Zapus Princeps Research Articles

Hibernation: Insights from Comparative Genomics of Zapus Species

Hibernating mammals employ unique metabolic strategies to survive harsh conditions. They become obese prior to the onset of winter, then conserve their stored energy during a long winter fast by slowing metabolism and becoming deeply hypothermic. Hibernation phenotypes may provide insights into control of metabolism and have applications in medicine, but little is known about the molecular mechanisms or genetic underpinnings of hibernation. We have begun using the meadow jumping mouse (Zapus hudsonius) as a laboratory hibernation model. We sequenced, de novo assembled, and annotated a meadow jumping mouse genome. We further generated whole genome sequences for six additional meadow jumping mice and seven western jumping mice (Zapus princeps), a closely related hibernator. Z. hudsonius uses photoperiod as the cue to initiate fall fattening, while Z. princeps ignores photoperiod and prepares for hibernation based on food availability. Preliminary comparative genomic analysis reveals a subset of ~1700 proteins that are significantly diverged between the species. These diverged proteins are enriched for genes involved in pheromone sensing and reproduction, immunity, and metabolism. Analysis of individual genes yields insights into speciation and may reveal candidate genes that explain the phenotypic differences between the two species.Support or Funding InformationWJI acknowledges support from the Sara and Frank McKnight Fund for Biochemical Research and an NIH Early Independence Award (DP5OD021365).

Phylogeography of the western jumping mouse (Zapus princeps) detects deep and persistent allopatry with expansion

Understanding how diversity is partitioned across the landscape provides perspectives on the environmental processes that have influenced the evolutionary history of organisms. We analyzed spatial demography, historical biogeography, and niche divergence of the western jumping mouse (Zapus princeps) using molecular sequence data from mitochondrial and nuclear DNA recovered from 7 of the 11 subspecies in western North America. Phylogeographic structure within Z. princeps was partitioned across 5 clades (Boreal, Northern Sierra, Southern Rockies, Southern Sierra, and Uinta). Two lineages detected in the Sierra Nevada of California (Northern Sierra and Southern Sierra) were more closely allied to Z. trinotatus than to other lineages of Z. princeps and species distribution models mirror these phylogenetic signatures by detecting wide overlap in niches for Sierran jumping mice and Z. trinotatus as compared to other Z. princeps. Four southern lineages are deeply divergent and limited to disjunct mesic and montane habitats within the xeric southwestern United States, whereas the 5th lineage is widespread, extending from Wyoming to Alaska and reflecting expansion northward following deglaciation, a common pattern in boreal mammals.

Delimiting Geographic Distribution and Population History of Jumping Mice (Zapus trinotatusandZapus princeps) in the Pacific Northwest

The Cascade Range has generally partitioned sister species and populations into western and eastern forms, although north-south phylogeographic breaks within the Cascades have also been documented. We examined the relationships between and within 2 species of jumping mice, Zapus trinotatus (Pacific Jumping Mouse) and Z. princeps (Western Jumping Mouse), in Washington, Oregon, and southern British Columbia. From 24 localities we sampled 135 specimens and generated sequence data for 782 base pairs of mitochondrial DNA (mtDNA) control region and cytochrome-b. The 2 species were geographically partitioned to the east and west in concordance with the Cascades. However, in both northern Washington and southern Oregon, we found individuals with mtDNA haplotypes assigned to both species in syntopy, at the same sampling localities. Within Z. trinotatus, clades were further subdivided north and south, with a genealogical break across the Columbia River. Zapus princeps clades were also divided north and south, but with deeper divergences than within Z. trinotatus. We conclude that while the Cascade Range has contributed to the historic and contemporary partitioning of these 2 species, it does not represent an absolute barrier, as evidenced by syntopic localities.

