Wood Mice Apodemus Sylvaticus Research Articles

Predation of wood mice (Apodemus sylvaticus) on hibernating bats

AbstractBat hibernacula with high numbers of bats can become high‐risk areas, as they attract flying and non‐flying predators. In order to protect hibernating bats effectively, more knowledge about mortality factors is needed. During the winters of 2003–2015, we found 214 dead bats in 12 hibernacula in The Netherlands province of Zuid‐Holland. Most bat remains were found in December and January, with a second peak in April. Their remains showed a typical pattern of lesions consistent with those caused by predation by the wood mouse (Apodemus sylvaticus). Trail camera surveys showed that wood mice actively searched for bats. Predation pressure seemed to vary between winters, with a peak in the winters of 2004, 2011 and 2015. The annual mortality (relative to the maximum winter population size) caused by wood mouse predation varied between 0.1 and 8.8 %, with a maximum local effect of 83.6 %. The years with high wood mouse predation pressure were characterized by a long frost period and a low mast production of common oak in the preceding autumn. The size of a hibernaculum and the population density of its bats had an effect on predation‐dependent mortality. The highest predation risk occurred near the entrance of bunkers. From these results we tentatively conclude that predation is not incidental and that wood mice actively search for and kill hibernating bats or scavenge for weakened individuals.

Response of small mammals to variable agricultural landscapes in Central Europe

The Central European agricultural landscape has undergone a number of changes over recent decades, with overall field area decreasing and adjacent habitats increasing. Here, we document changes in small mammal communities associated with crop fields and adjacent fallow land in a highly agriculture landscape of the Czech Republic.The most numerous species overall were wood mice (Apodemus sylvaticus) and common voles (Microtus arvalis). Highest diversity, species richness and abundance were observed in fallow habitats and in crops providing long-term vegetation cover. Community composition and abundance were dependent on crop and season. Mice used all habitats depending on instantaneous vegetation stage, though some habitats only for a short period during seeding or harvest. Common voles reached highest densities in habitats providing a stable food supply. Mice and voles both preferred perennial “non-crop” plots during winter as they provided a diverse food supply and undisturbed nesting opportunities.Overall, fallow habitats supported the most abundant, diverse and stable small mammal communities and, as such, they have high biodiversity value.

A novel approach to field identification of cryptic Apodemus wood mice: calls differ more than morphology

AbstractField identification of European wood mice Apodemus spp. is challenging due to their morphological resemblance and frequent sympatry. We developed discriminant functions based on body mass and acoustic variables of distress calls to identify three cryptic species of wood mice (Apodemus alpicola, Apodemus flavicollis and Apodemus sylvaticus) in Italy. We achieved an overall correct classification rate of 86–98%; the best results (100% correct classification) were obtained for Apodemus sylvaticus calls. This minimally invasive, effective and low‐cost method highlights the potential role of bioacoustics as a powerful tool for field discrimination of cryptic species of terrestrial mammals.

Reduced helminth parasitism in the introduced bank vole (Myodes glareolus): More parasites lost than gained.

Introduced species are often less parasitised compared to their native counterparts and to ecologically similar hosts in the new environment. Reduced parasitism may come about due to both the loss of original parasites and low acquisition of novel parasites. In this study we investigated the intestinal helminth parasites of the introduced bank vole (Myodes glareolus) in Ireland. Results were compared to data from other European studies and to the intestinal helminth fauna of an ecologically similar native rodent in Ireland, the wood mouse (Apodemus sylvaticus). The helminth fauna of introduced bank voles exhibited low diversity with only 3 species recovered: Aspiculuris tianjinensis; Aonchotheca murissylvatici and Taenia martis larvae. In particular, no adult parasites with indirect life-cycles were found in bank voles suggesting that indirectly transmitted parasites are less likely to establish in invasive hosts. Also, the results of this study add support to the enemy release hypothesis.

