Cyclic voles and shrews and non-cyclic mice in a marginal grassland within European temperate forest

Cyclic population dynamics of small mammals are not restricted to the boreal and arctic zones of Eurasia and North America, but long-term data series from lower latitudes are still less common. We demonstrated here the presence of periodic oscillations in small mammal populations in eastern Poland using 22-year (1986–2007) trapping data from marginal meadow and river valley grasslands located in the extensive temperate woodland of Białowieża Primeval Forest. The two most common species inhabiting meadows and river valleys, root vole Microtus oeconomus and common shrew Sorex araneus, exhibited synchronous periodic changes, characterised by a 3-year time lag as indicated by an autocorrelation function. Moreover, the cycles of these two species were synchronous within both habitats. Population dynamics of the striped field mouse Apodemus agrarius was not cyclic. However, this species regularly reached maximum density 1 year before the synchronized peak of root voles and common shrews, which may suggest the existence of interspecific competition. Dynamics of all three species was dominated by direct density-dependent process, whereas delayed density dependent feedback was significant only in the root vole and common shrew. Climatic factors acting in winter and spring (affecting mainly survival and initial reproduction rates) were more important than those acting in summer and autumn and affected significantly only the common shrew. High temperatures in winter and spring had positive effects on autumn-to-autumn changes in abundance of this species, whereas deep snow in combination with high rainfall in spring negatively affected population increase rates in common shrew.     

Multiple captures provide evidence of small mammal social behavior

Social behavior of small mammals living under natural conditions often is inferred from live-trapping data, particularly from incidents in which two or more individuals are captured together in a trap. We examined whether multiple-capture data from a long-term study of prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) were consistent with well-known species differences in social behavior (whereas prairie voles are highly social and display monogamy, meadow voles are less social and promiscuous). When possible, we also examined multiple captures of two nontarget species, northern short-tailed shrews (Blarina brevicauda) and western harvest mice (Reithrodontomys megalotis). Percent of total captures that were multiple captures and percent of total adult captures that were male–female captures were highest for prairie voles and lowest for meadow voles; values for harvest mice and shrews were in between those of the vole species, but more similar to values for meadow voles. Repeat captures of the same male–female pair occurred most commonly in prairie voles, and multiple captures of this species typically involved individuals from the same social group. Multiple captures of adults and juveniles were more common in prairie voles than meadow voles, except for captures of at least one adult male and at least one juvenile, which did not differ between the two vole species. Multiple capture data for prairie voles and meadow voles were largely consistent with established species differences in social behavior, suggesting that such data can provide an accurate indication of social and mating systems of small mammals.     

Genetic structure is influenced by environmental barriers: empirical evidence from the common voleMicrotus arvalis populations

One of the major challenges in population biology is the identification of barriers to gene flow and/or secondary contacts between differentiated entities. The level of genetic differentiation among eight populations of the common voleMicrotus arvalis (Pallas, 1779) around the Biebrza Wetlands, NE Poland was examined by analyzing seven microsatellite loci for 140 voles and testing for the presence of barriers to gene flow. Overall population differentiation was moderate and significant (F _ST = 0.081,p < 0.001) and there was no correlation between geographical and genetic distances among populations. We found a relatively high level of genetic variability within the populations studied. This could be explained by male bias in dispersal, a phenomenon recently found inM. arvalis. Patterns of genetic structure visualized in synthetic genetic maps showed clear gradients along a southeast-northwest axis across the study area, as well as the presence of a potential barrier to dispersal. The position of a barrier to gene flow identified using Monmonier’s maximum difference algorithm likely corresponds to humid habitats of the Biebrza Wetlands. These results suggest that the presence of environmental barriers to gene flow and drift may be responsible for the observed spatial genetic structure ofM. arvalis in the Biebrza Valley. Institute of Biology, University of Białystok, OEwierkowa 20 B, 15-950 Białystok, Poland,     

Dampening of population cycles in voles affects small mammal community structure,decreases diversity,and increases prevalence of a zoonotic disease

Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.     

