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Biological consequences of Chernobyl: 20 years after the disaster 4
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Anders Pape Møller1 and Timothy A. Mousseau2 6
7 1Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, 8
Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, 9
Case 237, F-75252 Paris Cedex 05, France 10 2Department of Biological Sciences, University of South Carolina, 11
Columbia, SC 29208, USA 12
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Corresponding author: Møller, A.P. ([email protected]) 14
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The disaster at the nuclear power plant in Chernobyl in 1986 released 19
80 Petabecquerel of radioactive caesium, strontium and plutonium into 20
the atmosphere, polluting 200000 km2 of land in Europe. Thus, 21
conditions were established for the long-term field study of the 22
ecological and evolutionary consequences of both high and low levels of 23
radiation. Several studies have since shown associations between levels 24
of radiation and the abundance, distribution, life history and mutation 25
rates of plants and animals. However, this research is the consequence 26
of investment by a few individuals rather than a concerted research 27
effort by the international community, despite the fact that the effects 28
of the Chernobyl disaster are continent-wide. A coordinated 29
international research effort is now needed to further investigate the 30
effects of high and low levels of radiation, knowledge can be of benefit 31
if there are nuclear accidents including the threat of a “dirty bomb”. 32
3
Introduction 33
34
One of the four nuclear reactors of the Chernobyl Nuclear Power 35
Plant exploded on 26 April 1986 as a consequence of human errors due to a 36
temporary shutdown of the cooling system. This explosion transported vast 37
amounts of radioactive material into the atmosphere, with much of this 38
material subsequently deposited in the vicinity of the power plant in 39
Ukraine, Russia and Belarus, but also over large parts of Europe and other 40
continents. On the 20th anniversary of the worst environmental nuclear 41
disaster in history, there is still much disagreement among government 42
agencies, health professionals and scientists over the long-term effects of 43
low level nuclear contaminants. The official UN position [1] suggests that 44
the consequences to human health are much lower than expected, the park-45
like appearance of the 2044.4 km2 Chernobyl exclusion zone, with large 46
mammals appearing to be increasing in numbers, suggests an ecosystem on 47
the rebound. However, the UN report, and interpretations of it in the 48
popular and scientific press (e.g. [2,3]), has generated an optimism that 49
might be unfounded. 50
Here, we discuss the information available concerning wild plant and 51
animal populations, but also humans, affected by the Chernobyl event. We 52
summarise published data for phenotypic and fitness effects related to 53
exposure to Chernobyl-derived contaminants. We also provide an extensive 54
review of studies of mutation rates caused by elevated levels of radiation. It 55
is our hope that this information will serve as a foundation for future 56
studies investigating the long-term ecological and evolutionary 57
repercussions of chronic exposure to low-level radioactive contaminants. 58
59
A brief history of the Chernobyl event 60
On 26 April 1986, during a test of the ability of the Chernobyl 61
Nuclear Reactor to generate power while undergoing an unplanned 62
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shutdown, safety systems were turned off leading to an explosion and 63
nuclear fire that burned for ten days releasing between 9.35 x103 PBq and 64
1.25 x 104 PBq of radionuclides into the atmosphere (by contrast, the Three 65
Mile accident in Pennsylvania, USA on 27 March 1979 released just 0.5 66
TeraBecquerel). Although many of these radionulcides either dissipated or 67
decayed within days (e.g. 131Iodine), 137Caesium (137Cs) still persists in the 68
environment even hundreds of kilometres from Chernobyl (Fig. 1). 69
Likewise, 90Strontium (90Sr) and 239Plutonium (239Pu) isotopes are common 70
within the exclusion zone. Given the 30, 29 and 24000 yr half-life for 137Cs, 71 90Sr and 239Pu, respectively, these contaminants are likely to be of 72
significance for many years to come. 73
74
75
Physiological and genetic effects of radiation 76
Immediately following the accident at the Chernobyl nuclear power 77
plant, humans exposed to high-level radiation suffered from acute radiation 78
sickness, including dizziness, vomiting and fatigue [1]. The long-term 79
physiological effects of immediate and later exposure have shown changes 80
in levels of antioxidants, immunity and hormones, as described below. 81
Most of the long-term consequences of the Chernobyl disaster stem 82
from the inhalation and ingestion and of radionuclides generated by the 83
explosion and nuclear fire (Box 1) which is in contrast to the effects due to 84
direct radiation from exposure to nuclear blasts. The genetic consequences 85
of radiation exposure will depend on the received dose, dose rate, and other 86
indirect effects (Box 2). 87
Radiation can reduce levels of antioxidants such as carotenoids and 88
