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Nuclear accidents underpin the need to quantify the ecological mechanisms which determine injury to ecosystems from chronic low-dose radiation. Here, we tested the hypothesis that ecological mechanisms interact with ionizing radiation to affect natural populations in unexpected ways. We used large-scale replicated experiments and food manipulations in wild populations of the rodent, Myodes glareolus, inhabiting the region near the site of the Chernobyl disaster of 1986. We show linear decreases in breeding success with increasing ambient radiation levels with no evidence of any threshold below which effects are not seen. Food supplementation of experimental populations resulted in increased abundances but only in locations where radioactive contamination was low (i.e., below % 1 lSv/h). In areas with higher contamination , food supplementation showed no detectable effects. These findings suggest that chronic low-dose-rate irradiation can decrease the stability of populations of key forest species, and these effects could potentially scale to broader community changes with concomitant consequences for the ecosystem functioning of forests impacted by nuclear accidents.
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Ecological mechanisms can modify radiation effects in a key forest
mammal of Chernobyl
TAPIO MAPPES,
1,
ZBYSZEK BORATY
NSKI,
1,2
KATI KIVISAARI,
1
ANTON LAVRINIENKO,
3
GENNADI MILINEVSKY,
4
TIMOTHY A. MOUSSEAU,
5
ANDERS P. M ØLLER,
6
EUGENE TUKALENKO,
1,3,7
AND PHILLIP C. WATTS
1,3
1
Department of Biological and Environmental Science, University of Jyv
askyl
a, P.O. Box 35, Jyv
askyl
a FI-40014 Finland
2
CIBIO/InBIO, Research Center in Biodiversity and Genetic Resources, University of Porto, Vair~
ao PT-4485661 Portugal
3
Ecology and Genetics, University of Oulu, Oulu FI-90014 Finland
4
Physics Faculty, Taras Shevchenko National University of Kyiv, 64/13 Volodymyrska Street, Kyiv UA-01601 Ukraine
5
Department of Biological Sciences, University of South Carolina, Columbia, South California 29208 USA
6
Ecologie Syst
ematique Evolution, Universit
e Paris-Sud, CNRS, AgroParisTech, Universit
e Paris-Saclay, Orsay Cedex F-91405 France
7
National Research Center for Radiation Medicine of the National Academy of Medical Science, Kyiv 04050 Ukraine
Citation: Mappes, T., Z. Boraty
nski, K. Kivisaari, A. Lavrinienko, G. Milinevsky, T. A. Mousseau, A. P. Møller, E.
Tukalenko, and P. C. Watts. 2019. Ecological mechanisms can modify radiation effects in a key forest mammal of
Chernobyl. Ecosphere 10(4):e02667. 10.1002/ecs2.2667
Abstract. Nuclear accidents underpin the need to quantify the ecological mechanisms which determine
injury to ecosystems from chronic low-dose radiation. Here, we tested the hypothesis that ecological mech-
anisms interact with ionizing radiation to affect natural populations in unexpected ways. We used large-
scale replicated experiments and food manipulations in wild populations of the rodent, Myodes glareolus,
inhabiting the region near the site of the Chernobyl disaster of 1986. We show linear decreases in breeding
success with increasing ambient radiation levels with no evidence of any threshold below which effects are
not seen. Food supplementation of experimental populations resulted in increased abundances but only in
locations where radioactive contamination was low (i.e., below 1lSv/h). In areas with higher contami-
nation, food supplementation showed no detectable effects. These ndings suggest that chronic low-
dose-rate irradiation can decrease the stability of populations of key forest species, and these effects could
potentially scale to broader community changes with concomitant consequences for the ecosystem
functioning of forests impacted by nuclear accidents.
Key words: Chernobyl; chronic radiation; food supplementation; forest ecosystem; ionizing radiation; key species;
Myodes vole; nuclear accident; population increase; population sensitivity; reproductive success.
Received 19 September 2018; revised 19 February 2019; accepted 25 February 2019. Corresponding Editor: Robert R.
Parmenter.
Copyright: ©2019 The Authors. This is an open access article under the terms of the Creative Commons Attribution
License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
E-mail: tapio.mappes@jyu.
INTRODUCTION
We have entered the Anthropocene, a period
when human actions dominate the well-being
and functioning of the Earths environment.
