Ecology, 88(8), 2007, pp. 1911–1916
? 2007 by the Ecological Society of America
ENDEMIC HANTAVIRUS INFECTION IMPAIRS THE WINTER
SURVIVAL OF ITS RODENT HOST
EVA R. KALLIO,1,2,3,6LIINA VOUTILAINEN,2OLLI VAPALAHTI,3,4,5ANTTI VAHERI,4,5HEIKKI HENTTONEN,2
ESA KOSKELA,1AND TAPIO MAPPES1
1Department of Biological and Environmental Science, P.O. Box 35, FIN-40014, University of Jyva ¨skyla ¨, Finland
2Vantaa Research Unit, Finnish Forest Research Institute, P.O. Box 18, Vantaa FIN-01301 Finland
3Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, University of Helsinki, P.O. Box 66,
FIN-00014 University of Helsinki, Finland
4Department of Virology, Haartman Institute, P.O. Box 21, FIN-00014 University of Helsinki, Finland
5HUCH Laboratory Diagnostics, P.O. Box 403, Helsinki FIN-00029 HUS Finland
infection ecology. Hantaviruses have coevolved with their hosts and are generally thought to
have little or no effect on host survival or reproduction. We examined the effect of Puumala
virus (PUUV) infection on the winter survival of bank voles (Myodes glareolus), the host of
this virus. The data were collected by monitoring 22 islands over three consecutive winters (a
total of 55 island populations) in an endemic area of central Finland. We show that PUUV
infected bank voles had a significantly lower overwinter survival probability than antibody
negative bank voles. Antibody negative female bank voles from low-density populations living
on large islands had the highest survival. The results were similar at the population level as the
spring population size and density were negatively correlated with PUUV prevalence in the
autumn. Our results provide the first evidence for a significant effect of PUUV on host survival
suggesting that hantaviruses, and endemic pathogens in general, deserve even more attention
in studies of host population dynamics.
The influence of pathogens on host fitness is one of the key questions in
dynamics; Puumala hantavirus; survival.
bank vole; endemic pathogen; infection; mortality factor; Myodes glareolus; population
The effect of parasite infection on the host population
is one of the major questions in infectious disease
ecology (Anderson and May 1979, Dobson and Hudson
1995). In wildlife, a parasite’s impact on its host
population may also affect the parasite’s own persis-
tence, and furthermore, the infection risk to other
species, including humans. Endemic parasites tend to
persist for long times in host populations with rather
stable prevalence. They do not usually induce severe
pathogenicity or obvious decreases in survival or
reproduction of their hosts (Anderson and May 1979,
Grenfell and Dobson 1995). Yet, they may induce
deleterious effects, and thus, decrease the fitness of the
hosts. These effects may be difficult to separate from
other factors that influence fitness of wildlife popula-
tions (Dobson and Hudson 1995, Feore et al. 1997,
Telfer et al. 2002, 2005).
For population-level regulation, the parasite must
influence the host reproduction or survival in a density-
dependent manner (Gulland 1995, Tompkins and Begon
1999). Although host regulation by parasitism is best
demonstrated by experimental studies, evidence for
parasites regulating their hosts is still rare. All informa-
tion on the influence of parasitism on host fitness, both
at individual and population levels, is valuable in
evaluating the role of parasites in host population
dynamics (Hudson et al. 1998, Tompkins and Begon
1999, Telfer et al. 2002, 2005 Cavanagh et al. 2004,
Burthe et al. 2006).
