Population connectivity in voles (Microtus sp.) as a gauge for tall grass prairie restoration in midwestern North America

Ecological restoration can promote biodiversity conservation in anthropogenically fragmented habitats, but effectiveness of these management efforts need to be statistically validated to determine ’success.’ One such approach is to gauge the extent of recolonization as a measure of landscape permeability and, in turn, population connectivity. In this context, we estimated dispersal and population connectivity in prairie vole (Microtus ochrogaster; N = 231) and meadow vole (M. pennsylvanicus; N = 83) within five tall-grass prairie restoration sites embedded within the agricultural matrix of midwestern North America. We predicted that vole dispersal would be constrained by the extent of agricultural land surrounding restored habitat patches, spatially isolating vole populations and resulting in significant genetic structure. We first employed genetic assignment tests based on 15 microsatellite DNA loci to validate field-derived species-designations, then tested reclassified samples with multivariate and Bayesian clustering to assay for spatial and temporal genetic structure. Population connectivity was further evaluated by calculating pairwise FST, then potential demographic effects explored by computing migration rates, effective population size (Ne), and average relatedness (r). Genetic species assignments reclassified 25% of initial field identifications (N = 11 M. ochrogaster; N = 67 M. pennsylvanicus). In M. ochrogaster population connectivity was high across the study area, reflected in little to no spatial or temporal genetic structure. In M. pennsylvanicus genetic structure was detected, but relatedness estimates identified it as kin-clustering instead, underscoring social behavior among populations rather than spatial isolation as the cause. Estimates of Ne and r were stable across years, reflecting high dispersal and demographic resilience. Combined, these metrics suggest the agricultural matrix is highly permeable for voles and does not impede dispersal. High connectivity observed confirms that the restored landscape is productive and permeable for specific management targets such as voles and also demonstrates population genetic assays as a tool to statistically evaluate effectiveness of conservation initiatives.

Metapopulation connectivity in Voles (Microtus sp.) as a gauge for tallgrass prairie restoration in midwestern North America

Applying quantifiable metrics to validate the success of restoration efforts is crucial for ongoing management programs in anthropogenically fragmented habitats. Estimates of dispersal can provide such baseline data because they measure not only the extent to which restored patches are colonized and interconnected, but also their metapopulation source/sink dynamics. In this context, we estimated dispersal and population connectivity among prairie (Microtus ochrogaster; N=231) and meadow vole (M. pennsylvanicus; N=83), sampled from eight restored plots at five tallgrass prairie sites embedded within the agricultural matrix of midwestern North America. Our expectation was that extensive distances separating these restored habitats (i.e., 48–246 km) would spatially isolate vole metapopulations, resulting in significant genetic differentiation. We first used molecular taxonomy to validate the field-identifications of all sampled individuals, then used pairwise FST derived from 15 microsatellite DNA loci to estimate genetic connectivity among the species-delimited study populations. Metapopulation stability was gauged by assessing migration rates and deriving effective population sizes (Ne). We also calculated relatedness values (r) as a potential surrogate for contact in prairie vole, a primary vector for Lyme disease. Molecular species-assignments contravened field-identifications in 25% of samples (11 prairie/67 meadow) and identified two instances of species-hybridization (0.6%). Local effects (i.e., population crash/drought) were manifested at two sites, as documented by significant temporal declines in Ne and r. Overall, high migration rates and non-significant (10/15) pairwise FST values underscored elevated metapopulation connectivity. A single site that recorded five significant FST values also displayed significant r-values indicating the inadvertent sampling of closely related individuals. This highlights the close social groupings among cooperatively-breeding prairie vole that can exacerbate Lyme disease transmission. Thus, while elevated population connectivity aligns with prairie restoration goals, it also reinforces a need in adaptive management to evaluate environmental matrices for their permeability to vector-borne diseases.

