Microtine Rodents Research Articles

Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors

Several lines of evidence have implicated the neurohypophyseal peptide, vasopressin (VP), in the mediation of complex social behaviors including affiliation, aggression, juvenile recognition and parental behavior. Recent studies in microtine rodents using cellular, molecular and behavioral approaches provide additional evidence suggesting a role for VP in the formation of pair bonding and male parental care. Monogamous and promiscuous voles differ in social behaviors such as mating-induced pair bonding, selective aggression, and male parental care. Comparative studies have demonstrated that they also differ in dynamics of VP synthesis and release associated with reproduction, in the distribution pattern and regional quantity of VP receptors, and in the promoter sequence of the V1a receptor gene. In monogamous prairie voles, (Microtus ochrogaster), brain administration of VP induces pair bonding and male parental care whereas administration of the VP antagonist diminishes these behaviors. Together, these data suggest that VP is involved in the regulation of social behaviors in monogamous voles and differences in the brain VP system may underlie species differences in behavior and life strategy in voles.

Sex differences in spatial learning and prefrontal and parietal cortical dendritic morphology in the meadow vole, Microtus pennsylvanicus

The prefrontal and parietal cortex has been implicated in the mediation of spatially related behaviors in male and female laboratory rats. Meadow voles, Microtus pennsylvanicus, are diurnally–crepuscularly active microtine rodents that exhibit a variety of sexually dimorphic spatially associated behaviors in both the laboratory and wild. In the present study we examined both the spatial Morris water maze performance and dendritic architecture and branching of neuronal cells in the prefrontal and parietal cortex of reproductive male and female meadow voles. Males learned the location of the hidden platform in the water task faster than estrous females and on probe trials they spent more time in the previously correct quadrant than females. Dendritic analysis with Golgi–Cox stained sections showed that male voles had significantly more dendritic arborization in the medial prefrontal and parietal cortex than females. These sex differences in both spatial navigation ability and in neural structures related to spatial navigation in meadow voles suggest that the size of neural areas might be shaped by ecological pressures associated with sexually dimorphic spatial behaviors.

Body mass dynamics in the Mediterranean pine vole Microtus duodecimcostatus

The occurrence of large individuals in fluctuating populations of microtine rodents (the Chitty effect) has received considerable attention. Recent studies showed that there are no causal relationships between the Chitty effect and the multi-annual population cycles of voles and lemmings. We studied five populations of Microtus duodecimcostatus in southern France with capture-recapture methods. Mean body mass was constant in all populations. Maximum observed body mass was more variable, and slightly positively correlated with density, except in the most fluctuating population where the correlation was strong. A careful study of the occurrence of large voles in these populations showed that most were pregnant females, and that the few large males were present when density was high and sample sizes were large. Comparison with published studies indicates that the Chitty effect, though not restricted to microtines, is not a general phenomenon in small mammal populations. Our field results and laboratory data on the same species suggest that M. duodecimcostatus has a determinate body growth, contrary to some Microtus species which have an indeterminate growth.

Body mass dynamics in the Mediterranean pine vole Microtus duodecimcostatus

AbstractThe occurrence of large individuals in fluctuating populations of microtine rodents (the Chitty effect) has received considerable attention. Recent studies showed that there are no causal relationships between the Chitty effect and the multi‐annual population cycles of voles and lemmings. We studied five populations of Microtus duodecimcostatus in southern France with capture‐recapture methods. Mean body mass was constant in all populations. Maximum observed body mass was more variable, and slightly positively correlated with density, except in the most fluctuating population where the correlation was strong. A careful study of the occurrence of large voles in these populations showed that most were pregnant females, and that the few large males were present when density was high and sample sizes were large. Comparison with published studies indicates that the Chitty effect, though not restricted to microtines, is not a general phenomenon in small mammal populations. Our field results and laboratory data on the same species suggest that M. duodecimcostatus has a determinate body growth, contrary to some Microtus species which have an indeterminate growth.

