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ORIGINAL PAPER
Tree rings reveal extent of exposure to ionizing radiation
in Scots pine Pinus sylvestris
Timothy A. Mousseau •Shane M. Welch •Igor Chizhevsky •
Oleg Bondarenko •Gennadi Milinevsky •David J. Tedeschi •
Andrea Bonisoli-Alquati •Anders Pape Møller
Received: 14 December 2012 / Revised: 12 April 2013 / Accepted: 30 May 2013
ÓSpringer-Verlag Berlin Heidelberg 2013
Abstract Tree growth has been hypothesized to provide a
reliable indicator of the state of the external environment.
Elevated levels of background ionizing radiation may
impair growth trajectories of trees by reducing the annual
growth. Such effects of radiation may depend on the
individual phenotype and interact with other environmental
factors such as temperature and drought. We used stan-
dardized growth rates of 105 Scots pine Pinus sylvestris
located near Chernobyl, Ukraine, varying in the level of
background radiation by almost a factor 700. Mean growth
rate was severely depressed and more variable in
1987–1989 and several other subsequent years, following
the nuclear accident in April 1986 compared to the situa-
tion before 1986. The higher frequency of years with poor
growth after 1986 was not caused by elevated temperature,
drought or their interactions with background radiation.
Elevated temperatures suppressed individual growth rates
in particular years. Finally, the negative effects of radio-
active contaminants were particularly pronounced in
smaller trees. These findings suggest that radiation has
suppressed growth rates of pines in Chernobyl, and that
radiation interacts with other environmental factors and
phenotypic traits of plants to influence their growth tra-
jectories in complex ways.
Keywords Chernobyl Growth Interaction between
stressors Ionizing radiation Tree height Tree rings
Introduction
On 26 April 1986, one of the Chernobyl nuclear power
plant reactors exploded and a nuclear fire burned for
10 days releasing between 9.35 910
3
and 1.25 910
4
PetaBq of radionuclides into the atmosphere. By contrast,
the Three Mile accident in PA, USA on 27 March 1979
released just 0.0005 PetaBq. Although many of these
radionuclides either dissipated or decayed within hours,
days or weeks [e.g., iodine-131 (
131
I)], cesium-137 (
137
Cs)
still persists today in the environment even hundreds of
kilometers from Chernobyl (Shestopalov 1996; Zakharov
and Krysanov 1996; Møller and Mousseau 2006; Yablokov
et al. 2009). Likewise, strontium-90 (
90
Sr) and plutonium-
239 (e.g.,
239
Pu) isotopes are common within the Cher-
nobyl Exclusion Zone and in areas in Russia and Belarus.
Given the 30, 29 and 24,000 years half-life for Cs-137,
Sr-90 and Pu-239, respectively, these contaminants are
likely to be of significance in the health of plants and
animals including humans for many years to come. This
accident provides a unique, but relatively unexploited
Communicated by A. Braeuning.
T. A. Mousseau S. M. Welch A. Bonisoli-Alquati
Department of Biological Sciences, University of South
Carolina, Columbia, SC 29208, USA
I. Chizhevsky O. Bondarenko
Chornobyl Radioecological Centre, Chernobyl, Ukraine
G. Milinevsky
Space Physics Laboratory, Taras Shevchenko National
University of Kyiv, 64, Volodymyrska Str., Kyiv 01601, Ukraine
D. J. Tedeschi
Department of Physics and Astronomy, University
of South Carolina, Columbia, SC 29208, USA
A. P. Møller (&)
Laboratoire d’Ecologie, Syste
´matique et Evolution,
CNRS UMR 8079, Universite
´Paris-Sud, Ba
ˆtiment 362,
91405 Orsay Cedex, France
e-mail: anders.moller@u-psud.fr
123
Trees
DOI 10.1007/s00468-013-0891-z
opportunity to study the effects of ionizing radiation under
field conditions. Many recent studies have documented the
large effects of radiation on the abundance and reproduc-
tive success of different taxa (e.g., Møller and Mousseau
2007a,b,2008,2009). In particular, the accident provides a
unique opportunity to conduct common garden or reci-
procal transplant experiments (e.g., Kovalchuk et al. 2000)
that will allow tests of environmental and genetic effects of
radiation, and hence tests of adaptation to radiation.
Trees are particularly suitable for studies of the negative
impact of environmental conditions (such as ionizing
radiation) on growth, because growth parameters of the
same individual are stored permanently in tree rings and
these can readily be compared between years with and
without exposure to the environmental condition, while
simultaneously using trees in control areas as untreated
controls (e.g., Ceulemans and Mousseau 1994; Cherubini
et al. 2003;Ufar2007). Previous studies of the effects of
radiation on tree growth are few and the scope of these
studies is very limited. Based on subjective and qualitative
assessments, Arkhipov et al. (1994) suggested that doses of
less than 0.1 Gy did not cause any immediate visible
external damage to trees, although internal damage was not
quantified. Although many studies have indicated that
radioactive fallout from nuclear tests or nuclear bombs can
be traced in tree rings, this effect may vary among radio-
active isotopes due to differences in migration among
isotopes across the tree trunk (e.g., Kagawa et al. 2002).