Bison (Bison bison) activity fragments subnivean tunnels of small mammals

Ecological interactions between ungulates and small mammals are generally not well understood. Here, we report an observation of unusually extensive small mammal (likely Meadow Vole [Microtus pennsylvanicus] or Tundra Vole [Microtus oeconomus]) tracks above the snow, exiting from trails and bed sites created by Bison (Bison bison) in northern Canada. We believe that weather and snow conditions were optimal for this observation. Although alteration of above-snow activity of small mammals in response to snow compaction by ungulates is probably not a rare event, it is not often reported. The effect on voles of exiting their subnivean tunnels as a result of Bison activity is unclear, but may be detrimental to their overwinter survival. Ungulate activity compacts snow, fragmenting small mammal tunnels resulting in loss of their insulative value for voles, and making it harder for them to dig new tunnels. Clearly, determining the effect of snow disturbance by gregarious ungulates on voles or other microtines, particularly regarding their overwinter survival, requires detailed investigation. Nevertheless, this observation provides new information on the ecological interactions between ungulates and small mammals, particularly from the boreal forest, where such information is largely lacking.

A precarious future for distinctive peripheral populations of meadow voles (Microtus pennsylvanicus)

Conservation efforts rely on robust taxonomic assessments that should be based on critical assessment of interspecific boundaries, infraspecific variation, and potentially distinctive peripheral populations. The meadow vole (Microtus pennsylvanicus) is widely distributed across North America, including 28 morphologically defined subspecies and numerous isolated populations. Because some subspecies are of high conservation concern, we examined geographic variation across the range of the species to test existing infraspecific taxonomy in terms of local and regional diversification. We sequenced mitochondrial DNA (mtDNA) from 20 subspecies of M. pennsylvanicus and contextualized infraspecific variation through comparison of pairwise genetic distances derived from an extended data set of 63 species of Microtus. We found strong support for at least three divergent clades within M. pennsylvanicus, with observed intraspecific clade divergence exceeding that between several pairwise comparisons of sister species within Microtus. Six nuclear genes were then sequenced to test the validity of mtDNA structure and to further evaluate the possibility of cryptic, species-level diversity using Bayes factor species delimitation (BFD) analyses. BFD consistently and decisively supported multiple species based on the multilocus approach. We propose that taxonomic revision of the meadow vole is required, with the eastern clade now identified as M. pennsylvanicus (Ord 1815), the western clade as M. drummondii (Audubon and Bachman 1853), and the coastal Florida clade as M. dukecampbelli (Woods, Post, and Kilpatrick 1982). We suggest that such an arrangement would more closely reflect evolutionary history and provide critical context for further examination of distinctive southern peripheral populations that harbor novel evolutionary legacies and adaptive potential.

Understanding Habitat Quality for Preble's Meadow Jumping Mouse: How Survival Responds to Vegetation Structure and Composition

Habitat loss is the primary conservation concern for many rare species; yet, it is unclear what habitat components are vital for the persistence of many rare species. The Preble's meadow jumping mouse Zapus hudsonius preblei (PMJM) was listed as Threatened under the Endangered Species Act because of habitat loss in Colorado and Wyoming. The PMJM is restricted to dense shrub cover and dense herbaceous vegetation along wetland and riverine systems. Although it is well established by researchers that PMJM infrequently leave these habitat types, it is unclear what riparian vegetation structure and composition is important to PMJM survival. We collected and analyzed a 14-y PMJM vegetation-monitoring data set and a PMJM mark–recapture data set to assess the influence of vegetation structure and composition on PMJM annual survival. Using individual, group, and site-specific covariates we estimated survival and evaluated the influence of such covariates on annual survival. Annual survival for PMJM was low (< 10%), increasing with body mass, grass cover, and shrub cover, and decreasing with meadow vole Microtus pennsylvanicus captures. The PMJM use of and occupation of dense riparian habitats may increase individual survival, and likely increases population persistence. Thus, habitat modifications that reduce grass cover and shrub regeneration, such as grazing, suburban development, and development-altered hydrology, will be detrimental to PMJM populations. Given the low annual survival of PMJM, it is important for conserving PMJM populations to minimize disturbances to the vegetation structure, composition, and density, and the hydrologic processes that support them.