POPULATION CYCLES IN SMALL MAMMALS: THE PROBLEM OF EXPLAINING THE LOW PHASE

Cycles characterize the demography of many populations of microtine rodents and snowshoe hares. A phase of low numbers often follows the decline and introduces a lag that lengthens the cycle. This low can last 1–3 yr in microtines and 2–4 yr in hares. Understanding the low phase is critical in explaining population cycles. Two major classes of hypotheses try to account for the low phase. The first proposes that something may be “wrong” with the extrinsic environment. The most promising of these extrinsic explanations is that predation, acting either directly or indirectly, has delayed density-dependent effects on prey populations during the low phase. The second class of hypotheses proposes that something may be “wrong” with the animals themselves. The most likely intrinsic factors are maternal effects or age effects on fitness during the low phase. Experimental tests for each of these sets of hypotheses are needed, and we suggest replicated experiments on focal species in two continents to resolve these unknowns.

Stearic acid oxidation in the Alaskan red-backed vole: effects of cold and norepinephrine

Saturated fatty acids constitute a considerable energy reserve that could convey survival value under chronic cold exposure. It was investigated whether acclimation to cold was associated with a change in the ability of a small microtine rodent, the red-backed vole ( Clethrionomys rutilis), to increase the use of saturated fatty acids during thermogenesis. The C-14 labeled stearic acid, a typical saturated fatty acid (FA), was used to determine the rate of utilization through oxidation. In warm acclimated (WA, 20°C) and cold acclimated (CA, 5°C) voles, acute cold exposure (WA at 5°C, −2°; CA at −5°C) and norepinephrine (NE) injection increased metabolic rate ( V ̇ O 2 , V ̇ CO 2 ) and mobilization of lipid reserves. Acute cold exposure increased percent blood stearate oxidized in a linear fashion with both metabolic rate and stearate concentration in both WA and CA voles. The CA voles at 5°C had increased stearate irreversible loss (1.5×) and oxidation rate (2×) compared to WA voles at 20°C. The CA voles at −5°C increased stearate irreversible loss and oxidation linearly with metabolic rate and blood stearate concentration. In CA voles the contribution made by stearate oxidation to V ̇ CO 2 , increased with the level of cold exposure and NE injection. In contrast, for WA voles stearate irreversible loss and the contribution made by stearate oxidation to V ̇ CO 2 were unaffected by acute cold exposure. Thus, cold acclimation involves: (1) a modest increase (1.5×) in the use of stearate as a fuel substrate; and (2) a greater stearate oxidation and contribution to overall metabolism during acute cold exposure (−5°C).

Social organization of the vole Clethrionomys rufocanus and its demographic and genetic consequences: A review

AbstractRecent findings on the relationship between social interaction and demographic process in the gray‐sided vole Clethrionomys rufocanus are reviewed with reference to the findings in other microtine rodents. Social behavior was particularly focused on spacing and dispersal, and their effects on population dynamics are discussed. Female territoriality can limit a population abundance as a density‐dependent factor, although its regulatory effect is controversial. Female philopatry and male‐biased dispersal should bring about the clumped distribution of female relatives and genetically random distribution of males during the breeding season. The sexual difference in dispersal patterns can contribute to the mating behavior of the vole; promiscuous mating and low frequency of incestuous mating. However, effects of social structure, including kinship, on reproduction and survival of individuals still remains to be clarified. Molecular markers may help to solve these issues and provide new field of population ecology in microtine rodents.

Frontiers in population ecology of microtine rodents: A pluralistic approach to the study of population ecology

AbstractCurrent challenges for the study of population ecology of microtine rodents are reviewed. Comparisons with other taxonomic groups (other mammals, birds and insects) are given throughout. A major challenge is to link patterns and processes (i.e. mechanisms) better than is the case today. Other major challenges include the furthering of our understanding of the interaction between deterministic and stochastic processes, and as part thereof, the interaction between density‐dependent and density‐independent processes. The applicability of comparative studies on populations exhibiting different temporal dynamical patterns is, in this connection, emphasized. Understanding spatiotemporal dynamical patterns is another major challenge, not the least from a methodological point of view. Long‐term and large‐scale ecological data on population dynamics (in space and time) are critical for this purpose. Looking for consistency between hypothesized mechanisms and observed patterns is emphasized as a good platform for further empirical and theoretical work. The intellectual feedback process between different approaches to the study of microtine population ecology (observational studies, experimental manipulative studies, statistical modeling and mathematical modeling) are discussed. We recommend a pluralistic approach (involving both observational and experimental as well as theoretical studies) to the study of small rodent ecology.

