The impact of wildlife and environmental factors on hantavirus infection in the host and its translation into human risk.

Identifying factors that drive infection dynamics in reservoir host populations is essential in understanding human risk from wildlife-originated zoonoses. We studied zoonotic Puumala orthohantavirus (PUUV) in the host, the bank vole (Myodes glareolus), populations in relation to the host population, rodent and predator community and environment-related factors and whether these processes are translated into human infection incidence. We used 5-year rodent trapping and bank vole PUUV serology data collected from 30 sites located in 24 municipalities in Finland. We found that PUUV seroprevalence in the host was negatively associated with the abundance of red foxes, but this process did not translate into human disease incidence, which showed no association with PUUV seroprevalence. The abundance of weasels, the proportion of juvenile bank voles in the host populations and rodent species diversity were negatively associated with the abundance index of PUUV positive bank voles, which, in turn, showed a positive association with human disease incidence. Our results suggest certain predators, a high proportion of young bank vole individuals, and a diverse rodent community, may reduce PUUV risk for humans through their negative impacts on the abundance of infected bank voles.

Age-related effects of chronic hantavirus infection on female host fecundity.

1. Pathogens often cause detrimental effects to their hosts and, consequently, may influence host population dynamics that may, in turn, feed back to pathogen transmission dynamics. Understanding fitness effects of pathogens upon animal host populations can help to predict the risks that zoonotic pathogens pose to humans. 2. Here we determine whether chronic infection by Puumala hantavirus (PUUV) affects important fitness-related traits, namely the probability of breeding, reproductive effort and mother and offspring condition, in the bank vole (Myodes glareolus). Using 9 years empirical data in a PUUV endemic area in Central Finland, we found differences between reproductive characteristics of PUUV-infected and uninfected female bank voles. 3. Young infected females had a significantly higher, and old individuals lower, likelihood of reproducing than uninfected animals during the middle of the breeding season. The implication is that PUUV infection may have long-term deleterious effects that are observed at old age, while in young individuals, the infection may enhance breeding probability by directing resources towards current breeding. 4. Moreover, PUUV infection was related with the mother's body condition. Infected mothers were in poorer condition than uninfected mothers in the early breeding season, but were in better condition than uninfected mothers during the middle of the breeding season. Offspring body condition was positively associated with mother's body condition, which, in turn, was related to the PUUV infection status of the mother. 5. Our findings indicate that chronic infection may affect the reproduction of female hosts, but the effect is dependent on the host age. The effect of chronic hantavirus infection was small and density-independent and hence unlikely to contribute to the cyclic population dynamics of the host. However, the effects on a female's reproductive output might affect the abundance of young susceptible individuals in the population and hence influence the transmission and persistence of the pathogen. Although experimental and long-term capture-mark-recapture studies are required to further clarify the fitness effects of hantavirus infection and their consequences for pathogen dynamics, this study shows that the infection may have complex effects that are dependent on the age of the individual and the time of the breeding season.

Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history.

1. The effects of environment experienced during early development on phenotype as an adult has started to gain vast amounts of interest in various taxa. Some evidence on long-term effects of juvenile environment is available, but replicated experimental studies in wild animals are still lacking. 2. Here we report the first replicated experiment in wild mammals which examines the long-term effects of juvenile and adult environments on individual fitness (reproduction, survival and health). The early development of bank vole (Myodes glareolus) individuals took place in either food-supplemented or un-supplemented outdoor enclosures. After the summer, adult individuals were reciprocally changed to either a similar or opposite resource environment to overwinter. 3. Adult environment had an overriding effect on reproductive success of females so that females overwintering in food-supplemented enclosures had a higher probability of breeding and advanced the initiation of breeding. However, the characteristics of their litters were determined by juvenile environment: females initially grown in food-supplemented conditions subsequently produced larger litters with bigger pups and a male-biased sex ratio. 4. In males, individuals growing in un-supplemented conditions had the highest survival irrespective of adult environment during winter, whereas in females, neither the juvenile nor adult environments affected their survival significantly. The physiological condition of voles in spring, as determined by haematological parameters, was also differentially affected by juvenile (plasma proteins and male testosterone) and adult (haematocrit) environments. 5. Our results suggest that (i) life-history trajectories of voles are not strictly specialized to a certain environment and (ii) the plastic life-history responses to present conditions can actually be caused by delayed effects of the juvenile environment. More generally, the results are important for understanding the mechanisms of delayed life-history effects as well as recognizing their population dynamic consequences.

Yersinia spp. in Wild Rodents and Shrews in Finland.

