Wheat or barley?: Feeding preferences affect distribution of three rodent species in agricultural landscape

Spatial distribution of voles and mice and their abundances in agricultural landscape are largely influenced by their food preferences and the distribution of preferred crops. Here we examined the correspondence between food preferences of dominant rodent species (two mice and one vole) for two cereals (wheat and barley) estimated in the lab and the long-term field abundances observed at the harvest time in southern Moravia, Czech Republic. In the first laboratory trial, harvested culms of wheat and barley were offered. The pygmy field mouse preferred (100%) the seed head of wheat, also the wood mouse (87%) and common vole (60%) showed low preference for wheat. In the second trial, we observed similar preferences in consuming the offered grains of both cereals, the wheat being preferred by the pygmy field mouse, and the wood mouse, while with the common vole showing no preference. Laboratory analysis of the harvested grains indicated a lower fibre content in wheat compared with barley. In the field, rodent abundances in wheat were higher than those in barley, especially in mice. This suggests that food preferences in the laboratory correspond closely to field distribution of these rodents and their abundances. Therefore, studying diet preferences may be of essential in predicting small rodent abundances in changing agricultural landscape.     

Evidence for different bottom-up mechanisms in wood mouse ( Apodemus sylvaticus ) and bank vole ( Myodes glareolus ) population fluctuations in Southern Norway

Animals that feed on forest tree seeds, such as Apodemus mice, increase in number after a mast year. At high latitudes, there is a similar delayed response by Myodes voles to high seed crops of bilberry (Vaccinium myrtillus), but here the mechanism is hypothesised to be increased forage quality, caused by a trade-off between reproduction and defence in the plants. Both Apodemus mice and Myodes voles eat berries, but only the latter feed on bilberry plants. Hence, only Myodes voles are predicted to respond to bilberry peak years. A second prediction is that the effect should last longer than any possible direct impacts of bilberries, because the plants would not be able to rebuild their defence until the succeeding summer. During a 21-year snap-trapping study of small rodents in Southern Norway, the spring population of bank vole (Myodes glareolus) was positively related to a bilberry seed index of the previous year, indicating increased winter survival, whereas the wood mouse (Apodemus sylvaticus) was not affected. Also the succeeding autumn population index of the bank vole was positively related to the bilberry index of the previous year, even when controlling for spring population levels. The wood mouse population responded to mast years of sessile oak (Quercus petraea), whereas seeds of Norway spruce (Picea abies) seemed to have some impact on both species. It is concluded that these rodents are mainly limited from below, but by different mechanisms for the granivorous and the herbivorous species.     

The effect of varying calcium intake on calcium metabolism in wild rodent species

Calcium is essential for mammals but distributed heterogeneously in the environment and so the calcium content of the diet of wild small mammals can vary with habitat geology. The effect of varying the calcium intake of two wild rodent species, the granivorous wood mouse Apodemus sylvaticus and the herbivorous bank vole Clethrionomys glareolus , was investigated. Wood mice were similar to laboratory rodents in their calcium metabolism. Net calcium gut absorption efficiency was 11–15% in wood mice fed either high (0˙87%) or low (0˙30%) calcium diet. No more than the equivalent of 6% of the ingested calcium load was excreted in urine but this was sufficient to eliminate the equivalent of all the extra calcium absorbed across the gut when mice were fed the high calcium diet. In contrast, mean net calcium gut absorption efficiency in bank voles was high and increased from 28% to 42% when dietary calcium content was tripled. Urine was important for excreting calcium, the equivalent of up to 23% of intake being eliminated by this route. Despite this, bank voles fed the high calcium diet assimilated three times more calcium than voles fed the low calcium diet; this was in direct proportion to the three-fold difference in dietary calcium concentration. Possible implications for wild rodents in calcium-rich and calcium-poor habitats are discussed.     