vitamins A and E that are used for protecting DNA and other molecules 89
from damage caused by free radicals [4-8]. Consistent with the prediction 90
that the concentration of antioxidants is reduced by radiation, barn 91
swallows studied in 2000 had significantly reduced amounts of carotenoids 92
5
and vitamins A and E in blood and liver in the most-contaminated areas [9] 93
(Box 3), although the level of radiation was low compared to previous 94
studies of humans [4-8] (Box 4). These reductions were the best predictor 95
of increased frequency of abnormal sperm from male barn swallows in 96
such areas [9]. 97
Antioxidants can have important consequences for immunity owing 98
to their immuno-stimulating effects (reviewed in [10]). Studies of staff at 99
the Chernobyl nuclear plant involved in cleaning-up immediately after the 100
accident have revealed impaired immune function compared with matched 101
control individuals [11-13]. Likewise, barn swallows from Chernobyl had 102
depressed levels of several types of leukocytes and immunoglobulins, and 103
reduced spleen mass compared with individuals from control areas [14], 104
suggesting a reduced ability to raise an efficient immune response. The 105
ratio of two types of leukocytes (heterophil: lymphocyte ratio), which is an 106
important physiological indicator of stress [15], was also elevated in barn 107
swallows from Chernobyl compared with control individuals. 108
The elevated frequency of partial albinism in barn swallows, humans 109
and other organisms can also be linked to the deficiency of antioxidants in 110
individuals from the Chernobyl region [16,17]. Normal plumage or skin 111
colour is produced by the migration of melanocytes from the skin (so-112
called melanoblasts) to feathers; such migration can be disrupted or 113
melanocytes can die prematurely owing to low concentrations of 114
antioxidants in the skin resulting in albinism. Mutations in plumage colour 115
genes can have a similar effect [17]. This hypothesis is supported by the 116
finding that feathers with melanin-based colour are paler in barn swallows 117
from Chernobyl compared with those from individuals from control areas 118
[14]. 119
Surprisingly there has so far been no study of the level of 120
corticosterone or heat shock proteins from organisms from the Chernobyl 121
region, despite these being commonly used indicators of stress. 122
6
In Table 1 we list 33 studies that have investigated mutations or 123
cytogenetic effects of increased radiation around Chernobyl and in control 124
areas in a variety of plant and animal species, including humans. This list is 125
unlikely to be exhaustive, given that most such studies were published in 126
Russian, Belarusian or Ukrainian journals (usually only in the Russian 127
language) and are thus relatively inaccessible to western scientists. There 128
is considerable heterogeneity in results, with 25 of the studies showing an 129
increase in mutations or cytogenetic abnormalities. Several studies showed 130
an increase in mutation rates for some loci, but not for others [18,19]. 131
However, many studies were based on small sample sizes, with a resulting 132
low statistical power being unable to show differences of 25% as being 133
statistically significant. Only four of these studies investigated germline 134
mutations [18-21], and these all found significant increases. Many of these 135
studies were not included in the review by the UN Chernobyl Forum 136
Expert Group [1], implying that the conclusions of this group were not 137
based on available information. 138
Fitness consequences of these increases in mutation rates or 139
chromosomal aberrations remain largely unknown. Ellegren et al. [19] 140
reported an association with between partial albinism and reduced survival 141
in barn swallows, and a subsequent study of standardised differences in 142
phenotype for over 30 different characters of barn swallows between study 143
populations near Chernobyl and in relatively uncontaminated control areas 144
revealed a positive relationship between difference in phenotype and effect 145
of the trait on mating success [22]. Mutations with slightly negative fitness 146
effects could potentially easily be exported out of the contaminated areas, 147
with consequences even for populations than have not been directly 148
exposed to radiation from the Chernobyl disaster. Furthermore, 149
accumulation of mutations in individuals living in the contaminated areas 150
may increase the susceptibility of individuals to adverse environmental 151
conditions, although that remains to be tested experimentally. Although the 152
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official UN report provided estimates of excess human cases of death 153
attributed to the Chernobyl incident perhaps in the order of 10000 [1], we 154
consider these estimates to be premature given the current level of 155
knowledge of mutational impact on humans and other organisms. More 156
research is needed. 157
158
Ecological consequences of radiation 159
There has been, until now, little research on the ecological 160
consequences of the Chernobyl disaster. Although studies of the abundance 161
of common species of vertebrates and invertebrates can easily be done at a 162
low cost, we are only aware of a single empirical study investigating the 163