Puumala virus (PUUV) is a member of the genus
Hantavirus, each of which is carried by a specific rodent
host species; the host of PUUV is the bank vole (Myodes
[earlier, Clethrionomys] glareolus). Hantavirus infection
in the rodent host is chronic, i.e., the immune response
of the host does not clear the infection and virus
replication is persistent. Consequently, the host may be
infectious for the duration of life (Meyer and Schmal-
john 2000) and transmission of hantavirus is horizontal
(Gavrilovskaya et al. 1990, Kallio et al. 2006a). Despite
some evidence of cellular-level effects, hantavirus
infections have been thought to be asymptomatic in
their rodent hosts because of long coevolution between
them. No clinical illness, increased mortality, or reduced
fecundity caused by hantaviruses have been reported in
rodent hosts (e.g., Gavrilovskaya et al. 1990, Bernshtein
et al. 1999, Netski et al. 1999, Compton et al. 2004,
Kallio et al. 2006b). An exception was reported by
Calisher et al. (2005), who observed lower survival in Sin
Manuscript received 26 September 2006; revised 20 February
2007; accepted 27 March 2007. Corresponding Editor: M. F.
6Present address: Finnish Food Safety Authority, Mus-
tialankatu 3, Helsinki FIN-00790 Finland.
Nombre virus seropositive deer mice. However, as the
authors pointed out, the results may also be caused by
the older age of the infected mice. In humans, PUUV
causes a mild form of hemorrhagic fever with renal
syndrome; in Europe thousands of cases are diagnosed
annually (Vapalahti et al. 2003).
We studied the overwinter survival of bank voles in
relation to PUUV infection status over three consecutive
winters in a total of 55 island populations. The survival
of free-living voles was monitored by live-trapping the
populations in October and in May and analysed by
simultaneously measuring the individuals’ sex and age,
and population density.
Bank voles are characterized by a mean life expec-
tancy of only a few months, as only a fraction of
individuals survive over one winter (Pre ´ vot-Julliard et al.
1999). In central Finland, reproduction occurs from
May until mid-September (Koivula et al. 2003).
Successful overwintering is crucial for fitness of late
summer cohorts, as they usually delay breeding until the
following summer (Pre ´ vot-Julliard et al. 1999). Bank
vole populations show seasonal and multi-annual
fluctuations in abundance in most of Fennoscandia
and in our study area as well (Hansson and Henttonen
1985, Hanski et al. 1991).
Study site and design
The study was conducted on 55 island populations of
bank voles. A total of 22 islands were sampled over three
consecutive winters (21, 12, and 22 islands in 2002, 2003,
and 2004, respectively) in Lake Konnevesi, in central
Finland (628370N, 268200E). The sizes of the islands
varied from 0.24 to 3.20 ha and the minimum distance
from the mainland was 180 m. The islands were covered
by boreal forests (Hakkarainen et al. 2007), the natural
habitat for bank voles. As a part of a separate long-term
study examining the life histories of voles on islands
(unpublished data), new bank vole populations were
established on the islands each year in early June. For
the purposes of the current study, the island populations
were live trapped just before winter in late October for
three consecutive years. The trapping was conducted
using Ugglan Special live traps (Grahnab AB, Sweden)
baited with sunflower seeds and potatoes. The trap
density was 25 traps/ha spaced about 20 m from each
other. Prebaited traps were left on the islands for two
nights, after which they were set and checked over the
three consecutive days. The effectiveness of this trapping
procedure in catching the bank voles on small island
populations was separately studied by trapping 27 island
populations for several days (E. Kallio et al., unpublished
data). In that study, out of a total of 284 trapped bank
voles, 82% (233 individuals) were trapped during the
first night, 17% (48) on the second and only three new
individuals (1%) on the third night.
The voles trapped in October were transferred into the
laboratory, where they were individually marked, sexed,
and weighed to the nearest 0.1 g. The ages of the voles
were determined on the basis of the fur coat and whether
they were previously marked: marked individuals were
those trapped as adults the previous spring and thus
were more than a year old. A blood sample was taken
from each individual’s retro-orbital sinus with 18 lL
capillary tubes (Hemacrit tube, Hirschmann Laborger-
a ¨ te, Germany). Infection status was determined by
detecting the PUUV-specific IgG-antibodies using im-
munofluorescence assay (IFA; Vapalahti et al. 1995).