Small mammals cycles in northern Europe: patterns and evidence for a maternal effect hypothesis

1. Voles undergo pronounced oscillations over periods of 3–5 years in northern Europe. A latitudinal gradient of cycle periods and amplitudes has been reported for Fennoscandia, with periods and amplitudes increasing towards northern latitudes. 2. This study formulates a discrete time model based on maternal effects to explain the density fluctuation patterns of microtine rodents. The phenotypic transmission of quality from mothers to offspring generates delayed density dependence, which produces cyclic behaviour in the model. 3. The dynamic patterns predicted by the maternal effect model agree with data. We conclude that the maternal effect hypothesis is a plausible, parsimonious explanation for vole‐density cycles in northern Europe.

DETERMINANTS OF GEOGRAPHIC VARIATION IN GROWTH AND REPRODUCTIVE TRAITS IN THE ROOT VOLE

I studied growth rate and reproduction in two geographically distinct strains of root voles, Microtus oeconomus, in the laboratory to unravel the mechanisms underlying the observed increase in body size from south to north among European microtine rodents. In the field, adult northern root voles are 51% heavier than southern. Many proximate and ultimate mechanisms underlying this geographic pattern have been suggested, but none has been adequately tested. I measured offspring growth rates in one northern and one southern strain over three consecutive laboratory generations, employing two separate experimental protocols (cross-mating and cross-fostering) to control for differential maternal investment. Paternal investment in the young was evaluated in separate tests. Northern root voles were larger at birth and grew faster than southern voles. Litter size and litter mass at birth were largest in the southern strain, when maternal body mass was adjusted for, indicating a larger prenatal reproductive expenditure in southern females. Cross-fostering and cross-breeding experiments demonstrated that the north-south difference in body mass is of genetic origin. Postnatal growth rate of cross-bred litters was intermediate between the two purebred strains, thus being consistent with an additive genetic mechanism. In contrast, neonatal mass of offspring from cross-bred pairs was similar to that of the southern strain, consistent with southern genetic dominance. Cross-fostering between the two strains showed that parental investment had no discernible effects on postnatal growth rate, although southern fathers showed more parental care than did northern fathers. Together, the cross-fostering and the cross-breeding experiments suggest that the growth rate of southern root voles was con- strained by their own genotype and not by the characteristics of their mothers. Low en- vironmental predictability in southern habitats and high productivity of northern habitats probably result in different selection pressures on growth rates and reproductive effort.

PATTERNS OF PREDATION ON NONCYCLIC LEMMINGS

Noncyclic populations of microtine rodents may be limited within a relatively constant range of densities by generalist predators with a prey base sufficiently diverse to sustain them when rodents are scarce (generalist predator hypothesis). Collared lemmings (Dicrostonyx kilangmiutak) at Pearce Point, Northwest Territories, Canada, are noncyclic and limited to fairly constant low densities in summer by predation, principally by red fox and Rough-legged Hawks. We tested four predictions of the generalist predator hypothesis as a possible explanation for relatively constant lemming densities: (1) predators do not show strong numerical responses to lemming density; (2) the proportion of lemming biomass in predator diets declines with declining lemming abundance, compensated for by increased consumption of alternative prey; (3) predators show a type-III functional response to lem- ming density; and (4) at low densities, predation on lemmings ceases. The first prediction was not satisfied by the principal predators: at very low lemming densities, Rough-legged Hawks did not settle, and breeding success of red foxes and hawks was limited by lemming abundance. However, a number of generalist predators (Golden Eagle, grizzly bear, arctic ground squirrel, Peregrine Falcon, and Gyrfalcon) did not respond numerically to the lowest lemming densities. The second prediction was partly supported: all predators consumed lemmings at a lower rate as lemming densities declined. However, Rough-legged Hawks were not able to compensate fully for the declining consumption by increasing their use of alternative prey, and red foxes were able to do so in one of three years. Regarding the third prediction, foxes showed some evidence of a type-III functional response but hawks did not. As for the fourth prediction, most predators still consumed lemmings at very low densities; lemmings lacked a secure refuge. The Pearce Point system differs from those where microtine dynamics are relatively constant and nonirruptive because of persistent predation by generalists. In terms of biomass, lemmings are the principal prey for their dominant predators. These predators (the semi- generalist red fox and the specialist Rough-legged Hawk) rely on lemmings to breed, but drive them to densities too low to sustain breeding by these same predators in the subsequent spring. In this regard, the system is similar to one driven by specialists. In some winters, however, populations recover because lemmings breed under the snow and most summer predators are absent. As a result, lemming densities in spring are often high enough for specialists and semigeneralists to initiate breeding. When winter breeding and survival fail to allow population growth, hawks and foxes may fail to breed and then leave the system. Even so, summer generalists still persist and continue to consume lemmings, curtailing potential irruptive growth. In this regard, the system is similar to one where prey are relatively constant because of generalists. Community dynamics at Pearce Point can best be understood as a combination of three dominant processes. Summer predation by specialists and semigeneralists results in desta- bilizing declines. Winter breeding, coupled with good survival, can lead to destabilizing growth. However, this growth is curtailed in the following summer by either destabilizing specialist predation or the stabilizing influence of generalist predation. When lemmings are scarce, the semigeneralist red fox and some generalist predators rely on arctic ground squirrels as their primary prey or their principal alternative prey. The ground squirrel appears to be the critical species maintaining this relatively diverse arctic tundra predator community and the relatively constant lemming densities.