Detrimental effects of human actions on biota are
well-documented ranging from global impacts,
such as climate change and ocean acidication,
to more local events, such as loss of habitat, and
pollution by metals or nutrients. One particularly
controversial source of human impact is related
to the accidental release of radionuclides. The
Chernobyl nuclear accident (1986) is a model for
studies of the impact of chronic exposure to low-
dose radioactive contaminants on wildlife
(Anspaugh et al. 1988). The explosion at the for-
mer Chernobyl Nuclear Power Plant (NPP)
released a wide array of ssion products, includ-
ing cesium-137 and strontium-90, and unspent
nuclear fuel (plutonium-239), that were
www.esajournals.org 1April 2019 Volume 10(4) Article e02667
dispersed widely (about 200,000 km
2
) over large
parts of Northern Ukraine, southeastern Belarus,
and western Russia, with less but still
detectable contaminants distributed over much
of Fennoscandia and Central Europe (Evangeliou
et al. 2013). Contamination levels derived from
the former Chernobyl NPP are highly variable
with background radiation levels sometimes
varying by two orders of magnitude between
places separated by a few hundred meters
(Fig. 1). This variation in contamination levels,
where high and low levels of radiation rate occur
in relatively close proximity, allows for sensitive
and replicated analyses of biological effects of
exposure to radioactive contamination (Mous-
seau and Møller 2011).
Despite an extensive literature concerning
radionuclide movement in the environment and
associated genetic damage (Chesser et al. 2001,
Geraskin et al. 2008, Yablokov 2009), there are
no experimental tests concerning the ecological
mechanisms which determine possible radiation
effects in the Chernobyl ecosystem (Møller and
Mousseau 2013b). For example, the only
Fig. 1. Map of the Chernobyl Exclusion Zone (Ukraine) with locations where bank voles were trapped. The g-
ure is created using Esri ArcGIS 10.0. Satellite imagery CNES/Airbus DS, Earthstar Geographics Source: Esri,
DigitalGlobe, GeoEye, i-cubed, Earthstar Geographics, CNES/Airbus DS, USDA, USGS, AEX, GetMapping,
AeroGRID, IGN, IGP, swisstopo, and the GIS User Community, Esri, HERE, DeLorme. Please note that several
sampling sites were located at short distances as indicated by overlapping circles.
www.esajournals.org 2April 2019 Volume 10(4) Article e02667
MAPPES ET AL.
experiments quantifying the impact of exposure
to radiation upon reproductive capability, and
the concomitant population dynamics of small
mammals, were conducted by manipulating the
external radiation levels (Mihok et al. 1985,
Mihok 2004). These experiments, in a North
American small rodent system, suggest that ani-
mals can be very resistant to external radiation
doses if other sources of radiation exposure (e.g.,
via ingestion of contaminated food) and ecosys-
tem effects are excluded. Here, our aim was to
experimentally test the hypothesis that ecological
mechanisms (namely availability of food
resources) can modify some of the putative detri-
mental effects of radiation in natural popula-
tions. This question is particularly relevant given
recent ndings that organisms living under natu-
ral conditions appear to be many times more sen-
sitive to the deleterious effects of ionizing
radiation (Garnier-Laplace et al. 2013).
The biological effects of low-dose (<100 mSv)
radiation exposure are strongly debated (Bonner
2003, Calabrese and OConnor 2014). Much con-
troversy surrounds the validity of the Threshold
model; whereby, exposure to low radiation doses
is predicted to have non-signicant, or even
benecial (hormesis; Boonstra et al. 2005, Feinen-
degen 2005) effects on individuals with detri-
mental consequences of radiation occurring only
above a threshold dose (Tubiana et al. 2009). The
alternative hypothesis of Linear No-Threshold
(LNT) model has been widely tested (and sup-
ported) in laboratory animals and in epidemio-
logical studies of humans (Land 2002, Brooks
2005, Council 2006), but much less is known con-
cerning the shape of radiation response curves
for natural ecosystems (although see Møller and
Mousseau 2011, Garnier-Laplace et al. 2015).
Here, we tested predictions of the LNT model
that radiation has a proportional relationship
with individual tness measures and concomi-
tant population growth rates, without any evi-
dence for a threshold below which negative
effects are not observed.
We conducted a large-scale, replicated study of
the effects of radioactive contamination on the
breeding characteristics and abundances of a
small mammal, the bank vole Myodes glareolus.
In addition, we experimentally determined how
food limitation interacted with radiation to affect
population characteristics. The bank vole is a
common and abundant terrestrial vertebrate that
inhabits Eurasian forest ecosystems (Macdonald
and Barrett 1993), which makes it an attractive
indicator species for the health of forest ecosys-
tems that may have been injured by anthro-
pogenic activities.
MATERIALS AND METHODS
Study species
The bank vole is abundant (typically between
10 and 80 individuals per hectare) in most types
of forest (from deciduous to coniferous) in Eur-
ope and Asia (Macdonald and Barrett 1993). Its
diet is highly variable and may include various
herbs, seeds, buds, roots, berries, fruits, mosses,
lichens, fungi, and small invertebrates (Calandra
et al. 2015). Bank voles are important prey of
many owls and hawks and mammalian preda-
tors from weasels to foxes (Krebs 1996). The bank
vole breeding season lasts from May to Septem-
ber when females produce up to four litters, each
with two to ten offspring (Koivula et al. 2003,
Mappes and Koskela 2004). In the wild, bank
voles can live up to 1.5 yr, including one over-
wintering and one breeding season (Innes and
Millar 1994).