Body mass and attractivity of female offspring are negatively affected by food restriction of meadow vole (Microtus pennsylvanicus) dams during lactation

The environment experienced by pups during lactation (nutrition and maternal behaviour) can contribute not only to sexual development, but also to individual differences in offspring sexual behaviour. We tested the hypothesis that female offspring of meadow vole dams (Microtus pennsylvanicus) that were 30% food restricted (FR) during days 1–7 of lactation (FR 1–7), days 8–14 of lactation (FR 8–14), or days 15–21 of lactation (FR 15–21) show negative effects on their food intake, growth, and the three components of sexual behaviour (attractivity, proceptivity and receptivity) as compared with female offspring of control dams. With the exception of age 29 days or age 34 days, the body weights of female offspring of FR 1–7 dams and FR 8–14 dams between days 21 and 48 were lower than the body weights of female offspring of FR 15–21 dams and those of control dams. Female offspring of FR 1–7 dams maintained a lower body weight than the other female offspring throughout the study. Female offspring of FR 8–14 and FR 15–21 dams produced odours that were less attractive to males than odours produced by those of FR 1–7 and control dams. Female offspring of FR dams and control dams did not differ in their measures of proceptivity and receptivity. However, the total amount of time allocated for copulation by males was shorter for those males that were paired with female offspring of FR 1–7 dams than it was for those that were paired with the female offspring of FR 8–14, FR15–21, and control dams. The results of this study, coupled with those found in a study conducted on the male offspring of FR dams, indicate that for female offspring days 1–7 and for male offspring days 8–14 of lactation are the time periods during which food restriction of dams had the greatest impact on deficits in sexual behaviour and body mass in meadow voles.

Parental behaviour of prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus) in relation to sex of offspring

Monogamous parents are predicted to invest equally in male and female offspring whereas polygynous parents in good condition are predicted to invest more in male than female offspring. Sex-biased parental investment can occur in three ways: (1) mothers and fathers invest different amounts of care in their offspring (effect of parent sex); (2) parents invest different amounts of care in male and female offspring (effect of offspring sex); and (3) one parent, but not the other, invests different amounts of care in male and female offspring (interaction between parent sex and offspring sex). Studies of parent–offspring interactions in rodents have focused on either effect of parent sex or effect of offspring sex, but not the interaction between parent sex and offspring sex, and most studies have examined only one species. We studied prairie voles (Microtus ochrogaster), a monogamous species, and meadow voles (M. pennsylvanicus), a polygynous (or promiscuous) species, under laboratory conditions designed to simulate field conditions. For each species, we recorded the frequency and duration with which mothers and fathers licked their male and female offspring. We found that meadow vole fathers licked male offspring for longer durations than female offspring. However, prairie vole fathers, prairie vole mothers, and meadow vole mothers did not lick male and female pups for different durations. From the standpoint of the pups, male prairie vole pups, female prairie vole pups, and female meadow vole pups were licked for longer durations by their mothers than by their fathers. In contrast, for male meadow vole pups there was no difference in the duration with which they were licked by mothers and fathers. We also detected effects of litter size: as litter size increased, the frequency and duration of pup licking decreased for mothers and increased for fathers. For duration (but not frequency) of pup licking, these changes were more dramatic in meadow voles than in prairie voles. Our data are generally consistent with predictions that monogamous parents, such as prairie voles, should invest equally in male and female offspring whereas polygynous (or promiscuous) parents, such as meadow voles, should invest more in male offspring when conditions are favourable. Our data also highlight the complexity of parent–offspring interactions in rodents and emphasize the need to examine whether male and female offspring within a species differ in their behaviour or ability to obtain parental care.

Fertilisation, cattle grazing and voles: collapse of meadow vole populations in young forests?