Body mass and measurements of the European bison during postnatal development

Body mass of the European bisonBison bonasus (Linnaeus, 1758) was determined for 152 animals (86 males, 66 females) from captive breeding centre in Białowieża and for 492 (248, 244) animals from the free-ranging herd in the Białowieża Forest. Body measurements were taken for a total of 472 bison (204, 268). Age-related changes in body mass and measurements of 375 bison (165, 210) were analysed. Bison body mass was significantly correlated with age. Captive bison were heavier than those from a free-ranging herd. Measurements showed the changes in bison body structure in the postnatal development. All measurements were highly correlated with age and mass of the animals and increased most intensively during the first year of life. Sex-related differences in body mass and measurements were most pronounced in bison ≥ 3 years old. Physical development of females ends at the age of 5 years, and that of males at the age of 7 years.     

Reproductive investment under fluctuating predation risk: Microtine rodents and small mustelids

Summary We studied the reproductive investment of microtine rodents (bank vole (Clethrionomys glareolus),Microtus epiroticus andMicrotus agrestis) in western Finland under predation risk from small mustelids. During 1984–1992, the yearly mean litter size of overwintered bank voles was smaller at high least weasel and stoat densities than at low densities (close to 3 versus 4–5). In addition, the annual mean litter size of young bank voles was negatively correlated to the least weasel density. In youngM. agrestis voles, the yearly late summer litter size was negatively associated with the autumn density of small mustelids. In the crash phase of the vole cycle (1989 and 1992), we removed small mustelids (mainly least weasels) from four unfenced areas in late April to late May and studied the reproduction of voles in four removal and comparable control areas (each 2–4 km²). Reduction of small mustelids significantly increased the proportion of pregnant bank vole females, but not that of pregnantMicrotus vole females. We conclude that predation risk apparently reduced reproductive investment of free-living bank vole females; these voles appear to trade their current parental investment against future survival and reproductive prospects. Accordingly, the presence of small mustelids (or their scent) may slow down the reproductive rate of voles. As antipredatory behaviours occurred on a large scale, our results add evidence to the hypothesis that crashes in multiannual vole cycles are driven by small mustelid predators.     

Does avian predation risk depress reproduction of voles?

Reproductive output and the growth of captive voles were quantified under high and low avian predation risk in a semi-natural experiment. Voles were exposed to Eurasian kestrels (Falco tinnunculus), the main avian predator of vole species studied (Clethrionomys glareolus, Microtus agrestis and M. rossiaemeridionalis). Vole pairs were housed in cages settled under nest-boxes occupied by breeding kestrels or in control cages settled under empty nest-boxes for 2 weeks. The experiment was conducted in mid-summer when kestrels had half-grown nestlings, because in that time hunting adults and begging nestlings produce noise and scats which may indicate significant predation threat to voles housed underneath the nest-boxes. The risk of kestrel predation did not have any obvious impact on pregnancy rates, mean litter sizes, or growth rates of kestrel-exposed voles compared with control voles studied. These results indicate that the risk of avian predation does not depress the reproductive investment of voles. Received: 3 November 1997 / Accepted: 16 February 1998     

The effect of diet quality on gut anatomy in British voles (Microtinae)

Three species of British voles, the bank vole Clethrionomys glareolus, the field vole Microtus agrestis and the water vole Arvicola terrestris were maintained on diets of seed and plant leaf material to investigate changes in gut anatomy. C. glareolus and M. agrestis showed significant changes in most regions of the gut; they developed longer and heavier tracts when on a highfibre diet. This response may be important in enabling these animals to withstand seasonal changes in diet quality.     

