Pine Voles Research Articles

Breeding characteristics of the Lusitanian pine vole, Microtus lusitanicus

Abstract Little is known about the breeding characteristics of the Lusitanian pine vole, Microtus lusitanicus, a Terricola representative from south-western Europe. The scarce information on this subject is surprising since, as with other arvicolines, in high population densities these animals can be agricultural pests. In this study we report on the reproduction of the species in a locality of El Bierzo (province of León, northwestern Spain), a zone where this vole frequently damages orchards, crops, and vegetable gardens. The sample analysed consisted of approximately 300 specimens, captured by farmers over several years, which were donated to us for study. Results revealed that reproduction in this population probably occurs all year round, although sexual activity could be slightly lower in winter. In males and females monthly mean of adult body mass did not vary significantly during the year. Sexual monomorphism in adult body size, the relatively small testes of mature males, and the balanced sex ratio observed both in non-mature and mature specimens suggest that in this population M. lusitanicus has a monogamous mating system. In general, mean litter size increased with body mass (age) and showed a seasonal variation, with significantly higher values in spring than in autumn. In comparison with other Microtus species, the mean litter size found in M. lusitanicus was low, indicative of a K-selection pattern.

Spatial and temporal ecology of the Lusitanian pine vole (Microtus lusitanicus) in a Mediterranean polyculture

Abstract In this study we report the first data on the spatial ecology of the Lusitanian pine vole (Microtus lusitanicus). Data report to the breeding season and to a traditional Mediterranean agricultural landscape in Central Portugal, using radio-telemetry methods. We documented large home range areas with values of 1042 m2 for males and 862 m2 for females (MCP method; 95% kernel method with values of 229 m2 and 159 m2 for males and females, respectively). Although no significant differences between sexes or reproductive status were found, longer daily movements were observed in reproductively inactive males. Pair bonding and home range overlap was observed between males and females, as well as between females and sub-adults. Voles showed no distinct preference for day or night for activity periods and movements. However, this result was dependent on sex, reproductive status and time of day. Voles revealed habitat preference for both spatial scales of analysis: they selected verges, vines and olives, within the study area, and used more verges within their home ranges, when compared to the other habitat types. The use of space by Microtus lusitanicus, in comparison with other microtines, suggests the occurrence of spatial associations between males and females in monogamous pairs. The importance of verges and linear habitats within an agricultural context is apparent, once they provide food and shelter from predators and human interventions.

Factors influencing large-scale distribution of two sister species of pine voles (Microtus lusitanicus and Microtus duodecimcostatus): the importance of spatial autocorrelation

The Lusitanian pine vole ( Microtus lusitanicus (Gerbe, 1879)) and the Mediterranean pine vole ( Microtus duodecimcostatus de Selys-Longchamps, 1839) are sister species with burrowing habits and a restricted European distribution. Our aim was to assess the relative effect of environmental, soil, and spatial characteristics on the distribution of these species in Portugal, and obtain predicted occurrence maps for each species, particularly to identify areas of sympatry. We used spatial eigenvector mapping (SEVM) to describe the spatial autocorrelation in species data, and we partitioned the variance in species distributions to quantify the relative effects of environmental, soil, and spatial characteristics. The spatial variables explained the major part of variability in both species distributions and were more important than environmental or soil variables. The Lusitanian pine vole occurs in areas outside landscape units of grassland, higher rainfall, frost, and cambisols, with mostly acid soils, lower abundance of litosols, and presence of solonshaks. The Mediterranean pine vole is distributed in grassland areas within intermediate values of soil pH, dominated by litosols and luvisols, and lower rainfall, frost, and cambisols. Our results showed disjunct sympatric areas of small size and a parapatry boundary for the centre of Portugal, suggesting that contact zones are probably narrow.

The Woodland Vole on Konza Prairie Biological Station, Kansas

The Woodland Vole on Konza Prairie Biological Station, Kansas

Using presence signs to discriminate between similar species

The Lusitanian and the Mediterranean pine voles (Microtus lusitanicus Gerbe, 1879 and Microtus duodecimcostatus de Selys-Longchamps, 1839) are fossorial sister species and have an allopatric pattern of distribution in Portugal, which includes a potential sympatry area in the centre of the country. The present study aimed to determine the validity of using presence signs in the field for discrimination of the two species in an area of sympatry (Northern Alentejo) and the characteristics that achieve the best classification accuracy. A total of 175 trapping plots were sampled across the study area. Prior to the set up of traps, ten presence signs were randomly selected for measurements of four variables: proportion of soil mounds, mean diameter of mounds, proportion of burrow openings and mean diameter of burrow openings. On the basis of a classification tree analysis, results showed that presence signs can be used to discriminate plots inhabited by one or the other species in the studied sympatry area. The characteristic that most accurately enables species identification is the proportion of burrow openings: for every ten presence signs found in a plot, if more than eight have an opening, then it is inhabited by M. lusitanicus (i.e. mostly burrow openings with few or no mounds present); if eight or fewer have an opening, M. duodecimcostatus is present (i.e. mostly mounds with few or no burrow openings).