Abundance index and breeding of females
Abundances of bank voles were estimated in
early summer (30 May7 June 2011, 48 locations,
960 trap nights) and in winter (1520 February
2016, 38 locations, 760 trap nights) within 50 km
of the former Chernobyl NPP, Ukraine (Fig. 1).
At each location, 20 traps were placed in line for
one night, with each trap separated by about
10 m. Animals were caught with Ugglan Special2
live traps (Grahnab, Sweden) in summer 2011
(with sunower seeds and potato as a bait), and
with snap traps in winter 2016 (with bread and
peanut oil as bait). The minimum distance
between trapping locations was 500 m. To quan-
tify habitat variation among locations, percentage
vegetation cover was estimated within a 1 m
radius around each trap at three layers: forest lit-
ter (vegetation of 050 cm high), bushes (0.5
2 m), and in the tree canopy. We selected these
three measures of habitat to estimate whether
contaminated and control areas are different in
key components of habitat structure. Litter cover
and bushes are a proxy for habitat in which bank
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MAPPES ET AL.
voles burrow and take refuge (Flowerdew and
Ellwood 2001), and a cover of tree canopy can
determine a general habitat selection of this forest
species (Zwolak et al. 2016). Breeding character-
istics (breeding or not, and litter size) were mea-
sured for all adult females caught in 2011
(n=25, 18 locations) and in August 2013 (n=34,
an additional trapping in 24 locations). The
breeding probability of females was estimated by
taking all captured females to the laboratory
where their possible pregnancy and breeding
were followed. Number of offspring (litter size)
was measured when pregnant females gave
birth. Head width (a proxy of body size) was
measured to the nearest 0.1 mm with a digital
caliper, and animals were weighed to the nearest
0.1 g using a digital balance. Sample size (num-
ber of trapping locations) was maximized during
the research periods, with time limits constrained
by safety issues for humans as determined by the
Chernobyl Exclusion Zone administration.
Measurements of ambient radiation
Ambient radiation levels at trapping locations
were measured at 1 cm above the ground with a
handheld GM dosimeter (Gamma-Scout w/
ALERT Radiation detector/Geiger Counter,
Gamma-Scout GmbH and Co. KG, Germany)
calibrated to measure Sieverts per hour (Sv/h).
The mean ambient radiation levels varied among
trapping locations from 0.01 to 95.55 lSv/h
(Fig. 1). Given the long half-life of 137Cs, such
measurements of radiation are highly repeatable
among days and even years (Møller and Mous-
seau 2013a).
Feeding experiment
The experimental populations for the feeding
experiment were chosen at the beginning of the
2014 breeding season. We chose 18 feeding loca-
tions from contaminated areas (range 1.16
30.54 lSv/h, mean 7.45 lSv/h) and 18 locations
from control areas (range 0.100.22 lSv/h, mean
0.15 lSv/h). Both contaminated and control loca-
tions were divided randomly into three experi-
mental groups (six populations each). The
experimental groups were as follows: control (no
food manipulation), rodent food (RM1, Special
Diet Services), and rodent food containing the
potential radio-protectant/mitigant, indole-3-car-
binol (Fan et al. 2013). Since indole-3-carbinol
did not affect bank vole abundance (F=0.305,
df =2,17, P>0.587) or interact with the radia-
tion level (F=0.001, df =2,17, P>0.996), the
two food supplementation groups were com-
bined into a single food treatment in the subse-
quent analyses. Food was provided ad libitum at
each feeding station; the minimum distance
between the feeding stations was 1 km. The sam-
ple size (number of feeding places) was maxi-
mized according to the constraints caused by
material (e.g., food) and time limits determined
by safety regulations imposed by the Chernobyl
Exclusion Zone administration on human
research activity. Abundance of bank voles was
estimated prior to the beginning of the experi-
ment (early June) and after the breeding season
(early October) using a 3 93 trapping grid, with
an inter-trap distance of 20 m; the feeding station
was located in the middle of the trapping grid.
The trapping period was ve days in each feed-
ing area. As the experiment was conducted in
open populations, the bank vole abundances rep-
resent a combination of reproduction and mor-
tality, as well as immigration and emigration:
These different ecological mechanisms could not
be separated in the present study. In general,
bank vole females defend breeding territories of
up to 0.6 ha (Mazurkiewicz 1983) (corresponding
to 4050 m radius circle), but males and non-
breeding females are not territorial and they can
disperse up to 1 km (Kozakiewicz et al. 2007).