Reversal of fortune: plant suppression and recovery after vole herbivory

It is not clear how plant species preferred as forage by rodents persist in prairie vegetation. To test permanence of suppression of wet-mesic prairie vegetation by vole (Microtus pennsylvanicus) herbivory in synthetic experimental communities, access treatments were reversed after 9 years of vole exclusion or access. Between 1996 and 2004, rye grass Elymus virginicus (Poaceae) and tick-trefoil Desmodium canadense (Fabaceae) achieved mean cover of up to 30 and 25%, respectively, in plots where voles were excluded, but disappeared from plots where voles had access. To determine whether these species remained vulnerable to vole herbivory as established adults, and to determine whether the species could recover if vole herbivory were removed, access treatments were reversed at the end of the 2004 growing season and monitored through 2007. Repeated measures ANOVA demonstrated dramatic vole suppression of established E. virginicus, but not D. canadense, indicating continuing vulnerability of the grass but not of the adult legume. Release from vole herbivory resulted in re-growth of rye, but not tick-trefoil, which was apparently suppressed by established vegetation. Two additional common planted species did not respond to treatment reversal, nor did 11 much less common planted species that comprised a minor portion of the vegetation. Dominant perennial black-eyed Susan Rudbeckia subtomentosa (Asteraceae) did not change in plant numbers by year or treatment, but expanded or contracted in stems per plant and cover as E. virginicus was suppressed or released by vole herbivory or its absence. Results indicate that preferred food plants may persist through capacity to quickly recover during periods of relative vole scarcity, or reach a refuge in maturity.     

Sheep grazing and rodent populations: evidence of negative interactions from a landscape scale experiment

Inter-specific competition, facilitation and predation influence herbivore assemblages, but no study has experimentally explored the interactions between large ungulates and small rodents. In a fully replicated, landscape scale experiment, we manipulated densities of domestic sheep in mountain pastures in Norway. We then determined population growth and densities of rodents by live trapping in each of the areas with different sheep densities. We found that the (summer) population growth rate and autumn density of the field vole (Microtus agrestis) was lower at high sheep density. This provides the first experimental evidence of negative interactions between an ungulate and small rodent species. There was no effect on the bank vole (Clethrionomys glareolus), whose diet differs from sheep. Sheep density, therefore, potentially alters the pattern of inter-specific population synchrony amongst voles. Our study shows that negative interactions between large ungulates and small rodents may be species-specific and negative population consequences for the rodent population appear above threshold ungulate densities.Electronic supplementary material is available for this article at     

Effects of competition and season on survival and maturation of young bank vole females

In territorial microtines intra-specific density dependent processes can limit the maturation of individuals during the summer of their birth. This may have demographic consequences by affecting the number and the age distribution of breeding individuals in the population. Little is known about this process on a community level, though populations of many northern microtine species fluctuate in synchrony and are known to interfere socially with each other. We experimentally studied the influence of the field vole Microtus agrestis on maturation, breeding, space use and survival of weanling bank voles, Clethrionomys glareolus. Two additive competition experiments on bank vole populations were conducted in large outdoor enclosures, half of them additionally housing a field vole population. In a mid-summer experiment low population density and absence of older breeding females minimised intra-specific competition. Survival was not affected by the presence of field voles. Season had a significant effect on both the probability of maturation and breeding of the weanlings. Competition with field voles significantly delayed breeding, and coupled with seasonal effects decreased the probability of breeding. In a late-summer experiment breeding and survival of bank vole weanlings were studied for three weeks as part of a high density breeding bank vole population. Weanlings did not mature at all nor were their space use and survival affected by the presence of field voles. Our results show that competition with other species can also have an impact on breeding of immatures. In an extreme seasonal environment, even a short delay of breeding may decrease survival chances of offspring. Seasonal and competition effects together may thus limit the contribution of year born females to reproductive output of the population. Other studies have shown that adult breeding bank voles suffer lower survival in the presence of field voles, but this study showed no survival effects on the weanlings. Thus it might be beneficial for weanlings to stay immature especially in the end of the breeding season and postpone reproduction to the next breeding season if densities of competing species are high.     