Schmitt et al. (2000) showed for a very small sample of
Pinus sylvestris pine trees grown near Chernobyl that
xylem formation decreased during 1987–1989, but had
recovered by 1990. Ionizing radiation had no direct effect
on the cambium in 1986, but affected the differentiation of
xylem mother cells in that year. Schmitt et al. (2000)
concluded that reduced wood formation was due to mas-
sive loss of needles in 1986 rather than uptake of radio-
biologically active elements, although this conclusion was
based on only three trees felled at 1, 8 and 20 km from
Chernobyl. Woodwell and Miller (1963) reported that pitch
pine Pinus rigida exposed to chronic levels of radiation for
several years in the 1950s at the Brookhaven facility
reduced the width of growth rings, with reductions being
the greatest at the base of the tree. This reduction was
affected by the size of the crown and climate, with trees
with large crowns showing small effects, and such effects
increasing in years with greater climate perturbations.
Again, these results were based on just a few trees making
it difficult to draw general conclusions.
The objectives of our study were to investigate to what
extent radiation from Chernobyl affected means and vari-
ances in the growth rate of trees. We relied on comparisons
of growth rate before and after 1986 in the same individual
trees, using the additional design feature of including trees
that ranged in exposure from normal background radiation
of 0.05 lSv/h to 34.5 lSv/h, or an increase in level of
radiation by almost a factor 690 compared to normal
background radiation. This sampling design allowed us to
assess the change in mean and variance in growth rate
before and after 1986 for a large number of trees. Scots
pines were not often found in areas of contamination above
30 lSv/h, having been killed by exposure during the
disaster with little or no recruitment in the more highly
contaminated areas since that time.
All previous studies of the effects of radiation on growth
rate suffered from problems of small sample sizes, and we
avoided this problem by studying more than 100 trees
across 12 different sites. A second objective of our study
was to investigate the effects of alpha and beta radiation
compared to gamma radiation on trees differing in size,
assuming that small trees would be more susceptible to the
negative impact of radiation (Woodwell and Miller 1963)
because they could only extract water and nutrients from
the topmost part of the soil where most of the radioactive
material resided (Shestopalov 1996). A third objective was
to investigate variation in annual mean growth rates due to
radiation and other environmental factors, because radia-
tion is not the only possible environmental stressor and the
effects of radiation could interact with other stressors. In
fact, we expected that radiation would have an effect on
growth rate, but that this effect would be exacerbated by
the impact of other environmental factors such as high
temperatures and drought in the sandy soils of Chernobyl.
We used Scots pine as a study organism because it is
common and widespread in the region, but also because
previous studies have shown that these pines are more
susceptible to the negative impact of radiation than many
other species of trees (Arkhipov et al. 1994; Kal’chenko
and Fedotov 2001; Kal’chenko et al. 1993a,b; Kovalchuk
et al. 2003; Rubanovich and Kal’chenko 1994; Shevchenko
et al. 1996).
Methods
Study sites and choice of study specimens
A radiation protection suit was worn in the most contam-
inated areas. With permission from the Ukrainian author-
ities, we collected tree cores from Scots pine during 30
January to 5 February 2009 within the Chernobyl Exclu-
sion Zone or in areas adjacent on the southern and western
borders ensuring that we covered a wide range of radiation
levels (Fig. 1). A total of 8 Scots pine trees from each of 14
different sites, in total 112, were selected based on their
size, to enhance the likelihood of sampling trees older than
30 years of age and hence present before 1986. We could
Trees
123
not record tree rings for seven of these trees because the
tree core disintegrated, resulting in a final sample of 105
trees. All trees were at the edge of forests and all were
undamaged, because we excluded trees that had lost major
branches, had large holes or showed signs of fungal attack.
Tree cores and phenotype of trees
We extracted tree cores at a height of 1.5 m using a 7 mm
increment borer (Suunto). We measured the height of trees
at an accuracy of 0.5 m using a Nikon hypsometer. The
diameter of the tree at 1.5 m was measured at an accuracy
of 1 cm with a DBH tape. Tree cores were subsequently
removed and stored for later treatment and measurement at
the laboratory.
Quantifying tree growth rates
We used standard dendrochronology methods (Cook and
Kairiukstis 1990) and digital imaging software to measure
the annual growth rings and quantify tree growth rates
before and after the 1986 Chernobyl accident. Tree incre-
ment cores were properly oriented and mounted in grooved
wooden boards. Increment cores were then sanded with
successively finer grades of abrasive paper until a polished
surface was obtained and individual cell walls were clearly
visible under a 209dissecting microscope. Cores were
then scanned at a 1,200 dpi resolution on a flatbed scanner
(Canon, Canoscan 8800f). To ensure suitable detail to be
captured in the digital images, a dissecting microscope was
used to compare each core to its scanned image. The digital
imaging software, (CooRecorder 7, Cybis Elektronik and
Data AB, http://www.cybis, Larsson 2008a), was used to
register coordinates for the annual growth ring boundaries
in the scanned images. The distances between annual ring
boundary coordinates were recorded at an accuracy of
0.1 mm and used to calculate raw annual growth rates. We
used the software program CDendro (Larsson 2008b)to
standardize the annual growth rate by applying the Baillie
and Pilcher normalization and negative exponential
Fig. 1 Location of Scots pine trees and levels of background radiation at the ground level from Cs-137 around Chernobyl. Partly developed from
Shestopalov (1996)
Trees
123
detrending procedure that uses a 2-year running average to
calculate the proportion of growth attributable to the cur-
rent year relative to the previous year, followed by the use
of a negative exponential regression of within-tree varia-
tion in growth to remove (i.e., detrend) the effects of sys-
tematic changes in growth as the tree ages. Standardized
data were used to control the effects of tree age and site-
specific conditions (e.g., soil type) on annual tree ring
width, allowing comparisons among differently aged trees
and sampled sites. Thus, we derived standardized growth
rates and detrended growth rates as a second standardized
measure of tree growth rate. All annual growth rings were
dated to year based on the time of collection. All mea-
surements were made blindly with respect to the level of
background radiation for the trees.