Small mammal populations in relation to hedgerow structure in an arable landscape

The population ecology of small mammals in hedgerows in arable farmland in eastern England is described. Features of hedgerows of importance to individual species are examined. Some 97% of the total 3042 mammals captured were wood mouse Apodemus sylvaticus , yellow-necked mouse Apodemus flavicollis , bank vole Clethrionomys glareolus and common shrew Sorex araneus . Small numbers of harvest mice Micromys minutus , field voles Microtus agrestis , pygmy shrews Sorex minutus and water shrews Neomys fodiens were also caught. Wood mouse, the most numerous species, showed a typical pattern of large numbers in autumn and winter, followed by a simultaneous decline over all hedges in early spring. Population changes were less clear in yellow-necked mouse and bank vole but the yellow-necked mouse was more scarce in the second year of study. Common shrews were most numerous in summer and declined rapidly in autumn. Hedgerow coppicing had a marked effect on yellow-necked mouse numbers but not on wood mouse. In an extensive survey of mammal numbers in relation to hedgerow features, ground cover was found to be the single largest factor influencing size of bank vole populations. Hedgerow condition (lack of gaps) was important to yellow-necked mice, which thrived only in well-established hedgerows. Wood mice appeared little influenced by the characteristics of the hedge. Common shrews were more abundant in hedgerows with adjacent permanent water.     

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.     

Changes in population structure and reproduction during a 3-yr population cycle of voles

Cyclic changes in population growth rate are caused by changes in survival and/or reproductive rate. To find out whether cyclic changes in reproduction are an important part of the mechanism causing cyclic fluctuations in small mammal populations, we studied changes in the population structure and reproduction of field voles ( Microtus agrestis ), sibling voles ( M. rossiaemeridionalis ), bank voles ( Clethrionomys glareolus ), and common shrews ( Sorex araneus ) in western Finland during 1984–1992, in an area with 3-yr vole cycles. We also modelled the population growth of voles using parameter values from this study. The animals studied were collected by snap trapping in April, May, June, August, September, and, during 1986–1990, also in October. We found several phase-related differences in the population structure (age structure, sex ratio, proportion of mature individuals) and reproduction (litter size, length of the breeding season) of voles. In non-cyclic common shrews, the only significant phase-related difference was a lower proportion of overwintered individuals in the increase phase. According to the analyses and the vole model, phase-related changes in litter size had only a minor impact on population growth rate. The same was true for winter breeding in the increase phase. The length and intensity of the summer breeding season had an effect on yearly population growth but this impact was relatively weak compared to the effect of cyclic changes in survival. The population increase rates of Microtus were delayed dependent on density (8–12-month time lag). Our results indicate that cyclic changes in reproduction are not an important part of the mechanism driving cyclic fluctuations in vole populations. Low survival of young individuals appeared to play an important role in the shift from the peak to the decline phase in late summer and early autumn.     

Mast Pulses Shape Trophic Interactions between Fluctuating Rodent Populations in a Primeval Forest

How different functional responses of consumers exploiting pulsed resources affect community dynamics is an ongoing question in ecology. Tree masting is a common resource pulse in terrestrial ecosystems that can drive rodent population cycles. Using stable isotope (δ¹³C, δ¹⁵N) analyses, we investigated the dietary response of two fluctuating rodent species, the yellow-necked mouse Apodemus flavicollis and the bank vole Myodes glareolus, to mast events in Białowieża Forest (NE Poland). Rodent hair samples were obtained non-invasively from faeces of their predators for an 11-year period that encompassed two mast events. Spectacular seed crops of deciduous trees, namely oak Quercus robur and hornbeam Carpinus betulus, occur after several intermediate years of moderate seed production, with a post-mast year characterised by a nil crop. While a Bayesian isotopic (SIAR) mixing model showed a variety of potential vegetation inputs to rodent diets, the isotopic niche of the yellow-necked mouse was strongly associated with mast of deciduous trees (>80% of diet), showing no variation among years of different seed crop. However, bank voles showed a strong functional response; in mast years the vole shifted its diet from herbs in deciduous forest (∼66% of diet) to mast (∼74%). Only in mast years did the isotopic niche of both rodent species overlap. Previous research showed that bank voles, subordinate and more generalist than mice, showed higher fluctuations in numbers in response to masting. This study provides unique data on the functional response of key pulse consumers in forest food webs, and contributes to our understanding of rodent population fluctuations and the mechanisms governing pulse–consumer interactions.     

