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Options for field anesthetics are somewhat limited for wild animals, particularly for small game mammals. We evaluated the efficacy of a reversible field anesthetic, “BAM” (butorphanol, azaperone, medetomidine; Wildlife Pharmaceuticals, Inc., Windsor, CO) in yellow-bellied marmots (Marmota flaviventris). BAM is widely used in large game mammals, but has not been tested in smaller animals. We found that 0.20-0.25 mL of BAM was most effective, but marmots were anesthetized using as little as 0.06 mL. We found no relationship between the dosage of BAM and the time to first effects, sternal recumbency time or approachable time. Increasing dosages of BAM to levels at or above 0.20 mL was associated with less excitability and muscle rigidity, as well as a better overall quality of anesthesia. BAM differentially affected vital signs, as heart rates increased considerably during anesthesia; however, these changes lessened with increased time under anesthesia. There was no relationship between heart rate, oxygen saturation or body temperature and the dosage of BAM. Reversal drugs showed a wide dosage range, as additional reversal drugs were generally not required. Marmots were successfully reversed using concentrations of only 0.05 mL/kg atipamezole and naltrexone. Overall, our results indicate that BAM is a safe and effective, easily reversible field anesthetic for use in small game mammals.

The complexity of a community can play a fundamental role in the prevalence of pathogens by altering interactions among hosts and pathogen transmission. Information on the frequency of contacts between individuals and the distribution of contact rates in a population is critical to predicting pathogen prevalence. However, contact rates are notoriously difficult to document especially in small, nocturnal species. We have been documenting the contact rates of deer mice (Peromyscus maniculatus) in nature with respect to infection with Sin Nombre virus (SNV), a zoonotic pathogen, and the biodiversity of the mammalian community. Our long-term field studies, as well as those of others, revealed that prevalence of SNV in deer mice is related to the complexity of the mammalian community such that pathogen prevalence is lower in more diverse communities. Using a combination of techniques, we found evidence that contact rates between deer mice differ with respect to biodiversity. Deer mice in more complex communities had fewer intraspecific interactions than those in less diverse communities. Contact rates of individual deer mice were highly variable with a minority of the deer mice accounting for a majority of the interactions. Infection with SNV was related to risk-taking behavior; animals categorized as “bold” were 3 times more likely to be infected than “shy” deer mice. Results of these studies have implications for pathogen management in wildlife and humans.

Simultaneous infections with multiple pathogens can alter the function of the host's immune system, often resulting in additive or synergistic morbidity. We examined how coinfection with the common pathogens Sin Nombre virus (SNV) and Bartonella sp. affected aspects of the adaptive and innate immune responses of wild deer mice ( Peromyscus maniculatus). Adaptive immunity was assessed by measuring SNV antibody production; innate immunity was determined by measuring levels of C-reactive protein (CRP) in blood and the complement activity of plasma. Coinfected mice had reduced plasma complement activity and higher levels of CRP compared to mice infected with either SNV or Bartonella. However, antibody titers of deer mice infected with SNV were more than double those of coinfected mice. Plasma complement activity and CRP levels did not differ between uninfected deer mice and those infected with only Bartonella, suggesting that comorbid SNV and Bartonella infections act synergistically, altering the innate immune response. Collectively, our results indicated that the immune response of deer mice coinfected with both SNV and Bartonella differed substantially from individuals infected with only one of these pathogens. Results of our study provided unique, albeit preliminary, insight into the impacts of coinfection on immune system function in wild animal hosts and underscore the complexity of the immune pathways that exist in coinfected hosts.

Sin Nombre virus (SNV) is a hantavirus hosted almost exclusively by deer mice (Peromyscus maniculatus) that causes high (∼40%) mortality in humans. Transmission patterns of SNV in natural host populations are not well understood and, as such, represent a knowledge gap that has significant implications for human health. Since its identification in the early 1990s, the Four Corners region of the southwestern United States (i.e. geographic area encompassing southeastern UT, northeastern AZ, southwestern CO and northwestern NM) has remained a “hotspot” for SNV infections in both deer mice and humans; however, the reason for this skewed geographic distribution of SNV remains unclear. Therefore, our objective was to observe regional patterns of SNV prevalence in deer mice along a latitudinal gradient in the Four Corners region and determine the extent to which prevalence is influenced by factors including deer mouse density, small mammal diversity, vegetation cover, plant moisture content, soil pH and...

