rodent captured in Slovakia. Rickettsia sp. closely related to R. felis was first time detected in A. flavicollis in suburban site of Slovakia.The highest species diversity of rickettsiae was observed in A. flavicollis, and the highest prevalence of bacteria was recorded in M. glareolus. The highest occurrence of rickettsiae-positive small mammals was recorded during the spring and autumn months, May, June and September, respectively. This may be related with the seasonal activity of the tick vectors. This study confirms the long-term persistence of Rickettsia spp. in small mammals in natural and suburban habitats of Slovakia.Some rodent species that have a wider ecological valency may contribute to the maintenance, circulation and dissemination of rickettsiae within and out the natural foci more significantly than those species that have narrower relation to the certain type of habitat.

Taxonomic Interpretation of Allopatric Mammalian Forms on the Example of Two Karyoforms of Microtus (Terricola) subterraneus (Rodentia, Arvicolinae) from Eastern Europe.

New European pine vole records from the Novgorod, Kaluga, Voronezh, and Belgorod oblasts were studied by sequencing of the mtDNA cytb gene (1143 bp) and by karyotyping (routine staining and G-banding techniques). The results enabled us to summarize chromosome variability of this species throughout Eastern Europe. In the sample studied, two geographically replacing chromosomal forms have been identified: northern, 2n = 54 (Novgorod and Kaluga oblasts), and southern, 2n = 52 (Voronezh and, presumably, Belgorod oblasts). Our data make the boundaries of these two karyoforms in Eastern Europe more precise and testify to intraspecific level of their taxonomic differentiation.

Simultaneous population fluctuations of rodents in montane forests and alpine meadows suggest indirect effects of tree masting

Resource pulses can generate cross-habitat dispersal of consumers, and therefore affect organisms even in areas where the resource pulses do not occur. We investigated this phenomenon at the elevational treeline in the Carpathian Mountains, where beech (Fagus sylvatica) masting caused an increase in abundance of forest rodents and intensified their use of alpine meadows. We tested 3 hypotheses concerning the impact of forest rodent spillover on the abundance of meadow-dwelling pine voles (Microtus subterraneus): 1) the competition hypothesis: if the spillover affects pine voles mostly through intensified competitive interactions, then pine voles should decline when forest rodents reach their peak abundance, i.e., 1 year after masting; 2) the apparent competition hypothesis: if predators switch to alternative prey when populations of forest rodents collapse, then pine voles should decline 2 years after masting; and 3) the apparent mutualism hypothesis: if the increase of forest rodents temporarily releases pine voles from predatory pressure, pine voles should increase in synchrony with forest rodents—1 year after masting. Our results, while correlative in nature, supported the apparent mutualism hypothesis: 1 year after masting, both forest rodents and pine voles strongly increased their abundance. Two years after masting, when populations of forest rodents crashed, abundance of pine voles returned to pre-masting levels rather than collapse. These findings suggest that pulsed spillover, known mostly from negative effects on organisms in recipient habitats, can also create indirect positive interactions. Furthermore, they illustrate how density-dependent spillover of animals might increase the spatial scale of masting effects beyond the habitats where seeds are released.

Small terrestrial mammals of Albania: distribution and diversity (Mammalia, Eulipotyphla, Rodentia).

In this paper new records are reported for 23 species of small terrestrial mammals (STM) of Albania collected during the field work campaigns organised in the framework of the project “Strengthening capacity in National Nature Protection – preparation for Natura 2000 network” (NaturAL) in Albania during the summer and autumn of 2016 and 2017 Data on small mammals were primarily collected through Sherman live-trapping campaigns in six high priority protected areas of Albania: Korab-Koritnik, Bredhi i Hotovës, Tomorri, Llogara-Karaburun, Divjakë-Karavasta, Liqeni i Shkodrës (Skadar lake), Lëpushë-Vermosh. Other data were obtained by analysis of owl pellets or by direct observation of individuals (dead or alive) in the field. For 21 species Erinaceus roumanicus, Neomys anomalus, Crocidura suaveolens, Crocidura leucodon, Suncus etruscus, Talpa stankovici/caeca, Myocastor coypus, Sciurus vulgaris, Glis glis, Dryomys nitedula, Muscardinus avellanarius, Microtus levis/arvalis, Microtus subterraneus, Microtus thomasi, Microtus felteni, Myodes glareolus, Apodemus sylvaticus, Apodemus flavicollis, Apodemus epimelas, Mus musculus, and Mus macedonicus additional records are provide and their distributions reviewed, while the presence of two new species of shrews (Sorex araneus and Sorex minutus) for Albania is reported for the first time. A comprehensive review of the published and unpublished distribution records of STM species of the country is made, together with an updated checklist and distribution maps of the species.

Aspects biogéographiques de la distribution des micromammifères dans le Limousin

SUMMARY - Investigations were carried out in the granite part of the Limousin to study almost twenty thousand pellets of Tyto alba and analyse the distribution of small Mammals found in these pellets. Their study showed the existence of twenty-two small Mammals and emphasized the diversity of the country. Several ecological factors such as the wet and closed or drier and open landscape, the number of days with frost, artificial meadows mainly acted on the distribution of species. Only Microtus subterraneus and Muscardinus avellanarius were in the southwestern limit of their areas of distribution. The gaps in the distribution of Apodemus flavicollis, Arvicola terrestris, Microtus arvalis, Myoxus glis and Neomys anomalus are discussed. The central European group and the southwestern European group of small Mammals contributed to the population of the Limousin.