Yersinia enterocolitica and Yersinia pseudotuberculosis are important zoonotic bacteria causing human enteric yersiniosis commonly reported in Europe. All Y. pseudotuberculosis strains are considered pathogenic, while Y. enterocolitica include both pathogenic and nonpathogenic strains which can be divided into six biotypes (1A, 1B, and 2-5) and about 30 serotypes. The most common types causing yersiniosis in Europe are Y. enterocolitica bioserotypes 4/O:3 and 2/O:9. Strains belonging to biotype 1A are considered as nonpathogenic because they are missing important virulence genes like the attachment-invasion-locus (ail) gene in the chromosome and the virulence plasmid. The role of wild small mammals as a reservoir of enteropathogenic Yersinia spp. is still obscure. In this study, the presence of Yersinia spp. was examined from 1840 wild small mammals, including voles, mice, and shrews, trapped in Finland during a 7-year period. We isolated seven Yersinia species. Y. enterocolitica was the most common species, isolated from 8% of the animals; while most of these isolates represented nonpathogenic biotype 1A, human pathogenic bioserotype 2/O:9 was also isolated from a field vole. Y. pseudotuberculosis of bioserotype 1/O:2 was isolated from two shrews. The ail gene, which is typically only found in the isolates of biotypes 1B and 2-5 associated with yersiniosis, was frequently (23%) detected in the nonpathogenic isolates of biotype 1A and sporadically (6%) in Yersinia kristensenii isolates. Our results suggest that wild small mammals, especially voles, may serve as carriers for ail-positive Y. enterocolitica 1A and Y. kristensenii. We also demonstrate that voles and shrews sporadically excrete pYV-positive Y. enterocolitica 2/O:9 and Y. pseudotuberculosis 1/O:2, respectively, in their feces and, thus, can serve as a contamination source for vegetables by contaminating the soil.

Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment.

We manipulated the primary brood size of Eurasian treecreepers (Certhia familiaris) breeding in different sized forest patches (0.5-12.8 ha) in moderately fragmented landscapes. We examined the effects of brood size manipulation (reduced, control, enlarged) and forest patch size on physiological stress (heterophil-lymphocyte ratios; H/L), body condition and cell-mediated immunocompetence (phytohaemagglutinin test). Nestlings' H/L ratios were negatively related to forest patch area in control and enlarged broods, whereas no effects were found in reduced broods. The effects of forest patch area were strongest in enlarged broods, which had, in general, twofold higher H/L ratios than control and reduced broods. The elevated H/L ratios were positively related to nestling mortality and negatively correlated with body-condition indices suggesting that the origin of stress in nestlings was mainly nutritional. Cell-mediated immunity of nestlings was not related to brood manipulation or to forest patch size. Also, the H/L ratios of adults were not related to brood manipulation or forest patch size. In addition, parental H/L ratios and body condition were not related to nestling H/L ratios. Our results suggest that during the breeding period the deleterious effects of habitat loss are seen explicitly in growing young.

Forest management is associated with physiological stress in an old-growth forest passerine.

We investigated how physiological stress in an area-sensitive old-growth forest passerine, the Eurasian treecreeper (Certhia familiaris), is associated with forest fragmentation and forest structure. We found evidence that the concentrations of plasma corticosterone in chicks were higher under poor food supply in dense, young forests than in sparse, old forests. In addition, nestlings in large forest patches had lower corticosterone levels and a better body condition than in small forest patches. In general, corticosterone levels were negatively related to body condition and survival. We also found a decrease in corticosterone levels within the breeding season, which may have been a result of an increase in food supply from the first to the second broods. Our results suggest that forest fragmentation may decrease the fitness of free-living individual treecreepers.

Forest fragmentation is associated with primary brood sex ratio in the treecreeper (Certhia familiaris).

We studied the primary brood sex ratio of an old-growth forest passerine, the Eurasian treecreeper (Certhia familiaris), along a gradient of forest fragmentation. We found evidence that male nestlings were more costly to produce, since they suffered twofold higher nestling mortality and were larger in body size than females. Furthermore, the proportion of males in the brood was positively associated with the provisioning rate and the amount of food delivered to the nestlings. During the first broods, a high edge density and a high proportion of pine forests around the nests were related to a decreased production of males. The densities of spiders, the main food of the treecreeper, were 38% higher on spruce trunks than on pine trunks. This suggests that pine-dominated territories with female-biased broods may have contained less food during the first broods. The observation was further supported by the fact that the feeding frequencies were lower in territories with high proportions of pines. In the second broods, territories with a high forest patch density produced female-biased broods, whereas high-quality territories with a large amount of deciduous trees and mixed forests produced male-biased broods. Our results suggest that habitat quality as measured by habitat characteristics is associated with sex allocation in free-living birds.