Microtus bavaricus discovered in Croatia: Southern refugium or geographical variation?

According to phylogenetic analyses based on the mitochondrial cytochrome b (cytb) gene and the control region (CR), three morphologically cryptic vole species of the genus Microtus (subgenus Terricola, Arvicolinae, Rodentia) represent a well supported monophyletic group (Haring et al. 2000; Martinkova et al. 2007) referred to as Microtus multiplex complex. After Martinkova et al. (2007) the primary divergence within the complex occurs between M. multiplex sensu stricto and the sister species M. liechtensteini (Wettstein, 1927) and M. bavaricus (Konig, 1962). Molecular analysis of mitochondrial DNA from M. bavaricus and M. liechtensteini revealed the lowest observed divergence between any vole species indicating a very recent origin of the two taxa (Haring et al. 2000; Martinkova et al. 2007). Microtus bavaricus, the Bavarian pine vole, was considered as an endemic species of the Alps – only one locality in Bavaria, Germany (terra typica at GarmischPartenkirchen) was known (Konig 1982) before genetic analyses revealed that it exists also in northern Tyrol (Rofan Mt) in Austria (Haring et al. 2000) (Fig. 1). In Germany, intensive surveys have failed to find the species both in the type locality and elsewhere (H. Meinig, pers. comm. 2006). Most probably due to the loss of suitable habitat it is locally extinct by now. Thus, the Rofan population was considered to be the

Does time after pair bond disruption affect subsequent reproduction in the socially monogamous woodland vole (Microtus pinetorum)?

Disruption of the pair bond between socially monogamous animals leads to changes in behavior, which may have reproductive consequences. There are two alternative hypotheses to explain the effect of the length of time since pair bond disruption on subsequent reproduction. One hypothesis predicts that voles housed immediately with a new opposite-sex conspecific will be as likely to produce litters and will produce them as quickly as voles separated from their initial mate for longer. Alternatively, if attachment between mates is enduring, we expect that more voles separated longer from their previous mates will produce litters and produce them sooner than voles re-paired immediately after separation from their initial mates. Woodland voles, paired with opposite-sex conspecifics, remained together until parturition. Mates were then separated for 0, 7, or 14 days until re-pairing with an opposite-sex conspecific. Pair bond disruption did not prevent males and females from mating subsequently, which was consistent with data from our breeding colony. In addition, the length of time an individual remained alone after pair bond disruption did not affect the latency to produce a litter. Our results show that having been paired previously does not affect subsequent reproduction in this socially monogamous vole.

Selective feeding of pine voles on roots of tree seedlings

Previous studies have implicated numerous physical and biotic factors as contributing to the failure of oak to regenerate successfully throughout substantial portions of eastern North America. Recent field evidence in southern Indiana implicated belowground herbivory by pine voles ( Microtus pinetorum (LeConte, 1830)) as a potentially important but overlooked mortality agent for oak seedlings. We used cafeteria-style feeding trials to determine whether selection of hardwood seedlings by captive pine voles differed according to species or age. White oak ( Quercus alba L.) was selected more frequently and experienced a greater proportion of root removal by pine voles than same-age seedlings of the other four species tested. Yellow poplar ( Liriodendron tulipifera L.) was never eaten. White oak seedlings 3 and 6 weeks of age suffered proportionately greater root removal than conspecific seedlings 12 and 15 weeks of age; pine voles removed roughly constant levels of root biomass irrespective of seedling age. Our results confirm that pine voles selectively feed on oak seedlings. In areas where pine voles are abundant, belowground herbivory could limit regeneration of oak by reducing seedling growth and survival. The importance of pine voles as factors influencing the success of oak regeneration warrants closer scrutiny in future field studies.