Changes within Small Mammal Communities since the 1988 Huckleberry Mountain Fire

This study is a continuation of investigations conducted at Huckleberry Mountain to determine the effect of the 1988 Greater Yellowstone fire on the small mammal community, and document changes in this community over the 22 years since this natural disturbance. Previous research was conducted in 1993, 1994, 1997, and 1998 and we sampled the same communities in 2009 and again in 2010 using the identical sampling methodology. During the summer of 2010 we live trapped 252 Southern Red-backed Vole (Myodes gapperi), 57 North American Deermouse (Peromyscus maniculatu), 22 Least Chipmunk (Tamias minimus), 12 Western Jumping Mouse (Zapus princeps), four Montane Vole (Microtus montanus), one Northern Pocket Gopher (Thomomys talpoides), four Cinereus Shrew (Sorex cinereus), and five Dusky Shrew (S. monticolus). These results are similar to our results from 2009 and corroborate findings from other investigations indicating early dominance of P. maniculatus in burned forests and M. gapperi in control unburned areas. M. gapperi and P. maniculatus accounted for the majority (87%) of captures. In addition more M. gapperi were found in control sites than P. maniculatus, and as the burned habitat recovers over time, the relative numbers of P. maniculatus are decreasing, and the number of M. gapperi are increasing, suggesting that the burned habitats are returning to a more natural pre-disturbance community structure. However, community diversity indices (which include all mammal species and their relative proportions) suggest that there are still considerable differences between burned and unburned sites. Despite the numbers of voles and deermice changing over time (as predicted), the burned and control small mammal communities are still quite different from one another even after 22 years.

Arthropod Vectors and Vector-Borne Bacterial Pathogens in Yosemite National Park

Ticks, fleas, and vector-borne pathogens were surveyed in diverse small mammals in Yosemite National Park, California, from 2005 to 2007. A total of 450 unique captures of small mammals was collected during a 3-yr period and yielded 16 species of fleas and 10 species of ticks, including known vectors of Anaplasma phagocytophilum and Borrelia burgdorferi and plague. Serology was performed for A. phagocytophilum, spotted fever group Rickettsia spp., B. burgdorferi, and Yersinia pestis. A. phagocytophilum exposure was identified in 12.1% of all wild small mammals tested, with seropositive animals in 10 species, notably Belding's ground squirrels (Spermophilus beldingi), jumping mice (Zapus princeps), and voles (Microtus sp.). Spotted fever group Rickettsia spp. exposure was detected in 13.9% of all small mammals tested, with seropositive animals in eight species. Additionally, 37.0% of rodents in five species tested were seropositive for B. burgdorferi. No individuals were seropositive for Y. pestis. No animals were polymerase chain reaction positive for any pathogen tested. These results provide baseline data for future research and prediction of emerging vector-borne disease in Yosemite National Park, as well as adding to the known ranges and host species for tick and fleas in California.

Long-Term Response of Small Mammal Communities to the 1988 Huckleberry Mountain Fire

Biologists have long been interested in the response of small mammals and their habitat following natural disturbances. The Greater Yellowstone Area (GYA) fires of 1988 have provided opportunities to study short and long term responses. This study continues investigations conducted in the 1990’s following identical methodology at the same sites now 21 years post-fire. We live trapped 256 Clethrionomys gapperi (Red-backed Vole), 116 Peromyscus maniculatus (Deer Mouse), 44 Tamius minimus (Least Chipmunk), 28 Zapus princeps (Western Jumping Mouse), two Microtus montanus (Montane Vole), 1 Thomomys talpoides (Northern Pocket Gopher) and 37 shrews (Sorex ssp.). These results support findings from other investigations regarding the initial early dominance of P. maniculatus in burn areas and C. gapperi in control or non-burn areas, and as time has progressed since the burn, differences between burn and control sites (as measured by community diversity indices) has decreased. As expected calculated Shannon diversity indices (H’) in 2009 are higher for at least one of the burn sites than in previous years as the habitat recovers to pre-burn conditions.

Riparian and Upland Small Mammals on the East Slope of the Cascade Range, Washington

Differences in small mammal diversity and abundance between riparian and upland areas have not been consistently shown in the Pacific Northwest, and the issue is expected to be complex along the east slope of the Cascade Range with its complex bio geography and forest landscape structure. The information is important for evaluating buffer zone management and the potential impacts of fuel reduction projects. We quantified small mammal species’ abundances, diversity, and indicator species in riparian and upland forest along three third-order streams. Each location had a set of four 5 x 6 pitfall kill-trapping grids with 15 m spacing and the first grid row 5 m from the water. One site had an additional set of four grids. We trapped for two weeks during late June and early July during 1997 and 1998 for a total trap effort of 13,411 trap nights. We captured 1,104 individuals of 14 species. Insectivores were 69% and rodents 31% of the captures. Sorex trowbridgii was the most abundant species (54% of all captures). Peromyscus keeni and P. maniculatus combined dominated the rodent community with 43% of rodent captures. Species richness and individuals captured generally were highest within 20-35 m of the stream. Sorex palustris, P. keeni, Microtus longicaudus, S. vagrans, and Zapus princeps showed strong affinities to the immediate riparian zone ( <5 m from the stream). No species were indicators or most abundant in the upland forest away from the riparian areas. Refuge and corridor functions for small mammals in riparian areas would be maintained by current buffer-width standards of 60-100 m.