To quantify measurement errors, we randomly chose 18
cores and scanned each twice, and each image was digi-
tized twice. Repeatability Rbetween scans was 0.99
(SE =0.00), F=2,129.80, d.f.=450, 1,349, r
2
=0.999,
P\0.0001, and repeatability between digitizing events
was 0.99 (SE =0.00), F=2,117.79, d.f.=452, 1,347,
r
2
=0.999, P\0.0001.
Measuring background radiation levels
We measured radiation levels in the field and cross-vali-
dated these with measurements by the Ministry of Emer-
gencies, at ground level at each tree using a handheld
dosimeter (Model: Inspector, SE International, Inc., Sum-
mertown, TN, USA). We measured levels two to three
times at each site and averaged the measurements. Such
data have previously been validated with correlation against
data from governmental measurements at ground level pub-
lished by Shestopalov (1996), estimated as the midpoint of the
ranges published. These analyses showed a high degree of
consistency between the two methods (Møller and Mousseau
2007a). Radiation levels vary greatly at a local scale due to
heterogeneity in deposition of radioactive material after the
Chernobyl accident (Fig. 1; Shestopalov 1996).
Dosimetry
A subsample of 44 trees was used to estimate radionuclide
activity within cores using gamma spectrometry. All
measurements were conducted using a Berkeley Nucleon-
ics SAM940 radionuclide identifier system equipped with a
10 910 cm NaI detector housed within a ‘‘cave’’ com-
prising about 1,200 kg of lead shielding. This amount of
shielding resulted in a very low background radiation level
of about 7.5 gcps, thus permitting very high sensitivity.
System calibration was accomplished using a 0.204 mic-
roCi source. Counts were recorded for the known source to
produce a calibration factor used to convert the counts from
unknown samples to Ci. The source was approximately the
same size and shape as the samples and was placed in the
same configuration for reading as the samples, thus
ensuring the same geometry. Cores were usually counted
between 2 and 12 h, depending on the expected activity
levels, with higher activities requiring shorter counting
times for measurement. Twenty-cm-long cores were cut
into four 5-cm pieces to fit atop the scintillation detector.
The average 20-cm
3
core had a dry mass of 0.81 g. A
subsample of 12 cores was counted twice to determine the
repeatability of measurements. Activity measurements on
these cores was highly repeatable [linear regression:
activity (2) =0.034 ?1.056 * activity (1); F=7.39,
d.f.=1, 10, P\0.0001, r
2
=0.92]. The outer 5-cm pie-
ces for 13 cores were counted individually to assess whe-
ther radionuclides were evenly distributed throughout the
core or concentrated toward the outer regions of the tree
trunk. Gamma spectra generated for each sample were
inspected and compared to a background reference spec-
trum.
137
Cs activity was estimated by integrating the
activity above the background threshold at 662 keV, the
energy level for
137
Cs photon decay products. Following
counting, cores were weighed on a Mettler electronic bal-
ance and individual mass was used to standardize radio-
activity across samples for most samples. Small pieces of
some cores were destroyed during the measurement pro-
cess and a mass based on the average for all cores was used
to estimate mass for these damaged samples.
Meteorology
We used the E-OBS gridded dataset (version 2.0) main-
tained by the European Climate Assessment & Dataset
(ECA&D) for studying temperature and rainfall (Haylock
et al. 2008). We calculated mean temperature and rainfall
for the main growing season April–August for each year.
Statistical analyses
The background radiation level was log
10
-transformed. We
developed statistical models to assess the relationship
between standardized growth rate and radiation, as imple-
mented in the statistical software JMP (SAS 2012). We
tested for differences in the mean growth rate using Welch
ANOVA, while simultaneously testing for the significance
of a difference in variance among years using Bartlett’s
test.
We tested for differences in means and variances in
growth rates in relation to the level of background radiation
using a repeated-measures design that allowed for tests
among periods. Means and standard deviations were
recorded for the five 5-year periods 1981–1985, 1986–1990,
1991–1995, 1996–2000 and 2001–2005.
Trees
123
We developed three generalized linear models. First, we
developed a model of the relationship between the mean
standardized tree growth rate in 1981–1985 and
1986–1990, using a repeated-measures design to partition
the effects of radiation and period. We used a similar
model for standard deviation in standardized tree growth
rate for the two periods. Second, we used a model of the
difference in standardized growth rate between 1981–1985
and 1986–1990 as the response variable, and radiation,
height and their interaction as predictors. Third, we
developed a full-factorial model of standardized growth
rate as the response variable, and background radiation,
temperature, rainfall, period (1950–1985 vs. 1986–2008)
and their two-way interactions and the only three-way
interaction that approached statistical significance as
predictors.