Because of the chronic nature of hantavirus infection,
the presence of IgG antibodies indicates a current
infection (Meyer and Schmaljohn 2000). Within a few
days of these procedures, the voles were returned to their
respective islands of capture.
The populations were re-monitored each spring (in
May) using similar trapping protocols as in the autumn.
All trapped individuals were taken to the laboratory
where they were identified and blood samples were
taken. Then they were either kept in the laboratory for
other studies or released back to the islands as part of
the summer studies.
Our sampling design may have resulted in a degree of
correlation between observations because groups of
samples were taken from the same islands during the
same winters. To control these potential sources of
pseudoreplication, we used generalized linear mixed
models (GLMM; Paterson and Lello 2003), which take
the potential spatial and temporal correlations of the
observations into account. The survival of bank voles
from October to May was analysed with GLMM with a
logit link function and binomial errors (as the survival of
each individual was a binary measure), and the
parameters were estimated using restricted maximum-
likelihood procedures (REML). PUUV infection status
(PUUV? or PUUVþ), sex (female or male) and age (,1
year or .1 year old) were used as categorical fixed
factors. Body mass, bank vole population density
(number of individuals per hectare) in October, and
the size of the island (ha) were used as continuous fixed
factors. Island identity and year were included in the
models as random factors. In addition, the following
population-level analyses were conducted: (1) the
extinction of bank vole populations during winter (no
voles vs. at least one vole in the population, binary
population-level outcome), (2) PUUV persistence until
spring (presence or absence of PUUV infected individ-
uals in the spring in the population, binary population-
level outcome), (3) bank vole population size (number of
bank voles on an island) in the spring, and (4) density
(number of bank voles per the size of the island [ha]) in
the spring (continuous response variables). Year was
included in these models as a random effect. The
explanatory variables were the host population size
EVA R. KALLIO ET AL. 1912Ecology, Vol. 88, No. 8
(number of individuals per island), the host population
density on the islands, the size of the islands, and PUUV
prevalence in the host population in the autumn.
Moreover, the PUUV prevalence in the spring (individ-
ual-level binary outcome, logit link function, and
binomial error) was studied using the island and year
as random factors.
The multicollinearity among the explanatory variables
in the full models was assessed by variance inflation
factors and tolerance values. In the case of collinearity,
variables were omitted based on biological meaning and
consequently the largest variance inflation factor was
1.42 and the lowest tolerance value 0.7, suggesting no
bias in the standard errors of regression coefficients
among the variables used in the models. In the absence
of model selection criteria, such as the Akaike Informa-
tion Criterion as standard method for comparing
GLMMs (Burnham and Anderson 2002, Johnson and
Omland 2004) we followed a step-down procedure to
select the final models. We started from the full models
including all variables that did not violate the collinear-
ity assumptions as main effects and two-way interac-
tions of the biologically meaningful possibilities. We
then simplified the model by removing the interaction
terms first and followed by nonsignificant variables (at
5% significance level) one by one. The fit statistics for the
models with binary outcomes were performed and the
outcome of generalized chi-square values divided by the
degrees of freedom was always ?1. This indicated that
no overdispersion was detected in our models. The
analyses were performed using SAS v. 9.1 statistical
software (SAS Institute 2002).
In total, 751 bank voles were released on the islands in
October during the three years of the study. Out of
these, 153 (20.5%) were PUUVþ, of which 89 (58.2%)
were females and 64 (41.8%) were males. A total of 107
individuals (14.3%) survived over the winter (Table 1).
Only five individuals (PUUVþ, one case; PUUV?, four
cases) were found to have moved to another island
between trapping sessions. Because the exact time of the
dispersal could not be determined, these individuals
were included in the analyses of the islands where they
were originally released in the autumn.
PUUV-infected bank voles had a significantly lower
overwinter survival than noninfected individuals. In
addition, survival was influenced by sex, population
density in autumn, and island size (Table 2, Fig. 1). The
age and body mass of individuals did not affect the
survival probability. Thus, the survival was highest in
non-infected females that inhabited large islands with
low bank vole density.