Microsatellite DNA markers for assessing phylogeographic and population structure in Preble's meadow jumping mice (Zapus hudsonius preblei) and cross‐amplification among neighbouring taxa

AbstractWe document the isolation and characterization of 14 tetranucleotide microsatellite DNA markers in Preble's meadow jumping mouse (Zapus hudsonius preblei). The identified markers displayed moderate levels of allelic diversity (averaging 4.9 alleles per locus) and heterozygosity (averaging 55.1%). Genotypic and allelic frequencies in a collection of 30 individuals conformed to Hardy–Weinberg equilibrium expectations and indicated no linkage disequilibrium. High levels of cross‐amplification (95% overall) among neighbouring subspecies and two congeners (Zapus princeps and Zapus trinotatus) were observed. Multilocus genotypes resulting from these markers appear to provide ample genetic diversity for studies assessing individual‐ and population–level ecological interactions within Z. h. preblei and evolutionary relationships among neighbouring subspecies (Z. h. campestris, Z. h. intermedius, Z. h. pallidus and Z. h. luteus).

Mistaken view of taxonomic validity undermines conservation of an evolutionarily distinct mouse: a response to Ramey et al. (2005)

1 Department of Biology, University of Washington, Seattle, WA, USA 2 Department of Fisheries and Wildlife Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA 3 Department of Biology, Valdosta State University, Valdosta, GA, USA 4 New Mexico Museum of Natural History, Albuquerque, NM, USA 5 Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, CO, USA 6 School of Molecular and Life Sciences, University of Limpopo, Sovenga, South Africa

DISTINGUISHING ZAPUS HUDSONIUS PREBLEI FROM ZAPUS PRINCEPS PRINCEPS BY USING REPEATED CRANIAL MEASUREMENTS

Preble's meadow jumping mouse (Zapus hudsonius preblei), a federally listed threatened subspecies, and the western jumping mouse (Zapus princeps princeps) typically occur parapatrically but in some areas may be syntopic. Field differentiation between the taxa is difficult so we investigated the use of cranial characteristics as a basis for identification. We developed a discriminant function conducted on the means of repeated measurements to distinguish between the taxa from an initial sample of 105 specimens (n = 71 Z. p. princeps and n = 34 Z. h. preblei). We found that measurement error can contribute significantly to erroneous reclassification of specimens when only a single measurement set is used. Use of only presence or absence of the anterior median toothfold of M3 is not a reliable method for distinguishing between the subspecies. We used the discriminant function to identify 8 of 16 specimens collected in southeastern Wyoming as Z. h. preblei.

Resource availability and population dynamics of Nicrophorus investigator, an obligate carrion breeder

Summary1. Food resources for rearing young may influence insect populations. This is particularly true for insects that breed obligately on rare, ephemeral resources such as dung, fungi, or carrion.2. Beetles in the genus Nicrophorus bury small vertebrate carcasses for rearing their young. Studies reviewed by Scott (1998) have found a positive relationship between carcass mass and total brood size. It is likely that access to carcasses suitable for breeding, and not food or mates, limits reproduction in both male and female Nicrophorus. Thus, small mammal densities could determine Nicrophorus population sizes.3. The work reported here examined the relationship between Nicrophorus investigator (Coleoptera: Silphidae) population size and small mammal abundance at two sites over a 4‐year period.4. Nicrophorus investigator buried and reared young on all the native small rodent species trapped at two sites in south‐western Colorado, U.S.A. (Peromyscus maniculatus, Microtus montanus, Zapus princeps, Tamias minimus, Thomomys talpoides). They preferred to bury and reproduce on rodent carcasses weighing between 16 and 48 g; rodents of this size represented 82% of captures.5. Population sizes of N. investigator and small rodents were estimated simultaneously using mark‐recapture censuses over a 4‐year period. Considering only rodents within the size range used by N. investigator, the estimated small mammal biomass per hectare in one year and the beetle population size in the following year were correlated significantly.