Statistical analyses
Breeding characteristics of individuals were
analyzed with a generalized linear mixed model
(GLMM), where either breeding probability (bi-
nomial error distribution and logit link function)
or litter size (multinomial error distribution and
logit link function) was the dependent variable,
and ambient radiation level (log
10
transformed)
was the predictor. As the breeding characters
were studied in the two different years 2011 and
2013, we rst tested whether the effects of radia-
tion differed between years. These analyses
showed that the main effect of year and its inter-
actions with radiation were not signicant (for
breeding probability: the main effect, P=0.375;
interaction, P=0.521; and for litter size: the main
effect, P=0.095; interaction, P=0.111). Conse-
quently, we combined the data for the two years
in the same analyses. In the subsequent analyses
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MAPPES ET AL.
of breeding characteristics, year and location
were included as random factors. Curve estima-
tions (Curve Fit) were used to analyze linear or
quadratic relationship between dependent vari-
ables and radiation (both log
10
transformed).
Vegetation cover variables were arcsine trans-
formed. The effects of food supplementation
were analyzed at the population level also using
a GLMM, with abundance index as the depen-
dent variable, and food supplementation, radia-
tion level (low or high radiation level), and their
interaction as predictors (Table 1). Location was
included in all models as a random factor. All
statistical tests were performed using IBM SPSS
v.20.0 (IBM SPSS, Chicago, Illinois, USA).
RESULTS
The probability of a bank vole being pregnant
decreased signicantly with increasing ambient
radiation level (GLMM, binary logistic regres-
sion; coefcient 0.591, t=2.073, df =57,
P=0.043; linear equation: t=2.407, P=0.019;
quadratic equation: t=1.516, P=0.135; Fig. 2a).
Litter size of bank voles varied between 1 and 8
(mean =5.17, SE =0.280) and decreased signi-
cantly with increasing radiation levels (GLMM,
multinomial logistic regression; coefcient
0.651, t=2.206, df =29, P=0.048; linear
equation: t=2.800, P=0.008; quadratic equa-
tion: t=0.831, P=0.412; Fig. 2b). Linear equa-
tions of both the probability of being pregnant
and litter size were more signicant compared to
their quadratic equations, consistent with the
Linear No-Threshold (LNT) model for radiation
effects.
Size of females was not signicantly related to
radiation (t=1.776, df =57, P=0.081), and
there was no interactive effect of female size with
radiation on breeding probability or litter size
(t=0.231, df =55, P=0.818 and t=0.336,
df =27, P=0.739, respectively). Abundance of
bank voles was not correlated with breeding
probability or litter size (t=0.622, df =55,
P=0.537; t=0.444, df =27, P=0.660) and
did not have an interactive effect with radiation
levels (t=0.336, df =55, P=0.738; t=0.860,
df =27, P=0.397). These results suggest that
radiation did not indirectly affect the breeding
success of voles by changing their structural size
or by modifying population densities and its pos-
sible consequences (e.g., level of intra-specic
competition).
Abundances of bank voles
Abundance index varied from 0 to 11 individu-
als per trapping location. Both summer (Fig. 2c)
and winter (Fig. 2d) abundances of bank voles
decreased signicantly with increasing ambient
radiation (in summer: r
2
=0.209, t=3.490, df =
47, P=0.001; linear equation, t=3.103, P=
0.003; quadratic equation, t=0.348, P=0.730;
in winter: r
2
=0.242, t=3.394, df =37, P=
0.002; linear equation, t=2.239, P=0.032;
quadratic equation, t=0.201, P=0.842). As
with radiation effects on probability of pregnancy
and litter size described above, the signicant lin-
ear terms support the predictions of the LNT
model. Ambient radiation levels also negatively
covaried with abundance indexes of control pop-
ulations in the feeding experiment in 2014 (see
below).
Radiation effects on bank vole populations
could be biased by environmental differences
between contaminated and control areas. Indeed,
the vegetation cover of bushes (0.52 m) and tree
canopy decreased with increasing radiation
levels (coefcient =0.058, t=0.333, P=
0.021; coefcient =0.076, t=0.288, P=0.047,
respectively). However, the most important veg-
etation variable for bank voles (cover of forest lit-
ter: 050 cm) was not signicantly correlated
with radiation (coefcient =0.034, t=0.182,
P=0.216). Moreover, any effect of vegetation on
bank voles was minimal as vegetation cover,
either forest litter, bushes, or tree canopy, was
not correlated with abundance indexes of bank
voles (coefcient =0.955, t=0.416, P=0.678;
coefcient =1.138, t=0.443, P=0.658; coef-
cient =2.457, t=1.448, P=0.149, respectively).
And most importantly, these vegetation variables
Table 1. Results of GLMM tests of the effects of food
supplementation and background radiation on
abundance index of bank voles in Chernobyl.
Effects Coefcient SE tP
Abundance
Food 1.387 0.667 2.080 0.038
Radiation 0.463 0.464 0.999 0.318
Food 9radiation 1.609 0.771 2.087 0.037
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MAPPES ET AL.
did not interact signicantly with radiation level
(coefcient =0.718, t= 0.237, P=0.813; coef-
cient =1.380, t=0.364, P=0.716; coef-
cient =3.457, t=1.392 P=0.165, respectively).
Radiation clearly affected the response of the
bank vole populations to environmental changes.