Coxiella burnetii Genotypes in Iberian Wildlife.

To investigate if Coxiella burnetii, the causative agent of Q fever, genotypes circulating in wildlife are associated with those infecting livestock and humans, multiple-locus variable number tandem-repeat analysis (MLVA-6-marker) was carried out over C. burnetii obtained from red deer (Cervus elaphus), Eurasian wild boar (Sus scrofa), European wild rabbit (Oryctolagus cuniculus), black rat (Rattus rattus), and wood mouse (Apodemus sylvaticus). MLVA typing was performed by using six variable loci in C. burnetii: Ms23, Ms24, Ms27, Ms28, Ms33, and Ms34. The C. burnetii cooperative database from MLVABank 5.0 was employed to compare genotypes found in this study with 344 isolates of diverse origin. Twenty-two genotypes from wildlife and two genotypes from domestic goats were identified. Some MLVA genotypes identified in wildlife or in farmed game clustered with genotypes of human Q fever clinical cases, supporting the idea that humans and wildlife share C. burnetii genotypes. The major part of genotypes identified in coexisting red deer and rabbits clustered according to their host of origin, suggesting host specificity for particular C. burnetii genotypes. These findings provide important insights to understand the epidemiology of C. burnetii at the wildlife-livestock-human interface.

Rodent food quality and its relation to crops and other environmental and population parameters in an agricultural landscape

The diet, its quality and quantity considerably influence population parameters of rodents. In this study, we used NIRS methods for estimation of nitrogen content in stomachs of rodent populations. The study was carried out in diverse arable landscape in South Moravia, Czech Republic. Rodents were sampled in cultural crops (alfalfa, barley, wheat, sunflower, maize and rape) as well as in fallow habitats (herbal set-aside and old orchard). Influence of habitat, date, year, individual parameters (body length, sex, breeding and age), and relative abundance on quality of consumed food was studied. Under conditions of higher population density, dominant species [wood mouse (Apodemus sylvaticus) and common vole (Microtus arvalis)] consumed food richer in nitrogen. Also the strong effect of crop and date (season) was found in both species. There was no significant effect of the other parameters studied on food quality (N-content).

Predicting forest management effects on oak–rodent mutualisms

Wood mice Apodemus sylvaticus are the main dispersers of acorns in highly managed Mediterranean holm‐oak woodlands. Mice mobilize and cache acorns to store them for winter consumption. They carry acorns away from potential competitors, face predation risks during mobilization, and cache acorns in areas where pilfering risks are low. However, mice can act either as net predators or as moderately efficient dispersers, depending on the way landscape management affects intraspecific competition for acorns and shelter availability. To assess the influence of landscape structure and mouse behavior on acorn dispersal, we developed an agent‐based model (ABM) that translates forest management into changes in key environmental factors driving mouse foraging decisions.The model was able to predict accurately acorn dispersal patterns in a wide range of forest management practices based on information on forest habitat availability, stem density and shrub cover. Sensitivity analysis revealed that caching rates emerged from the interplay between intraspecific competition for seeds and predation risk accepted during mobilization. It also showed that intraspecific competition for acorns decreased with increasing habitat loss (due to positive edge effects on acorn production) while landscape resistance to mouse movements increased. As a result, the net benefits of caching declined and acorn predation became the dominant strategy. Finally, we assessed the effects of shrub encroachment as a management practice to enhance dispersal services in savanna‐like landscapes (dehesas). The model predicted non‐linear responses with a 65% threshold of shrub cover needed to achieve relatively high levels of acorn dispersal. This value may not be compatible with the traditional exploitation of dehesas (livestock rearing). Our study shows that integrated approaches that combine environmental change driven by management with behavioral responses of dispersers improve our understanding of the causes of recruitment bottlenecks, and are useful tools for evaluating conservation strategies aimed at enhancing dispersal services.

Disentangle the Causes of the Road Barrier Effect in Small Mammals through Genetic Patterns.