Competition, predation and interspecific synchrony in cyclic small mammal communities

Although competition and predation are considered to be among the most important biotic processes influencing the distribution and abundance of species in space and time, the relative and interactive roles of these processes in communities comprised of cyclically fluctuating populations of small mammals are not well known. We examined these processes in and among populations of field voles, sibling voles, bank voles and common shrews in western Finland, using spatially replicated trapping data collected four times a year during two vole cycles (1987–1990 and 1997–1999). Populations of the four species exhibited relatively strong interspecific temporal synchrony in their multiannual fluctuations. During peak phases, we observed slight deviations from close temporal synchrony: field vole densities peaked at least two months earlier than those of either sibling voles or bank voles, while densities of common shrews peaked even earlier. The growth rates of all four coexisting small mammal species were best explained by their own current densities. The growth rate of bank vole populations was negatively related to increasing densities of field voles in the increase phase of the vole cycle. Apart from this, no negative effects of interspecific density, direct or delayed, were observed among the vole species. The growth rates of common shrew populations were negatively related to increasing total rodent (including water voles and harvest mice) densities in the peak phase of the vole cycle. Sibling voles appeared not to be competitively superior to field voles on a population level, as neither of these Microtus voles increased disproportionately in abundance as total rodent density increased. We suggest that interspecific competition among the vole species may occur, but only briefly, during the autumn of peak years, when the total available amount of rodent habitat becomes markedly reduced following agricultural practices. Our results nonetheless indicate that interspecific competition is not a strong determinant of the structure of communities comprised of species exhibiting cyclic dynamics. We suggest that external factors, namely predation and shortage of food, limit densities of vole populations below levels where interspecific competition occurs. Common shrews, however, appear to suffer from asymmetric space competition with rodents at peak densities of voles; this may be viewed as a synchronizing effect.     

Spatio-temporal patterns of habitat use in voles and shrews modified by density, season and predators

1.?Although the intrinsic habitat preferences of a species can be considered to be fixed, the realized habitat use depends on the prevailing abiotic and biotic conditions. Often the core habitats are occupied by dense and stable populations, while marginal habitats become occupied only at times of high density. In a community of interacting species, habitat uses of different species become inter-related, for example an increased density of a strong competitor forcing a weaker competitor to use more marginal habitats. 2.?We studied the spatio-temporal distribution patterns of three common small mammal species, the bank vole Myodes glareolus; the field vole Microtus agrestis; and the common shrew Sorex araneus, in a 4-year trapping study carried out on six large islands, each containing a mixture of three main habitat types (forest, field and clear-cut). We experimentally released least weasels (Mustela n. nivalis) to some of the islands to see how the focal species respond to increased predation pressure. 3.?Both vole species were largely restricted to their core habitats (bank voles to forests and field voles to fields) at times of low population density. With increasing density, the relative habitat use of both species increased in the clear-cut areas. The common shrew was a generalist in its habitat use at all population densities. 4.?The release of the weasels changed the habitat use of all study species. 5.?The vole species showed a stronger aggregated pattern than the common shrew, especially at low population density. The vole aggregations remained in the same localities between seasons, except in the case of bank voles after the weasels were released. 6.?Bank voles and field voles avoided each other at high density. 7.?We conclude that intrinsically differential habitat requirements and flexibility to modify habitat use facilitate the coexistence of the two competing vole species in mosaic landscapes consisting of boreal forests and open habitats.     

Prion protein amino acid determinants of differential susceptibility and molecular feature of prion strains in mice and voles

The bank vole is a rodent susceptible to different prion strains from humans and various animal species. We analyzed the transmission features of different prions in a panel of seven rodent species which showed various degrees of phylogenetic affinity and specific prion protein (PrP) sequence divergences in order to investigate the basis of vole susceptibility in comparison to other rodent models. At first, we found a differential susceptibility of bank and field voles compared to C57Bl/6 and wood mice. Voles showed high susceptibility to sheep scrapie but were resistant to bovine spongiform encephalopathy, whereas C57Bl/6 and wood mice displayed opposite features. Infection with mouse-adapted scrapie 139A was faster in voles than in C57Bl/6 and wood mice. Moreover, a glycoprofile change was observed in voles, which was reverted upon back passage to mice. All strains replicated much faster in voles than in mice after adapting to the new species. PrP sequence comparison indicated a correlation between the transmission patterns and amino acids at positions 154 and 169 (Y and S in mice, N and N in voles). This correlation was confirmed when inoculating three additional rodent species: gerbils, spiny mice and oldfield mice with sheep scrapie and 139A. These rodents were chosen because oldfield mice do have the 154N and 169N substitutions, whereas gerbil and spiny mice do not have them. Our results suggest that PrP residues 154 and 169 drive the susceptibility, molecular phenotype and replication rate of prion strains in rodents. This might have implications for the assessment of host range and molecular traceability of prion strains, as well as for the development of improved animal models for prion diseases.     

