A damped precipitation‐driven,bottom‐up model for deer mouse population abundance in the northwestern United States

Small‐mammal population densities can be regulated by bottom‐up (food availability) and top‐down (predation) forces. In 1993, an El Niño Southern Oscillation event was followed by a cluster of human hantavirus with pulmonary syndrome in the southwestern United States. An upward trophic cascade hypothesis was proposed as an explanation for the outbreak: Increased plant productivity as a consequence of El Niño precipitations led to an unusual increase in distribution and abundance of deer mice (Peromyscus maniculatus ; reservoir host of Sin Nombre virus). Could such drastic events occur in mesic habitats, where plant productivity in response to climate conditions is likely to be much less dramatic? In this work, we investigate to what extent deer mouse populations follow a precipitation‐driven, bottom‐up model in central and western Montana and discuss important conditions for such a model to be possible. We found positive correlations between deer mouse abundance and on‐the‐ground measured plant productivity with a several‐month lag in three of six study sites. This effect was weaker when deer mouse populations were more abundant, indicating density‐dependent effects. Dispersal resulting from territoriality may be important in attenuating local density increments in spite of high food availability. In addition, there is evidence that population abundance in the study area could respond to other abiotic factors. In particular, precipitation in the form of snow may reduce deer mice survival, thus compensating the benefits of improved plant productivity. Deer mouse populations in Montana study sites follow complex dynamics determined by multiple limiting factors, leading to a damped precipitation‐driven bottom‐up regulation. This prevents dramatic changes in rodent abundances after sudden increments of food availability, such as those observed in other regions.     

Using MODIS satellite imagery to predict hantavirus risk

Aims Sin Nombre virus (SNV), a strain of hantavirus, causes hantavirus pulmonary syndrome (HPS) in humans, a deadly disease with high mortality rate (> 50%). The primary virus host is the deer mouse, and greater abundance of deer mice has been shown to increase the human risk of HPS. Our aim is to identify and compare vegetation indices and associated time lags for predicting hantavirus risk using remotely sensed imagery. Location Utah, USA. Methods A 5‐year time‐series of moderate‐resolution imaging spectroradiometer (MODIS) satellite imagery and corresponding field data was utilized to compare various vegetation indices that measure productivity with the goal of indirectly estimating mouse abundance and SNV prevalence. Relationships between the vegetation indices and deer mouse density, SNV prevalence and the number of infected deer mice at various time lags were examined to assess which indices and associated time lags might be valuable in predicting SNV outbreaks. Results The results reveal varying levels of positive correlation between the vegetation indices and deer mouse density as well as the number of infected deer mice. Among the vegetation indices, the normalized difference vegetation index (NDVI) and the enhanced vegetation index (EVI) produced the highest correlations with deer mouse density and the number of infected deer mice using a time lag of 1.0 to 1.3 years for May and June imagery. Main conclusions This study demonstrates the potential for using MODIS time‐series satellite imagery in estimating deer mouse abundance and predicting hantavirus risk. The 1‐year time lag provides a great opportunity to apply satellite imagery to predict upcoming SNV outbreaks, allowing preventive strategies to be adopted. Analysis of different predictive indices and lags could also be valuable in identifying the time windows for data collection for practical uses in monitoring rodent abundance and subsequent disease risk to humans.     

A temporal dilution effect: hantavirus infection in deer mice and the intermittent presence of voles in Montana

The effect of intermittently occurring, non-reservoir host species on pathogen transmission and prevalence in a reservoir population is poorly understood. We investigated whether voles, Microtus spp., which occur intermittently, influenced estimated standing antibody prevalence (ESAP) to Sin Nombre hantavirus (SNV, Bunyaviridae: Hantavirus) among deer mice, Peromyscus maniculatus, whose populations are persistent. We used 14 years of data from central Montana to investigate whether ESAP among deer mice was related to vole presence or abundance while controlling for the relationship between deer mouse abundance and ESAP. We found a reduction in deer mouse ESAP associated with the presence of voles, independent of vole abundance. A number of studies have documented that geographic locations which support a higher host diversity can be associated with reductions in pathogen prevalence by a hypothesized dilution effect. We suggest a dilution effect may also occur in a temporal dimension at sites where host richness fluctuates. Preservation of host diversity and optimization of environmental conditions which promote occurrence of ephemeral species, such as voles, may result in a decreased ESAP to hantaviruses among reservoir hosts. Our results may extend to other zoonotic infectious diseases.     