We surveyed a summer population of Tadarida brasiliensis mexicana in south-central Colorado to gain an initial characterization of the resident mycobiome (i.e., fungal biota) present on their body surfaces. We cultured fungal spores from bats captured in early and late summer and then conducted DNA barcoding analysis for taxonomic identification. Phylum Ascomycota dominated the ectomycotal (i.e., fungi present on body surfaces) community, with the most common genera including Aspergillus, Penicillium, Cladosporium, and Eurotium. Phylum Basidiomycota constituted a smaller proportion of fungal isolates and was composed primarily of Cryptococcus, Peniophora, Cystofilobasidium, and Sistotrema. We found seasonal differences in fungal community composition, with diversity and evenness increasing from June to August. There were notable differences in fungal communities present on adult vs. juvenile bats, with juveniles having a greater number of unique genera, greater fungal diversity, and lower species evenness compared with adults. We isolated a number of fungal species that are capable of growing at low temperatures, indicating that T. b. mexicana harbors viable psychrophilic fungi.

Sin Nombre virus (SNV) causes hantavirus pulmonary syndrome (HPS) in humans, a disease with high (∼36%) mortality. Deer mice (Peromyscus maniculatus) are the primary host of SNV and, unlike humans, deer mice infected with SNV have few overt signs of disease. The reasons for such mild infections in deer mice have not been well studied; however, this information may be useful in uncovering therapies that could reduce human HPS mortality. Therefore, the objective of this study was to evaluate the immune response of deer mice to SNV by examining their patterns of white blood cell production. We quantified the number of lymphocytes, eosinophils, basophils, neutrophils, and monocytes produced by wild deer mice in both the early and late stages of SNV infection. Deer mice captured in the early season had greater basophil, lymphocyte, and eosinophil levels compared to deer mice captured in the late season. Conversely, monocyte levels were greater in deer mice captured in the late season. SNV infection status appeared to influence production of both neutrophils and monocytes, with SNV-infected mice having greater neutrophil levels but lower monocyte levels than uninfected mice. Collectively, the results seem to support the notion that immune stressors faced by wild deer mice shift from early to late season, and these differences are reflected by differential leukocyte production that occurs across seasons. Furthermore, our results indicate some potential differences between wild deer mice and lab-bred deer mice, as well as some possible similarities between wild deer mice and humans in their immune responses to SNV infection.

We examined how climate-mediated forest dieback regulates zoonotic disease prevalence using the relationship between sudden aspen decline (SAD) and Sin Nombre virus (SNV) as a model system. We compared understory plant community structure, small mammal community composition, and SNV prevalence on 12 study sites within aspen forests experiencing levels of SAD ranging from10.0% crown fade to95.0% crown fade. Our results show that sites with the highest levels of SAD had reduced canopy cover, stand density, and basal area, and these differences were reflected by reductions in understory vegetation cover. Conversely, sites with the highest levels of SAD had greater understory standing biomass, suggesting that vegetation on these sites was highly clustered. Changes in forest and understory vegetation structure likely resulted in shifts in small mammal community composition across the SAD gradient, as we found reduced species diversity and higher densities of deer mice, the primary host for SNV, on sites with the highest levels of SAD. Sites with the highest levels of SAD also had significantly greater SNV prevalence compared to sites with lower levels of SAD, which is likely a result of their abundance of deer mice. Collectively, results of our research provide strong evidence to show SAD has considerable impacts on vegetation community structure, small mammal density and biodiversity and the prevalence of SNV.