Context A puzzling aspect of microtine population fluctuations is the damping out or collapsing of cycles over the last three decades, particularly in northern Europe. Occasional population fluctuations of Microtus may also have been damped out in temperate and boreal forests of the Pacific North-west of North America. One cause might be the presence of cattle (Bos taurus) grazing in forest habitats that offer summer forage. Aims We tested hypotheses (H) that abundance, population fluctuations, and demographic parameters of reproduction, recruitment and survival, of Microtus pennsylvanicus would be driven by understory plant productivity. Two predictions follow from this hypothesis: (H1) enhanced abundance and demography in fertilised stands, and (H2) reduced abundance and demography in stands with cattle grazing. Methods Study areas were located in ‘grazed’ and ‘ungrazed’ young forests in south-central British Columbia, Canada. Each study area had four replicate units of unfertilised and repeatedly fertilised stands. Herbaceous vegetation and meadow vole (M. pennsylvanicus) populations were sampled from 1993 to 2002. Key results Mean abundance of total herbs, grasses, and fireweed (Epilobium angustifolium) increased dramatically (8 to 34 times higher) with fertilisation in the ungrazed stands. Mean abundance of meadow voles was 3.1 to 8.5 times higher in the nutrient-enriched herbaceous vegetation in the ungrazed fertilised than grazed fertilised stands. Demographic variables also followed this pattern of abundance. Except for two years, mean abundance of meadow voles was similar between fertilised and unfertilised stands at the grazed area, with some degree of fluctuations generated in grazed stands. Thus, H1 and H2 were at least partly supported for M. pennsylvanicus in fertilised stands. Conclusions In high-quality habitats where cover and other attributes of vegetation are substantial enough to generate population increases and fluctuations of Microtus, grazing of vegetation by cattle or other livestock may indeed lead to potential collapse of fluctuations. Degree of grazing pressure would be crucial, but considering the widespread nature of grazing in the continuum of post-harvest forested sites in the Pacific North-west of North America, moderate to heavy grazing pressure is common. Implications Reductions in populations of microtines have serious consequences for predator communities and other ecological functions.

Ecological correlates of stress for a habitat generalist in a biofuels landscape

Understanding the success of habitat generalist species requires knowledge of how individuals respond to stressors that vary across habitats within landscapes. Habitat structure can affect stress by altering predation risk, conspecific densities, and densities of heterospecific competitors. Increased demand for biofuels will alter habitat structure for species in agroecosystems worldwide. We measured stress responses of deer mice (Peromyscus maniculatus (Wagner, 1845)), a widespread habitat generalist, in a biofuels landscape. We quantified fecal corticosterone concentrations for individuals in four biofuel crops: switchgrass (Panicum virgatum L.), miscanthus (Miscanthus × giganteus Greef & Deuter ex Hodkinson & Renvoize), mixed prairie, and corn (Zea mays L.). We also evaluated stress responses of deer mice to the annual harvesting of corn. Deer mice inhabiting switchgrass and mixed prairie had higher fecal corticosterone concentrations compared with mice in corn and miscanthus. Fecal corticosterone concentrations correlated positively with abundances of conspecifics and behaviorally dominant voles (prairie vole, Microtus ochrogaster (Wagner, 1842); meadow vole, Microtus pennsylvanicus (Ord, 1815)) across habitats. Stress levels of deer mice depended on how habitat structure modified the competitive environment. Deer mice did not exhibit increased fecal corticosterone concentrations in response to corn harvest, a rapid and extensive habitat disturbance common to agroecosystems. Our research is the first to investigate how landscape change due to biofuels expansion can affect stress levels of individuals.

Coat color and its effect on preference for the scent marks of opposite-sex conspecifics in the meadow vole Microtus pennsylvanicus

Many mammal species can distinguish between opposite-sex conspecifics that differ in a certain trait. In that coat coloration is associated with differences in physiological and behavioral traits, coat color may affect the attractiveness of odor cues produced by conspecifics. Individuals may be able to respond preferentially to conspecifics with a particular coat color. In the present study, we test the hypothesis that scent marks of brown and blond voles differ in their attractiveness to male and female conspecifics. Male voles and brown females did not discriminate between blond- and brown-coated opposite-sex conspecifics suggesting that they are neither selecting potential mates dissociatively nor associatively. However, blond females behaved as if the scent marks of blond males were more attractive than were the scent marks of brown males. Our data suggest that blond females who are already conspicuous to predators, may select blond males as mates because they do not appreciably increase the risk of detection to predators, particularly avian predators. Moreover, because these conspicuous males have survived to mate they may have good genes that reflect their relatively higher quality [Current Zoology 58 (2): 221–227 , 2012].