Water Vole Research Articles

Artificial neural networks enable discrimination of taxa using morphological characters: an example with a problematic small mammal, the water vole (genus Arvicola) (Rodentia, Cricetidae)

The aim of this study is to assess the reliability of different artificial neural networks as tools for identifying taxonomic or ecotypic subdivisions in European water voles (genus Arvicola). Self-organizing maps show that taxa at subspecies or species level are organized along morphological gradients correlated with ecotypes (from extreme forms of fossorial Arvicola terrestris to strictly aquatic Arvicola sapidus). An automatic discrimination process based on a multilayer feed-forward network, working with 17 French and one Spanish reference populations, proved able to correctly identify species in test samples from France, but sometimes misidentified specimens from other countries. Three morpho-ecotypes were identified using a self-organizing map with a single-species dataset (Arvicola terrestris only). However, there were no clues as to how these morpho-ecotypes might correlate with the known phylogenetics of the species. Our model can identify species on the basis of a limited range of cranial measurements which are available from vole skull fragments commonly found in owl pellets. This can have very practical risk-assessment applications as it allows easier identification of the more fossorial Arvicola terrestris populations which are a threat to crops.

American mink control on inland rivers in southern England: An experimental test of a model strategy

Invasive species are an important driver of global biodiversity loss. Under international legislation, the UK has an obligation to eradicate or to control the alien, invasive American mink. Using a large-scale field experiment, we tested the effectiveness of a specified mink removal strategy, identified through earlier modelling work, in reducing the relative abundance of mink. We found that mink removal could be effective in reducing mink populations with four months or less of trapping per year, over only 2–3 years, but that for small sites (c. 20 km) a flexible, reactive approach, coupled with continual monitoring for mink presence is necessary. Survival of reintroduced water voles at four sub-sites within our mink removal sites suggest that the reactive mink removal strategy adopted in this study was sufficient for water vole protection. We discuss the use of an adaptive management approach in local mink management, and consider the wider implications of our results for invasive species control on mainlands.

Spatio‐temporal variation in the strength and mode of selection acting on major histocompatibility complex diversity in water vole (Arvicola terrestris) metapopulations

Patterns of spatio-temporal genetic variation at a class II major histocompatibility complex (MHC) locus and multiple microsatellite loci were analysed within and between three water vole metapopulations in Scotland, UK. Comparisons of MHC and microsatellite spatial genetic differentiation, based on standardised tests between two demographically asynchronous zones within a metapopulation, suggested that spatial MHC variation was affected by balancing selection, directional selection and random genetic drift, but that the relative effects of these microevolutionary forces vary temporally. At the metapopulation level, between-year differentiation for MHC loci was significantly correlated with that of microsatellites, signifying that neutral factors such as migration and drift were primarily responsible for overall temporal genetic change at the metapopulation scale. Between metapopulations, patterns of genetic differentiation implied that, at large spatial scales, MHC variation was primarily affected by directional selection and drift. Levels of MHC heterozygosity in excess of Hardy-Weinberg expectations were consistent with overdominant balancing selection operating on MHC variation within metapopulations. However, this effect was not constant among all samples, indicating temporal variation in the strength of selection relative to other factors. The results highlight the benefit of contrasting variation at MHC with neutral markers to separate the effects of stochastic and deterministic microevolutionary forces, and add to a growing body of evidence showing that the mode and relative strength of selection acting on MHC diversity varies both spatially and temporally.

Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole ( Arvicola terrestris )

The fundamental role of the major histocompatibility complex (MHC) in immune recognition has led to a general consensus that the characteristically high levels of functional polymorphism at MHC genes is maintained by balancing selection operating through host-parasite coevolution. However, the actual mechanism by which selection operates is unclear. Two hypotheses have been proposed: overdominance (or heterozygote superiority) and negative frequency-dependent selection. Evidence for these hypotheses was evaluated by examining MHC-parasite relationships in an island population of water voles (Arvicola terrestris). Generalized linear mixed models were used to examine whether individual variation at an MHC class II DRB locus explained variation in the individual burdens of five different parasites. MHC genotype explained a significant amount of variation in the burden of gamasid mites, fleas (Megabothris walkeri) and nymphs of sheep ticks (Ixodes ricinus). Additionally, MHC heterozygotes were simultaneously co-infected by fewer parasite types than homozygotes. In each case where an MHC-dependent effect on parasite burden was resolved, the heterozygote genotype was associated with fewer parasites, and the heterozygote outperformed each homozygote in two of three cases, suggesting an overall superiority against parasitism for MHC heterozygote genotypes. This is the first demonstration of MHC heterozygote superiority against multiple parasites in a natural population, a mechanism that could help maintain high levels of functional MHC genetic diversity in natural populations.