We calculated the mean residual standard growth rate
for different years and used these data in a logistic
regression model with suppressed growth (1—suppressed
growth less than -0.10 for mean standardized growth rate,
0—for normal growth) as the response variable, and period
(0—before 1986, 1—1986 or later), temperature, precipi-
tation and their two-way interactions as predictors.
A more detailed investigation of the relationship
between radioactivity contained within the tree cores and
annual growth rates was performed by calculating the mean
difference in absolute growth (mm per year) for the 5 years
after the disaster versus the growth for the 5 years before
1986 and relating this to the level of radioactivity measured
within each tree core (Fig. 5b). To minimize the potential
effects of tree size on changes in growth, only large trees
older than 10 years (mean =22.6 years) at the time of the
accident in 1986 were included.
We evaluated the magnitude of associations using effect
sizes estimated as Pearson product–moment correlation
coefficients. Cohen (1988) proposed explicit criteria for
evaluation of small (Pearson r=0.10, explaining 1 % of
the variance), intermediate (9 % of the variance) and large
effects (25 % of the variance).
Results
We measured 3,758 tree rings from 105 Scots pines.
Annual growth increments were on average 2.93 mm
(SE =0.03, median 2.55 mm, range 0.12–13.49 mm).
Residual growth rates were on average -0.042 (SE =
0.004, median =-0.014, range -2.46 to 0.71). Detrended
standardized annual growth (det_bail) was on average
-0.038 (SE =0.004, median =-0.010, range 0.707 to
-2.456). These two standardized growth rates were
strongly positively correlated (Pearson r=0.999), and,
therefore, we used det_bail in all subsequent analyses
(these are listed as standardized growth rates in the rest of
the paper). Individual annual standardized growth rates had
a lognormal distribution (KSL test, D=0.00, P=0.15).
Trees were 7–25 m tall, mean 15.6 m (SE =0.4, med-
ian =15.8 m), had a diameter of 19–49 cm, mean 29.3 cm
(SE =0.52, median =29 cm), and were 9–94 years old,
mean 42.1 years (SE =0.3, median =42 years).
Radioactivity within tree cores varied from below
detection levels to as high as 23,738 (SE =135) Bq/kg of
cesium-137 on measuring the full 20-cm core (Table 1).
The highest readings were from trees located in the Red
Forest area. The average activity across all measured cores
was 3,530 Bq/kg (SE =895). Radionuclides were not
evenly distributed across cores with approximately 46 % of
total core activity found within the outer 5 cm of the core
(liner regression, outer activity =-0.005 ?0.464 * Total
activity, F=207.2, d.f.=1, 11, P\0.0001; r
2
=0.95).
The highest estimated activity for outer wood cores was
65,815 (SE =374) Bq/kg (Table 1).
The Cs-137 activity measured from the tree cores was
highly correlated with background radiation levels at the
base of the tree measured using a handheld Geiger counter
[linear regression, log(Activity (Bq/kg)) =1.33 ?1.70 *
log(Background), F=93.3, d.f.=1, 42, P\0.0001,
r
2
=0.68; Fig. 2], indicating that simple field measure-
ments of background radiation provide a reliable estimate
of the likely dose experienced by the tree.
The change in tree growth rate at the time of the
Chernobyl accident is clearly visible in pine logs from the
Chernobyl Exclusion Zone (Fig. 3). Growth varied signif-
icantly among years (Welch ANOVA: F=4.54, d.f.=90,
115.12, P\0.0001), with significant differences in vari-
ance among years (Bartlett’s test, F=5.37, d.f.=90,
P\0.0001). While growth varied little during 1914–1985
(F=1.86, d.f.=67, 806.84, P=0.0062; F=2.08,
d.f.=67, P\0.0001), there was considerably greater
variation during 1986–2008 (F=15.72, d.f.=22, 807.33,
P\0.0001; F=15.72, d.f.=22, P\0.0001). In fact,
the variance during 1986–2008 was significantly greater
than during 1914–1985 (variance ratio test, F=1.19,
d.f.=1,521, 2,173, P\0.0001).