Further Studies on Leptospirosis in Small Rodents and Shrews in Finland. A Report on Investigations Made in 1963-64

In previous investigations on small mammals in Finland (Rislakki & al 1954, Rislakki & Salminen 1955, Salminen 1956), the Leptospira icterohaemorrhagiae-frequency in rats (Rattus norvegicus) was rather high (43.1 %). Leptospira-positive cases were also found in house mice (L. sejroe 23.3 %), harvest mice (L. hataviae 9.0 %), yellow necked field mice (L. poi 12.5 %), common voles (L. sejroe and L. bataviae together 12.1 %), field voles (L. sejroe and L. bataviae together 10.7 %) and in common shrews (L. poi 1.2 %). Specimens of other species sent in for investigation (Norway rat, common red backed vole, large tooth backed vole, northern red backed vole, root vole, water vole, wood lemming, Laxmann's shrew, lesser shrew and water shrew) gave negative results.     

Food deprivation in the common vole (<Emphasis Type="Italic">Microtus arvalis</Emphasis>) and the tundra vole (<Emphasis Type="Italic">Microtus oeconomus</Emphasis>)

Arvicolinae voles are small herbivores relying on constant food availability with weak adaptations to tolerate prolonged food deprivation. The present study performed a comparative analysis on the responses to 4–18 h of food deprivation in the common vole (Microtus arvalis) and the tundra vole (Microtus oeconomus). Both species exhibited rapid decreases in the plasma and liver carbohydrate concentrations during phase I of fasting and the decline in the liver glycogen level was more pronounced in the tundra vole. The plasma thyroxine concentrations of the common vole decreased after 4 h. Lipid mobilization (phase II of fasting) was indicated by the increased plasma free fatty acid levels after 8–18 (the common vole) or 4–18 h (the tundra vole) and by the elevated lipase activities. In the tundra vole, the plasma ghrelin concentrations increased after 12 h possibly to stimulate appetite. Both species showed increased liver lipid concentrations after 4 h and plasma aminotransferase and creatine kinase activities after 12–18 h of food deprivation implying liver dysfunction and skeletal muscle damage. No signs of stimulated protein catabolism characteristic to phase III of fasting were present during 18 h without food.     

内蒙古典型草原区狭颅田鼠集群数量与被捕食风险的关系

2005年9月15日—30日,在内蒙古锡林郭勒盟西乌珠穆沁旗的典型草原上研究了狭颅田鼠(Microtus gregalis)冬季集群与来自艾虎(Mustela eversmanni)的捕食风险。采用鼠洞口数量作为狭颅田鼠集群大小的指标,分析了艾虎对不同大小狭颅田鼠集群的捕食优先选择偏好。对实验样地内狭颅田鼠的洞群洞口数进行了调查统计(样地内总共涉及102个狭颅田鼠有效洞群),并计数此期间的艾虎粪便堆数以及攻击掘开狭颅田鼠洞群的情况。运用非参数的Mann-Whitney U检验法进行数据分析,结果表明:从艾虎遗留的粪便痕迹来看,没有被艾虎访问过的田鼠洞群与被艾虎访问过的洞群之间差异达到极显著水平;另外,从狭颅田鼠洞口被艾虎掘开的痕迹来分析,没有被艾虎挖掘的洞群与被艾虎挖掘的洞群之间的差异也达到极显著的水平;另外,随着田鼠洞群洞口数量的增加,出现艾虎粪便和掘洞的频次和概率就越高。表明艾虎对狭颅田鼠集群洞口数的选择差异性非常显著,明显倾向于选择在洞口数量多的狭颅田鼠洞群停留,同时也更倾向于掘开洞口数量较高的狭颅田鼠洞群作为捕食对象。     

Coexisting small mammals display contrasting strategies for tolerating instability in arable habitat