Experimental translocation of juvenile water voles in a Scottish lowland metapopulation

AbstractPopulation density affects dispersal success because residents can hinder or facilitate immigration into a new site, via a “social fence effect” or “social attraction” (or “conspecific attraction”), respectively. These mechanisms can affect the dynamics of fragmented populations and the success of translocations. However, information on the settlement behaviour of dispersers is rare. We conducted a manipulative field experiment using wild water voles, which exist in metapopulations along waterways in Scotland. We translocated 17 young of dispersal age into either an occupied site or a vacant site containing good habitat, which had recently become extinct due to a feral predator (American mink) moving through. We monitored the movements of translocated voles using radio telemetry. Translocated voles were less likely to settle in occupied sites with higher densities of residents, suggesting a possible social fence effect at high density. There was evidence of a social attraction mechanism, because voles never remained at new sites unless another individual arrived soon after translocation, and they were more likely to settle in occupied or colonised sites than vacant ones. Voles remained in the transient phase of dispersal for many days, and often followed a “stepping stone” trajectory, stopping for several days at successive sites. We suggest that trajectories followed by dispersing water voles, the time scale and long dispersal distances found in this species are conducive to locating conspecifics at low density and colonising vacant habitat. These results are encouraging for prospects of metapopulation persistence and future translocation success.

Serological Evidence of Viruses Naturally Associated with the Montane Water Vole (Arvicola scherman) in Eastern France

We surveyed 12 populations of the montane water vole (Arvicola scherman), previously known as the fossorial form of the water vole A. terrestris, in eastern France for antibodies (immunoglobulin G) to Puumala virus (PUUV), lymphocytic choriomeningitis virus (LCMV), and cowpox virus (CPXV). Antibodies to PUUV were found in 9 (5.5%) of 164 voles from 7 populations, antibodies to LCMV were found in 13 (26.0%) of 50 voles from 2 populations, and antibodies to CPXV were found in 66 (41.8%) of 158 voles from 7 populations. Antibody status to CPXV was statistically associated with the phase of the A. scherman population density cycle and the percentage of grassland areas surrounding the sampling sites.

Effects of habitat quality upon reintroduction success in water voles: Evidence from a replicated experiment

Reintroductions are an important tool in conservation biology but frequently fail. Factors influencing reintroduction ‘success’ are rarely tested experimentally. We examined the relationship between habitat quality and reintroduction success in an experimental reintroduction of populations of water voles ( Arvicola terrestris) in the UK. We released cohorts of 44 water voles into 12 replicate 800 m stretches of river, each supporting a different habitat abundance. Water voles initially established at nine sites, failing to establish at three sites due to predation from American mink (two sites) and atypically severe flooding post-release (one site). For sites where voles established, at those with higher vegetation abundance more of the release cohort survived (initial survival rates range 0.43–0.61), and post-establishment survival rates (range 0.45–0.80) and population densities (range 2.1–5.4 voles per 100 m of habitat) were higher. A further two populations were lost to American mink predation post-establishment. Reintroductions are commonly designated as either a ‘success’ or a ‘failure’. The principal cause of a failed release in our study was insufficient mink control. However, whilst seven of our 12 reintroductions were ‘successful’, our results indicated substantial variation in the population densities and survival rates that the replicate habitats could support. This highlights the need to ensure that any habitat selected for a reintroduction is the best obtainable.

Body condition and reproductive characteristics of female water voles (Arvicola terrestris L.)

The relationship between long-term dynamics of reproductive parameters and body condition were studied in female water voles from a cycling population. Body condition was estimated from the deviation of body weight (excluding the weight of the uterus with embryos) from the theoretically expected weight calculated from the equation of body weight regression with respect to body length. As the index of body condition increases upon transition from decline to peak in the population cycle, the numbers of corpora lutea and live embryos also increase and the risk of resorption of the entire litter becomes lower.