Immunocompetence of animals fluctuates seasonally, However, there is little consensus on the cause of these fluctuations. Some studies have suggested that these patterns are influenced by changes in reproductive condition, whereas others have suggested that differences result from seasonal variations in energy expenditures. The objective of our study was to examine these contrasting views of immunity by evaluating seasonal patterns of immune response and reproduction in wild populations of deer mice Peromyscus maniculatus exposed to Sin Nombre virus (SNV). Over three consecutive fall (September, October, November) and three consecutive spring (March, April, May) sampling periods, we used titration enzyme-linked immunosorbent assay (ELISA) to quantify virus-specific antibody production in 48 deer mice infected with SNV. Levels of reproductive hormones were quantified using ELISA. SNV antibody titers reached their lowest level during November (geometric mean titer [GMT] = 420) and their highest levels during September (GMT = 5,545) and May (GMT = 3,582), suggesting that the immune response of deer mice to SNV has seasonal patterns. The seeming decrease in antibody titer over winter coupled with the consistency in body masses suggests that during winter, immunocompetence may be compromised to offset the energetic costs of maintenance functions, including those associated with maintaining body mass. Deer mice showed distinct sex-based differences in SNV antibody production, with males producing higher antibody titers (GMT = 3,333) than females (GMT = 1,477). Levels of reproductive hormones do not appear to influence antibody production in either males or females, as there was no correlation between estradiol concentrations and SNV antibody titer in female deer mice (r² = 0.26), nor was there a significant relationship between levels of testosterone and SNV antibody titers in males (r² = 0.28). Collectively, this study demonstrates that immunocompetence of wild deer mice is seasonally variable; however, reproduction is not the primary stressor responsible for this variation. Rather, the data suggest that deer mice may compromise immunocompetence during winter to offset other maintenance costs during this period.

Species diversity has been shown to decrease prevalence of disease in a variety of host-pathogen systems, in a phenomenon termed the Dilution Effect. Several mechanisms have been proposed by which diversity may decrease prevalence, though few have been tested in natural host-pathogen systems. We inves- tigated the mechanisms by which diversity influenced the prevalence of Sin Nombre virus (SNV), a directly transmitted virus in deer mice (Peromyscus maniculatus). We monitored both intra and interspecific encounters of deer mice using foraging arenas at five sites in the Great Basin Desert with disparate levels of species diversity to examine two potential mechanisms which may contribute to the dilution of SNV preva- lence: (1) reduced frequency of encounters between deer mice, or (2) reduced duration of contacts between deer mice. We also investigated the relationship between deer mouse density and these mechanisms, as density is often predicted to influence both inter and intraspecific encounters. Results of our study indicate that frequency of intraspecific interactions between deer mice was reduced with increased diversity. Species diversity did not impact average duration of encounters. Density was correlated with absolute, but not relative rates of encounters between deer mice, suggesting that encounters may be influenced by factors other than density. Our study indicates that species diversity influences the dynamics of SNV by reducing encounters between deer mice in a trade-off between intra and interspecific interactions.

Heterogeneities within disease hosts suggest that not all individuals have the same probability of transmitting disease or becoming infected. This heterogeneity is thought to be due to dissimilarity in susceptibility and exposure among hosts. As such, it has been proposed that many host–pathogen systems follow the general pattern whereby a small fraction of the population accounts for a large fraction of the pathogen transmission. This disparity in transmission dynamics is often referred to as ‘20/80 Rule’, i.e. approximately 20 per cent of the hosts are responsible for 80 per cent of pathogen transmission. We investigated the role of heterogeneity in contact rates among potential hosts of a directly transmitted pathogen by examining Sin Nombre virus (SNV) in deer mice ( Peromyscus maniculatus ). Using foraging arenas and powder marking, we documented contacts between wild deer mice in Great Basin Desert, central Utah. Our findings demonstrated heterogeneity among deer mice, both in frequency and in duration of contacts with other deer mice. Contact dynamics appear to follow the general pattern that a minority of the population accounts for a majority of the contacts. We found that 20 per cent of individuals in the population were responsible for roughly 80 per cent of the contacts observed. Larger-bodied individuals appear to be the functional group with the greatest SNV transmission potential. Contrary to our predictions, transmission potential was not influenced by breeding condition or sex.