Limit cycles in Norwegian lemmings: tensions between phase–dependence and density-dependence

Ever since Elton, the 3–5 year density cycles in lemmings (and other microtines) in Fennoscandia have troubled scientists. Explanations have involved intrinsic regulation and trophic interactions. We have analysed yearly changes in fall abundances for lemmings over 25 years from two local mountain sites in South Norway. These time series appear to have an underlying nonlinear structure of order two. Fitting a piece-wise linear threshold model of maximum order two, the most parsimonious model was, however, of first order for both series. The resulting dynamics from this model is a limit cycle. Reformulating the model in terms of abundances yields a model which combines (delayed) density-dependent effects and the influence of the cyclic phase. The delayed density-dependence of one part of the model is consistent with an effect of specialist predators during the peak and crash phases of the cycle, although other trophic interactions cannot be excluded.

Cross-species amplification of microsatellite DNA in Old World microtine rodents with PCR primers for the gray-sided vole, Clethrionomys rufocanus.

Cross-species amplification of microsatellite DNA in Old World microtine rodents with PCR primers for the gray-sided vole, Clethrionomys rufocanus.

Is spacing behaviour coupled with predation causing the microtine density cycle? A synthesis of current process-oriented and pattern-oriented studies.

Current ecological information on periodically fluctuating microtine populations are demonstrated to support a hypothesis involving both predation and intrinsic self-regulation as necessary and sufficient factors for explaining the "microtine density cycle'. The structure of the cyclic time series is largely two dimensional with strong delayed density dependence. Together with recent field studies on rodent demography, our modelling suggests that trophic interaction is a likely candidate to generate the dimensionality observed for northern microtine rodent dynamics. It is shown that the trophic interaction must be fairly strong. This suggests that specialist predation is the most likely one among the classes of trophic interactions. We also argue that some - but not too strong - self-regulation must occur to generate the structure of the available time series on northern European microtines.

Why lemmings have indoor plumbing in summer

The faeces and urine of microtine rodents are visible in ultraviolet light, and diurnal raptors, such as European kestrels (Falco tinnunculus) and rough-legged buzzards (Buteo lagopus), have the ability to see in ultraviolet light. It has been reported that in Fennoscandia, these raptors use this ability to concentrate their hunting activity in spring on areas where microtines are abundant. We hypothesized that in arctic tundra areas in summer, intense avian predation pressure and short vegetation should select for microtine behaviour that would minimize their exposure to these raptors. We dug up 62 collared lemming (Dicrostonyx groenlandicus) burrows in the Canadian Arctic and all had underground latrines. Latrines are not hidden underground in winter, when lemmings live under the snow, build nests above ground, and defecate above ground, nor does this occur in microtine species living in temperate areas, where summer vegetation growth is greater. Thus, high predation risk may influence not only where prey forage but also where they defecate.

Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: A quantitative comparative study

The genus Microtus includes several closely related species of voles with diverse patterns of social organization. Comparative studies of these species have previously tested hypotheses related to the evolution of monogamy and affiliation. In earlier studies, monogamous voles have been reported to differ from closely related nonmonogamous voles in the neural distribution of oxytocin and vasopressin receptors. These receptors have also been implicated in the behavioral differences relevant to monogamy, as oxytocin and vasopressin influence pair-bond formation in the monogamous species. In the current study, two monogamous and two nonmonogamous vole species were compared for the distribution of oxytocin and vasopressin immunoreactivity. Contrary to our predictions, gender dimorphisms in vasopressin immunoreactivity were as evident in the monogamous as in the nonmonogamous species. Also, species differences in oxytocin and vasopressin staining were subtle relative to the profound species differences previously reported for receptor binding. These results are consistent with the hypothesis that neuroendocrine systems may evolve by changes in receptor distribution rather than by restructuring the presynaptic pathway. © 1996 Wiley-Liss, Inc.

Experimental analysis of behaviour of meadow voles (Microtus pennsylvanicus) to odours of the short-tailed weasel (Mustela erminea)

Abstract:Studies of the indirect effect of predators, particularly mustelids, on microtine rodents has not received as much attention as direct effects. Here we present the results of three experiments (two laboratory and one outdoor enclosure) of the response of two meadow vole populations, one from an island devoid of terrestrial predators and one from the mainland with terrestrial predators, to the odour of the short-tailed weasel. Meadow voles from both populations avoided weasel odours under laboratory conditions but not in the field experiment. The response to weasel odours appeared to be short term. Although weasels represent a real danger to voles, odours left by these predators may only represent a strong short-term avoidance stimulus. The implications of these findings are discussed.

Invasion of the Meadow Vole (Microtus pennsylvanicus) in Southeastern Kentucky and Its Possible Impact on the Southern Bog Lemming (Synaptomys cooperi)

-Robinson Forest is a 4450-ha eastern deciduous forest located in southeastern Kentucky on the Cumberland Plateau. Historically, the southern bog lemming (Synaptomys coopen) was the dominant microtine rodent in forest clearings. However, within the last 15 yr, the meadow vole (Microtus pennsylvanicus) has expanded its range southward into southeastern Kentucky and has invaded clearings in Robinson Forest. Recent trapping efforts revealed that M. pennsylvanicus was the most abundant microtine in clearings, accounting for 48% of all small mammals caught. It invaded an isolated, grass-dominated clearing within 3 yr of tree removal. By contrast, S. cooperi was the most rarely caught small mammal in these clearings and tended to occupy herb-dominated clearings where fewer M. pennsylvanicus occurred. Synaptomys cooperi has become rarer since the arrival of M. pennsylvanicus, possibly due to competitive exclusion. Extensive deforestation, coupled with a 50-yr period of climatic cooling, may have led to the range expansion of M. pennsylvanicus.

Chaos in microtine populations

On the basis of nonlinear time-series analysis of vole data, Turchin (1993) proposed that there is a latitudinal shift from stability to chaos in the dynamics of vole populations. Falck et al. (1995) question several aspects of the approach I used. In particular, they point out that no measure of uncertainty has been calculated for each point estimate of the dominant Lyapunov exponent (a positive Lyapunov exponent implies chaos, while a negative one implies stability). In this note I respond to the criticisms of Falck et al. (1995). As part of my response, I analyse fluctuations of pooled numbers of microtine rodents at all European locations for which I currently have data. Treating each geographic location as a replicate, I show that the mean Lyapunov exponent is significantly greater than zero in northern populations (latitude greater than 60 degrees N).

Isla Vista virus: a genetically novel hantavirus of the California vole Microtus californicus.

Prospect Hill virus (PH) was isolated from a meadow vole (Microtus pennsylvanicus) in 1982, and much of its genome has been sequenced. Hantaviruses of other New World microtine rodents have not been genetically characterized. We show that another Microtus species (the California vole M. californicus) from the United States is host to a genetically distinct PH-like hantavirus, Isla Vista virus (ILV). The nucleocapsid protein of ILV differs from that of PH by 11.1% and a portion of the G2 glycoprotein differs from that of PH by 19.6%. ILV antibodies were identified in five of 33 specimens of M. californicus collected in 1975 and 1994-1995. Enzymatic amplification studies showed that 1975 and 1994-1995 ILV genomes were highly similar. Secondary infection of Peromyscus californicus was identified in Santa Barbara County, California. A long-standing enzootic of a genetically distinct hantavirus lineage is present in California voles.