Kinetics of bromadiolone in rodent populations and implications for predators after field control of the water vole, Arvicola terrestris

We document the kinetics of bromadiolone in two rodent populations after a field control of water voles, and their implications for predator exposure. Water voles and common voles were trapped aboveground and underground from 1 to 135 days after bromadiolone treatment in the field. Livers, digestive tracts, and rests of the body were analyzed separately. Our results indicate that 99.6% of the water voles trapped underground and 41% of the common voles trapped aboveground contain bromadiolone residues. Concentrations were maximal between 3.3 and 6.5 days after treatment, according to the tissues examined and the model applied for water voles, and after 1.3 to 3.7 days for common voles. Water voles appeared available almost exclusively for foraging predators. Common voles, found less likely to be poisoned and exhibiting weaker concentrations, were mainly sampled aboveground. The liver, primarily eaten by some predators and scavengers, contains a larger bromadiolone quantity (59% of the total amount found in water voles). The rejection of the digestive tract by those species may lead to a subsequent consumption of voles with higher bromadiolone concentrations (from + 3.8 to + 5.8% of concentration) and provide a moderate risk increase. After 135 days, eight of the ten water voles and one of the two common voles exhibited detectable residues. Additionally, one specimen presented higher concentrations than the others, and similar to those measured in Voles trapped between the first 15–20 days. This may have consequences on predator intoxications several months after treatment. These results integrate individual differences for the two main rodent species present in treated areas. Implications for predator exposure were investigated at the end of the study and suggest that, if the risk of secondary poisoning is maximal during the first 15–20 days when the rodent densities remain high, exposure conditions are maintained for at least 135 days.

Effects of forage availability on growth and maturation rates in water voles

1. In populations of small mammals, food supplementation typically results in higher population densities, body weights, growth rates and reproductive rates. However, few studies have demonstrated a relationship between forage levels and demographic rates in wild populations in the absence of supplementation. 2. We examined the association of levels of available forage with individual growth rates and time to sexual maturity in eight re-introduced and three naturally occurring populations of water voles (Arvicola terrestris). 3. Range sizes were smaller at sites with higher population densities. Mean forage availability and individual growth rates covaried with range size at each site. 4. The weight at which water voles became sexually mature was 112 g for females and 115 g for males and did not vary between study sites. Differences in growth rates therefore translated into differences in the time taken to reach maturity between sites. 5. In the re-introduced populations, mean days to maturity varied inversely with mean range length. Females took 7 days (18%, range 40-47 days) longer and males 5 days (13%, range 40-45 days) longer to reach breeding condition at the sites with the shortest mean range lengths. 6. Evidence from this study suggests a possible mechanism by which increased population densities may reduce maturation rates in water voles through a reduction in mean range size, thereby limiting the availability of forage to each individual.

Multiple parasites mediate balancing selection at two MHC class II genes in the fossorial water vole: insights from multivariate analyses and population genetics

We investigated the factors mediating selection acting on two MHC class II genes (DQA and DRB) in water vole (Arvicola scherman) natural populations in the French Jura Mountains. Population genetics showed significant homogeneity in allelic frequencies at the DQA1 locus as opposed to neutral markers (nine microsatellites), indicating balancing selection acting on this gene. Moreover, almost exhaustive screening for parasites, including gastrointestinal helminths, brain coccidia and antibodies against viruses responsible for zoonoses, was carried out. We applied a co-inertia approach to the genetic and parasitological data sets to avoid statistical problems related to multiple testing. Two alleles, Arte-DRB-11 and Arte-DRB-15, displayed antagonistic associations with the nematode Trichuris arvicolae, revealing the potential parasite-mediated selection acting on DRB locus. Selection mechanisms acting on the two MHC class II genes thus appeared different. Moreover, overdominance as balancing selection mechanism was showed highly unlikely in this system.

Ecological and biological factors involved in the transmission ofEchinococcus multilocularisin the French Ardennes

In order to identify the respective importance of the ecological and biological factors involved in the transmission of Echinococcus multilocularis, we estimated grassland vole intermediate host (Microtus sp. and Arvicola terrestris) population densities, in relation to the diet of the definitive host (red fox, Vulpes vulpes) and with the prevalence of E. multilocularis in the fox population. The study was conducted in the Ardennes, north-eastern France, which is an area with a high incidence of alveolar echinococcosis. Surface index methods showed that Microtus was the most abundant intermediate host in the area. Furthermore, Microtus was present in one-third of the 144 faeces and 98 stomach content samples examined and represented more than two-thirds of the rodent occurrences. Red fox predation on Microtus was significantly correlated with Microtus relative abundance. In contrast, the relative abundance of A. terrestris was very low. This species, as well as Clethrionomys glareolus and Apodemus sp., was little consumed. E. multilocularis prevalence in foxes was determined from carcasses and reached 53% (95% confidence interval 45-61%). Intensity of infection varied from 2 to 73,380 worms per fox, with 72% of the sampled worm burden harboured by 8% of the sampled foxes. The selected explanatory variables (sex, year, age class, health and nutritional condition, and season) failed to predict prevalence rate and worm burden. The high prevalence rate in foxes indicates the possibility of intense E. multilocularis transmission, apart from periods, or in landscapes, favourable to large population outbreaks of grassland rodents.