Road barrier effect is among the foremost negative impacts of roads on wildlife. Knowledge of the factors responsible for the road barrier effect is crucial to understand and predict species’ responses to roads, and to improve mitigation measures in the context of management and conservation. We built a set of hypothesis aiming to infer the most probable cause of road barrier effect (traffic effect or road surface avoidance), while controlling for the potentially confounding effects road width, traffic volume and road age. The wood mouse Apodemus sylvaticus was used as a model species of small and forest-dwelling mammals, which are more likely to be affected by gaps in cover such as those resulting from road construction. We confront genetic patterns from opposite and same roadsides from samples of three highways and used computer simulations to infer migration rates between opposite roadsides. Genetic patterns from 302 samples (ca. 100 per highway) suggest that the highway barrier effect for wood mouse is due to road surface avoidance. However, from the simulations we estimated a migration rate of about 5% between opposite roadsides, indicating that some limited gene flow across highways does occur. To reduce highway impact on population genetic diversity and structure, possible mitigation measures could include retrofitting of culverts and underpasses to increase their attractiveness and facilitate their use by wood mice and other species, and setting aside roadside strips without vegetation removal to facilitate establishment and dispersal of small mammals.

Differences in the ectoparasite fauna between micromammals captured in natural and adjacent residential areas are better explained by sex and season than by type of habitat

We compared the ectoparasite fauna in 608 micromammals (chiefly 472 wood mice Apodemus sylvaticus, 63 Algerian mice Mus spretus, and 51 greater white-toothed shrews Crocidura russula) captured in natural and adjacent residential areas in spring and autumn during three consecutive years in four areas in periurban Barcelona (NE Spain). We found little support for an association of urbanization with differences in infestation by ectoparasites. Prevalence of Rhipicephalus sp. tick in wood mice and shrews was significantly higher in residential than in natural habitats, and the opposite was found for the flea Ctenophtalmus andorrensis catalanensis in shrews. Marked differences in the prevalence of the flea Leptopsylla taschenbergi amitina in wood mice between seasons were observed in natural but not in residential habitats, probably due to enhanced flea survival probabilities in the latter. However, as a rule, males were more frequently and heavily infested than females, and the prevalence was higher in autumn than in spring. Our results suggest that the ectoparasite fauna of periurban micromammals is shaped more by other factors than by habitat modification. People living in residential areas are at risk of contact with the arthropods borne by non-commensal micromammals and the pathogens transmitted by them.

The effects of a sudden urbanization on micromammal communities: a case study of post-earthquake L’Aquila (Abruzzi Region, Italy)

The earthquake that occurred in L’Aquila (Abruzzi Region, Italy) on 6 April 2009 caused the destruction of many buildings and the deaths of 309 people. In summer 2009, new settlements were built in rural areas near L’Aquila to host part of the population whose houses were uninhabitable or had been totally destroyed. Our study is focused on the impact of these “new towns”, analyzing the variation of the micromammal community, from 2002 to 2013, through a barn owl pellet analysis. The study area is a 3-km buffer plot sited in the northwest of L’Aquila and affected by the so-called Progetto CASE (“Complessi Antisismici Sostenibili ed Ecocompatibili”) and Progetto MAP (“Moduli Abitativi Provvisori”). This analysis shows how the micromammal community has changed, qualitatively and quantitatively, because of the improvised and inadequately planned earthquake urbanization. For example, more sensitive species, such as wood mouse (Apodemus sylvaticus) and Savi’s pine vole (Microtus savii), both abundant before the earthquake, were replaced by the more anthropophilous house mouse (Mus domesticus) after the construction of the new settlements.

Effect of landscape features on the relationship between Ixodes ricinus ticks and their small mammal hosts.