Effects of supplemental feeding and density of white-tailed deer on rodents

Spatial distribution, population density, and reproductive success of many wildlife species may be altered by changes in vegetation composition, habitat structure, and availability of food. Altered distributions of key herbivores such as white-tailed deer (Odocoileus virginianus) may impact all of these factors. Our objective was to determine the direct and indirect effects of supplemental feeding of deer on rodent populations in south Texas. We modeled effects of supplemental feeding and habitat change due to deer browsing through surveys of rodents. Rodents have a short generation time and populations respond quickly to change, so they are a suitable indicator of changes in habitat structure brought about by deer browsing pressure. We sampled rodent populations near to and far from deer feeders within twelve 81-ha enclosures containing three different densities of deer with and without supplemental feed. The three deer densities were low (8.1 ha/deer), medium (3.2 ha/deer), and high (2 ha/deer). We conducted rodent trapping during March and April of 2007 and 2008. Abundance of rodents was much higher (P < 0.001) in 2008 than in the previous year due to an increase in rainfall. However, we found little effect of deer density, supplemental feeding of deer, or distance from deer feeders on rodent populations. Thus we conclude that supplemental feeding of deer and deer density had little influence on rodent communities in this environment. Rodent species native to semi-arid environments are probably adapted to large changes in vegetative productivity brought about by the highly variable annual rainfall patterns, therefore they can adapt to the less abrupt habitat changes resulting from changing densities of deer. Conservation concerns that providing supplemental feed to deer in semi-arid rangeland will disrupt the ecology of the land through changes in rodent populations were not supported. © 2011 The Wildlife Society.     

A newly recognized virus associated with a fatal case of hantavirus pulmonary syndrome in Louisiana.

Genetic analysis of virus detected in autopsy tissues of a fatal hantavirus pulmonary syndrome-like case in Louisiana revealed the presence of a previously unrecognized hantavirus. Nucleotide sequence analysis of PCR fragments of the complete S and M segments of the virus amplified from RNA extracted from the tissues showed the virus to be novel, differing from the closest related hantavirus, Sin Nombre virus, by approximately 30%. Both genome segments were unique, and there was no evidence of genetic reassortment with previously characterized hantaviruses. The primary rodent reservoir of Sin Nombre virus, the deer mouse Peromyscus maniculatus, is absent from Louisiana. Thus, the virus detected in Louisiana, referred to here as Bayou virus, must possess a different rodent reservoir.     

How Host Population Dynamics Translate into Time-Lagged Prevalence: An Investigation of Sin Nombre Virus in Deer Mice

Human cases of hantavirus pulmonary syndrome caused by Sin Nombre virus are the endpoint of complex ecological cascade from weather conditions, population dynamics of deer mice, to prevalence of SNV in deer mice. Using population trajectories from the literature and mathematical modeling, we analyze the time lag between deer mouse population peaks and peaks in SNV antibody prevalence in deer mice. Because the virus is not transmitted vertically, rapid population growth can lead initially to reduced prevalence, but the resulting higher population size may later increase contact rates and generate increased prevalence. Incorporating these factors, the predicted time lag ranges from 0 to 18 months, and takes on larger values when host population size varies with a longer period or higher amplitude, when mean prevalence is low and when transmission is frequency-dependent. Population size variation due to variation in birth rates rather than death rates also increases the lag. Predicting future human outbreaks of hantavirus pulmonary syndrome may require taking these effects into account.     