The population living with additional food
resources increased only in low radiation areas,
(up to 1 lSv/h), but decreased from 1 lSv/h to
30 lSv/h (quadratic equation: t=2.836,
P=0.010; Fig. 3, Table 1). Abundance indexes of
the populations living without supplemental
food tended to decrease linearly with increasing
ambient radiation levels (t=1.909, P=0.085;
Fig. 3).
DISCUSSION
The results presented here refute the hypothe-
sis of there being a threshold level of radiation
below which there are no effects in natural popu-
lations of animals (Tubiana et al. 2009). Support
for a threshold hypothesis would be derived
from a non-linear relationship between low-dose
Fig. 2. (a) Background radiation level predicts the breeding probability of bank vole females in Chernobyl
where fty-nine adult females were caught (2011: n=25; 2013: n=34), of which 36 (61%) were pregnant. Predic-
tive curve (95% CI) is estimated by binary logistic regression (coefcient 0.591, t=2.073, df =57, P=0.043).
(b) Litter size of breeding females (n=36) decreased with an increase in ambient radiation levels (y=0.71
(0.25) 9log(x)+4.94 (0.27)) (GLMM, multinomial logistic regression; coefcient 0.651, t=2.061, df =29,
P=0.048). Abundances of bank voles decreased with increasing the mean ambient radiation level at the trapping
area (n=48) in summer (c) (y=1.14 (0.33) 9log(x)+1.63 (0.27), r
2
=0.209, t=3.490, df =47, P=0.001)
and in winter (d) (n=38) (y=1.15 (0.44) 9log(x) +3.67 (0.42), r
2
=0.242, t=3.394, df =37, P=0.002).
www.esajournals.org 6April 2019 Volume 10(4) Article e02667
MAPPES ET AL.
radiation and its consequences, such that there
are non-signicant negative effects (or even bene-
cial effects, e.g., hormesis; Boonstra et al. 2005,
Feinendegen 2005) of low radiation levels (here
at 0.510 lSv/h) and with harmful effects begin-
ning, and increasing signicantly thereafter, fol-
lowing a specic threshold level of radiation
exposure. Contrary to the threshold hypothesis,
harmful and signicant radiation effects on bank
vole populations can be observed even at very
low levels of ambient radioactivity (1 lSv/h or
less) and these effects increase linearly with
exposure above these levels. However, our nd-
ings also show that ecological mechanisms can
modify linear effects of radiation. Here, the sup-
plemental food resources increased vole abun-
dances up to a low level of radiation (1lSv/h),
but higher levels were associated with decreased
abundances independently of supplemental food
resources.
Chronic exposure to ionizing radiation is
widely believed to have direct and indirect
effects on natural populations of animals. Direct
effects of radiation exposure include an
increased frequency of mutations (Møller and
Mousseau 2015, but see cf. Kes
aniemi et al.
2018) and/or damage to DNA that causes devel-
opmental disorders, tumors, and cancers (Møller
et al. 2007). Moreover, birds inhabiting areas of
high radiation have impaired sperm morphol-
ogy (Møller et al. 2008), potentially providing
one explanation for the lower breeding probabil-
ity of bank voles. Certainly, bank voles inhabit-
ing areas contaminated by radionuclides
derived from the former Chernobyl NPP show
signs of molecular stress, such as upregulation
of some DNA damage response genes (Jernfors
et al. 2018) and altered telomere homeostasis
(Kes
aniemi et al. 2019). These biological effects
could be caused by direct exposure to gamma
radiation from the surrounding environment or
by exposure to alpha and beta particles accumu-
lated in animals from food (Sazykina and Kry-
shev 2006). For example, mushrooms, an
essential component of the diet of bank voles
(Hansson 1979), can be an enormous source of
alpha- and beta-emitting radionuclides (Mihok
et al. 1989, Gralla et al. 2014). At this time, we
cannot yet distinguish the direct effects of radia-
tion from its indirect effects. Such indirect
effects could be modied by quantity or quality
of food resources as affected by radiation. For
example, food resources of voles (mainly plants,
fungi, and small invertebrates; Calandra et al.
2015) are likely altered in contaminated areas
(Tikhomirov and Shcheglov 1994) and we found
some impact of radiation on cover of trees and
bushes. With this in mind, a high level of
radionuclides is associated with an altered gut
microbiota in bank voles (Lavrinienko et al.
2018), potentially indicating that radiation expo-
sure is associated with a change in diet. Another
important ecological factor, predation rate, may
also be lower in contaminated areas, since, for
example, both avian (Møller and Mousseau
2009) and mammalian predators (Møller and
Mousseau 2013a) of rodents decrease in abun-
dance in contaminated areas. The absence of
these ecological mechanisms could be the main
reasons for differences between our results and
those of earlier studies where populations of
small mammals were manipulated only by
exposure to external radiation (Mihok et al.
1985, Mihok 2004).
