Phylogenetic assessment within a species complex of a subterranean rodent (Geomys bursarius) with conservation implications for isolated subspecies.

Range contraction and expansion from glaciation has led to genetic divergence that may be particularly pronounced in fossorial species with low dispersal. The plains pocket gopher (Geomys bursarius) is a fossorial species that ranges widely across North America but has a poorly understood phylogeny. We used mitogenomes (14,996 base pairs) from 56 individuals across seven subspecies, plus two outgroup species, to assess genetic divergence from minimum spanning trees, measure genetic distances, and infer phylogenetic trees using BEAST. We found G. b. wisconsinensis was monophyletic with recent divergence. Further assessment is needed for G. b. major because it was paraphyletic and exhibited inconsistent groupings with other clades. Importantly, we identified G. b. illinoensis as being genetically distinct and monophyletic likely due to a unique colonization event eastward across the Mississippi River. Because G. b. illinoensis faces continued pressures from niche reduction and habitat loss, we recommend that G. b. illinoensis be considered an evolutionary significant unit warranting conservation actions to promote connectivity and restore suitable habitat. Such conservation efforts should benefit other grassland species including those originating from clades west of the Mississippi River that may also be evolutionary significant units.

Testing the niche reduction hypothesis for a fossorial rodent (Geomys bursarius) experiencing agricultural intensification.

Habitat loss and fragmentation from conversion to agriculture are known threats to grassland species. However, continued agricultural intensification may further reduce a species distribution and realized niche. Here, we create species distribution models (SDMs) for the plains pocket gopher (Geomys bursarius), an ecosystem engineer in grasslands, for historic and contemporary eras in a dynamic agroecosystem and test the "niche reduction hypothesis." We compare SDMs created from gopher occurrences from the historic era (~1950s, pre-agricultural intensification) and the contemporary era (post-agricultural intensification) and assess model transferability. We evaluate shifts in environmental relationships, changes in limiting factors, and an overall decline in niche hypervolume. SDMs were nontransferable between the historic and contemporary eras. Environmental drivers of gopher distribution shifted from elevation, precipitation, and land cover in the 1950s to land cover, soil texture, and soil drainage presently. There also were shifts in environmental associations with gophers now occurring at lower elevations, in sandier soils, and less often in agriculture. Dominant limiting factors of gophers shifted from precipitation to land cover. Gophers were not detected at historic locations during recent resurveys. Contemporary niche hypervolume was reduced compared with the historic niche hypervolume. We found support for the niche reduction hypothesis for a fossorial, grassland species. Further application of the niche reduction hypothesis in landscapes experiencing agricultural intensification is warranted. Understanding niche reduction allows for conservation efforts that promote continued persistence in the contemporary niche while also identifying areas to restore within the historic niche.

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.

Declines in rodent abundance and diversity track regional climate variability in North American drylands.

Regional long-term monitoring can enhance the detection of biodiversity declines associated with climate change, improving future projections by reducing reliance on space-for-time substitution and increasing scalability. Rodents are diverse and important consumers in drylands, regions defined by the scarcity of water that cover 45% of Earth's land surface and face increasingly drier and more variable climates. We analyzed abundance data for 22 rodent species across grassland, shrubland, ecotone, and woodland ecosystems in the southwestern USA. Two time series (1995-2006 and 2004-2013) coincided with phases of the Pacific Decadal Oscillation (PDO), which influences drought in southwestern North America. Regionally, rodent species diversity declined 20%-35%, with greater losses during the later time period. Abundance also declined regionally, but only during 2004-2013, with losses of 5% of animals captured. During the first time series (wetter climate), plant productivity outranked climate variables as the best regional predictor of rodent abundance for 70% of taxa, whereas during the second period (drier climate), climate best explained variation in abundance for 60% of taxa. Temporal dynamics in diversity and abundance differed spatially among ecosystems, with the largest declines in woodlands and shrublands of central New Mexico and Colorado. Which species were winners or losers under increasing drought and amplified interannual variability in drought depended on ecosystem type and the phase of the PDO. Fewer taxa were significant winners (18%) than losers (30%) under drought, but the identities of winners and losers differed among ecosystems for 70% of taxa. Our results suggest that the sensitivities of rodent species to climate contributed to regional declines in diversity and abundance during 1995-2013. Whether these changes portend future declines in drought-sensitive consumers in the southwestern USA will depend on the climate during the next major PDO cycle.

Rapid genetic restoration of a keystone species exhibiting delayed demographic response.