Out of a total of 55 island populations monitored for
overwintering survival, 38 populations survived until the
following spring. None of the predictor variables (bank
vole population density in autumn, PUUV prevalence in
autumn, island size) were related to extinction proba-
bility of the vole population during winter (P . 0.1 for
all of the effects). However, in the 38 surviving
populations, PUUV prevalence in the autumn was
related to lower bank vole population density and size
in spring (Table 3).
PUUV-infected individuals were present in 34 popu-
lations in the autumn and in 15 populations in the
spring. The persistence of PUUV in the populations
during the spring in the 38 populations that survived was
relation to PUUV (Puumala virus) infection status, sex, and
age in autumn.
Bank voles surviving from October to May in
.1 year old
,1 year old
estimates for the random factors.
Parameter estimates (logit scale) for a model of bank vole overwinter survival, including the covariance parameter
Source of variationStandard estimateErrordftP
Density in autumn
Note: Intercept represents a young female not infected with PUUV.
August 20071913 HANTAVIRUS IMPAIRS THE HOST’S SURVIVAL
positively related to autumn prevalence (F1,34¼7.79, P¼
0.009) and population density in the spring (F1,34¼8.28,
P ¼ 0.007). A spring blood sample was available from
103 out of the 107 individuals that survived, of which 34
were infected. In spring the individual-level infection
probability was not predicted by any of the individual or
population-level variables (see Table 2; P . 0.1 for all of
This study suggests that Puumala virus infection
significantly decreased the overwinter survival of its
rodent hosts in natural populations, despite the expec-
tation that hantaviruses have become well adapted to
their rodent hosts during the millions of years of co-
evolution (Nemirov et al. 2004). Therefore, despite some
cell-level pathological alterations (e.g., Gavrilovskaya et
al. 1990, Netski et al. 1999, Compton et al. 2004),
hantavirus infections have traditionally been considered
asymptomatic in their rodent hosts. No clinical illness or
decreases in fecundity and survival have been found to
be caused by hantavirus infections (Childs et al. 1989,
Gavrilovskaya et al. 1990, Bernshtein et al. 1999, Netski
et al. 1999, Compton et al. 2004, Kallio et al. 2006b). An
exception is from Calisher et al. (2005), who observed
lower survival in Sin Nombre virus seropositive deer
mice (Peromyscus maniculatus). As the authors pointed
out, however, the result may have been caused by the
greater age of infected mice, as old individuals are more
often infected than young ones. In our study, age did not
influence the survival of the bank voles (Table 2). We
cannot say much about dispersal differences between
infected and non-infected voles, but in general dispersal
seemed to be very low. This suggests that dispersal
would not explain the observed results.
Our novel results on the negative influence of
hantavirus infection on the rodent host may arise for
several reasons. We worked on relatively small islands
over periods of five to six months of frost and snow, so
that harsh environmental conditions, together with a
relatively large sample size in our study, may have
revealed the deleterious effects of PUUV infection.