Fig. 3. The effects of feeding experiments on bank
vole populations in 18 control areas (range 0.10
0.22 lSv/h, mean 0.15 lSv/h) and 18 contaminated
areas (range 1.1630.54 lSv/h, mean 7.45 lSv/h). In
the areas where additional food was provided
(n=24), abundances of bank voles increased with
radiation level up to about 1 lSv/h and then decreased
above this radiation level. In the areas without addi-
tional food, populations tended to decrease linearly
with the increase in radiation level (see statistics in the
Results).
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MAPPES ET AL.
A novel element of the study reported here was
the use of experimental manipulations of food
resources in order to test whether the effects of
food stress correlate with other environmental
stressors (here exposure to environmental
radionuclides). The effect of food supplementa-
tion in natural populations depends upon study
species and its environment. Nonetheless, food
supplementation generally does not strongly
increase population densities when environmen-
tal conditions are good (Boutin 1990) while densi-
ties often increase in populations experiencing
harsh environments (Huitu et al. 2003, Forbes
et al. 2014, Johnsen et al. 2017). Accordingly,
additional food did not increase bank vole abun-
dances in the control populations but the food
treatment did have a positive effect on abundance
in contaminated areas at low (<1lSv/h ambient
dose rates) radiation levels. However, above this
level of radiation, the increasing radiation levels
had a clear negative effect on abundances of bank
voles despite food supplementation. Thus, the
food supplementation can mitigate the detrimen-
tal effects of an environment contaminated by
radionuclides up to a certain point only. We sug-
gest that the relevant environment of bank voles
can be altered at many trophic stages. For exam-
ple, predation risk of avian predators could be
already reduced at the elevated radiation levels
(1 lSv/h) (Møller and Mousseau 2013a), and thus,
these predators might be unable to limit popula-
tion increases when food stress of voles is arti-
cially relaxed. Furthermore, many parasites and
diseases of voles might not regulate their popula-
tions in a density-dependent manner in elevated
radiation levels (Sibly and Hone 2002), although
the interactions between these important ecologi-
cal processes and radiation are still unknown
(Morley 2012).
The interaction between ionizing radiation and
other environmental stressors on natural popula-
tions is being increasingly recognized as poten-
tially signicant. For example, in a meta-analysis
of the effects of Chernobyl-derived radioactive
contaminants on 19 species of plants and animals
living under natural conditions (Garnier-Laplace
et al. 2013), it was found that organisms in the
wild were more than eight times more sensitive
to negative radiation effects than these same spe-
cies living under laboratory or model conditions.
Similarly, a study of pine trees (Pinus sylvestris)
living across a wide range of ambient radiations
levels in Chernobyl found very strong negative
effects on growth during the rst three years
after the disaster in 1986, with large negative
effects persisting for 2.5 decades following the
disaster during years of signicant drought
(Mousseau et al. 2013). And, a study of pollina-
tors, fruit trees, and frugivores in Chernobyl
found evidence for signicant interactions
among these guilds that varied across ambient
radiation levels (Møller et al. 2012). These studies
suggest a very large effect of ecological interac-
tions on the susceptibility of organisms to the
deleterious effects of ionizing radiation.
To conclude, in this study we used experimen-
tal manipulation of food resources to demon-
strate signicant effects of radiation on a key
forest mammal. These ndings are particularly
important given the potential for ecosystem-wide
consequences of the observed effects on rodents.
These results suggest that rodent populations,
and by implication, entire ecosystems, are likely
to have been affected across perhaps
200,000 km
2
in Eastern, Northern, and even Cen-
tral Europe where radioactive contaminants
stemming from the Chernobyl disaster are still
measurable in a large diversity of different spe-
cies and are known to accumulate in the food
chain (e.g., wild boars Sus scrofa in Germany,
reindeer Rangifer tarandus in Finland and Sweden
(Hohmann and Huckschlag 2005, Strebl and
Tataruch 2007, Semizhon et al. 2009)). Although
the consequences of exposure to low-dose radia-
tion are very difcult to detect under most cir-
cumstances because of the complexity of biotic
and abiotic factors shaping individual tness
and population processes, the experimental stud-
ies presented here provide irrefutable evidence
that even very low doses can lead to signicant
consequences for individuals, populations, and
likely even entire ecosystems.
ACKNOWLEDGMENTS
We gratefully acknowledge logistic support and help
in Ukraine by Igor Chizhevsky and the Chernobyl
EcoCenter. This study was nancially supported by
Academy of Finland grants to TM (268670) and PCW
(287153), Emil Aaltonen Foundation and Oskar Ound
Foundation to KK, the postdoctoral grantee from the
Portuguese Foundation for Science and Technology
www.esajournals.org 8April 2019 Volume 10(4) Article e02667
MAPPES ET AL.
(RH/BPD/84822/2012) to ZB, and the Graduate School of
the University of Oulu to AL. Additional support was
provided by the CNRS (France), the Samuel Freeman
Charitable Trust, the Fulbright Program, the American
Council of Learned Societies, and the College of Arts
and Sciences at the University of South Carolina.