Closer inspection of mean annual values revealed
severely depressed growth less than -0.10 in 1987–1989,
and again in 1992, 1996, 2003 and 2006 (Fig. 4). In con-
trast, there was only a single year with clearly elevated
growth greater than ?0.10 (1982). The probability of
having 3 years in a row with depressed growth (1987–
1989) was 7/29 years =0.2414 to the third power, which
equals 0.0141. A logistic regression with a poor year
with reduced growth as the response variable (a score of
1—poor year, 0—normal year) and period (before or after
the accident in 1986), temperature, rainfall and all two-way
interactions as predictors produced a significant model
Trees
123
Table 1 Radiation activity levels for Scots pine trees in the vicinity of the Chernobyl nuclear power plant
Location Background radiation (lSv/h) Full core (Bq/kg) SE Outer 5 cm (Bq/kg) SE
Red Forest 25.1 23,738 135 65,815 374
Red Forest 18.6 19,917 169 27,499 233
Red Forest 18.9 17,545 292 44,171 736
Red Forest 16.7 15,362 129 39,007 328
Red Forest 21.4 14,383 171 18,312 218
Red Forest 17.7 13,303 145 21,443 233
Korohod 34.5 6,322 126 11,489 230
Vesniane 10.6 6,072 164 11,928 322
Korohod 26.9 3,928 123 8,131 254
Red Forest 23.5 3,828 153 6,199 248
Korohod 26 3,692 119 6,105 197
Korohod 8.1 3,172 198 6,190 387
Red Forest 16.7 2,961 141 4,737 226
Red Forest 16 2,896 152 5,253 276
Red Forest 16 2,840 123 2,868 125
Fish pond 3.6 2,796 164 1,891 111
Red Forest 13 2,438 163 5,342 356
Red Forest 11 1,168 130 2,247 250
Korohod 9.1 1,005 167 2,121 353
Red Forest 12 949 136 2,743 392
Vesniane 17 943 157 1,212 202
Korohod 31.8 897 112 1,973 247
Korohod 9.9 873 146 1,566 261
Yampil 0.17 568 189 948 316
Vesniane 18.7 510 128 458 114
Fish pond 4.7 435 145 748 249
Vesniane 7.3 423 141 682 227
Red Forest 11 296 99 566 189
Red Forest 11 291 146 506 253
Prypiat 1.4 182 182 257 257
Varo 1.5 181 181 395 395
Prypiat 2.8 178 178 318 318
Stari 0.6 146 146 240 240
Stari 0.7 146 146 240 240
Stari 0.8 146 146 240 240
Varo 4 146 146 240 240
Dytiaku 0.18 146 146 240 240
Krashytichi 0.09 146 146 240 240
Bobor 0.8 146 146 240 240
Bobor 1.3 146 146 240 240
Varo 3 0 0 0 0
Krashytichi 0.08 0 0 0 0
Bobor 1.4 0 0 0 0
Pisky 0.11 0 0 0 0
Full-core estimates are for complete 20-cm cores that reflect average tree activity, while activity levels for the outer 5 cm are on average
significantly more radioactive on a per weight basis reflecting a higher concentration of Cs-137 in the cambium and the bark
Trees
123
(v
2
=13.68, P=0.033) that fitted the data (v
2
=25.55,
P=0.95). There was a significant effect of period
(v
2
=9.35, P=0.0022), while all other effects were small
and not significant (likelihood-ratio v
2
\0.45, P[0.50).
Among the 23 years 1986–2008, there were 7 years with
significant correlations between standardized annual growth
(det_bail) and background radiation (1986, 1988,1989, 1990,
1996, 1998, 2006), while 1.15 would be expected by chance.
The mean correlation coefficient was only -0.075
(SE =0.031), which was significantly different from zero
(one-sample ttest based on ztransformed Pearson correlation
coefficients: t=-2.45, d.f.=22, P=0.023).
Repeated-measures ANOVA revealed a highly signifi-
cant negative effect of background radiation on mean
growth rate, a significant effect of period (1981–1985 vs.
1986–1990) and a significant interaction (Table 2). This is
as expected, if tree growth was reduced only after 1986 and
only in trees from contaminated areas. A second repeated-
measures ANOVA revealed a significant positive effect of
background radiation on variation in growth rate as
reflected by the standard deviation (Table 2). In addition,
there was a significant effect of period and a significant
interaction.
When analyzing the level of depression of standardized
growth after and before 1986, we found that growth was
disproportionately reduced at high radiation levels with an
effect size that was intermediate (Table 3; Fig. 5a). Back-
ground radiation levels explained 13 % of the variance in
standardized tree growth. There was a highly significant
negative relationship between the change in mean growth
rate and the radioactivity measured within tree cores [linear
regression: change in mean growth rate =-0.42 radioac-
tivity in the wood (Bq/kg) ?0.91; F=6.87, d.f.=1, 23,
P=0.016] indicating that growth was significantly lower
following the disaster for trees with contaminated wood
Fig. 2 The relationship between Cs-137 activity (Bq/kg dry weight)
in tree cores and background radiation level (lSv/h) at the base of
each tree
Fig. 3 Difference in width of tree rings in pine logs from Chernobyl.
The year of the accident in 1986 is clearly visible from the change in
the color of the wood
Fig. 4 Mean (?SE) annual standardized growth rates of 105 Scots
pine trees around Chernobyl during 1980–2008. Severely depressed
growth is visible during 1987–1989 and also in several subsequent
years
Table 2 Repeated-measures analysis of variance of mean and stan-
dard deviation in residual standardized growth rate in relation to
background radiation level, period and their interaction for 105 Scots
pine trees
Source of
variation
Factor Fd.f.PSlope
(SE)
Means
Between
subjects
Radiation (R) 25.39 1, 103 \0.0001 -0.052
(0.011)
Within
subjects
Period (P) 7.89 4, 100 \0.0001
R9P6.75 4, 100 \0.0001
Standard deviations
Between
subjects
Radiation (R) 16.15 1, 102 \0.0001 0.061
(0.006)
Within
subjects
Period (P) 7.35 4, 99 \0.0001
R9P7.90 4, 99 \0.0001
Trees
123
relative to trees of low levels of contamination in the wood.
The level of radioactivity in wood accounted for 23 % of
the variance in standardized tree growth (Fig. 5b). Stan-
dardized growth was particularly reduced by radiation in
small trees (Fig. 5c).