Small mammal species are abundant and common throughout Europe and often utilise areas that are subject to agricultural land use. Arable farmland is an example of a frequently disturbed habitat, and this study questioned how such disturbance affected the two most common species in the region; one a habitat generalist and one a habitat specialist. We confirmed the prediction that wood mice (Apodemus sylvaticus, a habitat generalist) would make use of a variety of habitats and that bank voles (Myodes glareolus, a habitat specialist) would make greater use of the more stable portions of the study site. We surveyed the study site intensively in order to test whether there was continuity in the spatial arrangement of individuals of both species, given the strategy employed. The spatial arrangement of wood mice varied with season but remained stable for bank voles. We found no association, positive or negative, between the spatial distributions of the two species, suggesting that spatial competitive exclusion did not occur. This work provides further insight into how these small mammal species are affected by agricultural disturbance and predictions can be made about how the species will respond under CAP Reform greening practices.     

The effect of variation in calcium intake on the growth of wood mice and bank voles

Summary Calcium intake by wild rodents varies with season and habitat. This may have important ecological consequences; several studies have suggested that calcium availability may limit growth and reproduction. We studied the effect on growth of varying the calcium intake of captive wood mice Apodemus sylvaticus (L.) and bank voles Clethrionomys glareolus (Schreber 1780). To determine whether effects observed in the laboratory could be detected in free-living animals, we also compared the body weights and lengths of free-living animals on calcium-poor gritstone areas with those of rodents on calcium-rich limestone habitats where the dietary calcium concentration was between 2 and 5 times higher. Captive wood mice fed high calcium (0.87%) diet grew at the same rate as mice fed low calcium (0.30%) diet but continued growing for longer, thereby achieving higher asymptotic weights. In contrast, captive bank voles fed the high calcium diet grew more slowly and had lower asymptotic weights than voles fed the low calcium diet. As expected from the laboratory growth study, the higher calcium intake of free-living wood mice on the limestone was associated with greater body size compared with mice on the gritstone. However, bank voles were also larger on the limestone, even though high calcium intake impaired growth in captive animals. The contrast between wood mice and bank voles in the effects of calcium on growth, the reason why impaired growth may not be apparent in bank voles from calcium-rich habitats and the ecological significance of these results are discussed.     

Habitat use by three Acrocephalus warblers in an intensively used farmland area: the influence of breeding patch and its surroundings

Habitat use by the sedge warbler Acrocephalus schoenobaenus, reed warbler A. scirpaceus and marsh warbler A. palustris was studied during 1998–2000 in an intensively cultivated agricultural landscape in western Poland. The birds occupied mid-field marsh patches (0.05–9.84 ha) and drainage ditches. Using logistic regression models, habitat preferences for particular patch type, characteristics of breeding patch vegetation and surrounding crop type were investigated. All habitat measurements were done within 50-m radius circles around breeding territory centers. The most important factors that influenced species distributions were the proportions of particular habitats within patch area and the type of surrounding crops. Sedge and reed warblers preferred areas with a high proportion of reeds and meadows. Marsh warblers avoided emergents other than reeds, and favored herbaceous vegetation and bushes. Open water areas positively affected reed warbler distribution. Crop type had a significant influence on within-year territory distribution and changes in between-year occupation pattern. In general, birds preferred to settle near fields of oil seed rape, while root crops and spring cereals were avoided. Breeding patch type and structure of reedbeds had relatively little influence on the distribution of breeding territories. The results obtained show that the surrounding landscape may significantly influence habitat use of species breeding in habitat islands in farmland. Depending on their structure and food resources, crops might have different value to the birds.     

Disturbances of the mineral incorporation in various species of mice and shrews in the emission area of a phosphate plant

The Cd emission of a phosphate plant was clearly reflected by the Cd status of herbivorous European wood mice and common field voles as well as of European shrews taking in mostly animal food. The antagonistic effect of the emitted Cd and Mo better available for plants with high ground pH most probably caused the deterioration in the Cu status of the animals of both phases in the nutritional chain. The lower Ca, P, and Mg incorporation with European wood mouse and common field vole within the contaminated habitat might as well be owing to emission, whereas the lower Mn content in all three species rather has to be attributed to the lower Mn offer caused by the ground pH.     