Many diseases persist at a relatively low prevalence, seemingly close to extinction. For a chronic disease in a homogeneous population, reducing the transmission rate by a fraction proportional to the prevalence would be sufficient to eradicate the disease. This study examines how higher prevalence of the Sin Nombre virus in male deer mice (Peromyscus maniculatus) might contribute to disease persistence. Analyzing data from over 2,000 individual mice captured in 19 sites over 4 years, we found prevalences of 18.5% in males and 8.8% in females. By examining recaptures, we determined that males are more likely to contract the infection because of higher susceptibility or higher encounter rates. Comparing across 86 sampling periods, we found a higher proportion of males when population densities were low. A capture-recapture analysis indicates that males live longer than females. A mathematical model based on the measured parameters and population size trajectories suggests that the combined heterogeneity in encounters, susceptibility, and mortality may buffer the disease from extinction by concentrating disease in the subgroup most likely to transmit the disease. This buffering effect is not significantly stronger in a fluctuating population, indicating that these forms of heterogeneity might not be the key for disease persistence through host population bottlenecks.

Several laboratory studies have shown that the ingestion of dietary linoleic (18:2 ω6) acid before winter can promote deep and continuous torpor, whereas excess consumption of α-linolenic acid (18:3 ω3) can interfere with an animal's ability to reach and maintain low body temperatures during torpor. As mammalian heterotherms obtain linoleic and α-linolenic acid strictly from the diet, diet selection has been proposed as a mechanism that allows hibernators to ingest levels of linoleic and α-linolenic acid that promote favorable torpor patterns. Here diet, dietary nutrient content and patterns of forage preference of a representative hibernator, the Utah prairie dog Cynomys parvidens, and a facultative heterotherm, the black-tailed prairie dog Cynomys ludovicianus, were examined under natural field conditions. Diets of black-tailed (BTPD) and Utah prairie dogs (UTPD) differed across seasons (BTPD F26,108=9.59, P

We compared over-winter body temperature (Tb) patterns for more than 6 months in adult (>1 year) black-tailed (Cynomys ludovicianus) and Utah (C. parvidens) prairie dogs from colonies located along gradients of elevation in northern Colorado and southern Utah. In general, black-tailed prairie dogs entered torpor facultatively during winter, whereas Utah prairie dogs hibernated continuously for extended periods. Both black-tailed and Utah prairie dogs displayed significant differences in Tb patterns across elevations, with lower elevation populations entering more shallow and infrequent torpor than prairie dogs at higher elevations. Tb patterns of black-tailed prairie dogs followed 24-h cycles, as most prairie dogs entered into and aroused from torpor between 1100 and 1700 h and bout lengths were clustered around 24-h intervals and multiples thereof. Torpor in Utah prairie dogs did not display the same daily patterns; they entered into and aroused from torpor at all times of the day, and bout leng...

Black-tailed prairie dogs (Cynomys ludovicianus) enter torpor intermittently during winter in the field but do not hibernate continuously from fall to spring. Previous studies have established that hibernators rely primarily on stored lipids during winter and that the storage of n–6 PUFAs in white adipose tissue (WAT) is required to maintain low body temperatures during this continuous torpor. Adult (>1 year) black-tailed prairie dogs were livetrapped in the fall, winter, spring, and summer (n = 10–12). To determine whether free-ranging black-tailed prairie dogs rely heavily on stored proteins during winter, we investigated seasonal changes in body composition of the prairie dogs with dual-energy X-ray absorptiometry scans. We also examined seasonal changes in lipid composition of the WAT and diet using gas–liquid chromatography to determine whether black-tailed prairie dogs lack the lipids necessary for hibernation. Seasonal changes in fat, lean, and total body mass indicate that black-tailed prairie dogs relied heavily on stored lipids during the winter and appeared to rely on proteins primarily during periods that coincided with reproductive activity. Seasonal changes in dietary and WAT lipids indicate that WAT n–6 PUFAs are used during winter and stored during summer, while WAT n–3 PUFAs are stored during winter and used during summer. These patterns of lipid use are different than those reported in free-ranging hibernators and may explain why black-tailed prairie dogs experience shallow and infrequent torpor bouts.