First reports of XXY aneuploidy in natural populations of Thomas’ pine vole Microtus thomasi (Rodentia: Arvicolidae) from Greece

As part of an extensive cytological study in natural populations of Thomas’ pine vole Microtus thomasi, two cases of XXY aneuploidy (2 n=45, FN=47) from different localities of NW Peloponnesus, Greece were recently recorded. These constitute the first report of sex chromosome aneuploidy for this species, in a sample of 366 individuals from 89 localities of Greece. Both individuals appeared with a male phenotype and normal morphology; however, measurements and histological examination in the testes of one of the two individuals imply a severely impaired fertility. The above findings translate to a relatively high rate of sex chromosome aneuploidy (0.55%) (upper 95% CI 1.96%) for the natural populations of Microtus thomasi and possible reasons for this are discussed.

Litter Size Influences Maternal but not Paternal Care in Three Species of Voles, as Measured by Nest Attendance

Total parental expenditure of mammals and birds has been predicted to increase with litter or brood size, but data from rodents provide little support for this prediction. We examined the effects of natural variation in litter size on parental nest attendance in pine (= woodland), prairie, and meadow voles housed in seminatural environments. In all 3 species, mothers spent less time in the nest with large litters than with small; time spent in the nest by fathers was unaffected by litter size. We suggest that failure to meet the prediction of increased parental expenditure with increased litter size reflects basic differences in the manner in which mammals and birds feed altricial young.

Distribution of Corticotropin-Releasing Factor and Urocortin 1 in the Vole Brain

Brain receptor patterns for the corticotropin-releasing factor (CRF) receptors, CRF1 and CRF2, are dramatically different between monogamous and promiscuous vole species, and CRF physiologically regulates pair bonding behavior in the monogamous prairie vole. However, it is uncertain whether species differences also exist in the neuroanatomical distribution of the endogenous ligands for the CRF1 and CRF2 receptors, such as CRF and urocortin-1 (Ucn1). We compared the expression of CRF and Ucn1 in four vole species, monogamous prairie and pine voles, and promiscuous meadow and montane voles, using in situ hybridization of CRF and Ucn1 mRNA. Our results reveal that CRF mRNA expression patterns in all four vole species appear highly conserved throughout the brain, including the olfactory bulb, nucleus accumbens, bed nucleus of the stria terminalis, medial preoptic area, central amygdala, hippocampus, posterior thalamus, and cerebellum. Similarly, Ucn1 mRNA primarily localized to the Edinger-Westphal nucleus in all four vole species. Immunocytochemistry in prairie and meadow voles confirmed localization of CRF and Ucn1 protein to these previously identified brain regions. These data demonstrate a striking dichotomy between the extraordinary species diversity of brain receptor patterns when compared to the highly conserved brain distributions of their respective ligands. Our findings generate novel hypotheses regarding the evolutionary mechanisms underlying the neural circuitry of species-typical social behaviors.

Diet of the Jalapan Pine Vole (Microtus quasiater) in Mature Mountain Cloud Forest: Fig. 1

We determined the feeding habits, including seasonal and annual variations in diet composition, of the Jalapan pine vole (Microtus quasiater), an endemic rodent from Mexico. During 3 annual cycles, feces were collected on a monthly basis from a population located in a mountain cloud forest at Apulco, Puebla, Mexico. Microscope slides were prepared from each fecal sample, and fragments of food items were identified by comparison with photomicrographic references. Thirty-six plant species occurred in the diet, representing more than 60% of the identified plant species in our study area. Roots, sedge heads, seeds, dicotyledonous flowers, and fungi each contributed less than 10% of the diet. This rodent consumed 85% of the monocotyledonous species present in the area, but only 50% of the dicotyledonous species. The diet showed seasonal and yearly differences. M. quasiater remained highly selective in its diet.

Assemblages of dipterans (Diptera) in burrows of the European pine vole Microtus (Terricola) subterraneus Sel.-Long. in the “Les na Vorskle (Forest on the Vorskla River)” Nature Reserve (Belgorod Province)

Six species of bothrobiontic flies of 3 families (Phoridae, Helomyzidae, and Sphaeroceridae) were recorded from nests of the European pine vole Microtus (Terricola) subterraneus Sel.-Long. in Belgorod Province (“Forest on the Vorskla River” Nature Reserve). Four species are recorded in the fauna of Russia for the first time.