Niche separation between the weasel Mustela nivalis and the stoat M. erminea in Belarus

We investigated three main niche components (diet composition, habitat use and diel activity rhythms) to examine how the weasel Mustela nivalis and the stoat M. erminea, both specialised predators of small rodents, could permanently coexist in Belarus. Our research was carried out in temperate forests of Belarus, in two study areas with different environmental conditions: 1) continuous dry-land forest interspersed by a variety of swampy biotopes and aquatic ecosystems (Paazerre, northern Belarus) and 2) extended wetland with large forest patches (Palesse, southern Belarus). The habitat use and diel activity rhythms of seven weasels and eight stoats were analysed by radio-tracking over about 300 km2 in Paazerre. Snow-tracking was also applied to study habitat use by the two mustelid species. Diet composition was examined by analysing 365 weasel scats and 606 stoat scats. Our results suggest that while the weasel and stoat occur in close proximity to each other, they use different micro-habitats, are most active during different times of the day, and prey primarily on different small rodent species. Most weasels selected forest and forest edge habitats, where they predominantly preyed on smaller rodent species (bank voles Clethrionomys glareolus and Apodemus mice); stoats selected wetlands, especially open grassy marshes, and preyed more frequently on larger rodents such as water voles Arvicola terrestris and Microtus voles. Weasels were mostly diurnal and adjusted their activity to the seasonally changing length of daylight, whereas stoats were much more active in twilight and during the night.

ACUTE POISONING OF RED KITES (MILVUS MILVUS) IN FRANCE: DATA FROM THE SAGIR NETWORK

Red Kites (Milvus milvus) are avian scavengers limited to Europe, and they currently are listed as an endangered species worldwide. Accidental poisoning is often listed as one of the threats to Red Kites throughout their range of distribution. The purpose of this article is to investigate the suspected poisoning cases reported to the French Wildlife Disease Surveillance System. Dead animals are submitted to a local veterinary laboratory for necropsy and when poisoning is suspected, samples are submitted to the Toxicology Laboratory of the College of Veterinary Medicine, Lyon, France. Over the period 1992-2002, 62 Red Kites suspected of poisoning were submitted, and poisoning was the confirmed cause of death for greater than 80% of these cases. The major toxicants found were cholinesterase inhibitors (carbamates and organophosphate insecticides) and anticoagulant compounds. The circumstances of exposure include secondary poisoning after the use of anticoagulants over vast areas to control water vole (Arvicola terrestric) populations, but they also include malicious poisoning with carbamates (aldicarb and cabofuran) in meat baits. Cases of poisoning vary throughout France, with observed mortality rates ranging between 0.1/100 hundred breeding pairs/10 yr and four cases/100 hundred breeding pairs/10 yr. Additional cases of poisoning likely go undetected, and our results suggest that acute poisoning is not uncommon in Red Kites and that it should be considered in the current restoration plans.

Neighbourhood landscape effect on population kinetics of the fossorial water vole (Arvicola terrestris scherman)

This paper addresses the issue of whether landscape structure affects A. terrestris population kinetics on a neighbourhood spatial scale, and if so, at what spatial scale is that effect at its maximum. We investigated how the growth of A. terrestris populations is influenced by the landscape context of parcels used for hay production in the French Jura Mountains. Five landscape metrics (relative area of grassland, mean patch area of grassland, patch density of grassland, woodland patch density in grassland, grassland-woodland edge density) were computed over an increasing radius around each parcel (max. 3 km). Redundancy analysis showed that the extent, rate and early onset of A. terrestris population growth were favoured in open grassland areas. Landscape effects on A. terrestris populations as determined by the five metrics are scale-dependent: mean patch area of grassland, patch density of grassland and woodland patch density in grassland had an impact on a grassland parcel within a neighbourhood radius of about 800 m, while relative area of grassland and grassland-woodland edge density had an impact within a neighbourhood radius of about 400 m. Those findings corroborate earlier hypotheses about a multifactorial regulation of A. terrestris populations and a spatial hierarchy of regulating factors. They have potential implications in terms of landscape management and small mammal pest control.

