Sin Nombre Virus and Rodent Species Diversity: A Test of the Dilution and Amplification Hypotheses

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.     

Bot fly parasitism of the red-backed vole: host survival,infection risk,and population growth

Parasites can play an important role in the dynamics of host populations, but empirical evidence remains sparse. We investigated the role of bot fly (Cuterebra spp.) parasitism in red-backed voles (Myodes gapperi) by first assessing the impacts of the parasite on the probability of vole survival under stressful conditions as well as on the reproductive activity of females. We then identified the main factors driving both the individual risk of infection and the abundance of bot flies inside red-backed voles. Finally, we evaluated the impacts of bot fly prevalence on the growth rate of vole populations between mid-July and mid-August. Thirty-six populations of red-backed voles were sampled in the boreal forest of Québec, Canada. The presence and the abundance of parasites in voles, two host life history traits (sex and body condition), three indices of habitat complexity (tree basal area, sapling basal area, coarse woody debris volume), and vole abundance were considered in models evaluating the effects of bot flies on host populations. We found that the probability of survival of red-backed voles in live traps decreased with bot fly infection. Both the individual risk of infection and the abundance of bot flies in red-backed voles were driven mainly by vole abundance rather than by the two host life history traits or the three variables of habitat complexity. Parasitism had population consequences: bot fly prevalence was linked to a decrease in short-term growth rate of vole populations over the summer. We found that bot flies have the potential to reduce survival of red-backed voles, an effect that may apply to large portions of populations. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Testing Mechanisms of the Dilution Effect: Deer Mice Encounter Rates, Sin Nombre Virus Prevalence and Species Diversity

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 investigated 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 prevalence: (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.     

Competition, predation and interspecific synchrony in cyclic small mammal communities

Although competition and predation are considered to be among the most important biotic processes influencing the distribution and abundance of species in space and time, the relative and interactive roles of these processes in communities comprised of cyclically fluctuating populations of small mammals are not well known. We examined these processes in and among populations of field voles, sibling voles, bank voles and common shrews in western Finland, using spatially replicated trapping data collected four times a year during two vole cycles (1987–1990 and 1997–1999). Populations of the four species exhibited relatively strong interspecific temporal synchrony in their multiannual fluctuations. During peak phases, we observed slight deviations from close temporal synchrony: field vole densities peaked at least two months earlier than those of either sibling voles or bank voles, while densities of common shrews peaked even earlier. The growth rates of all four coexisting small mammal species were best explained by their own current densities. The growth rate of bank vole populations was negatively related to increasing densities of field voles in the increase phase of the vole cycle. Apart from this, no negative effects of interspecific density, direct or delayed, were observed among the vole species. The growth rates of common shrew populations were negatively related to increasing total rodent (including water voles and harvest mice) densities in the peak phase of the vole cycle. Sibling voles appeared not to be competitively superior to field voles on a population level, as neither of these Microtus voles increased disproportionately in abundance as total rodent density increased. We suggest that interspecific competition among the vole species may occur, but only briefly, during the autumn of peak years, when the total available amount of rodent habitat becomes markedly reduced following agricultural practices. Our results nonetheless indicate that interspecific competition is not a strong determinant of the structure of communities comprised of species exhibiting cyclic dynamics. We suggest that external factors, namely predation and shortage of food, limit densities of vole populations below levels where interspecific competition occurs. Common shrews, however, appear to suffer from asymmetric space competition with rodents at peak densities of voles; this may be viewed as a synchronizing effect.     

Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species

Spatial structure in the distribution of pathogen infection can influence both epidemiology and host-parasite coevolutionary processes. It may result from the spatial heterogeneity of intrinsic and extrinsic factors, or from the local population dynamics of hosts and parasites. In this study, we investigated the effects of landscape, host dispersal and demography (population abundance and phase of the fluctuation) on the distribution of a gastro-intestinal nematode Trichuris arvicolae in the fossorial water vole Arvicola terrestris sherman. This rodent exhibits outbreaks occurring regularly in Franche-Comté (France). Thirteen out-of-phase populations were studied in autumn 2003. They exhibited highly different T. arvicolae prevalences. The heterogeneity in prevalences was not explained by population structure, landscape or vole abundance, but by the phase of the vole population fluctuations. Populations at the end of the high density phase showed null prevalence whereas populations in increase or outbreak phases exhibited higher prevalences. Population genetic analyses based on microsatellites revealed significant differentiation between vole populations, and higher dispersal rates of young voles compared with old ones. These younger individuals were also infected more frequently than older voles. This suggested a role of host dispersal in the distribution of T. arvicolae. However, there was a strong discrepancy between the spatial patterns of prevalence and of host genetics or demographic phase. Genetic differentiation and differences in demographic phase exhibited significant spatial autocorrelations whereas prevalence did not. We concluded that the distribution of T. arvicolae is influenced by vole dispersal, although this effect might be overwhelmed by local adaptation processes or environmental conditions.     