Authors after the rst author are listed in alphabetical
order. TM, ZB, KK, AL, GM, TAM, APM, ET, and PCW
designed the study and contributed to acquisition of
eld data and experiments; TM carried out the statistical
analyses and drafted the manuscript; TM, ZB, KK, AL,
GM, TAM, APM, ET, and PCW contributed to writing
the manuscript and gave nal approval for publication.
The authors declare no competing nancial interests.
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... There are many studies (e.g. Mappes et al., 2019;Møller & Mousseau, 2009 reporting effects on organisms in the Chornobyl Exclusion Zone at what appear extremely low-dose rates compared to natural background exposure and what are considered no effects exposure dose rates for regulatory assessment . Unfortunately, the underlying data for such papers is rarely published preventing independent reanalyses. ...
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Despite the ubiquity of pollutants in the environment, their long-term ecological consequences are not always clear and still poorly studied. This is the case concerning the radioactive contamination of the environment following the major nuclear accident at the Chernobyl nuclear power plant. Notwithstanding the implications of evolutionary processes on the population status, few studies concern the evolution of organisms chronically exposed to ionizing radiation in the Chernobyl exclusion zone. Here, we examined genetic markers for 19 populations of Eastern tree frog ( Hyla orientalis ) sampled in the Chernobyl region about thirty years after the nuclear power plant accident to investigate microevolutionary processes ongoing in local populations. Genetic diversity estimated from nuclear and mitochondrial markers showed an absence of genetic erosion and higher mitochondrial diversity in tree frogs from the Chernobyl exclusion zone compared to other European populations. Moreover, the study of haplotype network permitted us to decipher the presence of an independent recent evolutionary history of Chernobyl exclusion zone’s Eastern tree frogs caused by an elevated mutation rate compared to other European populations. By fitting to our data a model of haplotype network evolution, we suspected that Eastern tree frog populations in the Chernobyl exclusion zone have a high mitochondrial mutation rate and small effective population sizes. These data suggest that Eastern tree frogs populations might offset the impact of deleterious mutations because of their large clutch size, but also question the long term impact of ionizing radiation on the status of other species living in the Chernobyl exclusion zone.
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Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides, and from uncontaminated control sites elsewhere in Ukraine. Inhabiting the Chernobyl Exclusion Zone was associated with reduced TL in the liver and testis, and upregulation of telomerase in brain and liver. Thus upregulation of telomerase does not appear to associate with longer telomeres but may reflect protective functions other than telomere maintenance or an attempt to maintain shorter telomeres in a stressful environment. Tissue specific differences in the rate of telomere attrition and apparent radiosensitivity weaken the intra-individual correlation in telomere length among tissues in voles exposed to radionuclides. Our data show that ionizing radiation alters telomere homeostasis in wild animal populations in tissue specific ways.
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Gut microbiota composition depends on many factors, although the impact of environmental pollution is largely unknown. We used amplicon sequencing of bacterial 16S rRNA genes to quantify whether anthropogenic radionuclides at Chernobyl (Ukraine) impact the gut microbiome of the bank vole Myodes glareolus. Exposure to elevated levels of environmental radionuclides had no detectable effect on the gut community richness but was associated with an almost two-fold increase in the Firmicutes:Bacteroidetes ratio. Animals inhabiting uncontaminated areas had remarkably similar gut communities irrespective of their proximity to the nuclear power plant. Hence, samples could be classified to high-radiation or low-radiation sites based solely on microbial community with >90% accuracy. Radiation-associated bacteria had distinct inferred functional profiles, including pathways involved in degradation, assimilation and transport of carbohydrates, xenobiotics biodegradation, and DNA repair. Our results suggest that exposure to environmental radionuclides significantly alters vertebrate gut microbiota.
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Exposure to ionizing radiation (IR) from radionuclides released into the environment can damage DNA. An expected response to exposure to environmental radionuclides, therefore, is initiation of DNA damage response (DDR) pathways. Increased DNA damage is a characteristic of many organisms exposed to radionuclides but expression of DDR genes of wildlife inhabiting an area contaminated by radionuclides is poorly understood. We quantified expression of five central DDR genes Atm, Mre11, p53, Brca1, and p21 in the livers of the bank vole Myodes glareolus that inhabited areas within the Chernobyl Exclusion Zone (CEZ) that differed in levels of ambient radioactivity, and also from control areas outside the CEZ (i.e., sites with no detectable environmental radionuclides) in Ukraine. Expression of these DDR genes did not significantly differ between male and female bank voles, nor among sites within the CEZ. We found a near two-fold upregulation in the DDR initiators Mre11 and Atm in animals collected from the CEZ compared with samples from control sites. As Atm is an important regulator of oxidative stress, our data suggest that antioxidant activity may be a key component of the defense against exposure to environmental radioactivity.