BackgroundThe consequences of land use changes are among the most cited causes of emerging infectious diseases because they can modify the ecology and transmission of pathogens. This is particularly true for vector-borne diseases which depend on abiotic (e.g. climate) and biotic conditions (i.e. hosts and vectors). In this study, we investigated how landscape features affect the abundances of small mammals and Ixodes ricinus ticks, and how they influence their relationship.MethodsFrom 2012 to 2014, small mammals and questing I. ricinus ticks were sampled in spring and autumn in 24 sites located in agricultural and forest landscapes in Brittany, France. We tested the effects of landscape features (composition and configuration) on the abundances of small mammal species and immature ticks and their relationship. Additionally, we quantified the larval tick burden of small mammals in 2012 to better describe this relationship.ResultsThe nymph abundance was positively influenced by the larval occurrence and the wood mouse Apodemus sylvaticus abundance the previous spring because they hosted tenfold more larvae than the bank vole Myodes glareolus. The bank vole abundance in spring and autumn had a negative and positive effect, respectively, on the nymph abundance. In agricultural landscapes, wood mice were positively influenced by woodland cover and woodland/hedgerow-grassland ecotone, whereas bank voles showed the opposite or non-significant responses to these landscape variables. The woodland cover had a positive effect on immature ticks.ConclusionThe landscape configuration, likely by affecting the landscape connectivity, influences the small mammal communities in permanent habitats. Our study showed that the wood mouse, due to its dominance and to its tolerance to ticks, feeds a substantial proportion of larvae. The acquired resistance to ticks in the bank vole can reduce its role as a trophic resource over time. The nymph abundance seems indirectly influenced by landscape features via their effects on the small mammal community. To enhance our understanding of the epidemiology of tick-borne diseases within landscapes, further studies will integrate data on pathogen prevalence and investigate explicitly the effect of landscape connectivity on host-vector-pathogen systems.

Negative effect of the wild boar (Sus scrofa) on the population size of the wood mouse (Apodemus sylvaticus) in forest habitats of Sardinia

AbstractThe various activities of the wild boar (

Francisella species in ticks and animals, Iberian Peninsula

The presence of Francisella species in 2134 ticks, 93 lagomorphs and 280 small mammals from the Iberian Peninsula was studied. Overall, 19 ticks and 6 lagomorphs were positive for Francisella tularensis subsp. holarctica, suggesting, as described for other regions, that lagomorphs may have an important role in the maintenance of F. tularensis in nature. Of the 6 positive lagomorphs, 4 were identified as the European rabbit, Oryctogalus cuniculus. Additionally, 353 ticks and 3 small mammals were PCR positive for Francisella-like endosymbionts (FLEs) and one small mammal was also positive for Francisella hispaniensis-like DNA sequences. Among FLE positive specimens, a variety of sequence types were detected: ticks were associated with 5 lpnA sequence types, with only one type identified per tick, in contrast to 2 lpnA sequence types detected in a single wood mouse (Apodemus sylvaticus). To our knowledge, this is the first report of FLEs in free-living small mammals as well as the first detection of F. hispaniensis-like sequences in a natural setting.

Field identification of Apodemus flavicollis and Apodemus sylvaticus: a quantitative comparison of different biometric measurements

AbstractThe identification of the wood mouse

Further investigation of risk elements content in the bones of wild rodents from a polluted area in Slovakia.