The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes

Effects of population fluctuation of the gray-sided vole(Clethrionomys rufocanus) on the prevalence (infection rates) of the parasiteEchinococcus multilocularis in red fox(Vulpes vulpes) populations was investigated from 1985 to 1992 in eastern Hokkaido (Abashiri, Nemuro, and Kushiro area), Japan. This parasite needs two hosts to complete its life cycle; the gray-sided vole as its intermediate host and the red fox as its final host. We found that: (1) Infection rates in foxes depended on the current-year abundance of voles in all three study areas, particularly in Abashiri. (2) In addition to this direct density-dependence, delayed density-dependence between the infection rate and the prior-year abundance of voles was detected in Nemuro and in Kushiro. (3) The regional differences in density-dependence pattern were related to regional differences in the winter food habits of red foxes: in Abashiri the proportion of voles in the fox’s diet greatly decreases in winter, while the proportion remains high in winter in Nemuro and in Kushiro, probably because of shallower snowpack. These results suggest that infection rates in foxes in Abashiri were less influenced by the prior-year prevalence, since the infection cycle might be interrupted in winter, when voles became less important in fox’s diet. In contrast, the state of the prevalence may carry over from year to year in Nemuro and in Kushiro, because red foxes continue to eat a considerable amount of voles throughout year. The regionally contrasted results for the relationship between infection rate in foxes and vole abundance were parallel to the regional difference in fluctuation pattern of vole populations, which are highly variable in Abashiri area, but less variable in Kushiro-Nemuro area. Drastic change in vole populations appears to affect the host-parasite system.     

Analysis of ectoparasites (chigger mites,gamasid mites,fleas and sucking lice) of the Yunnan red‐backed vole (Eothenomys miletus) sampled throughout its range in southwest China

The Yunnan red‐backed vole Eothenomys miletus (Rodentia: Cricetidae) is an endemic rodent species and reservoir host of zoonoses in southwest China. Based on a large host sample (2463 voles collected from 39 localities between 2001 and 2013), a general analysis of four categories of ectoparasite (fleas, sucking lice, chigger mites and gamasid mites) on E. miletus across its entire range of distribution was made. This analysis identified a total of 71 895 ectoparasites belonging to 320 species (30 species of flea, 9 of sucking louse, 106 of gamasid mite and 175 of chigger mite) with a high prevalence (87%), mean abundance (29.19) and mean intensity (33.69). Of the 18 vector species of zoonoses found on E. miletus, the flea Ctenophthalmus quadratus (Siphonaptera: Hystrichopsyllidae) and chigger mite Leptotrombidium scutellare (Trombidiformes: Trombiculidae) were the dominant species; these are the main vectors of zoonoses in China. All of the dominant parasite species showed an aggregated distribution pattern. Male voles harboured more species of parasite than females. Chigger mites represented the most abundant species group on voles and their prevalence was positively correlated with mean abundance (r = 0.73; P < 0.05). As a single rodent species, E. miletus has a high potential to harbour abundant ectoparasites with high species diversity and high rates of infestation. The sex of the vole affects ectoparasite infestation.     

Long-term responses in population dynamics and diversity of small mammals in riparian and upland habitats within an agricultural landscape

Riparian zones in agricultural landscapes provide linear non-crop habitats for a variety of plant and mammal species, and hence are an important component of biodiversity. To date, variable responses of abundance, species richness, and species diversity of small mammals have been recorded in riparian and upland habitats. To address this variability, we provide a detailed analysis of seasonal changes in abundance and diversity of terrestrial small-mammal communities over a 7-year period within an agricultural landscape in south-central British Columbia, Canada. We tested the hypotheses (H) that abundance, species richness, and species diversity of communities of small mammals (H₁), and demographic parameters of reproduction, recruitment, and survival of the major species: deer mouse (Peromyscus maniculatus) and montane vole (Microtus montanus) (H₂), would be higher in riparian than upland habitats. Mean total abundance of small mammals was higher in summer and winter, and species richness higher in summer, in riparian than hedgerow habitats. Winter population data supported the total and species abundance patterns for small mammals, but species richness was similar, and diversity lower, in riparian than hedgerow sites during winter periods. Deer mice were the dominant species in terms of abundance and reproductive output for pregnancies and recruitment, but not survival, in riparian sites. Montane voles were similar in abundance and demographic parameters in the two habitats. House mice (Mus musculus) preferred hedgerows and wandering shrews (Sorex vagrans) riparian sites. Demographic parameters for deer mice and montane voles indicated that both riparian and hedgerow sites were “source” rather than “sink” habitats, and likely contribute to maintenance of mammal diversity in agricultural landscapes.     