Clearcutting and burning of northern spruce‐fir forests: implications for small mammal communities

1. This study was designed to test the hypotheses that (i) abundance and related demographic parameters of small mammal populations would decline after clearcutting of northern spruce‐fir forest, and (ii) prescribed burning, following clearcutting, an approach to emulating natural disturbance, would enhance the species richness and diversity of the small mammal community relative to unharvested and clearcut forests. 2. Intensive live‐trapping of small mammal populations was conducted in replicated forest (uncut), clearcut and clearcut‐burned sites from 1988 to 1992 in west‐central British Columbia, Canada. 3. Mean abundance of southern red‐backed voles Clethrionomys gapperi was significantly higher on forest sites (11·74 ha–1) than on clearcut (0·60 ha–1) or clearcut‐burned (0·02 ha–1) sites. Mean numbers of deer mice Peromyscus maniculatus were significantly higher on the clearcut‐burned sites (16·88 ha–1) than on forest sites (9·04 ha–1). Demographic parameters of reproduction, survival and body weight of deer mice were similar across all sites. 4. The long‐tailed vole Microtus longicaudus had a strong annual fluctuation in abundance, particularly on clearcut sites (14·04 ha–1), where there were significantly more animals than on either forest (1·53 ha–1) or clearcut‐burned (2·67 ha–1) sites. Meadow voles M. pennsylvanicus were relatively uncommon but occurred more often on clearcut and clearcut‐burned sites than on forest sites. 5. The north‐western chipmunk Tamias amoenus occurred at significantly higher numbers on clearcut (4·16 ha–1) and clearcut‐burned (3·88 ha–1) sites than on forest sites, where it was rarely captured. Shrews Sorex spp. were at similar numbers across forest, clearcut and clearcut‐burned sites. Weasels Mustela spp. were captured more often on clearcut and clearcut‐burned sites than on forest sites. A rare species, the western jumping mouse Zapus princeps, was captured on clearcut and clearcut‐burned sites only. 6. Mean species richness of small mammals was significantly higher on clearcut sites (3·51) than on forest (2·73) or clearcut‐burned (2·72) sites. Species diversity was similar over all sites. Although species composition was altered by clearcutting, abundance of all species, except C. gapperi, was the same or higher than that in uncut forest. 7. Prescribed burning of clearcuts may not be necessary to mimic natural disturbance regimes. Clearcutting of northern spruce‐fir forest may provide diverse habitats for small mammals through different stages of succession (along with old growth forest) much as wildfires formerly did.

Persistence of the Meadow Jumping Mouse, Zapus hudsonius luteus, in New Mexico

Zapus hudsonius luteus is a subspecies of the meadow jumping mouse (Hafner et al., 1981) that is restricted to New Mexico and Arizona, where it occupies mesic habitats in lowland valleys and along montane streams (Bailey, 1913; Findley et al., 1975; Hafner et al., 1981; Hoffmeister, 1986). The subspecies has been reported from 14 localities in New Mexico (Hafner et al., 1981; R. D. Ohmart and V. C. Hink, in litt.) and 11 localities in Arizona (Hafner et al., 1981; Hall, 1981; Hoffmeister, 1986). In New Mexico, these records are from the San Juan Mountains (El Rito area), Sangre de Cristo Mountains (North Williams Lake), Jemez Mountains (upper Guadalupe River drainage), Sacramento Mountains (Rio Penasco and Silver Springs Creek), and the Rio Grande Valley (Espanola to the Bosque del Apache National Wildlife Refuge; Fig. 1). Southwestern populations of the genus Zapus were initially described by Miller (1911) as a distinct species, Zapus luteus, then as a subspecies of the western jumping mouse, Zapus princeps (Z. p. luteus), by Krutszch (1954). Based on genetic relationships between southwestern Zapus and other representatives of the genus, Hafner et al. (1981) concluded that these peripheral isolates were instead conspecific with the meadow jumping mouse, Z. hudsonius, and, therefore, considered them to be Z. h. luteus.