Epizootiology of Sin Nombre and El Moro Canyon hantaviruses, southeastern Colorado, 1995-2000

Sin Nombre virus (SNV) is an etiologic agent of hantavirus pulmonary syndrome. To better understand the natural history of this virus we studied population dynamics and temporal pattern of infection of its rodent hosts in southeastern Colorado (USA) from 1995 to 2000. We present evidence for the presence of two hantaviruses, SNV in deer mice (Peromyscus maniculatus) and El Moro Canyon virus in western harvest mice (Reithrodontomys megalotis), at our study sites. Sin Nombre virus appeared only sporadically in deer mouse populations; overall prevalence of antibody to SNV was 2.6%. El Moro Canyon virus was enzootic: seroconversions occurred throughout the year; antibody prevalence (11.9% overall) showed a delayed-density-dependent pattern, peaking as relative abundance of mice was declining. Males of both host species were more frequently infected than were females. An apparently lower mean survivorship (persistence at the trapping site) for SNV antibody-positive deer mice could indicate a detrimental effect of SNV on its host, but might also be explained by the fact that antibody-positive mice were older when first captured.     

Predation has a greater impact in less productive environments: variation in roe deer, Capreolus capreolus, population density across Europe

Aim We aimed to describe the large‐scale patterns in population density of roe deer Caprelous capreolus in Europe and to determine the factors shaping variation in their abundance. Location Europe. Methods We collated data on roe deer population density from 72 localities spanning 25° latitude and 48° longitude and analysed them in relation to a range of environmental factors: vegetation productivity (approximated by the fraction of photosynthetically active radiation) and forest cover as proxies for food supply, winter severity, summer drought and presence or absence of large predators (wolf, Canis lupus, and Eurasian lynx, Lynx lynx), hunter harvest and a competitor (red deer, Cervus elaphus). Results Roe deer abundance increased with the overall productivity of vegetation cover and with lower forest cover (sparser forest cover means that a higher proportion of overall plant productivity is allocated to ground vegetation and thus is available to roe deer). The effect of large predators was relatively weak in highly productive environments and in regions with mild climate, but increased markedly in regions with low vegetation productivity and harsh winters. Other potentially limiting factors (hunting, summer drought and competition with red deer) had no significant impact on roe deer abundance. Main conclusions The analyses revealed the combined effect of bottom‐up and top‐down control on roe deer: on a biogeographical scale, population abundance of roe deer has been shaped by food‐related factors and large predators, with additive effects of the two species of predators. The results have implications for management of roe deer populations in Europe. First, an increase in roe deer abundance can be expected as environmental productivity increases due to climate change. Secondly, recovery plans for large carnivores should take environmental productivity and winter severity into account when predicting their impact on prey.     

Biogeographic and ecological regulation of disease: prevalence of Sin Nombre virus in island mice is related to island area, precipitation, and predator richness

The relative roles of top-down and bottom-up forces in affecting disease prevalence in wild hosts is important for understanding disease dynamics and human disease risk. We found that the prevalence of Sin Nombre virus (SNV), the agent of a severe disease in humans (hantavirus pulmonary syndrome), in island deer mice from the eight California Channel Islands was greater with increased precipitation (a measure of productivity), greater island area, and fewer species of rodent predators. In finding a strong signal of the ecological forces affecting SNV prevalence, our work highlights the need for future work to understand the relative importance of average rodent density, population fluctuations, behavior, and specialist predators as they affect SNV prevalence. In addition to illustrating the importance of both bottom-up and top-down limitation of disease prevalence, our results suggest that predator richness may have important bearing on the risk of exposure to animal-borne diseases that affect humans.     

Isolation and characterization of microsatellite markers in Oligoryzomys longicaudatus (Muridae, Sigmodontinae, Oryzomini), the natural reservoir of genotype Andes hantavirus

The rodent Oligoryzomys longicaudatus or long-tailed pygmy rice rat is the reservoir of the aetiological agent of the hantavirus pulmonary syndrome in southern Argentina and Chile. We characterize 11 polymorphic microsatellite loci which would be useful for studies on microgeographical population structure in the species. Amplification of these loci in 42 individuals from four natural populations revealed four to 21 alleles per locus, and values of observed heterozygosities ranging from 0.371 to 0.896. Cross-species amplifications showed that some of the primers designed may be useful for other species of the genus Oligoryzomys.     