Delayed density-dependent prevalence of Sin Nombre virus infection in deer mice (Peromyscus maniculatus) in central and western Montana

Understanding how transmission of zoonoses takes place within reservoir populations, such as Sin Nombre virus (SNV) among deer mice (Peromyscus maniculatus), is important in determining the risk of exposure to other hosts, including humans. In this study, we examined the relationship between deer mouse populations and the prevalence of antibodies to SNV, a system where the effect of host population abundance on transmission is debated. We examined the relationship between abundance of deer mice in late summer-early autumn and SNV antibody prevalence the following spring-early summer (termed delayed density-dependent [DDD] prevalence of infection) at both regional and local scales, using 12 live-trapping grids for 11-14 yr, across central and western Montana. When all trapping grids were combined (regional scale), there was a significant DDD relationship for individual months and when months within seasons were averaged. However, within individual grids (local scale), evidence of DDD prevalence of infection was observed consistently at only one location. These findings suggest that, although there is evidence of DDD prevalence of infection at regional scales, it is not always apparent at local scales, possibly because the regional pattern of DDD infection prevalence is driven by differences in abundance and prevalence among sites, rather than in autumn-spring delays. Transmission of SNV may be more complex than the original hypothesis of autumn-spring delayed density dependence suggests. This complexity is also supported by recent modeling studies. Empirical investigations are needed to determine the duration and determinants of time-lagged abundance and antibody prevalence. Our study suggests predicting local, human exposure risk to SNV in spring, based on deer mouse abundance in autumn, is unlikely to be a reliable public health tool, particularly at local scales.     

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.     

The role of deer in facilitating the spatial spread of the pathogen Borrelia burgdorferi

Borrelia burgdorferi is a vector-bourne zoonosis which propagates in wild populations of rodents and deer. The latter are incompetent for the pathogen but are required for the life cycle of hard-backed ticks which act as a vector for the pathogen. Increasing the diversity of hosts has previously suggested the presence of a ‘dilution effect’ in which such an increase reduces successful pathogen transmission as it increases the chance that a tick will encounter an incompetent host. This paper will produce a model which shows that whilst a dilution effect is possible for a system in which deer are the only incompetent host, this effect is not likely to be strong. Extending the population dynamics to include movement of deer into regions previously only inhabited by competent hosts, we find that, although ticks come in with the deer, there is a significant time lag before Borrelia appears.     

Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis

Many zoonotic diseases are caused by rodent-borne viruses. Major fluctuations in the transmission of these viruses have been related to large changes in reservoir host population numbers due to external factors. However, the impact of the pathogen itself on the demography of its reservoir host is often overlooked. We investigated the impact of Puumala virus (PUUV) on survival and reproductive maturation probability of its reservoir host, the bank vole (Myodes glareolus). Three years (2004-06) of data from nine independent sites in southern Belgium were collected and analyzed with a capture-mark-recapture (CMR) method that includes statistical correction for the variation in capture probability of voles. A multistate model based on four states of reproductive activity and PUUV immunoglobulin G (IgG) antibody status was used to estimate survival and probability of transition from one reproductive or infection state to another. Although survival estimates for reproductively active voles were similar between infected and noninfected individuals, PUUV infection in reproductively inactive voles decreased mean monthly survival by 14%. PUUV infection was associated with a threefold increase in the probability of reproductive maturation in bank voles. Moreover, the probability of PUUV IgG seroconversion was three times higher for reproductively active voles compared to reproductively inactive voles. Our model indicates that PUUV infection may alter bank vole population dynamics by affecting both survival and maturation in its host. Additional studies, using CMR methodology with shorter time intervals between trapping sessions and possibly a longer duration, are needed to confirm these findings.     

Dampening of population cycles in voles affects small mammal community structure,decreases diversity,and increases prevalence of a zoonotic disease

Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.     