effects of radiation on the distribution and abundance of individuals and 164
species. In that study, the occupation rate of nest boxes by small passerine 165
birds in several large areas within and outside the exclusion zone was 166
negatively related to background radiation level, showing a reduction in 167
nest box occupation by a factor of three in great tits Parus major and by a 168
factor ten in pied flycatchers Ficedula hypoleuca across a range of 169
background radiation [23]. Such a negative correlation between nest box 170
occupation and increasing radiation levels could be the result of breeding 171
birds avoiding contaminated areas, perhaps because of evidence of 172
reproductive failure in such areas reducing the probability of recruitment 173
by prospecting individuals. However, the relationship between nest box 174
occupation and radiation was already present in the first year of the study, 175
making this explanation unlikely. Second, reduced levels of antioxidants in 176
the body of adult birds caused by radiation could prevent birds from 177
becoming established breeders in highly contaminated areas. Finally, the 178
abundance of invertebrate prey might have been reduced by radiation, 179
causing contaminated sites to be avoided by nesting birds. This seems 180
unlikely given that the fledging success of nestlings was unrelated to level 181
of background radiation [23]. 182
8
Life-history consequences of radiation are expected because life-183
history traits are generally affected by many different physiological 184
pathways that, on their own, and in combination can be affected by 185
mutations or the physiological effects of radiation on antioxidant levels 186
[24]. Studies of the barn swallow have shown significant relationships 187
between background level of radiation and timing of reproduction, clutch 188
size, and hatching success, respectively [25]. Non-breeding females are 189
uncommon in temperate zone passerines, but 23% of female barn swallows 190
from Chernobyl were non-breeders and lacked a naked brood patch during 191
the breeding season (breeding female birds moult feathers on their belly to 192
facilitate incubation of eggs), whereas that fraction was close to zero in the 193
control area in Ukraine [25]. The fraction of non-breeders was negatively 194
related to level of background radiation at different sites [25]. Although 195
breeding date has a strong impact on the probability of recruitment in birds 196
[26], there was no delay in breeding associated with an increase in 197
background radiation by two orders of magnitude [23,25]. The clutch size 198
of barn swallows was reduced in sites with elevated radiation, whereas this 199
was not the case in the great tit or the pied flycatcher [23,25]. Finally, 200
hatching failure was associated with background radiation level in all three 201
species [23,25]. 202
Adult survival prospect is an important determinant of life-time 203
reproductive success [27], and any reduction in survival rate will have 204
important fitness consequences. Adult barn swallows breeding in 205
Chernobyl had survival rates that were reduced by 24% in comparison to 206
control areas for males and by 57% for females [25]. These differences are 207
very large compared with normal intraspecific variation in survival rate. 208
Reduced adult survival and reproduction suggests that extant 209
populations of these bird species in this area are unlikely to be viable; only 210
if there is significant immigration from source populations to the 211
Chernobyl sink can these populations be maintained. Based on our current 212
9
knowledge of source-sink dynamics [28] and known sex differences in 213
adult survival rate and dispersal rate in the barn swallow, we can predict 214
that the rate of immigration should be considerably greater into Chernobyl 215
than into control areas, but only after 1986 and not earlier. Migratory birds 216
winter in specific areas where they tend to return in subsequent years, and 217
the geo-chemical fingerprint of these wintering grounds is stored in the 218
stable isotope composition of feathers for those species that moult during 219
winter [29]. We used this fact to investigate to which extent variance in 220
stable isotope profile differed between barn swallows from Chernobyl and 221
control areas before 1986 (using museum material (Box 4)) and after the 222
disaster [30]. Stable isotope profiles of the population of adult barn 223
swallows from before (using museum material) and after the Chernobyl 224
disaster are more heterogeneous than are those of the control population 225
from control areas. Variances in stable carbon isotope content of feathers 226
(δ13C) of both sexes from post-1986 samples from Chernobyl were 227
significantly larger than variances for feather samples from the control 228
region, and compared with variances for historical samples from both 229
regions. This suggests that stable isotope measurements provide 230
information about population processes following environmental 231
perturbations. It also suggests that optimistic prospects for the future of 232
animal and plant populations reported by the Chernobyl Forum [1] are 233
biased because apparently healthy populations might be sink populations 234