Although facultative torpor has been observed in laboratory populations of black-tailed prairie dogs (Cynomys ludovicianus), it is widely believed that these animals remain normothermic throughout winter in the field. We monitored body temperatures (T b) of 5 blacktailed prairie dogs in the field for about 100 days during winter and spring 1998‐1999. All animals entered torpor during this period. Major torpor bouts averaged 140.5 h 6 2.4 SD (range 5 77.6‐214.4) with a minimum Tb of 19.0 6 3.68C. Minor torpor bouts averaged 46.2 6 20.9 h (9.5‐98.5), with minimum Tb reaching 30.3 6 2.38C. There was no distinct relationship between ambient air temperature (Ta) and entry into torpor. All torpor bouts occurred following a sudden reduction in Ta, but not all sudden reductions in Ta induced torpor. Precipitation was not associated with entry into or arousal from torpor. Our study demonstrates that facultative torpor occurs in free-ranging black-tailed prairie dogs in the field.

Climate change, human disturbance, and disease can have large impacts on the dynamics of a species by affecting the likelihood of survival and reproduction of individuals. We investigated the roles of precipitation, off-road vehicle (ORV) alteration of habitat, and infection with Sin Nombre virus on the survival and reproductive probabilities of deer mice (Peromyscus maniculatus). We used generalized linear mixed models to estimate the effects of these factors and their interactions by fitting capture-recapture data collected seasonally from 2002 to 2007 at 17 sites in the Great Basin Desert of central Utah, USA. During periods with high precipitation, we found no difference in survival and reproductive probabilities between seasons, but during drier periods, we found a reduction of overwinter survival and fall reproductive activity. Precipitation also interacted with disturbance to affect survival probabilities and female reproduction; in periods with low precipitation, deer mice on highly disturbed sites had extremely low survival probabilities and low reproductive probabilities of females compared to those of individuals from low-disturbance sites. However, high precipitation ameliorated the effect of disturbance on both parameters. Deer mice from sites with high impact of ORV disturbance also had low survival over summer. Additionally, male reproductive probabilities were diminished on highly disturbed sites in both seasons; in contrast, they were reduced only in the fall on low-disturbance sites. Density had an overall negative effect on survival and reproductive probabilities of deer mice. For females, the negative effect on reproductive activity was amplified in highly disturbed sites. We found no effect of hantavirus infection on survival probabilities of deer mice. Overall, this study revealed complexity in the determinants of deer mouse survival and reproduction given by the effects of a number of significant interactions among explanatory variables. Thus, factors that may not appear to have a strong effect when investigated alone can still be influential by modulating the effect of a different factor.

Background Species diversity is proposed to greatly impact the prevalence of pathogens. Two predominant hypotheses, the “Dilution Effect” and the “Amplification Effect”, predict divergent outcomes with respect to the impact of species diversity. The Dilution Effect predicts that pathogen prevalence will be negatively correlated with increased species diversity, while the Amplification Effect predicts that pathogen prevalence will be positively correlated with diversity. For many host-pathogen systems, the relationship between diversity and pathogen prevalence has not be empirically examined. Methodology/Principal Findings We tested the Dilution and Amplification Effect hypotheses by examining the prevalence of Sin Nombre virus (SNV) with respect to diversity of the nocturnal rodent community. SNV is directly transmitted primarily between deer mice (Peromyscus maniculatus). Using mark-recapture sampling in the Spring and Fall of 2003–2005, we measured SNV prevalence in deer mice at 16 landscape level sites (3.1 hectares each) that varied in rodent species diversity. We explored several mechanisms by which species diversity may affect SNV prevalence, including reduced host density, reduced host persistence, the presence of secondary reservoirs and community composition. We found a negative relationship between species diversity and SNV prevalence in deer mice, thereby supporting the Dilution Effect hypothesis. Deer mouse density and persistence were lower at sites with greater species diversity; however, only deer mouse persistence was positively correlated with SNV prevalence. Pinyon mice (P. truei) may serve as dilution agents, having a negative effect on prevalence, while kangaroo rats (Dipodomys ordii), may have a positive effect on the prevalence of SNV, perhaps through effects on deer mouse behavior. Conclusions/Significance While previous studies on host-pathogen systems have found patterns of diversity consistent with either the Dilution or Amplification Effects, the mechanisms by which species diversity influences prevalence have not been investigated. Our study indicates that changes in host persistence, coupled with interspecific interactions, are important mechanisms through which diversity may influence patterns of pathogens. Our results reveal the complexity of rodent community interactions with respect to SNV dynamics.

