Biological effects of chronic exposure
to radionuclides in plant populations
Stanislav A. Geras’kin
Russian Institute of Agricultural
Radiology and Agroecology,
Obninsk, Russia
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What’s actually going on in the populations
inhabiting radioactively contaminated sites?
What do we know about mutagenic effect of
chronic low dose-rate radiation exposure?
What do we know about the fate of induced by
radiation mutations in altered ecological
conditions?
Can chronic low dose-rate radiation exposure be
regarded as ecological factor changing the
genetic make-up of a population?
In which way chronic radiation exposure can
modify reproductive ability, species diversity and
community structure?
Species
Site & Time
Assay and/or endpoints
Winter rye and
10-km ChNPP zone (28-4834
wheat, spring barley µGy/h), Ukraine, 1986-1989
and oats
Morphological indices of seeds viability, mitotic
index, cytogenetic alterations in intercalary and
seedling root meristem (Geras’kin et al., 2003a)
Scots pine, coachgrass
30-km ChNPP zone (2.5-27
µGy/h), Ukraine, 1995
Cytogenetic alterations in seedling root meristem
(Geras’kin et al., 2003b)
Scots pine
Radioactive waste storage
facility, Leningrad Region,
Russia, 1997-2002
Cytogenetic alterations in needles intercalary and
seedling root meristems (Geras’kin et al., 2005;
Oudalova, Geras’kin, 2011)
Wild vetch, Scots
pine
Radium production industry
Germination capacity, survival rate of sprouts,
storage cell, Komi Republic,
embryonic lethals, proportion of abortive seeds,
Russia (1-320 μGy/h), 2003-2009 cytogenetic alterations in seedling root meristem
(Evseeva et al., 2009; Evseeva et al., 2011)
Scots pine
Bryansk Region radioactively
contaminated in the Chernobyl
accident (1-15 μGy/h), Russia,
2003-2012
Cytogenetic alterations in seedling root meristem,
enzymatic loci polymorphism, abortive seeds
(Geras’kin et al., 2010; Geras’kin et al., 2011;
Volkova, Geras’kin, 2012)
Crested hairgrass
Semipalatinsk Test Site (0.5-32
µGy/h), Kazakhstan, 2005-2008
Cytogenetic alterations in coleoptiles of germinated
seeds, length of sprouts (Geras’kin et al., 2012)
Phytoplankton
communities
Industrial reservoirs, Southern
Urals (2-130000 µGy/h), Russia,
2007-2012
Species diversity, abundance, biomass (Atamaniuk
et al., under preparation)
Scots pine
Pinus sylvestris L.
250-350 µR/h
Doses absorbed
in generative organs of pine trees
50-70 µR/h
Study
Dγ,biological
mGy Dβ, mGy consequences
Dsum, mGy
What
site
Bryansk region, Russia
2003-2012
180-220 µR/h
120-140 µR/h
can be expected in these
populations
experiencing
chronic exposure over 25 years?
Ref
0.124
0.013
0.14
Ref1
0.267
0.006
0.27
VIUA
6.62
0.344
7.
SB
22.7
0.156
23.
Z1
90.2
1.20
91.
Z2
129.4
0.506
130.
Geras’kin et al. Ecotoxicology. 2011. V. 20. 1195-1208
Scots pine Pinus sylvestris L. Bryansk region, Russia
2003-2012
2003
Aberrant cells, %
2,0
2004
1,5
2005
2006
1,0
2007
2008
0,5
2009
An increased level of cytogenetic alterations is a typical
0,14
0,27
6,96
22,9
91,4
129,9
phenomenon
for plant
populations
growing
in areas
Dose, mGy
with relatively low levels of pollution
0,0
correlation: r=63% p<5%
2,5
2010
Ref
hatched bars – significant difference
from reference level, p<5%
Aberrant cells, %
Ref1
VIUA
2,0
SB
1,5
Z1
Z2
1,0
Ряд7
0,5
Линейны
й (Ряд7)
0,0
0
0,5
1
Dose rate, μGy/h
Geras’kin et al. Ecotoxicology. 2011. V. 20. 1195-1208
1,5
Bryansk region, Russia
Scots pine Pinus sylvestris L.