Microhabitat selection by Eurasian lynx and its implications for species conservation

We studied microhabitat selection of the Eurasian lynxLynx lynx (Linnaeus, 1758) at 116 hunting and 88 resting sites in Białowieża Primeval Forest (Poland) to describe its characteristics and determine the importance of habitat structure for stalking prey and for security during resting. We identified lynx-used sites by radio-tracking 3 male and 3 female lynx. When hunting, the lynx did not select for any type or age class of forest. During both summer and winter, the lynx selected sites characterized by high complexity (number of structures useful for stalking: fallen logs and branches, root plates, patches of dense bushes) and low visibility. In summer, hunting sites were often located in the vicinity of small forest glades that provided good stalking opportunities for lynx and rich foraging resources for roe deer — the main prey of lynx. The habitat at kill sites was more open than at sites where the prey was cached, with higher visibility, lower density of trees and poorer undergrowth. The most important characteristic of resting sites was very low visibility that resulted mainly from using young pine or spruce thickets in the winter and dense undergrowth of oak-lime-hornbeam and ash-alder forests in the summer. The information provided by this study could have direct implications for Eurasian lynx conservation by guiding forest restructuring to better suit the species’ biological requirements.     

The seasonal dynamics of fleas (Siphonaptera) on bank voles (Clethrionomys glareolus) in the north part of Novgorod region

The twelve flea species were revealed on bank voles. Only four of them (Amalaraeus penicillige, Ctenophthalmus uncinatus, Megabothris turbidus, Peromescopsylla bidentata) were abundant in some seasons of the year. Four other species (Ct. agyrtes, Hystrichopsylla talpae, P. silvatica, Rhadinopsylla integella) are the parasites of bank vole too but their numbers were always low in the study area. The four last species (Amphypsylla rossica, M. walkeri, Doratopsylla dasycnema, Palaeopsylla soricis) are not peculiar to bank vole. They occurs on it occasionally from other animals--the voules of Mucrotus and shrews. The most species diversity of fleas on bank vole was observed at the period from August to October, the least one--in late winter, spring and early summer. The total abundance indices of fleas on the voles (mean number of the insects per host) ranged in different months from 0.17 to 5.65. The time of minimum flea numbers was August-September. The peak abundance was reached in springtime (March-April).     

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.     

Spatial interactions between grey wolves and Eurasian lynx in Białowieża Primeval Forest, Poland

Various species of large predators are reported to influence each other through interference or exploitation competition that may affect demography and survival of the subordinate species. We analyzed spatial relationships between grey wolf (Canis lupus) and Eurasian lynx (Lynx lynx) in Białowieża Primeval Forest (BPF, eastern Poland) to determine how they partitioned the space. The wolves (n = 8) and lynx (n = 14) were radio-tracked in 1991–1999. Three wolves and seven lynx were radio-tracked simultaneously in 1994–1996. Territories of wolf packs and home ranges of lynx overlapped considerably (76% of wolf territories and 50% of lynx home ranges, on average). In three cases, their core areas were also overlapping. Wolf-lynx dyads with overlapping home ranges were simultaneously located at distances from 0 to 28 km from each other. We found neither avoidance nor attraction between wolves and lynx occupying the same areas. We concluded that in BPF, the two large predators coexist due to specialization on different preferred prey and heterogeneous habitat.     