CRF receptors in the nucleus accumbens modulate partner preference in prairie voles

Recent evidence suggests a role for corticotropin-releasing factor (CRF) in the regulation of pair bonding in prairie voles. We have previously shown that monogamous and non-monogamous vole species have dramatically different distributions of CRF receptor type 1 (CRF 1) and CRF receptor type 2 (CRF 2) in the brain and that CRF 1 and CRF 2 receptor densities in the nucleus accumbens (NAcc) are correlated with social organization. Monogamous prairie and pine voles have significantly lower levels of CRF receptor type 1 (CRF 1), and significantly higher levels of type 2 (CRF 2) binding, in NAcc than non-monogamous meadow and montane voles. Here, we report that microinjections of CRF directly into the NAcc accelerate partner preference formation in male prairie voles. Control injections of CSF into NAcc, and CRF into caudate-putamen, did not facilitate partner preference. Likewise, CRF injections into NAcc of non-monogamous meadow voles also did not facilitate partner preference. In prairie voles, this CRF facilitation effect was blocked by co-injection of either CRF 1 or CRF 2 receptor antagonists into NAcc. Immunocytochemical staining for CRF and Urocortin-1 (Ucn-1), two endogenous ligands for CRF 1 and CRF 2 receptors in the brain, revealed that CRF, but not Ucn-1, immunoreactive fibers were present in NAcc. This supports the hypothesis that local CRF release into NAcc could activate CRF 1 or CRF 2 receptors in the region. Taken together, our results reveal a novel role for accumbal CRF systems in social behavior.

Cadmium accumulation in deer tongue grass ( Panicum clandestinum L.) and potential for trophic transfer to microtine rodents

Site 36 at the Crab Orchard National Wildlife Refuge includes a Cd-contaminated soil dominated by deer tongue grass ( Panicum clandestinum L.). Analysis of deer tongue grass from this site indicated that biomass and leaf surface area were reduced and that there was a linear relationship between both plant bioavailable soil Cd and total soil Zn and tissue Cd concentration. The Cd concentrations in stems and leaves were also used to estimate the dietary Cd exposures that might be experienced by prairie voles ( Microtus ochrogaster) and pine voles ( M. pinetorum) consuming deer tongue grass. Renal and hepatic Cd burdens predicted from exclusive consumption of deer tongue grass would be comparable to those that have resulted in chronic toxicity in rodents. The results suggest that for the contaminated soil at Site 36, conditions could allow for the accumulation of Cd in deer tongue grass to concentrations that may pose an ecological risk.

Habitat associations of small mammals in farmed landscapes: implications for agri-environmental schemes

Abstract The small mammal community in 21 localities of north-western Spain was evaluated in the light of land use composition. The two geomorphologic categories characterising the study area, the main use of the land (arable/pastoral) and main crop types of each sampling locality were used as potential predictors of the relative abundance of five common small mammal species. The Common vole, Microtus arvalis showed a weak relationship with land uses, probably due to the recent colonisation process this species experienced in the study area. The relative abundance of the Algerian mouse, Mus spretus and the Lusitanian pine vole, Microtus lusitanicus was best explained by models built at the broadest regional scale, the former being more abundant in the eastern area, the latter in the western area. The Greater white-toothed shrew, Crocidura russula showed a positive relationship with grassland coverage, whilst the Wood mouse, Apodemus sylvaticus benefited from increasing proportions of fallow lands within the landscape. These two species are then expected to respond positively to those agri-environmental schemes including the increase of fallows and grassy vegetation within the arable landscape (EU recommendations). However, further efforts are needed to predict, at least qualitatively, the response of other small mammal species to the changing farmed landscape. This is especially true for two endemic species occurring at this area: the Cabrera vole, Microtus cabrerae and the Lusitanian pine vole, and for which this kind of information is almost absent.

Oxytocin, vasopressin and pair bonding: implications for autism.

Understanding the neurobiological substrates regulating normal social behaviours may provide valuable insights in human behaviour, including developmental disorders such as autism that are characterized by pervasive deficits in social behaviour. Here, we review the literature which suggests that the neuropeptides oxytocin and vasopressin play critical roles in modulating social behaviours, with a focus on their role in the regulation of social bonding in monogamous rodents. Oxytocin and vasopressin contribute to a wide variety of social behaviours, including social recognition, communication, parental care, territorial aggression and social bonding. The effects of these two neuropeptides are species-specific and depend on species-specific receptor distributions in the brain. Comparative studies in voles with divergent social structures have revealed some of the neural and genetic mechanisms of social-bonding behaviour. Prairie voles are socially monogamous; males and females form long-term pair bonds, establish a nest site and rear their offspring together. In contrast, montane and meadow voles do not form a bond with a mate and only the females take part in rearing the young. Species differences in the density of receptors for oxytocin and vasopressin in ventral forebrain reward circuitry differentially reinforce social-bonding behaviour in the two species. High levels of oxytocin receptor (OTR) in the nucleus accumbens and high levels of vasopressin 1a receptor (V1aR) in the ventral pallidum contribute to monogamous social structure in the prairie vole. While little is known about the genetic factors contributing to species-differences in OTR distribution, the species-specific distribution pattern of the V1aR is determined in part by a species-specific repetitive element, or 'microsatellite', in the 5' regulatory region of the gene encoding V1aR (avpr1a). This microsatellite is highly expanded in the prairie vole (as well as the monogamous pine vole) compared to a very short version in the promiscuous montane and meadow voles. These species differences in microsatellite sequence are sufficient to change gene expression in cell culture. Within the prairie vole species, intraspecific variation in the microsatellite also modulates gene expression in vitro as well as receptor distribution patterns in vivo and influences the probability of social approach and bonding behaviour. Similar genetic variation in the human AVPR1A may contribute to variations in human social behaviour, including extremes outside the normal range of behaviour and those found in autism spectrum disorders. In sum, comparative studies in pair-bonding rodents have revealed neural and genetic mechanisms contributing to social-bonding behaviour. These studies have generated testable hypotheses regarding the motivational systems and underlying molecular neurobiology involved in social engagement and social bond formation that may have important implications for the core social deficits characterizing autism spectrum disorders.