Growth rate improved in warm and especially in rainy
years, and this effect was stronger when it was both warm
and rainy as shown by the temperature by precipitation
interaction (Table 4). The effects of temperature exacer-
bated the effect of radiation as shown by the temperature-
by-radiation interaction. The effect of temperature changed
in 1986, as shown by the interaction between temperature
and period. Thus, the effects of radiation were mediated by
the impact of temperature and drought. The other effects
including the interactions were either not significant or
marginal effects.
Discussion
The main findings of this study of growth rate of Scots pine
were that reduced growth increments and increased vari-
ance in the size of growth increments were associated with
elevated levels of background radiation. The magnitude of
the radiation effect depended on the size of trees, because
small trees showed disproportionately reduced growth
when exposed to radiation compared to large trees. Other
environmental stressors (e.g., temperature and low annual
precipitation) interacted with radiation to reduce growth.
While our data showed a 3-year continuous effect of
radiation on growth suppression, our observations indi-
cated greater variation in annual growth after 1986 and
suppressed growth in 1992, 1996, 2003 and 2006. Indeed,
standardized growth rate was significantly related to
background radiation in 8 years, with a significant mean
effect across all years, suggesting a continual mean effect
of the Chernobyl accident that extends to the present. This
effect size of an intermediate magnitude of 0.30 is similar
to the mean effect size of 0.28 found across all meta-
analyses in the biological sciences including meta-analyses
of the effects of CO
2
on plants (Møller and Jennions 2002).
This conclusion is supported by the fact that these excep-
tionally poor years in terms of growth are not associated
with elevated temperatures or drought, nor could we doc-
ument any interaction between weather and radiation.
The degree of suppression of the mean level of
growth during 1986–1990 (post-Chernobyl) compared to
1981–1985 (pre-Chernobyl) of individual trees was caused
by radiation interacting with tree height, with radiation
effects being disproportionately greater in small compared
to large trees. There are several possible interpretations.
First, more than 90 % of all radioactive material is located
in the topmost 20 cm of the soil. Short trees having shallow
root systems that do not extend deep into the soil may
extract more radionuclides than tall trees with deep root
systems. Second, growth rate effects may be more readily
discerned in small trees given the larger absolute growth
rates in short trees (Koch et al. 2004). Third, this may be
caused by an interaction related to differential effects of
radiation on mycorrhizae, which may significantly influ-
ence radionuclide uptake (Dighton et al. 2008).
The mean growth rate of Scots pines from Chernobyl
varied significantly among years, with a highly significant
difference in variance among years. High levels of varia-
tion in growth were much more pronounced during
1986–2009 following the accident in 1986 than during
Table 3 Difference in mean residual standardized growth rate of
Scots pine trees between 1986–1990 and 1981–1985 in relation to the
level of background radiation, tree height and their interaction
Variable Sum of
squares
d.f.FP Slope (SE)
Radiation (R) 0.184 1 9.48 0.003 -0.050 (0.016)
Height (H) 0.043 1 2.20 0.141 0.005 (0.003)
R9H0.109 1 5.60 0.020 0.009 (0.004)
Error 2.356 101
The model had the statistics F=6.79, d.f.=3, 101, r
2
=0.17,
P=0.0003
Fig. 5 Difference in mean standardized growth rate of 105 Scots pine trees around Chernobyl between 1986–1990 and 1981–1985 in relation to
abackground radiation level (lSv/h), bradioactivity of the wood (Bq/kg) and cheight of trees (m)
Trees
123
1914–1985. Suppression of growth occurred during three
subsequent years 1987–1989, and during 1992, 1996, 2003
and 2006, and this suppression was associated with radia-
tion, but not significantly with temperature, precipitation or
their interactions with radiation. Increasing variance in
growth can be a consequence of increasing age and stem
diameter (e.g., Fritts 1976; Carrer and Urbinati 2004)
although this explanation is difficult to reconcile with a
sudden change in mean and variance in standardized tree
growth in 1986. Schmitt et al. (2000) reported suppressed
xylem growth in Scots pine during 1987–1989, but not
during 1986, when the accident happened in spring. The
probability of having three consecutive years of suppressed
growth was significantly less than expected randomly,
suggesting that the run of 3 years of suppressed growth
during 1987–1989 was exceptional. Given that radiation
effects were not observed in all years after 1986, we can
conclude that other stressors interacted with radiation to
suppress growth. We hypothesize that the annual weather
patterns interacted synergistically with spatially congruent
patterns of site conditions (e.g., the sandy soils of Chernobyl)
and levels of Cs-137 deposition at the landscape scale to
produce significant growth suppression. This hypothesized
interaction is supported by our observations of greater varia-
tion in annual growth after 1986 and suppressed growth in
1992, 1996, 2003 and 2006, when both spatial and temporal
patterns of environmentalstressors matched to produceeffects
on growth. Repeated-measures analyses of variance con-
firmed these conclusions by demonstrating that means were
reduced and variances increased during some but not all
periods, that these effects were related to radiation, and that
radiation effects differed among periods. Thus, our data show
a 3-year continuous effect and ongoing effects for more than
20 years, which likely extends to the present.