Biological control agents elevate hantavirus by subsidizing deer mouse populations

Biological control of exotic invasive plants using exotic insects is practiced under the assumption that biological control agents are safe if they do not directly attack non-target species. We tested this assumption by evaluating the potential for two host-specific biological control agents ( Urophora spp.), widely established in North America for spotted knapweed ( Centaurea maculosa ) control, to indirectly elevate Sin Nombre hantavirus by providing food subsidies to populations of deer mice ( Peromyscus maniculatus ), the primary reservoir for the virus. We show that seropositive deer mice (mice testing positive for hantavirus) were over three times more abundant in the presence of the biocontrol food subsidy. Elevating densities of seropositive mice may increase risk of hantavirus infection in humans and significantly alter hantavirus ecology. Host specificity alone does not ensure safe biological control. To minimize indirect risks to non-target species, biological control agents must suppress pest populations enough to reduce their own numbers.     

Changes in the Spatial Configuration and Strength of Trophic Control Across a Productivity Gradient During a Massive Rodent Outbreak

Understanding the determinants of spatial and temporal differences in the relative strength of consumer–resource interactions is an important endeavour in ecology. Here, we explore the necessary conditions for temporal shifts in the relative strength of rodent–plant interactions in an area characterised by profound spatial differences in trophic control, with predator–prey interactions prevailing in productive habitats and rodent–plant interactions dominating unproductive habitats of the forest–tundra ecotone. We report data obtained during the exceptionally massive rodent outbreak of 2010–2012 in northernmost Fennoscandia, including an experimental manipulation of herbivore access to vegetation plots across a large-scale productivity gradient, multiple observational measures of plant–rodent interactions linked to rodent abundance data and a large-scale survey of breeding avian predators and mammalian predator activity. Unexpectedly, rodent grazing impacts documented during the rodent outbreak were uniformly strong across the landscape, regardless of habitat productivity. The runaway response in rodent populations was facilitated by a high population growth rate in the early phase of the outbreak due to the extended absence of predators in productive habitats, concomitant with an exceptionally long-lasting lemming outbreak in unproductive habitats. Our results showed that spatio-temporal variation in trophic control also occurs in ecosystems structured according to the exploitation ecosystems hypothesis and emphasises the importance of long-term studies to capture nonlinear and stochastic features that shape ecosystem functioning. In this context, the temporary release from top–down regulation in productive habitats caused strong grazing impacts that may be crucial for the resilience of tundra ecosystems under the threat of climate change-driven shrub encroachment.     

Investigating the Effects of Food Available and Climatic Variables on the Animal Host Density of Hemorrhagic Fever with Renal Syndrome in Changsha,China

Background

The transmission of hemorrhagic fever with renal syndrome (HFRS) is influenced by population dynamics of its main host, rodents. It is therefore important to better understand rodents’ characteristic in epidemic areas.

Methodology/Principal Findings

We examined the potential impact of food available and climatic variability on HFRS rodent host and developed forecasting models. Monthly rodent density of HFRS host and climate data in Changsha from January 2004 to December 2011 were obtained. Monthly normalized difference vegetation index (NDVI) and temperature vegetation dryness index (TVDI) for rice paddies were extracted from MODIS data. Cross-correlation analysis were carried out to explore correlation between climatic variables and food available with monthly rodent data. We used auto-regressive integrated moving average model with explanatory variables to examine the independent contribution of climatic variables and food supply to rodent density. The results indicated that relative rodent density of HFRS host was significantly correlated with monthly mean temperatures, monthly accumulative precipitation, TVDI and NDVI with lags of 1–6 months.

Conclusions/Significance

Food available plays a significant role in population fluctuations of HFRS host in Changsha. The model developed in this study has implications for HFRS control and prevention.     