Genetic founder effects are often expected when animals colonize restored habitat in fragmented landscapes, but empirical data on genetic responses to restoration are limited. We examined the genetic response of banner-tailed kangaroo rats (Dipodomys spectabilis) to landscape-scale grassland restoration in the Chihuahuan Desert of New Mexico, USA. Dipodomys spectabilis is a grassland specialist and keystone species. At sites treated with herbicide to remove shrubs, colonization by D. spectabilis is slow and populations persist at low density for ≥10 years (≥6 generations). Persistence at low density and low gene flow may cause strong founder effects. We compared genetic structure of D. spectabilis populations between treated sites and remnant grasslands, and we examined how the genetic response to restoration depended on treatment age, area, and connectivity to source populations. Allelic richness and heterozygosity were similar between treated sites and remnant grasslands. Allelic richness at treated sites was greatest early in the restoration trajectory, and genetic divergence did not differ between recently colonized and established populations. These results indicated that founder effects during colonization of treated sites were weak or absent. Moreover, our results suggested founder effects were not mitigated by treatment area or connectivity. Dispersal is negatively density-dependent in D. spectabilis, and we hypothesize that high gene flow may occur early in the restoration trajectory when density is low. Our study shows genetic diversity can be recovered more rapidly than demographic components of populations after habitat restoration and that founder effects are not inevitable for animals colonizing restored habitat in fragmented landscapes.

Summer Precipitation Predicts Spatial Distributions of Semiaquatic Mammals.

Climate change is predicted to increase the frequency of droughts and intensity of seasonal precipitation in many regions. Semiaquatic mammals should be vulnerable to this increased variability in precipitation, especially in human-modified landscapes where dispersal to suitable habitat or temporary refugia may be limited. Using six years of presence-absence data (2007-2012) spanning years of record-breaking drought and flood conditions, we evaluated regional occupancy dynamics of American mink (Neovison vison) and muskrats (Ondatra zibethicus) in a highly altered agroecosystem in Illinois, USA. We used noninvasive sign surveys and a multiseason occupancy modeling approach to estimate annual occupancy rates for both species and related these rates to summer precipitation. We also tracked radiomarked individuals to assess mortality risk for both species when moving in terrestrial areas. Annual model-averaged estimates of occupancy for mink and muskrat were correlated positively to summer precipitation. Mink and muskrats were widespread during a year (2008) with above-average precipitation. However, estimates of site occupancy declined substantially for mink (0.56) and especially muskrats (0.09) during the severe drought of 2012. Mink are generalist predators that probably use terrestrial habitat during droughts. However, mink had substantially greater risk of mortality away from streams. In comparison, muskrats are more restricted to aquatic habitats and likely suffered high mortality during the drought. Our patterns are striking, but a more mechanistic understanding is needed of how semiaquatic species in human-modified ecosystems will respond ecologically in situ to extreme weather events predicted by climate-change models.

Risk factors for Toxoplasma gondii exposure in semiaquatic mammals in a freshwater ecosystem.

We assessed risk factors for Toxoplasma gondii exposure in semiaquatic mammals in east-central Illinois, US. This agricultural region has extensive drainage systems that could potentially transport T. gondii oocysts into the watershed. We used muskrats (Ondatra zibethicus) and American mink (Neovison vison) as sentinels of watershed contamination. We predicted individuals from larger subwatersheds would more likely be antibody-positive for T. gondii, as they were exposed to drainage from larger areas. We also evaluated amount of urban land cover within the subwatershed, proximity to farmsteads, and age of individuals in competing models of T. gondii infection. Antibodies to T. gondii were assayed in animal sera by modified agglutination tests (titer 25 or higher) and detected in 18 (60%) of 30 muskrats and 20 (77%) of 26 mink. Infection rates were ≥1.7 times higher than those typical for mammals in upland habitats in this region. Subwatershed size and age class were important predictors of T. gondii infection in muskrats (R(2) = 0.35). Models incorporating urban land cover and proximity to farmsteads had little support. None of our models of antibody prevalence in mink were well supported, possibly because mink are less strictly associated with riparian habitats. Because ~91% of our study area is devoted to agricultural production and urbanization, transport of T. gondii into freshwater ecosystems is likely facilitated by modified drainage practices common in these areas.

Restoration Practices Have Positive Effects on Breeding Bird Species of Concern in the Chihuahuan Desert.

Woody plant encroachment into grasslands is a global concern. Efforts to restore grasslands often assume that removal of woody plants benefits biodiversity but assumptions are rarely tested. In the Chihuahuan Desert of the Southwestern United States, we tested whether abundances of grassland specialist bird species would be greater in plant communities resulting from treatment with herbicides to remove encroaching shrubs compared with untreated shrub-dominated areas that represented pre-treatment conditions. In 2010, we surveyed breeding birds and vegetation at 16 treated-untreated pairs. In 2011, we expanded the survey effort to 21 treated-untreated pairs, seven unpaired treatment areas, and five reference grassland areas. Vegetation in treatment areas had higher perennial grass foliar and basal cover and lower shrub foliar cover compared with untreated areas. Several regionally declining grassland specialists exhibited higher occurrence and relative abundance in treated areas. A shrubland specialist, however, was associated with untreated areas and may be negatively impacted by shrub removal. Bird community composition differed between treated and untreated areas in both years. Our results indicate that shrub removal can have positive effects on grassland specialist bird species, but that a mosaic of treated and untreated areas might be most beneficial for regional biodiversity.