There are uncertainties concerning the nature of Cher-
nobyl effects on tree growth including the mechanisms
underlying the effects of radionuclides on tree growth. The
effects on somatic and germline mutation rates are well
documented (Arkhipov et al. 1994; Kal’chenko and Fedo-
tov 2001; Kal’chenko et al. 1993a,b). The physiological
mechanisms of uptake of mixtures of radionuclides by
plants remain poorly known, as are the relative effects of
external exposure to radiation versus internal exposure to
radioactive heavy metals that are carried through the xylem
to growing tissues. Our observation of a dose-dependent
response provides support for the hypothesis that radio-
nuclides are in large part responsible for our results. By
using a sampling regime that included a relatively large
number of samples with a wide spatial distribution with
respect to contamination level (Fig. 1.), we were able to
test our hypothesis. In other words, depressed growth was
observed in trees exposed to even small levels of Cher-
nobyl-derived radioactive contaminants exceeding the
natural background level by a factor ten independently of
distance from the reactor site and this is most parsimoni-
ously explained by a direct effect of radioactive contami-
nants on growth.
Although we only investigated the effects of radiation
on growth rate, pines were clearly also affected in terms of
composition of the wood (Fig. 2). Changes in quality and
quantity of wood may not only have important implications
for decomposition and use as a construction material, but
also for forest fires that are known to be a significant threat
by redistribution of radionuclides to inhabited areas even
far outside the Chernobyl Exclusion Zone (Kashparov et al.
2000; Yoschenko et al. 2006a,b). The very high activity
levels of Cs-137 in tissues of trees in highly contaminated
areas reported here further emphasize the need for
Table 4 Relationship between residual standardized growth rate of Scots pine trees between 1950 and 2008 in relation to the level of
background radiation, temperature and rainfall during April–August, and whether the data were obtained before or after 1986
Variable Sum of squares d.f.FP Slope (SE)
Temperature (T) 0.277 1 4.59 0.032 0.011 (0.005)
Precipitation (P) 1.213 1 20.08 \0.0001 0.054 (0.012)
Radiation (R) 0.077 1 1.28 0.26 -0.005 (0.005)
Before/after 1986 (B) 0.003 1 0.05 0.82 0.001 (0.005)
T9P0.647 1 10.55 0.0012 0.048 (0.016)
T9R0.472 1 7.67 0.0056 -0.015 (0.005)
T9B0.643 1 10.45 0.0012 0.016 (0.005)
P9R0.176 1 2.86 0.091 0.020 (0.012)
P9B0.034 1 0.56 0.46 0.009 (0.012)
R9B0.570 1 9.26 0.0024 -0.016 (0.005)
T9P9B0.172 1 2.80 0.094 -0.026 (0.016)
Error 223.788 3,636
The model had the statistics F=5.69, d.f.=11, 3,587, r
2
=0.02, P\0.0001
Trees
123
investigation concerning the potential impacts of forest
fires on the dispersal of radionuclides in populated regions.
In conclusion, we have demonstrated a landscape-scale
effect of severely reduced growth in Scots pine during
three consecutive years following the nuclear disaster at
Chernobyl, and recurrently in several subsequent years
when environmental stressors were spatially and tempo-
rally congruent. Given that significant levels of radionuc-
lides were dispersed across 200,000 km
2
in Europe as a
consequence of the Chernobyl disaster, these findings
suggest that there may be ecosystem-scale impacts on
productivity that have not previously been suggested.
Acknowledgments We are grateful for logistic help during our
visits to Ukraine and Belarus from M. Bondarkov and A. Litvinchuk.
We also thank L. Dobbs for assistance with radio-dosimetry at USC.
We received funding from the University of South Carolina School of
the Environment, Bill Murray and the Samuel Freeman Charitable
Trust, the National Science Foundation, NATO, the Fulbright Pro-
gram, CRDF and the National Geographic Society to conduct our
research. We acknowledge the E-OBS dataset from the EU-FP6
project ENSEMBLES (http://www.ensembles-eu.org) and the data
providers in the ECA&D project (http://eca.knmi.nl).
References
Arkhipov NP, Kuchma ND, Askbrant S, Pasternak PS, Musica VV
(1994) Acute and long-term effects of irradiation on pine (Pinus
sylvestris) stands post-Chernobyl. Sci Total Environ 157:383–
386
Carrer M, Urbinati C (2004) Age-dependent tree-ring growth
responses to climate in Larix decidua and Pinus cembra.
Ecology 85:730–740
Ceulemans R, Mousseau M (1994) Effects of elevated atmospheric
CO
2
on woody plants. New Phytol 127:425–446
Cherubini P, Gartner BL, Tognetti R et al (2003) Identification,
measurement and interpretation of tree rings in woody species
from Mediterranean climates. Biol Rev 78:119–148
Cohen J (1988) Statistical power analysis for the behavioral sciences.