Microhabitat characteristics of Akodon montensis,a reservoir for hantavirus,and hantaviral seroprevalence in an Atlantic forest site in eastern Paraguay

Hantaviruses may cause serious disease when transmitted to humans by their rodent hosts. Since their emergence in the Americas in 1993, there have been extensive efforts to understand the role of environmental factors on the presence of these viruses in their host rodent populations. HPS outbreaks have been linked to precipitation, but climatic factors alone have not been sufficient to predict the spatial‐temporal dynamics of the environment‐reservoir‐virus system. Using a series of mark‐recapture sampling sites located at the Mbaracayú Biosphere Reserve, an Atlantic Forest site in eastern Paraguay, we investigated the hypothesis that microhabitat might also influence the prevalence of Jaborá hantavirus within populations of its reservoir species, Akodon montensis. Seven trapping sessions were conducted during 2005‐2006 at four sites chosen to capture variable microhabitat conditions within the study site. Analysis of microhabitat preferences showed that A. montensis preferred areas with little forest overstory and denser vegetation cover on and near the ground. Moreover, there was a significant difference in the microhabitat occupied by antibody‐positive vs antibody‐negative rodents, indicating that microhabitats with greater overstory cover may promote transmission and maintenance of hantavirus in A. montensis.     

Analyses of gene flow among populations of deer mice (Peromyscus maniculatus) at sites near hantavirus pulmonary syndrome case-patient residences

Gene flow and potential for Sin Nombre virus (SNV) trafficking of the deer mouse (Peromyscus maniculatus) was studied in Delta and Mesa counties of western Colorado (USA). The study areas included Grand Mesa and surrounding grazing and agricultural areas. This area has several natural potential barriers to rodent gene flow, including rivers, cliffs, and mountains. Ten study sites were utilized in a spatially nested design ranging from 0.65-81 km apart; four of these sites were at or near human hantavirus pulmonary syndrome (HPS) case-patient residences. One HPS case occurred on the north side of Grand Mesa in 1993; the other three (two confirmed, one presumptive) occurred on the south side of Grand Mesa between 1999-2000. Blood and tissue samples were collected from each of 221 deer mice captured from 1999-2000. Blood samples were tested for IgG antibody to SNV. At least one deer mouse had antibody to SNV at nine of 10 sites. Genomic DNA was isolated from tissue samples and alleles at six microsatellite loci were amplified by polymerase chain reaction (PCR). Polymorphisms were resolved on denaturing polyacrylamide gels and visualized by silver staining. Traditional population genetic analyses of this study indicated moderate population subdivision among the populations surveyed, slight evidence of isolation by distance, and that the Gunnison River system may hinder gene flow in this area. Application of assignment tests indicated that approximately 73-85% of mice were assigned to their population of capture. Many of the misclassifications occurred among sites less than 1 km apart; however, some long-distance misclassifications were noted. Additionally, some misclassifications were noted among study sites on different sides of the Gunnison River system, indicating that the riparian corridor of this system may facilitate some gene flow. Overall, these data indicate that SNV trafficking is more likely at the local level, but some long-distance trafficking may be possible, especially where select habitat variables favor long-distance movements.     

Serosurvey of wild rodents for hantaviruses in Panama, 2000-2002

Five hundred fifty-six samples representing 24 species of small mammals (two species of marsupials and 22 rodents) were collected in Panama between February 2000 and July 2002. The samples were examined for antibodies to hantaviruses by means of enzyme-linked immunosorbent assay or immunoblot assays. The serologic results indicated that several rodent species might act as hantaviral reservoirs in Panama: Costa Rican pygmy rice rat (Oligoryzomys fulvescens costaricensis), four positive of 72 tested (5.6%); Cherrie's cane rat (Zygodontomys brevicauda cherriei), five of 108 (4.6%); Mexican deer mouse (Peromyscus mexicanus), one of 22 (5%); Mexican harvest mouse (Reithrodontomys mexicanus), one of seven (14%); Chiriquí harvest mouse (Reithrodontomys creper), one of two (50%); and Sumichrast's harvest mouse (Reithrodontomys sumichrasti), three of four (75%). Hantavirus infection in Peromyscus mexicanus and the three species of Reithrodontomys was caused by Rio Segundo hantavirus, a species of virus not previously reported from Panama. At least three hantaviruses, therefore, are known to infect populations of wild rodents in the country. However, given the total number of animals tested, the role of these rodent species in the epidemiology and epizootiology of hantavirus infections remains unclear.     