Significant
increase with
dose
High mutation rates is intrinsic for
progeny of the affected pine trees, and
genetic diversity is essentially
influenced by radiation exposure
Volkova, Geras’kin Radiation Biology. Radioecology. 2012. V. 52. p. 370-380 (in Russian)
Could the high mutation rates revealed
Bryansk region, Russia
have any effect on population fitness?
Are there any consequences for a
Scots pine Pinus sylvestris L.
reproductive ability of pine trees?
Re f -0.14 mGy/year
Ref 1 -0.27 mGy/year
Abortive seeds, %
100
7.0 mGy/year
80
60
23.0 mGy/year
*
91.4 mGy/year
*
130.0 mGy/year
40
20
0
2007
2008
2009
2010
Year
Chronic exposure at dose rates studied had no effect on
the reproductive ability of the exposed populations
Geras’kin et al. Ecotoxicology. 2011. V. 20. 1195-1208
Are there any relationship between reproductive ability and
weather conditions?
2 years
6
100
R2 = 0.1797
r = -0.42
p < 0.05
Germination, %
Immature seeds, pieces
8
4
2
May
80
60
40
20
0
0
3400
3600
3800
4000
10
30
25000
August
20000
50
70
90
110
Precipitation, mm
Sum of effective temperatures, degree-day
Seeds in the cone,
pieces
R2 = 0.2318
r = -0.48
p < 0.05
R2 = 0.3658
r = -0.60
p < 0.05
15000
10000
IA
5000
0
0
1
2
3
Aridity index
4
5
P 10
Tn
130
What do we know about biological effects in plants exposed
to radiation over several generations in natural setting?
The 10 km Chernobyl NPP
zone
1987-1989
RYE
40
30
20
Autumn 1989
Rye, wheat
Aberrant cells, %
10
0
40
WHEAT
30
20
first generation
second generation
10
third generation
0
0
10
20
Dose, cGy
30
40
Geras’kin et al. J. Environmental
Radioactivity. 2003. V. 66. p.
155-169
Origin of plants from RIARAE’s experimental site
F0
F1
F2
Chernobyl, Red
Forest, 1986
Chernobyl, Red Forest
Self-seeding in 1987,
collection of seeds in 2004
2005 seeding in Moscow Region,
2010 transfer to the RIARAE’s
experimental site
Mass appearance of morphological disorders in second
generation after exposure
A memory of acute irradiation years ago may influence
plant response in subsequent years and generations
Southern Urals, the PA Mayak reservoirs, 2007-2012
Exposure
Absorbed by phytoplankton dose rate, µGy/h
ShR
N-2
R-11
R-4
R-10
Old Swamp
Karachai
External
0.00015 1.1
1.2
34.9
4.3
249.6
124167
Internal
0.0098
0.02
0.8
27.2
91.3
258.3
2883
Total
0.01
1.1
2.0
62.1
95.6
507.9
127050
Southern Urals, the PA Mayak
Reservoirs, 2007-2012
Under chronic exposure to radionuclides species diversity can
reduced due to a loss of sensitive species, which leads to
destruction of biocenotic connections, weakening of competition and
intensive development of the most resistant forms
What do we know about
adaptation processes in
plant populations under
chronic exposure
conditions?
Radioactive waste storage facility
Leningrad Region, Russia, 1997-2002
Scots pine Pinus sylvestris L.
Aberrant cells, %
3
3
2
2
1
1
0
1997
1998
1999
2000
2001
2002
Radioactive
wasteastorage
facility
The
seeds
from
the
impacted
Scots
pine
populations
show
higher
Exposure in field
Leningrad
Region, Russia, 1997-2002
resistance than seeds from the reference
population
Scots pine Pinus sylvestris L.