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Vole population cycles are a major force driving boreal ecosystem dynamics in northwestern Eurasia. However, our understanding of the impact of winter on these cycles is increasingly uncertain, especially because climate change is affecting snow predictability , quality, and abundance. We examined the role of winter weather and snow conditions, the lack of suitable habitat structure during freeze-thaw periods, and the lack of sufficient food as potential causes for winter population crashes. We live-trapped bank voles Myodes glareolus on 26 plots (0.36 ha each) at two different elevations (representing different winter conditions) in southeast Norway in the winters 2013/2014 and 2014/2015. We carried out two manipulations: supplementing six plots with food to eliminate food limitation and six plots with straw to improve habitat structure and limit the effect of icing in the subnivean space. In the first winter, all bank voles survived well on all plots, whereas in the second winter voles on almost all plots went extinct except for those receiving supplemental food. Survival was highest on the feeding treatment in both winters, whereas improving habitat structure had no effect. We conclude that food limitation was a key factor in causing winter population crashes. K E Y W O R D S climate, feeding experiment, habitat quality, population dynamics, rodents
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We reconstructed the radiological dose for birds observed at 300 census sites in the 50-km northwest area affected by the accident at the Fukushima Daiichi nuclear power plant over 2011–2014. Substituting the ambient dose rate measured at the census points (from 0.16 to 31 μGy h −1) with the dose rate reconstructed for adult birds of each species (from 0.3 to 97 μGy h −1), we confirmed that the overall bird abundance at Fukushima decreased with increasing total doses. This relationship was directly consistent with exposure levels found in the literature to induce physiological disturbances in birds. Among the 57 species constituting the observed bird community, we found that 90% were likely chronically exposed at a dose rate that could potentially affect their reproductive success. We quantified a loss of 22.6% of the total number of individuals per increment of one unit log 10-tansformed total dose (in Gy), over the four-year post-accident period in the explored area. We estimated that a total dose of 0.55 Gy reduced by 50% the total number of birds in the study area over 2011–2014. The data also suggest a significant positive relationship between total dose and species diversity.
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The coupled model LMDZORINCA has been used to simulate the transport, wet and dry deposition of the radioactive tracer 137Cs after accidental releases. For that reason, two horizontal resolutions were deployed and used in the model, a regular grid of 2.5° × 1.27°, and the same grid stretched over Europe to reach a resolution of 0.66° × 0.51°. The vertical dimension is represented with two different resolutions, 19 and 39 levels respectively, extending up to the mesopause. Four different simulations are presented in this work; the first uses the regular grid over 19 vertical levels assuming that the emissions took place at the surface (RG19L(S)), the second also uses the regular grid over 19 vertical levels but realistic source injection heights (RG19L); in the third resolution the grid is regular and the vertical resolution 39 levels (RG39L) and finally, it is extended to the stretched grid with 19 vertical levels (Z19L). The model is validated with the Chernobyl accident which occurred in Ukraine (ex-USSR) on 26 May 1986 using the emission inventory from Brandt et al. (2002). This accident has been widely studied since 1986, and a large database has been created containing measurements of atmospheric activity concentration and total cumulative deposition for 137Cs from most of the European countries. According to the results, the performance of the model to predict the transport and deposition of the radioactive tracer was efficient and accurate presenting low biases in activity concentrations and deposition inventories, despite the large uncertainties on the intensity of the source released. The best agreement with observations was obtained using the highest horizontal resolution of the model (Z19L run). The model managed to predict the radioactive contamination in most of the European regions (similar to De Cort et al., 1998), and also the arrival times of the radioactive fallout. As regards to the vertical resolution, the largest biases were obtained for the 39 layers run due to the increase of the levels in conjunction with the uncertainty of the source term. Moreover, the ecological half-life of 137Cs in the atmosphere after the accident ranged between 6 and 9 days, which is in good accordance to what previously reported and in the same range with the recent accident in Japan. The high response of LMDZORINCA model for 137Cs reinforces the importance of atmospheric modelling in emergency cases to gather information for protecting the population from the adverse effects of radiation.
Book
This book is the seventh in a series of titles from the National Research Council that addresses the effects of exposure to low dose LET (Linear Energy Transfer) ionizing radiation and human health. Updating information previously presented in the 1990 publication, Health Effects of Exposure to Low Levels of Ionizing Radiation: BEIR V, this book draws upon new data in both epidemiologic and experimental research. Ionizing radiation arises from both natural and man-made sources and at very high doses can produce damaging effects in human tissue that can be evident within days after exposure. However, it is the low-dose exposures that are the focus of this book. So-called "late" effects, such as cancer, are produced many years after the initial exposure. This book is among the first of its kind to include detailed risk estimates for cancer incidence in addition to cancer mortality. BEIR VII offers a full review of the available biological, biophysical, and epidemiological literature since the last BEIR report on the subject and develops the most up-to-date and comprehensive risk estimates for cancer and other health effects from exposure to low-level ionizing radiation. © 2006 by the National Academy of Sciences. All rights reserved.