rather than sources exporting individuals elsewhere. 235
We can only speculate about the underlying mechanisms that cause 236
the effects of radiation on life history. One possibility is that the reduction 237
in body antioxidant levels directly affects the timing of reproduction, clutch 238
size and survival prospects because female reproduction is limited by 239
antioxidant availability [31]. Similarly, a reduction in antioxidant levels 240
associated with radiation might also have a negative impact on survival 241
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prospects, especially in migratory birds that during the annual migration 242
produce large amounts of free radicals that must be eliminated to avoid 243
damage to DNA and other molecules [10]. 244
245
Future prospects for Chernobyl research 246
Research during the past 20 years has revealed important insights 247
into the consequences of low and high level radiation. Chernobyl 248
constitutes the most extensive ‘natural’ field laboratory for studies of 249
effects of radiation. However, this “facility” has yet to be fully exploited. It 250
is surprising that there are only a few studies of mutation rates in a small 251
number of species, and that the ecological and evolutionary consequences 252
of low level radiation remain poorly known. No study has to our 253
knowledge investigated whether the disaster has had any effects on 254
population densities of common plants or animals. Likewise, no study has 255
to our knowledge attempted to determine whether slightly deleterious 256
mutations arising from Chernobyl are migrating out of the contaminated 257
zone. 258
This lack of progress is probably a result of the remarkably low level 259
of investment in research at Chernobyl. Consider the 11 September 2001 260
event in New York, which resulted in > US $100 billion in funding for all 261
kinds of research including military research. By contrast, the Chernobyl 262
disaster attracted little research funding, with the total over the past 20 263
years not even reaching US $10 millions. This lack of funding is far from 264
what one might expect given the non-negligible threat of a “dirty” bomb, 265
the use of nuclear weapons, and future accidents at nuclear power plants. 266
Even the nuclear power industry and the over-seeing government agencies 267
should have a strong interest in large-scale research to elucidate these 268
scientific questions. 269
We strongly believe that a concerted research effort, funded by the 270
European Union, USA, Japan and to a lesser extent local governments 271
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would be desirable for several reasons. Such an effort could coordinate 272
research, establish a modern research facility, and boost local scientific 273
competence. A major international institute of radiation research supported 274
by the international community would make the most out of one of the 275
largest man-made environmental disasters, to the benefits of the local 276
community, the general scientific community and the world community at 277
large. 278
279
Acknowledgments 280
We thank G. Milinevski, A. M. Peklo, E. Pysanets, N. Szczerbak, S. 281
Gashack, M. Bondarkov and A. Tokar for logistic help during our visits to 282
Ukraine. We received funding from the CNRS (France), the University of 283
South Carolina School of the Environment, Bill Murray and the Samuel 284
Freeman Charitable Trust, The US Civilian Research & Development 285
Foundation, the National Science Foundation and National Geographic 286
Society to conduct this research. 287
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Box 1. Radiation Exposure Pathways. 288
i. Exposure by inhalation occurs when animals breathe 289
radioactive dust, smoke or gaseous radionuclides into the 290
lungs where radioactive particles often stay lodged for a 291
prolonged period [1]. This type of exposure is of most 292
concern for radionuclides that are alpha (e.g. 239Pu) or beta 293
(e.g. 137Cs and 90Sr) particle emitters, and is likely a major 294
pathway of exposure for those affected by Chernobyl 295
fallout. 296
ii. Exposure by ingestion occurs when an animal swallows 297
radionuclides. As with inhalation, alpha and beta emitters 298
are of greatest concern due to possible prolonged contact 299
with the entire digestive system. Also, since Cs, Sr and Pu 300
are all readily absorbed, internal organs and tissues are at 301
risk. 137Cs is thought to have a relatively short biological 302
half-life being relatively soluble; Sr and Pu are much more 303
likely to be fixed in bones, teeth or liver thus exposing 304
surrounding tissues for the life of the animal [1]. 305
iii. Direct or external exposure is of most relevance for gamma 306
radiation emitters (eg. 137Cs) but of limited concern for 307
alpha emitters as alpha particles cannot penetrate the outer 308
layer of skin. Contact with beta emitters can also generate 309
burns or eye damage but this requires very close contact as 310
beta particles have limited travel distance in the air [1]. 311
312
1 USEPA. 2005. Exposure Pathways. 313
http://www.epa.gov/radiation/understand/pathways.htm 314
315
316
Box 2. Dose, Rate and Bystander Effects of Radiation Exposure 317
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Ionizing radiation results from a stream of photons or charged particles 318