During winters some parts of the islands may become
deprived of food and chronically infected voles may not
be able to compensate for the energetic costs induced by
the persistent elevation of the immune response (Telfer
et al. 2002). Compton et al. (2004) assumed that insulitis
and hyperglycemia in hantavirus-infected rodents may
cause a diabetes-like condition in the host. This, together
with the chronic replication of PUUV in the bank voles
(particularly in the lungs) and persistent antibody
production (Meyer and Schmaljohn 2000) may cause
the deleterious consequences observed here (e.g., Shel-
don and Verhulst 1996, Lochmiller and Deerenberg
2000, Norris and Evans 2000). In addition, the meta-
bolic rate of the infected individuals may be higher than
in the non-infected individuals, which could be especial-
ly detrimental for successful overwintering. Still another
explanation for the observed effect may be that infection
increases the vulnerability of the infected hosts to
predation (e.g., Hudson et al. 1992, Skorping and
Ho ¨ gstedt 2001). Although least weasels (Mustela nivalis
nivalis (L.)) and birds of prey were observed on the study
islands, the significance of this possible mechanism for
poorer survival of PUUV-infected voles currently
That high PUUV prevalence in autumn is related to
lower the bank vole density and population size in the
spring further supports the conclusion that PUUV
infection decreases bank vole survival, even though the
probability of population extinction was not predicted
by PUUV prevalence. Although PUUV infection
seemed to regulate bank vole populations, the role of
PUUV in the cyclic vole fluctuations could not be
evaluated in this study. It is important to bear in mind
that the most characteristic feature of Fennoscandian
vole cycles is the synchronous crash of all sympatric
species (Hansson and Henttonen 1988). An endemic
relation to PUUV (Puumala virus) infection and population
density: dashed line, PUUV? individuals; solid line, PUUVþ
Predicted survival of bank voles over winter in
bank vole population density (no. individuals/ha) and the
bank vole population size (no. individuals per island) in
Effects of the significant explanatory variables on the
Source of variationF dfP
Population density in spring
PUUV prevalence in autumn
Population density in autumn
Population size in spring
PUUV prevalence in autumn
Population size in autumn
Note: Year was used as a random factor in both of the linear
mixed models (covariance parameter estimates of year, 0 and
,0.02, for the models of population density and size,
EVA R. KALLIO ET AL.1914 Ecology, Vol. 88, No. 8
pathogen should, therefore, be able to infect and
regulate all local vole species in a similar manner. Thus,
vole population cycles in northern Fennoscandia, which
are mostly attributed to predation by specialist preda-
tors (reviewed, e.g., by Hansson and Henttonen 1988,
Hanski et al. 1991, Korpima ¨ ki et al. 2003), cannot be
driven only by PUUV because it is a bank vole specific
pathogen. However, as earlier suggested, microparasites
could modify vole dynamics (Soveri et al. 2000,
Cavanagh et al. 2004).
Low host population size and density are unfavorable
for the long-term persistence of directly transmitted
parasites, and therefore the lower overwintering success
of infected individuals should be disadvantageous from
the virus’ point of view(e.g., Tompkins et al.2002, Begon
et al. 2003, Sauvage et al. 2003). Although PUUV
survives outside of the host for a prolonged period of
time, especially in winter-like conditions (Kallio et al.
2006a), the virus faded out from 22 of 34 island
populations during the winter. Not surprisingly, the
higher the autumn PUUV prevalence and spring popu-
lation sizes were, the higher the persistence probability
was. However, in populations where PUUV persisted
over winter, the spring prevalence was not explained by
any of the measured population-level variables.
To summarize, our study strongly suggests that
PUUV infection can decrease survival of its free-ranging
host, the bank vole. PUUV infection in bank voles
should be further studied to clarify the mechanisms
causing the negative effects observed here. Moreover,
the role of endemic pathogens as mortality factors
deserves attention in theoretical and empirical studies on
We are grateful to Michael Begon, Kirsi Palviainen, Jukka
Palo, Mikael Mokkonen, and Samuli Helle for constructive
comments on the manuscript. This study was financially
supported by the Finnish Cultural Foundation to E. R. Kallio,
Academy of Finland (grant numbers 63789, 202166, and
206091 to T. Mappes; 100143, 78777, and 103148 to E.
Koskela), EU (contract QLRT-2002-01358 to A. Vaheri and
H. Henttonen), and grant GOCE-2003-010284 EDEN. The
paper is catalogued by the EDEN Steering Committee as
EDEN0022 (catalog available at hhttp://www.eden-fp6project.
net/i). This research adhered to the Association for the Study of
Animal Behaviour/Animal Behavior Society Guidelines for the
Use of Animals in Research, the legal requirements in Finland,
and all institutional guidelines.
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