Changes of weight and size of European bison testes during postnatal development

The material for this study was obtained from culled European bison (Linnaeus, 1758) originating from both captive breeding and free-ranging populations in Białowieża and Borecka Forests (north-east Poland), and was mostly collected from November until April. Mass difference between the right and left testis of the same individual up to 30% was considered to be physiological asymmetry, which proved typical of the species. Hypoplasia or atrophy of the testes exceeding 30% in size, were found in 37 males (13.6% of the examined animals;n=272). Cryptorchidism was recorded in 20 bison culled in Białowieża Forest at the age over 1 year (10.6% of individuals at the same age;n=188). We registered the weight of testes of 259 males aged 2 months to 20 years. In the examined males, no distinct predominance in size and weight between the right and left testes was observed. The weight of testes was significantly correlated with age (r=0.85,p < 0.0001) and body weight (r=0.93,p < 0.0001). The heaviest testicles belonged to older and sexually mature bulls aged 6–12 years (mean 216 g) and to old ones over 13 years (mean 242 g). Two testis measurements (length and width) were taken from 136 culled males, while two additional measurements (total length with the cauda of epididymis and circumference) from 65 males. The length and width of the testes were moderately correlated with age (r=0.31 andr=0.20,p < 0.01) and highly significantly correlated with testis (r=0.79,p < 0.001) and body weight (r=0.92,p < 0.001).     

Sequence diversity of MHC class II DRB genes in the bank vole<Emphasis Type="Italic">Myodes glareolus</Emphasis>

In recent years, the bank voleMyodes glareolus (Schreber, 1780) has emerged as a model system for parasitological, behavioural and ecological studies and seems ideally suited to address questions concerning the importance of MHC variation at individual and population levels. Here, we provide the first extensive survey of sequence variation in the MHC class II DRB genes in this species. Among 34 analysed voles we found 15 unique sequences, representing most likely two loci, at least one of them expressed. Despite very high overall sequence divergence, particularly in the Antigen Binding Sites (ABS), we detected signatures of positive selection that has been acting on DRB in the bank vole. Phylogenetic analysis demonstrated that the bank vole DRB alleles do not form a monophyletic group but are intermingled with other rodent alleles that is consistent with long-term persistence of ancient allelic lineages maintained through balancing selection. Our sequence data will forward the design of efficient genotyping methods, which will permit testing hypotheses pertaining to the ecological causes and consequences of MHC variation in the bank vole.     

Will Environmental Stewardship enhance small mammal abundance on intensively managed farmland?

• 1 The creation of grassy field margins, as part of the UK Government's Environmental Stewardship (ES) scheme, is one of a number of measures proposed to mitigate the adverse effects of arable intensification on wildlife. Widespread development of these margins will potentially increase the amount of habitat available to small mammals in arable landscapes, as many species do not inhabit the cropped area.
• 2 The aim of this study was to determine what impact ES-type margins might have on small mammals. We compared small mammal abundance and biomass in spring and autumn on 3-m-wide and 6-m-wide grassy margins with that on conventionally managed field edges that have no margin (0 m wide) and are intensively cultivated to the field edge.
• 3 Bank voles Clethrionomys glareolus, wood mice Apodemus sylvaticus and common shrews Sorex araneus were the most abundant species; few field voles Microtus agrestis were captured on any margin. In autumn, bank vole and common shrew numbers were higher on the grassy margins than on conventional field edges, and margin width per se was positively associated with bank vole abundance. The number of wood mice captured did not differ among the different margin types.
• 4 Total small mammal biomass increased between spring and autumn on the 3-m- and 6-m-wide grassy margins, but decreased on the 0-m-wide margins. Total biomass in autumn was three times higher on 6-m-wide margins compared with the conventional arable field edges.

     

Species composition and activity of bats flying over rivers in the Białowieża Primeval Forest

Bats were netted at two sites over the forest rivers Narewka and Hwoźna in Białowieża Primeval Forest (E Poland), during the summer of 1994 and 1995. A total of 452 bats of 11 species were captured. The number of bats netted each night was positively correlated with the minimum air temperature. The rate at which the three commonest species —Nyctalus noctula, Myotis daubentonii andNyctalus leisleri — were caught varied significantly through the night, with a major peak after sunset. ForN. noctula air temperature was apparently positively related to the size of the morning peak.