Radio-adaptation
phenomenon
A divergence
of populations
terms ofofradioresistance
is connected with
Aberrant
cell frequency
in the rootinmeristem
seedlings
a selection
onacutely
the effectiveness
of repair
grown from
irradiated (15 Gy)
seeds systems
Aberrant cells, %
8
6
Experimental plots:
1 – Bolshaya Izhora (control);
2 – Sosnovy Bor town ;
3 – ‘Radon’ waste processing plant
4
2
1
2
3
1 2 3
1 2 3
2000
2001
0
1999
Geras’kin et al. Mutat. Res. 2005. V. 583. p. 55-66
Radium production industry storage cell territory
The Komi Republic, 2003-2009
up to 275
backgrounds
‘black’ dumps
Geras’kin et al. J. Env. Radioact. 2007.
V. 94. p. 151-182
Survival rate of sprouts of seeds, %
50
40
30
20
10
0
0.006 0.008 0.05 0.75 1.67 3.33
5
Survival rate of sprouts of seeds, %
70
60
50
40
30
20
10
0
0.006
0.083
0.421
weighted absorbed dose rate, mGr/day
weighted absorbed dose rate, mGr/day
Comparison
of findings fromFrequency
1980 and
2003: the high
levels
of both
Frequency
of chromosome
of chromosome
Frequency of chromosome
aberrations, %
aberrations, %
aberrations, %
3.5
5
genetic
and
morphologic
intrapopulation
variability
still persist
1
3
2.5
2
1.5
1
0.5
0
4
3
2
1
0
0.8
0.6
0.4
0.2
0
0.006 0.008 0.05 0.75 1.67 3.33
0.006
5
0.083
0.421
0.08
0.22
0.54
1.34
Seeds from the affected wild vetch
populations show rather high
radiosensitivity.
weighted absorbed dose rate, mGr/day
weighted absorbed dose rate,
weighted absorbed dose rate, mGr/day
An inherited character of this phenomenon was demonstrated.
mGr/day
40
35
30
25
20
15
10
5
0
Frequency of embryonic
lethal mutations, %
0.006 0.008 0.05 0.75 1.67 3.33
5
weighted absorbed dose rate, mGr/day
70
60
50
40
30
20
10
0
Frequency of embryonic
lethal mutations, %
0.006
0.083
0.421
weighted absorbed dose rate, mGr/day
Evseeva et al. Sci. Total
Environment. 2009. V.
407. p. 5335-5343.
Evseeva et al., Russian J
Ecology. 2011. V. 42, p.
382-387
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Why sometimes we failed to detect any signs of
radio-adaptation in plant populations?
Increased fitness in unfavorable environment is
associated with decreased fitness in favorable
environment. As a result, there are situations in which
enhanced radioresistance has not evolved or has not
persisted
In situations where radio-adaptation is observed in
one species often none is found in other despite
equivalent opportunity
The response of a population to radiation exposure
depends both on the type of organism and on the
biophysical characteristics of the radiation
Examples of lack of radio-adaptation in
plant populations
γ-exposure of pine seeds from the
Bryansk region (dose of 15 Gy, dose
rate of 36 Gy/h )
γ-exposure of crested hairgrass seeds from
the Semipalatinsk Test Site (2005, 2006 dose of 69 Gy, dose rate of 2790 Gy/h;
2007- dose of 50 Gy, dose rate of 39 Gy/h )
50
25
* *
*
+
Aberrant cells, %
20
*
15
RS
RS1
VIUA
10
SB
Z1
5
Z2
Aberrant cells, %
40
Ref
4,1 мГр
6,7 мГр
264,9 мГр
30
20
10
0
2005
0
2003
2004
2006
2006
2007
Year
Geras’kin et al. Ecotoxicology. 2011. V. 20. 1195- Geras’kin et al. J. Env. Radioactivity.
2012. V. 104. 55-63
1208
Main sources of uncertainty in field studies -1
Our ability to correctly estimate actual
exposures:
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spatial and temporal heterogeneity of the factors
influencing the effect under study;
non-radiation factors that may modify the effect
of radiation exposure;
weighting factors for different radiation types;
non-homogeneous radionuclides distribution
within the organism;
it is not always clear: to which organ and to what
period of time we should assess the absorbed
dose?