Erlbaum, Hillsdale
Cook ER, Kairiukstis LA (eds) (1990) Methods of dendrochronology:
applications in the environmental sciences. Kluwer Academic,
Dordrecht
Dighton J, Tugay T, Zhdanova N (2008) Fungi and ionizing radiation
from radionuclides. FEMS Microbiol Lett 281:109–120
Fritts HC (1976) Tree rings and climate. Academic Press, London
Haylock MR, Hofstra N, Klein Tank AMG, Klok EJ, Jones PD, New
M (2008) A European daily high-resolution gridded dataset of
surface temperature and precipitation. J Geophys Res (Atmo-
spheres) 113:D20119. doi:10.1029/2008JD10201
Kagawa A, Aoki T, Okada N, Katayama Y (2002) Tree-ring
strontium-90 and cesium-137 as potential indicators of radioac-
tive pollution. J Environ Qual 31:2001–2007
Kal’chenko VA, Fedotov IS (2001) Genetic effects of acute and
chronic ionizing irradiation on Pinus sylvestris L. inhabiting the
Chernobyl meltdown area. Russ J Genet 37:341–350
Kal’chenko VA, Arkhipov NP, Fedotov IS (1993a) Mutations of
enzyme loci, induced in megaspores of Pinus sylvestris L. by
ionizing radiation after the accident at the Chernobyl Atomic
Power Plant. Genetika 29:266–273
Kal’chenko VA, Rubanovich AV, Fedotov IS, Arkhipov NP (1993b)
Genetic effects of the Chernobyl meltdown on the germline cells
of common pine Pinus sylvestris L. Genetika 29:1205–1212
Kashparov VA, Lundina SM, Kadygriba AM, Protsaka VP, Levt-
chuka SE, Yoschenkoa VI, Kashpurb VA, Talerko NM (2000)
Forest fires in the territory contaminated as a result of the
Chernobyl accident: radioactive aerosol resuspension and expo-
sure of fire-fighters. J Environ Radioact 51:281–298
Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to
tree height. Nature 428:851–854
Kovalchuk O, Dubrova YE, Arkhipov A, Hohn B, Kovalchuk I
(2000) Wheat mutation rate after Chernobyl. Nature 407:583–
584
Kovalchuk O, Burke P, Arkhipov A, Kuchma N, James SJ,
Kovalchuk I, Pogribny I (2003) Genome hypermethylation in
Pinus sylvestris of Chernobyl—a mechanism for radiation
adaptation? Mutat Res 529:13–20
Larsson L (2008a) CooRecorder Program of the CDendro Package
Version 7.1. http://www.cybis.se
Larsson L (2008b) CDendro Program of the CDendro Package
Version 7.1. http://www.cybis.se
Møller AP, Jennions MD (2002) How much variance can be
explained by ecologists and evolutionary biologists? Oecologia
132:492–500
Møller AP, Mousseau TA (2006) Biological consequences of
Chernobyl: 20 years after the disaster. Trends Ecol Evol 21:
200–207
Møller AP, Mousseau TA (2007a) Determinants of interspecific
variation in population declines of birds from exposure to
radiation at Chernobyl. J Appl Ecol 44:909–919
Møller AP, Mousseau TA (2007b) Species richness and abundance of
birds in relation to radiation at Chernobyl. Biol Lett 3:483–486
Møller AP, Mousseau TA (2008) Reduced abundance of raptors
in radioactively contaminated areas near Chernobyl. J Orn
150:239–246
Møller AP, Mousseau TA (2009) Reduced abundance of insects and
spiders linked to radiation at Chernobyl 20 years after the
accident. Biol Lett 5:356–359
Rubanovich AV, Kal’chenko VA (1994) Altered segregation in Pinus
sylvestris L. populations exposed to chronic irradiation in the
region of the Chernobyl meltdown. Genetika 30:126–128
SAS Institute Inc (2012) JMP version 10.0. SAS Institute Inc., Cary,
NC
Schmitt U, Gru
¨nwald C, Eckstein D (2000) Xylem structure in pine
trees grown near the Chernobyl Nuclear Power Plant/Ukraine.
IAWA J 21:379–387
Shestopalov VM (1996) Atlas of Chernobyl exclusion zone. Ukrai-
nian Academy of Science, Kiev
Shevchenko VA, Abramov VI, Kal’chenko VA et al (1996) Genetic
consequences induced in plant populations as a result of
radioactive environmental pollution after the Chernobyl melt-
down. Radiat Biol Radioekol 36:531–545
Ufar K (2007) Dendrochronology and past human activity: a review
of advances since 2000. Tree Ring Res 63:47–60
Woodwell GM, Miller LN (1963) Chronic gamma radiation affects
the distribution of radial increments in Pinus rigida stems.
Science 139:222–223
Yablokov AV, Nesterenko VB, Nesterenko AV (2009) Chernobyl:
consequences of the catastrophe for people and nature. New
York Academy of Sciences, New York
Yoschenko VI, Kashparov VA, Levchuk SE, Glukhovskiy AS,
Khomutinin YV, Protsak VP, Lundin SH, Tschiersch J (2006a)
Resuspension and redistribution of radionuclides during grass-
land and forest fires in the Chernobyl exclusion zone: part II.
Modeling the transport process. J Environ Radioact 87:260–278
Trees
123
Yoschenko VI, Kashparov VA, Protsak VP, Lundin SM, Levchuk SE,
Kadygib AM, Zvarich SI, Khomutinin YV, Maloshtan IM,
Lanshin VP, Kovtun MV, Tschiersch J (2006b) Resuspension
and redistribution of radionuclides during grassland and forest
fires in the Chernobyl exclusion zone: part I. Fire experiments.
J Environ Radioact 86:143–163
Zakharov VM, Krysanov EY (eds) (1996) Consequences of the
Chernobyl catastrophe: environmental health. Center for Russian
Environmental Policy, Moscow
Trees
123