Asymmetry in age suppresses reproduction in female woodland voles, Microtus pinetorum

The partitioning of reproduction in animal societies is a topic of interest to those studying animal behaviour. Under some conditions, two or more females may breed, but lack of reproduction by the younger females occurs frequently. Lack of reproduction by young females may be due to kin asymmetry, dominance asymmetry, or incest avoidance. We conducted breeding experiments to distinguish among these three hypotheses. We show that female reproduction within woodland vole family groups becomes skewed as the asymmetry in age, which is correlated with dominance, between females increases. When daughters were housed with their mothers and a potential mate and the age difference between females was large, we found a high level of skew as compared to females housed with same-age sisters and a potential mate or females housed only with a potential mate. We argue that dominance asymmetry is the best explanation for reproductive skew seen in female woodland voles that have access to unfamiliar, unrelated mates based on reproductive and previous behavioural observations.

Estrogen receptor‐α distribution in male rodents is associated with social organization

It has been hypothesized that site-specific reduction of estrogen receptor-alpha (ERalpha) is associated with the expression of male prosocial behaviors. Specifically, highly social males are predicted to express significantly lower levels of ERalpha than females and less social males in brain regions associated with prosocial behavior including the bed nucleus of the stria terminalis (BST) and the medial amygdala (MeA). This hypothesis was tested by comparing ERalpha immunoreactivity (IR) in three species of microtines, the polygynous montane (Microtus montanus) and meadow (M. pennsylvanicus) voles and the monogamous pine vole (M. pinetorum), and two species of cricetines that differ in the extent of social pair-bond formation, Siberian (Phodopus sungorus) and Djungarian (P. campbelli) hamsters. As predicted, ERalpha-IR was sexually dimorphic in the BST and MeA of the highly social species, with females expressing more ERalpha-IR cells than males. Male and female montane voles did not differ. Male and female meadow voles differed in the ventromedial hypothalamus, with females expressing more ERalpha-IR cells. Male pine voles expressed lower levels of ERalpha-IR in the MeA than male montane and meadow voles and in the BST relative to montane males. Male Djungarian hamsters, which show higher levels of parental care, had fewer ERalpha-IR cells in the BST than male Siberian hamsters. Results indicate that the distribution of ERalpha differs relative to the continuum of species-typical affiliative behavior and supports the hypothesis that ERalpha has a significant role in regulating species-specific social organization.

Perinatal exposure to endocrine disrupting compounds alters behavior and brain in the female pine vole

Endocrine-disrupting chemicals (EDCs) are synthetic chemicals that arise from sources such as pesticides and have the ability to mimic or inhibit gonadal steroid hormones. The objective of this research was to examine the effects of EDCs on the behaviors associated with monogamy and the expression of related neuropeptide receptors. Pine voles, a novel experimental mammal, were chosen because they display strong monogamous pair bonding. Female pine voles were orally administered estrogenic diethylstilbestrol (DES) and methoxychlor (MXC) or oil control throughout gestation and lactation of pups. Exposed pups were tested as adults. Preference for the mate and maternal behaviors were assessed. While the ability to form partner preferences was intact, DES-exposed females showed increased aggression toward a stranger, while MXC exposed females showed a strong trend toward spending more time alone. Oxytocin (OT) receptor binding in the brain was assessed for possible effects on this behaviorally important neuropeptide signaling system. The cingulate cortex showed a reduction in OT binding in the MXC group. These findings demonstrate that exposure to EDCs during pre- and neonatal development can alter female adult neural phenotype and behavior related to monogamous behavior traits.