BackgroundWild rodents are suitable for monitoring environmental pollution and exposure risk assessment for people living in contaminated areas. The content of selected risk elements in the femora of bank vole (Myodes glareolus), yellow-necked mouse (Apodemus flavicollis) and wood mouse (Apodemus sylvaticus) was estimated from the Kolíňany area of Slovakia, which is characterized by a high degree of environmental pollution. The rodents were trapped in February 2011 using standard theriological methods. All animals (n = 32) were adult males in good physical condition. The concentrations of Fe, Cu, Zn and Ni in their bones were determined by atomic absorption spectrophotometry.ResultsThe highest concentrations of Fe and Cu were detected in the bones of yellow-necked mouse. Significant differences were observed for the content of Fe between A. flavicollis and M. glareolus (P < 0.05). The highest levels of Zn and Ni were found in the femora of wood mouse; however, significant differences were not detected between the rodents. Moreover, the concentrations of Cu, Zn and Ni were significantly higher in the bones of all three species (P < 0.05) in comparison with the values obtained in the same animal species at the same site in February 2007.ConclusionsOur results demonstrate an increased accumulation of Cu, Zn and Ni in the femora of M. glareolus, A. flavicollis and A. sylvaticus from the Kolíňany area and thus indicate towards ongoing contamination of this locality.

Survey of Wild and Domestic Mammals for Infection with Leishmania infantum following an Outbreak of Desert Zoonotic Visceral Leishmaniasis in Jiashi, People's Republic of China.

In 2008 and 2009, an outbreak of desert-subtype zoonotic visceral leishmaniasis occurred in Jiashi county, Xinjiang, China. So far, no animal reservoir has been identified for this type of visceral leishmaniasis. Therefore, we surveyed the most common mammals (wild and domestic) for Leishmania infections during the outbreak in 2008 and 2009 in order to identify the source of the visceral leishmaniasis in this region. Spleen, liver, bone marrow and blood samples collected from 86 wood mice (Apodemus sylvaticus), 61midday jirds (Meriones meridianus) and 27 Yarkand hares (Lepus yarkandensis) were tested for the presence of Leishmania by microscopy, culture and PCR. All of the animals were found to be negative for Leishmania infections; On the other hand, Leishmania DNA was detected in blood samples collected from livestock reared in the outbreak area: 30.36% (17/56) of sheep, 21.57% (11/51) of goats, 17.78% (8/45) of cattle, and 21.62 (8/37) of donkeys were positive for Leishmania DNA by PCR. The amplified kDNA sequences from the livestock samples matched Leishmania DNA sequences isolated from patients with visceral leishmaniasis in the study area. We suggest that these domestic mammals are a possible reservoir host for Leishmania infantum in the outbreak area.

Behavioural and physiological responses of wood mice (Apodemus sylvaticus) to experimental manipulations of predation and starvation risk

Body weight and the levels of stored body fat have fitness consequences. Greater levels of fat may provide protection against catastrophic failures in the food supply, but they may also increase the risk of predation. Animals may therefore regulate their fatness according to their perceived risks of predation and starvation: the starvation–predation trade-off model. We tested the predictions of this model in wood mice (Apodemus sylvaticus) by experimentally manipulating predation risk and starvation risk. We predicted that under increased predation risk individuals would lose weight and under increased starvation risk they would gain it. We simulated increased predation risk by playing the calls made by predatory birds (owls: Tyto alba and Bubo bubo) to the mice. Control groups included exposure to calls of a non-predatory bird (blackbird: Turdus merula) or silence. Mice exposed to owl calls at night lost weight relative to the silence group, mediated via reduced food intake, but exposure to owl calls in the day had no significant effect. Exposure to blackbird calls at night also resulted in weight loss, but blackbird calls in the day had no effect. Mice seemed to have a generalised response to bird calls at night irrespective of their actual source. This could be because in the wild any bird calling at night will be a predation risk, and any bird calling in the day would not be, because at that time the mice would normally be resting, and hence not exposed to avian predators. Consequently, mice have not evolved to distinguish different types of call but only to respond to the time of day that they occur. Mice exposed to stochastic 24h starvation events altered their behaviour (reduced activity) during the refeeding days that followed the deprivation periods to regain the lost mass. However, they only marginally elevated their food intake and consequently had reduced body weight/fat storage compared to that of the control unstarved group. This response may have been constrained by physiological factors (alimentary tract absorption capacity) or behavioural factors (perceived risk of predation). Overall the responses of the mice appeared to provide limited support for the starvation–predation trade-off model, and suggest that wood mice are much more sensitive to predation risk than they are to starvation risk.