Linking extinction-colonization dynamics to genetic structure in a salamander metapopulation.

Theory predicts that founder effects have a primary role in determining metapopulation genetic structure. However, ecological factors that affect extinction-colonization dynamics may also create spatial variation in the strength of genetic drift and migration. We tested the hypothesis that ecological factors underlying extinction-colonization dynamics influenced the genetic structure of a tiger salamander (Ambystoma tigrinum) metapopulation. We used empirical data on metapopulation dynamics to make a priori predictions about the effects of population age and ecological factors on genetic diversity and divergence among 41 populations. Metapopulation dynamics of A. tigrinum depended on wetland area, connectivity and presence of predatory fish. We found that newly colonized populations were more genetically differentiated than established populations, suggesting that founder effects influenced genetic structure. However, ecological drivers of metapopulation dynamics were more important than age in predicting genetic structure. Consistent with demographic predictions from metapopulation theory, genetic diversity and divergence depended on wetland area and connectivity. Divergence was greatest in small, isolated wetlands where genetic diversity was low. Our results show that ecological factors underlying metapopulation dynamics can be key determinants of spatial genetic structure, and that habitat area and isolation may mediate the contributions of drift and migration to divergence and evolution in local populations.

Hematologic and blood chemistry reference values for free-ranging muskrats (Ondatra zibethicus).

Baseline hematologic and serum chemistry values are used by veterinarians and wildlife biologists to identify abnormally high or low levels of particular blood parameters in a target species. This vital information can assist animal care providers in making informed decisions on the care of wildlife and help to determine diagnoses for certain illnesses. Published blood parameter values are not available for wild-caught muskrats (Ondatra zibethicus). We measured 27 blood parameter values from 29 free-ranging, riparian muskrats caught from June-November 2008 in east-central Illinois, USA, and compared mean values between adults and juveniles. Adult muskrats had higher levels of globulins (F(1,27)=6.394, P ≤ 0.018) and eosinophils (F(1,25)=6.883, P ≤ 0.015) than did juvenile muskrats, possibly because of increased exposure to parasites and allergens over time.

Prevalence of antibodies to Toxoplasma gondii in woodchucks across an urban-rural gradient.

Increasing urbanization has important consequences for wildlife, including the potential for higher prevalence of diseases within "urban adapter" species exposed to spillover from domestic animals. We investigated whether prevalence of antibodies to Toxoplasma gondii in woodchucks (Marmota monax) was related to urbanization in a Midwestern landscape. We collected serum samples from adult woodchucks captured across an urban-rural gradient in Illinois, USA in May-November 2007. We used an indirect fluorescent antibody test (IFAT) on the serum samples to detect T. gondii antibodies. Five of 35 (14.3%) sera from woodchucks had detectable T. gondii antibodies. Prevalence was related positively to urbanization. All positive samples were from individuals inhabiting areas in which urban land cover exceeded 70%. Urban woodchucks are likely exposed to high levels of T. gondii oocysts in the environment due to habitat overlap with the definitive hosts for the parasite, domestic and feral cats, which reach high densities in urban areas.

Enhancing the area-isolation paradigm: habitat heterogeneity and metapopulation dynamics of a rare wetland mammal.

Conservation of species in fragmented landscapes often is guided by spatially realistic metapopulation theory. However, convincing cases of metapopulation dynamics are uncommon, especially for vertebrates. Moreover, there is concern that the patch area and isolation paradigm for metapopulations is an oversimplification for heterogeneous landscapes. We tested predictions from metapopulation theory for a rare wetland mammal (round-tailed muskrat, Neofiber alleni) and asked whether it was necessary to use a habitat-informed version of the area-isolation paradigm that included patch quality and matrix heterogeneity. In each of two years, we surveyed 457 isolated wetlands in central Florida, USA, for presence-absence of Neofiber and evaluated logistic regression models of patch occupancy, extinction, and colonization. We documented metapopulation dynamics in which patch occupancy was constant between years (26% of patches occupied) due to balanced local extinctions (n = 45) and recolonizations (n = 46). Neofiber was both habitat and dispersal limited. Local extinctions were related negatively to patch area, patch quality (cover of maidencane grass, Panicum hemitomon), and distance to nearest roadside ditch. Patch colonization depended on patch area, patch quality, and spatial connectivity to potential source wetlands. Despite the importance of patch quality, Neofiber did not exhibit a habitat-tracking metapopulation on an annual time scale. Cost-distance modeling suggested effective distances that included high costs for moving through forested matrix habitats generally were better than Euclidean distances for predicting patch colonization and occupancy. Two dominant land uses were tied to turnover dynamics: cattle grazing decreased habitat quality of wetlands, and presence of pine (Pinus spp.) plantations decreased functional connectivity. The simple area-isolation paradigm was not adequate for characterizing spatial dynamics of the Neofiber metapopulation. Nevertheless, we contend that the metapopulation approach remains a useful conservation framework for many species if landscape heterogeneity is embraced and explicit effects of land-use practices on turnover processes are considered.