Reproduction by female Zapus princeps in relation to age, size, and body fat

Reproduction in female Zapus princeps, the western jumping mouse, was studied in relation to age, body size, and energy reserves in the form of fat content. Females were classified as reproductive if embryos, mammary tissue, or placental scars were present. Nonreproductive females were those showing no visible signs of pregnancy or lactation during midsummer, when breeding status could be determined with certainty. Only 9 of 22 (41%) 1-year-old females and 21 of 30 (70%) older females bred. Differences in size between breeders and nonbreeders were attributable to differences in age. Differences in fat content were attributed to size and breeding status, but could not be considered to reflect prebreeding condition. We speculate that the nonbreeding females were those in poor condition following hibernation. Most of these were yearlings.

Observations of intraspecific behavior of Meadow Jumping Mice, Zapus hudsonius, and escape behavior of a Western Jumping Mouse, Zapus princeps, in the wild

Observations of intraspecific behavior of Meadow Jumping Mice, Zapus hudsonius, and escape behavior of a Western Jumping Mouse, Zapus princeps, in the wild

Wzorzec aktywności u Zapus princeps przed hibernacją

Activity of Zapus princeps Allen, 1899 was studied in late summer. The animals showed a well defined, nocturnal pattern of activity with occasional short bursts of activity in daylight hours. Amount of activity gradually decreased over the 4 days prior to commencement of hibernation.

Ecological strategies of a small hibernator, the western jumping mouse Zapus princeps

The seasonal emergence, reproduction, diet, fat deposition, and immergence of six wild populations of Zapus princeps from elevations of 1860–2900 m were studied by trap–recapture methods and laboratory observations from April 1974 to November 1978. Emergence timing varied widely between and within sites in different years. It was not related to increasing elevation but to site quality. Vegetative growth was an excellent predictor of emergence timing at all sites. Emergence of males and females was synchronous except above 2200 m where males preceded females by 3–9 days. Field and laboratory experiments and observations were made on Z. princeps, including habitat preferences, competitive relationships, population density (maximum = 32.4/ha), length and timing of the active cycle (87 days), reproductive activity (1 litter/year), litter size [Formula: see text], age structure of populations, growth rates, seasonal fat deposition (0.65 g/day),and home-range size(0.17–0.61 ha). This attempts to formulate a coherent picture of the system of strategies by which a small hibernator adapts to its environment.

Circadian rhythms of body temperature and periodic arousal in hibernating Zapus princeps

Circadian rhythms of body temperature and periodic arousal in hibernating Zapus princeps

The Importance of Arthropods in the Diet of Zapus princeps in a Subalpine Habitat

The Importance of Arthropods in the Diet of Zapus princeps in a Subalpine Habitat

Origin and Evolution of the External Parasite Fauna of Western Jumping Mice, Genus Zapus

There are few ectoparasites regularly associated with jumping mice of the genus Zapus. The tiny hypopial glycyphagid mite, Dermacarus newyorkensis, is nearly restricted to Zapus, and is found on all species and almost throughout the range of the genus. Androlaelaps fahrenholzi, a large laelapid mite, is common on Zapus throughout its range and also on many other species of small mammals. However, A. fahrenholzi as it occurs on Zapus appears to be different from that species as it occurs on Microtus and Peromyscus. Chiggers, primarily of the Neotrombicula microti group, are common on Zapus in the W. This includes N. microti, common also on microtine rodents, and apparently a new species mostly on Zapus. A myobiid mite, Radfordia ewingi, is apparently more common in the E than in the W. A myocoptid mite, Gliricoptes zapi, is not common on Zapus, but was described as new from Zapus from the W. The tick, Ixodes angustus, occurs fairly regularly on Zapus in the W. A few other ectoparasites were found, but none regularly. Limited ectoparasite data suggest Zapus prince ps of British Columbia to be perhaps most similar to a progenitor stock of North American zapodids, and British Columbia to be perhaps a center of evolutionary activity in Zapus. It is hypothesized that Zapus progenitor stocks, including most ectoparasites, entered North America from Eurasia and that relatively little transfer of parasites occurred between Zapus and other North American mammalian species, although losses of parasites did occur.