The resource allocation hypothesis predicts that reproductive activity suppresses immunocompetence; however, this has never been tested in an endemic disease system with free-ranging mammals. We tested the resource allocation hypothesis in wild deer mice (Peromyscus maniculatus) with natural exposure to Sin Nombre Virus (SNV). Immunocompetence was estimated from the extent of swelling elicited after deer mice were injected with phytohemagglutinin (PHA); swelling is positively correlated with immunocompetence. After livetrapping deer mice, we determined their reproductive state and SNV infection status. Males were more likely to be seropositive for SNV than females (37% vs. 25%) and exhibited 10% less swelling after PHA injection. The swelling response of females differed with both infection status and reproductive condition. There was also a significant infection status by reproductive condition interaction: non-reproductive, seropositive females experienced the least amount of swelling, whereas females in all other categories experienced significantly greater swelling. The swelling response of males differed with both SNV infection status and reproductive condition, but there was no significant infection status by reproductive condition interaction. Seronegative males elicited greater swelling than seropositive males regardless of reproductive status. In contrast to the resource allocation hypothesis, these results do not indicate that reproductive activity suppresses immunocompetence of deer mice but rather suggest that chronic SNV infection reduces immunocompetence. Sex-based differences in swelling indicate that SNV modulates the immune system of female deer mice differently than it does that of males, particularly during reproduction. We propose that differences in resource allocation between males and females could result from inherent sex-based differences in parental investment.

Deer mice (Peromyscus maniculatus) are the primary reservoir for Sin Nombre virus (SNV), a North American hantavirus that causes disease with high mortality in humans. Recent studies have proposed that habitat disturbance affects prevalence of SNV in deer mice; however, the outcomes proposed in these studies are in opposition to each other. Our objectives were to test these divergent hypotheses by: (1) measuring SNV infection in deer mice within a patchwork of disturbance; and (2) evaluating the relationships between SNV prevalence, population density and demography as possible mechanisms. In 2003 and 2004, we sampled 1,297 deer mice from 17 sites with varying levels of disturbance in the Great Basin Desert. Across sites and years, SNV prevalence varied from 0.0 to 38.9%. We found a negative relationship between SNV prevalence and disturbance. Although we found no direct relationship between SNV prevalence and deer mouse density, we found that density was highest on sites with the lowest levels of disturbance. The number of deer mice that survived across seasons (e.g., trans-seasonal survivors) differed across levels of disturbance and was greatest on our least disturbed study sites $$ (\ifmmode\expandafter\bar\else\expandafter\=\fi{x} = 14.00\% ), $$ moderate on sites with intermediate levels of disturbance $$ (\ifmmode\expandafter\bar\else\expandafter\=\fi{x} = 5.61\% ) $$ and zero on highly disturbed sites. On low-disturbance sites, a greater proportion of trans-seasonal survivors were SNV seropositive (28.80%) compared to the intermediate-disturbance sites (16.67). Collectively, our results indicate that habitat disturbance plays a predictive role in SNV prevalence, with highly disturbed sites having reduced long-term survival of deer mice, including survival of infected individuals.

Mechanisms that influence body temperature patterns in black-tailed prairie dogs are not well understood. Previous research on both free-ranging and laboratory populations of black-tailed prairie dogs (Cynomys ludovicianus) has suggested that reductions in ambient temperature and food and water deprivation are the primary factors that stimulate torpor in this species. In other species, however, torpor has been shown to be influenced by a multitude of factors, including innate circadian and circannual timing mechanisms, energy status, and reproductive behaviors. Our objective was to clarify the influence of weather, sex, and intrinsic timing mechanisms on the body temperature patterns of free-ranging black-tailed prairie dogs. We monitored body temperatures of eight adult (1 yr) prairie dogs from November 1999 to June 2000. Prairie dogs showed distinct daily and seasonal body temperature patterns, which reflected changes in ambient temperatures that occurred during these periods. These patterns of daily and seasonal heterothermy suggest that body temperature patterns of black-tailed prairie dogs may be driven by an innate timing mechanism. All prairie dogs entered torpor intermittently throughout winter and spring. Torpor bouts appeared to be influenced by precipitation and reductions in ambient temperature. Our results also suggest that reproductive behaviors and circadian timing may influence torpor in this species.