Vole fluctuations,red fox responses,predation on fawns,and roe deer dynamics in a temperate latitude

The alternative prey hypothesis predicts that predators respond both functionally and numerically (with a time lag) to fluctuations in the main prey abundance, which affects the survival of alternative prey. This pattern was found in northern Europe in the community formed by voles (Microtidae), red foxes (Vulpes vulpes) and roe deer (Capreolus capreolus). We studied the same predator—prey community in a temperate latitude where, according to the predation hypothesis, only the functional response of predators to changes in main prey availability should occur. In the years 1997–2007, in western Poland, we estimated the index of common vole (Microtus arvalis) abundance (burrow counts), the density of foxes (spotlight counts), the young production in foxes (young/adult ratio), the index of fox predation on fawns (prey remains near dens) as well as the reproduction index (fawn/female ratio) and density of roe deer (total counts). The vole abundance fluctuated considerably, the young production in foxes did not correlate with the main prey availability, but the density of foxes showed direct numerical response. The index of fox predation on fawns decreased with the vole abundance and negatively affected the fawn/female ratio in roe deer. Thus, the relationships between voles and foxes were not fully consistent with the predation hypothesis. The direct numerical response of foxes should tend to stabilize this predator—prey community. It is suggested, however, that responses showed by vole-eating predators in temperate latitudes may sometimes affect their alternative prey, including animals with unfavourable conservation status.     

Host community structure and infestation by ixodid ticks: repeatability,dilution effect and ecological specialization

Abundance of a species in a location results from the interplay between the intrinsic properties of that species and the extrinsic properties, both biotic and abiotic, of the local habitat. Intrinsic factors promote among-population stability in abundance, whereas extrinsic factors generate variation among populations of a species. We studied (a) repeatability and (b) the effect of abundance and species richness of small mammals on the level of their infestation by larvae and nymphs of Ixodes ricinus (ecological generalist) and Ixodes trianguliceps (ecological specialist). We asked if tick infestation parameters are characteristic (=repeatable) for a particular host species or a particular stage of a particular tick species. We also asked how abundance and diversity of hosts affect the level of tick infestation on a particular host species. We predicted that the dilution effect (decrease in tick infestation levels with an increase of host abundance and/or species richness) will be better expressed in an ecological generalist, I. ricinus, than in an ecological specialist, I. trianguliceps. We found that (a) tick abundance, prevalence and aggregation were generally repeatable within tick species/stage; (b) tick abundance and prevalence, but not the aggregation level, were repeatable within host species; (c) the proportion of variance among samples explained by the differences between tick species and stages (as opposed to within-tick species and stage) was higher than that explained by the differences between host species (as opposed to within host species); and (d) the relationship between tick infestation parameters and host abundance and diversity revealed the dilution effect for I. ricinus but not for I. trianguliceps.     

Avian host community structure and prevalence of West Nile virus in Chicago,Illinois

Vertebrate host diversity has been postulated to mediate prevalence of zoonotic, vector-borne diseases, such that as diversity increases, transmission dampens. This “dilution effect” is thought to be caused by distribution of infective bites to incompetent reservoir hosts. We quantified avian species richness, avian seroprevalence for antibodies to West Nile virus (WNV), and infection of WNV in Culex mosquitoes, in the Chicago metropolitan area, Illinois, USA, a region of historically high WNV activity. Results indicated high overall avian seroprevalence and variation in seroprevalence across host species; however, there was no negative correlation between avian richness and Culex infection rate or between richness and infection status in individual birds. Bird species with high seroprevalence, especially northern cardinals and mourning doves, may be important sentinels for WNV in Chicago, since they were common and widespread among all study sites. Overall, our results suggest no net effect of increasing species richness to West Nile virus transmission in Chicago. Other intrinsic and extrinsic factors, such as variation in mosquito host preference, reservoir host competence, temperature, and precipitation, may be more important than host diversity for driving interannual variation in WNV transmission. These results from a fine-scale study call into question the generality of a dilution effect for WNV at coarser spatial scales.     

Temporal and Spatial Analysis of Sin Nombre Virus Quasispecies in Naturally Infected Rodents

Sin Nombre virus (SNV) is thought to establish a persistent infection in its natural reservoir, the deer mouse (Peromyscus maniculatus), despite a strong host immune response. SNV-specific neutralizing antibodies were routinely detected in deer mice which maintained virus RNA in the blood and lungs. To determine whether viral diversity played a role in SNV persistence and immune escape in deer mice, we measured the prevalence of virus quasispecies in infected rodents over time in a natural setting. Mark-recapture studies provided serial blood samples from naturally infected deer mice, which were sequentially analyzed for SNV diversity. Viral RNA was detected over a period of months in these rodents in the presence of circulating antibodies specific for SNV. Nucleotide and amino acid substitutions were observed in viral clones from all time points analyzed, including changes in the immunodominant domain of glycoprotein 1 and the 3' small segment noncoding region of the genome. Viral RNA was also detected in seven different organs of sacrificed deer mice. Analysis of organ-specific viral clones revealed major disparities in the level of viral diversity between organs, specifically between the spleen (high diversity) and the lung and liver (low diversity). These results demonstrate the ability of SNV to mutate and generate quasispecies in vivo, which may have implications for viral persistence and possible escape from the host immune system.     