Behaviour and resource use of two competing vole species under shared predation risk

Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the effect of predation risk imposed by the least weasel Mustela nivalis nivalis on space use, foraging and activity of two competing vole species, the grey-sided vole Myodes rufocanus, and the bank vole Myodes glareolus. The experiment was conducted in a large indoor arena, consisting of microhabitat structures providing food, shelter, trees for refuge and separated areas with high and low predation risk. Voles were followed for 5 days: 2 days before, 1 day during and 2 days after the presence of weasel. Our results suggest an effect of weasel presence on the vole community. Voles of both species shifted their activity from risky to less risky areas, climbed trees more often and were less active. Seed consumption was not affected by weasel presence. The time spent in the risky and less risky area did not differ between species, but bank voles spent more time in trees than grey-sided voles. Males of both species were more exposed to predation risk than females, i.e. generally spent more time in the risky area. Proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and use of trees were species dependent. We found no evidence for despotic distribution between our two species, although bank voles seemed to be more affected by coexistence, since they lost weight during the experiment. Based on our results we conclude that predator response was largely similar between species, while the sex-specific responses dominated. Besides a stronger escape response in the bank vole, the strongest individual differences were sex specific, i.e. males were more prone to take risks in space use and activity.     

Fox predation on cyclic field vole populations in Britain

The diet of the red fox Vulpes vulpes L. was studied during three winter periods in spruce pklantations in Britain, during which time the cyclic field vole Microtus agrestis L. populations varied in abundance. Field voles and roe deer Capreolus capreolus L. were the two main prey species in the diet of the red fox. The contribution of lagomorphs to fox diet never exceeded 35% and species of small mammal other than field voles were of minor importance. The contribution of field voles was dependent on vole density. The non-linear density dependent relationship with a rather abrupt increase of field voles in fox did when vole density exceeded ca 100 voles ha⁻¹ was consistent with a prey-switching response. The contribution of field voles to fox diet during the low phase of population cycles was lower in Kielder Forest than in other ecosystems with cyclic vole populations. The number of foxes killed annually by forestry rangers was consistent with the evidence from other studies that foxes preying on cyclic small rodents might show a delayed numerical response to changes in vole abundance. Estimates of the maximum predation rate of the fox alone (200–290 voles ha⁻¹ of vole habitat year⁻¹) was well above a previously predicted value for the whole generalist predator community in Kielder Forest. Our data on the functional response of red foxes and estimates of their predation rates suggest that foxes should have a strong stabilising impact on vole populations, yet voles show characteristic 3-4 yr cycles.     

Weed seed resources for birds in fields with contrasting conventional and genetically modified herbicide-tolerant crops

The UK Farm Scale Evaluations (FSEs) have shown that the use of broad spectrum herbicides on genetically modified herbicide-tolerant (GMHT) crops can have dramatic effects on weed seed production compared to management of conventional varieties. Here, we use FSE data and information on bird diets to determine how GMHT cropping might change the food resources available to farmland birds. More than 60 fields of each of four crops, spring- and winter-sown oilseed rape, beet and maize, were split, one half being sown with a conventional variety, the other with a GMHT variety. Seed rain from weeds known to be important in the diets of 17 granivorous farmland bird species was measured under the two treatments. In beet and spring oilseed rape, rain of weed seeds important in the diets of 16 bird species was significantly reduced in GMHT compared to conventional halves; for no species did it increase. In winter oilseed rape, rain of weed seeds important in the diets of 10 species was significantly reduced in GMHT halves; for only one species did it increase significantly. By contrast, in maize, rain of weed seeds important in the diets of seven species was significantly greater in GMHT halves; for no species was it reduced. Treatment effects for the total weed seed energy available to each bird species were very similar to those for seed rain alone. Measuring the effects on individual bird species was outside the scope of this study. Despite this, these results suggest that should beet, spring and winter rape crops in the UK be largely replaced by GMHT varieties and managed as in the FSEs, this would markedly reduce important food resources for farmland birds, many of which declined during the last quarter of the twentieth century. By contrast, GMHT maize would be beneficial to farmland birds.