Craniometric data of Apodemus sylvaticus in Slovakia

AbstractA craniometric analysis of skulls of the wood mouse (Apodemus sylvaticus) from three different parts of Slovakia (north-western, northern and south-eastern) was conducted. Twenty-nine skull and dental variables were measured and evaluated on a sample of 56 adult individuals. The overlap of the values of the measured traits was high. Moreover, the differences among the populations were different for each trait. The non-parametric Kruskal-Wallis test and Discriminant function analysis showed variations in the cranial variables among the different parts of country. We have identified six morphometric variables suitable for the differentiation of populations on the basis of discriminant analysis. Significant differences were confirmed in the characteristics between the analyzed regions; thus, we can speak about small-scale craniometric differentiation. In addition, the results could indicate the influence of altitude, even over a shorter geographic distance between 48-49º N. Moreover, restriction of genetic interaction between the populations may in the future lead to even greater differences between the populations in Slovakia.

Gammaherpesvirus infection modulates the temporal and spatial expression of SCGB1A1 (CCSP) and BPIFA1 (SPLUNC1) in the respiratory tract

Murine γ-herpesvirus 68 (MHV-68) infection of Mus musculus-derived strains of mice is an established model of γ-herpesvirus infection. We have previously developed an alternative system using a natural host, the wood mouse (Apodemus sylvaticus), and shown that the MHV-68 M3 chemokine-binding protein contributes significantly to MHV-68 pathogenesis. Here we demonstrate in A. sylvaticus using high-density micro-arrays that M3 influences the expression of genes involved in the host response including Scgb1a1 and Bpifa1 that encode potential innate defense proteins secreted into the respiratory tract. Further analysis of MHV-68-infected animals showed that the levels of both protein and RNA for SCGB1A1 and BPIFA1 were decreased at day 7 post infection (p.i.) but increased at day 14 p.i. as compared with M3-deficient and mock-infected animals. The modulation of expression was most pronounced in bronchioles but was also present in the bronchi and trachea. Double staining using RNA in situ hybridization and immunohistology demonstrated that much of the BPIFA1 expression occurs in club cells along with SCGB1A1 and that BPIFA1 is stored within granules in these cells. The increase in SCGB1A1 and BPIFA1 expression at day 14 p.i. was associated with the differentiation of club cells into mucus-secreting cells. Our data highlight the role of club cells and the potential of SCGB1A1 and BPIFA1 as innate defense mediators during respiratory virus infection.

Marked seasonal variation in the wild mouse gut microbiota.

Recent studies have provided an unprecedented view of the microbial communities colonizing captive mice; yet the host and environmental factors that shape the rodent gut microbiota in their natural habitat remain largely unexplored. Here, we present results from a 2-year 16 S ribosomal RNA gene sequencing-based survey of wild wood mice (Apodemus sylvaticus) in two nearby woodlands. Similar to other mammals, wild mice were colonized by 10 bacterial phyla and dominated by the Firmicutes, Bacteroidetes and Proteobacteria. Within the Firmicutes, the Lactobacillus genus was most abundant. Putative bacterial pathogens were widespread and often abundant members of the wild mouse gut microbiota. Among a suite of extrinsic (environmental) and intrinsic (host-related) factors examined, seasonal changes dominated in driving qualitative and quantitative differences in the gut microbiota. In both years examined, we observed a strong seasonal shift in gut microbial community structure, potentially due to the transition from an insect- to a seed-based diet. This involved decreased levels of Lactobacillus, and increased levels of Alistipes (Bacteroidetes phylum) and Helicobacter. We also detected more subtle but statistically significant associations between the gut microbiota and biogeography, sex, reproductive status and co-colonization with enteric nematodes. These results suggest that environmental factors have a major role in shaping temporal variations in microbial community structure within natural populations.