Brush mouse (Peromyscus boylii) population dynamics and hantavirus infection during a warm, drought period in southern Arizona

We monitored Limestone Canyon hantavirus (LSCV) antibody prevalence, host (brush mouse, Peromyscus boylii) abundance, and environmental variables (temperature and rainfall) in brush mice captured on three trapping webs in southern Arizona for 5 yr. Although seasonal patterns were subtle, we observed large multiyear variation in population abundance and antibody prevalence. Limestone Canyon hantavirus infection in brush mouse populations varied over time with prevalence ranging from 0% to 33%. At all trapping webs, evidence of infection disappeared completely for an extended period (up to 2 yr) and eventually reappeared, suggesting that dispersal may play a role in maintaining infection in brush mouse metapopulations. Weather during the study period was drier and warmer than average and these conditions, especially during spring through fall, may have contributed to low brush mouse population density and the local extinction of LSCV during the second year of the study. Nevertheless, population growth was associated with relatively warm, dry conditions during winter periods and a cool, wet spring and summer period in the fifth year of the study. After prolonged absence, LSCV infection was consistently detected only when brush mouse population abundance reached relatively high levels during that fifth year. Comparison of our results to similar studies suggests that stochastic events resulting in the loss or survival of a few infected mice in low-density host populations may result in local extinction of virus; reestablishment of infection may occur via immigration of infected individuals from adjacent populations, but may be successful only when populations are of sufficient density to support frequent rodent-to-rodent interactions and virus transmission.     

The oak browsing index correlates linearly with roe deer density: a new indicator for deer management?

Increasing populations of large herbivores during the last decades have had a major impact on vegetation. While several studies have looked for quantifying this impact in terms of plant biomass, plant survival or financial costs, the potential benefit of using the response of the vegetation to changes in browsing pressure by large herbivores to monitor their populations has been poorly investigated. As getting accurate estimates of density in populations of large herbivores is problematic, the use of indicators measuring the intensity of browsing might offer reliable alternative to managers. From the intensive monitoring of a roe deer population subject to an experimental manipulation of density, we looked for assessing the response of oak to changes of roe deer population size. Using a simple browsing index calculated from field data over 10 years, we found that this oak browsing index linearly increased with increasing population size of roe deer. This suggests that such an oak browsing index might be a reliable “indicator of ecological change” for monitoring roe deer populations in oak forests with natural regeneration.     

Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model

The mechanism(s) by which Sin Nombre (SN) hantavirus is maintained in deer mouse populations is unclear. Field studies indicate that transmission occurs primarily if not exclusively via a horizontal mechanism. Using an experimental deer mouse infection model in an outdoor laboratory, we tested whether infected rodents shed SN virus in urine, feces, and saliva, whether infected mice transmit infection to na?ve cage mates, and whether infected dams are able to vertically transmit virus or antibody to offspring. Using pooled samples of urine, feces, and saliva collected from mice infected 8 to 120 days postinoculation (p.i.), we found that a subset of saliva samples, collected between 15 and 90 days p.i., contained viral RNA. Parallel studies conducted on wild-caught, naturally infected deer mice showed a similar pattern of intermittent positivity, also only in saliva samples. Attempts to isolate virus through inoculation of cells or na?ve deer mice with the secreta or excreta of infected mice were uniformly negative. Of 54 attempts to transmit infection by cohousing infected deer mice with seronegative cage mates, we observed only a single case of transmission, which occurred between 29 and 42 days p.i. Dams passively transferred antibodies to neonatal pups via milk, and those antibodies persisted for at least 2 months after weaning, but none transmitted infection to their pups. Compared to other hantavirus models, SN virus is shed less efficiently and transmits inefficiently among cage mates. Transmission of SN virus among reservoir rodents may require factors that are not required for other hantaviruses.