Micromammals (rodents and insectivores) from the early Late Pleistocene cave site of Bois Roche (Charente, France): Systematics and paleoclimatology

We present the study of rodents and insectivores from the 1995 season of excavation at the early Late Pleistocene site of Bois Roche (Charente, France). The site is a small cave with a low ceiling, used as a den by hyenas. It contains a large herbivore assemblage (mainly bovids and equids) with a smaller representation of medium-size taxa (cervids), many microvertebrates, abundant coprolites and deciduous hyena teeth, and a few lithic artifacts (Middle Paleolithic) introduced into the cave by gravity and slope wash. The rodent fauna consists of Eliomys quercinus cf. quercinus, Apodemus sp., Microtus gregalis, Microtus oeconomus, Arvicola terrestris and Dicrostonyx torquatus. Insectivores are represented by Neomys cf. fodiens. The most common species is M. gregalis which forms 93.7% of the total MNI. The micromammal fauna suggests an open landscape, with some vegetation mainly of the steppe or tundra type, with areas of water and more wet vegetation and some areas with trees. The micromammal association of Bois Roche is characteristic of a cold or very cold dry climate.

Effect of mother’s physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole Arvicola terrestris

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother's physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother's body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother's nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother's physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother's body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.

Echinococcus multilocularis in Belgium: Prevalence in red foxes ( Vulpes vulpes) and in different species of potential intermediate hosts

Echinococcus multilocularis causes a rare but potentially lethal zoonotic infection in humans. This tapeworm is known to be endemic in foxes in several countries of Western and Central Europe. In Western Europe, the common vole ( Microtus arvalis) and the water vole ( Arvicola terrestris) are considered to be the most important intermediate host species of this cestode whereas the red fox is by far the most important final host. The purpose of this study was to provide data on the prevalences in Wallonia (Southern part of Belgium) both in the red fox and in different potential intermediate hosts. A total of 990 red foxes were examined between January 2003 and December 2004 for the presence of E. multilocularis. The average prevalence was 24.55% (22.38–27.87). Out of 1249 rodents or insectivores belonging to the species Apodemus sylvaticus, Arvicola terrestris, Clethrionomys glareolus, Microtus arvalis, Microtus agrestris and Sorex araneus, only one M. arvalis (out of 914–0.11% (0.003–0.61) and one C. glareolus (out of 23–4.3% (0.1–21.9) were found to be infected. However, the muskrat ( Ondatra zibethicus) seems to be a good intermediate host as 11.18% (9.72–12.76) of the animals ( n = 1718) were found to be infected. A positive correlation was found between the prevalences in foxes and in muskrats in each of the different geological regions. This study indicates that the muskrat is highly sensitive to this zoonotic tapeworm and could perhaps represent a good bioindicator when studying the epidemiology of this parasitic infection in Belgium and in other countries where the muskrat is present.

Reappraisal of ‘chronospecies’ and the use of Arvicola (Rodentia, Mammalia) for biochronology

The water vole, genus Arvicola, is characterised by a broad geographic distribution throughout Europe and is widespread during the late Middle and Upper Pleistocene. This genus is used as a major biostratigraphic tool within the Quaternary. Specific determinations using the Schmelzband-Differenzierung-Quotient or SDQ have identified many chronospecies within the fossil species Arvicola cantiana (Hinton, 1910). As SDQ calculation remains limited, this study reappraises the Arvicola genus in terms of morphodiversity and morphospace using outline analysis which takes into account the tooth as a whole. Outline analysis suggests that one single species of Arvicola, A. cantiana, was present during the Pleistocene. This species shows great variability with no trends or patterns in morphospace. Thus, these results call into question the reliability of SDQ for specific determinations and throw doubt on the biochronological framework based on Arvicola.

What limits male range sizes at different population densities? Evidence from three populations of water voles

AbstractIn many mammalian species, females compete with each other for food and space to raise offspring, while males compete with each other for access to females. Few studies have examined the factors which limit male range sizes or the degree of overlap between male ranges. We deduced four possible responses of the range ‐sizes of non‐territorial male small mammals to increasing population density and/or levels of forage abundance. These were: (1) male range sizes might remain the same irrespective of population density; (2) at high population densities males may become territorial, and their ranges small and non‐overlapping; (3) at high forage abundance/population densities, males' ranges may become smaller but remain intra‐sexually overlapping; (4) at high forage abundance, male range sizes may increase. We examined the relationship between population density, range lengths and range overlaps and body weights of both sexes in a comparative study of three populations of water voles Arvicola terrestris. Male range sizes were smaller at higher population densities, but their ranges remained both inter‐ and intra‐sexually overlapping. Heavier males had larger ranges than did lighter males at all sites. These results comply with what would be expected if male range sizes were at least partially restricted by the number of ranges of other individuals with which they overlapped. Although we could not discount the hypothesis that forage abundance may also have had a direct effect on male range sizes, our results implied that male range sizes were at least partially determined by social factors.