Main sources of uncertainty in field studies -2
Our ability to correctly estimate biological effects:
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radio-adaptation;
sinergistic and antagonistic effects of combined
exposure;
information about status of biological system
before exposure;
non-target effects: epigenetics, genomic
instability, and bystander effect
Temporal heterogeneity in radiation exposure in
early days after the Chernobyl accident
The maximum biota
exposure fell within the first
10–20 days after the
accident
 First large-scale and reliable
estimation of radioactive
contamination and dose
rate were performed at the
We have very limited and poor information
about of
theacute
first,
end of the period
most important period when exposure
up to 90%starting
of the doses
from 15
absorbed by non-human biota was accumulated
day after the accident

Geras’kin et al. Env. Internat. 2008. V. 34.
880-897
Non-radiation factors play an important role in biological
effects formation in wild vetch population from radium
production industry storage cell territory
Germination
Survival of seedlings
Evseeva et al. Radiation Biology. Radioecology. 2013. V. 53. in press (in Russian)
Multi-pollutant exposures
acute -radiation
chronic radiation
heavy metals
pesticides
artificial and naturally occurring radionuclides
Chlorella vulgaris
Tradescantia (clon 02)
Allium cepa
Hordeum vulgare
Synergetic and antagonistic effects are most often registered at
combinations of low doses and concentrations
Moreover, these nonlinear effects can make substantial contribution to a
plant response
Combined exposure Hordeum vulgare L.
Aberrant cells, %
(Geras’kin et al. Mutat. Res. 2005. V. 586. p. 147-159)
25
Observed effect
20
Additive model
15
10
5
0
1
2
3
4
5
6
7
8
9
An application
of in
findings
from single
impacts
to on
Aberrant
cell frequecny (%)
intercalar meristem
of spring
barley grown
soil contaminated with Cs-137 and Cd
predict biological effects of combined exposure is
1 – 1.48 MBq/m +and
2 mg/kg;may
2 – 1.48 cause
MBq/m + essential
10 mg/kg; 3 – 1.48deviations
MBq/m + 50 mg/kg;
unacceptable
from
4 - 7.4 MBq/m + 2 mg/kg; 5 – 7.4 MBq/m + 10 mg/kg; 6 – 7.4 MBq/m + 50 mg/kg;
7 – 14.8 MBq/m + 2 mg/kg;
8 – 14.8 MBq/m
+ 10 mg/kg;data
9 – 14.8 MBq/m + 50 mg/kg
actually
observed
2
2
2
2
2
2
2
2
2
Uncertainties related with ecological dosimetry issues
The ERICA Tool, default values
Exposure
Absorbed by phytoplankton dose rate, µGy/h
ShR
N-2
R-11
R-4
R-10
Old Swamp
Karachai
0.92
54.2
2.2
750
170833
833
70833
1500000
71 583
1 670 833
External
0.00019 0.79
Internal
0.19
1.8×10-6
225
833
Total
0.19
0.79
226
887.2 835.2
Our calculations, weighting factor of 5 for α-radiation + actual data on
radionuclides content in phytoplankton
Exposure
Absorbed by phytoplankton dose rate, µGy/h
ShR
N-2
R-11
R-4
R-10
Old Swamp
Karachai
External
0.00015 1.1
1.2
34.9
4.3
249.6
124167
Internal
0.0098
0.02
0.8
27.2
91.3
258.3
2883
Total
0.01
1.1
2.0
62.1
95.6
507.9
127 050
CONCLUSIONS
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To properly understand the effect of real-world
contaminant exposures, we should consider
actual field conditions. Specifically, we need to
plan new well-directed field studies to fill a
major gaps in our knowledge
To reduce the uncertainties associated with the
spatial and temporal heterogeneity it will be
useful to develop the unified standards for
sampling in field studies
CONCLUSIONS-2
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
To predict radiation exposure in a robust way it is
necessary to develop a process-based transfer and
dosimetric models taking into account current, a
more profound understanding of environmental
processes
To reduce the uncertainties associated with the
biological effects assessment, we should pay more
attention on fundamental research focused on
mechanisms
such
phenomena
as
To addressunderlying
all these issues,
a close
international
cooperation in radioecological
research
is needed
radio-adaptation,
sinergistic and
antagonistic
effects of combined exposure and non-target
effects
That’s all!