Woodland recovery after suppression of deer: cascade effects for small mammals, wood mice (Apodemus sylvaticus) and bank voles (Myodes glareolus)

Over the past century, increases in both density and distribution of deer species in the Northern Hemisphere have resulted in major changes in ground flora and undergrowth vegetation of woodland habitats, and consequentially the animal communities that inhabit them. In this study, we tested whether recovery in the vegetative habitat of a woodland due to effective deer management (from a peak of 0.4-1.5 to <0.17 deer per ha) had translated to the small mammal community as an example of a higher order cascade effect. We compared deer-free exclosures with neighboring open woodland using capture-mark-recapture (CMR) methods to see if the significant difference in bank vole (Myodes glareolus) and wood mouse (Apodemus sylvaticus) numbers between these environments from 2001-2003 persisted in 2010. Using the multi-state Robust Design method in program MARK we found survival and abundance of both voles and mice to be equivalent between the open woodland and the experimental exclosures with no differences in various metrics of population structure (age structure, sex composition, reproductive activity) and individual fitness (weight), although the vole population showed variation both locally and temporally. This suggests that the vegetative habitat--having passed some threshold of complexity due to lowered deer density--has allowed recovery of the small mammal community, although patch dynamics associated with vegetation complexity still remain. We conclude that the response of small mammal communities to environmental disturbance such as intense browsing pressure can be rapidly reversed once the disturbing agent has been removed and the vegetative habitat is allowed to increase in density and complexity, although we encourage caution, as a source/sink dynamic may emerge between old growth patches and the recently disturbed habitat under harsh conditions.     

The effect of landscape heterogeneity and host movement on a tick-borne pathogen

Landscape heterogeneity can be instrumental in determining local disease risk, pathogen persistence and spread. This is because different landscape features such as habitat type determine the abundance and spatial distributions of hosts and pathogen vectors. Therefore, disease prevalence and distribution are intrinsically linked to the hosts and vectors that utilise the different habitats. Here, we develop a simplified reaction diffusion model of the louping-ill virus and red grouse (Lagopus lagopus scoticus) system to investigate the occurrence of a tick-borne pathogen and the effect of host movement and landscape structure. Ticks (Ixodes ricinus), the virus-vector, are dispersed by a virally incompetent tick host, red deer (Cervus elephus), between different habitats, whilst the virus infects only red grouse. We investigated how deer movement between different habitats (forest and moorland) affected tick distribution and hence prevalence of infected ticks and grouse and hence, the effect of habitat size ratio and fragmentation on infection. When habitat type has a role in the survival of the pathogen vector, we demonstrated that habitat fragmentation can have a considerable effect on infection. These results highlight the importance of landscape heterogeneity and the proximity and size of adjacent habitats when predicting disease risk in a particular location. In addition, this model could be useful for other pathogen systems with generalist vectors and may inform policy on possible disease management strategies that incorporate host movements.     

Spatiotemporal dynamics of Puumala hantavirus in suburban reservoir rodent populations

The transmission of pathogens to susceptible hosts is dependent on the vector population dynamics. In Europe, bank voles (Myodes glareolus) carry Puumala hantavirus, which causes nephropathia epidemica (NE) in humans. Fluctuations in bank vole populations and epidemics in humans are correlated but the main factors influencing this relationship remain unclear. In Belgium, more NE cases are reported in spring than in autumn. There is also a higher incidence of human infections during years of large vole populations. This study aimed to better understand the link between virus prevalence in the vector, vole demography, habitat quality, and human infections. Three rodent populations in different habitats bordering Brussels city, Belgium, were studied for two years. The seroprevalence in voles was influenced first by season (higher in spring), then by vole density, vole weight (a proxy for age), and capture site but not by year or sex. Moreover, voles with large maximal distance between two captures had a high probability for Puumala seropositivity. Additionally, the local vole density showed similar temporal variations as the number of NE cases in Belgium. These results showed that, while season was the main factor influencing vole seroprevalence, it was not sufficient to explain human risks. Indeed, vole density and weight, as well as the local habitat, were essential to understanding the interactions in these host‐pathogen dynamics. This can, in turn, be of importance for assessing the human risks.