which, when interacting with biological molecules, deposit energy by 319
ionization and/or excitation. Intracellular DNA is extremely sensitive to 320
radiation exposure with the DNA helix easily broken by just a few tens of 321
electron volts exposure. A double strand break is often lethal for the cell. 322
Double strand breaks are difficult for cells to repair correctly, and often 323
lead to loss of chromosomal material at cell division and to cell death. 324
Incorrectly repaired DNA may lead to mutations and carcinogenesis [1]. 325
326
Dose, Rate and Bystander Effects of Radiation Exposure: 327
i. Point mutations (i.e. single base pair substitutions) generally 328
show a linear dose response and are more prevalent at low 329
doses. Intermediate doses are often associated with frame 330
shifts (i.e. single base-pair insertions or deletions), while high 331
doses often lead to multiple mutations which can generate 332
intergenic lesions that result in the loss of multiple genes. 333
Intergenic lesions increase with the square of dose [2]. 334
ii. The rate at which a dose is received also influences 335
mutagenesis. In general, there is a linear relationship between 336
mutation rate and dose rate at low dose rates, and a curvilinear 337
(i.e. exponential) response at high dose rates. Based on 338
observations of DNA repair deficient cell cultures, low dose 339
rates allow for DNA repair, leading to lower mutation rates. 340
Some intragenic lesions (i.e. deletions) are induced by two-hit 341
events and show dose rate dependence [2]. 342
iii. Independent multilocus mutations are sometimes generated by 343
the ame low energy track as a consequence of the folding 344
patterns of DNA [2]. 345
iv. Recent studies of cell cultures exposed to highly focused low 346
dose radiation have shown so-called “bystander” effects 347
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whereby non-target cells neighboring exposed cells show 348
mutagenic effects. The mechanisms underlying bystander 349
effects appear to be diverse and reflect complex pathways of 350
biochemical signaling among cells [1]. 351
352
353
1 Prise, K.M. et al. (2003) A review of the bystander effect and its 354
implications for low-dose exposure. Radiat. Protection Dosimetry 104, 355
347-355 356
357
2 Evans, H.H. and DeMarini, D.M. (1999) Ionizing radiation-induced 358
mutagenesis: radiation studies in Neurospora predictive for results in 359
mammalian cells. Mutat. Res. Rev. Mutat. Res. 437, 135-150 360
361
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Box 3. Medical effects of radiation 362
363
Radiation emergency workers (so-called liquidators) at the 364
Chernobyl plant during and immediately following the accident had very 365
high radioactive doses and died (57 in total). Subsequent investigations of 366
medical effects of radiation from Chernobyl suggested increases in rates of 367
congenital defects, cancers and cardiovascular disease in exposed humans 368
compared to controls. For example, thyroid cancer arising from inhalation 369
of radioactive dust has increased dramatically after 1986, as have 370
congenetical defects and spontaneous abortions in contaminated areas near 371
Gomel, Belarus (Figure 1). In contrast, there was no evidence of increased 372
frequency of disease in an epidemiological study in several Western 373
European countries [1]. 374
Perhaps surprisingly, several studies have also reported increases in 375
the frequency of medical effects of radiation even for control areas, where 376
humans were exposed to elevated radiation levels [2]. This raises serious 377
problems of interpretation, with some scientists suggesting that effects of 378
‘worry’ rather than radiation are the cause of such increases. A more 379
probable explanation might be the transition from communism to free 380
market societies around 1990, causing dramatic reductions in income, 381
nutritional condition and medical service for large numbers of the human 382
population. Unless the confounding effects of such changes can be 383
controlled statistically, there is little possibility of interpreting available 384
medical records reliably. This situation also makes studies of animal or 385
plant models all the more important, both because of their shorter 386
generation times and the lack of importance of ‘worries’ as a cause of any 387
effects. 388
For example, the Belarussian President, Alexander Lukashenko 389
recently encouraged the resettlement of contaminated zones for agriculture 390
purposes, although for now he is promoting this use primarily for refugees. 391
16
This optimism is based mainly on predictions that < 10000 people are 392
likely to die of Chernobyl-related cancers. Even the best-case scenarios do 393
not include non-cancer mortality or increased morbidity of any sort. 394
Neither is there any assessment of the human costs associated with medical 395
treatment. Given the unprecedented nature of the Chernobyl disaster, it 396
seems prudent to be sensitive to the possible unpredicted impacts given that 397
many human diseases have long latency periods (consider that smoking-398
related illnesses often only appear following 20-30 years of exposure). 399
Finally, even an optimistic prediction of 10000 excess human deaths is not 400
trivial. 401
402
1 Dolk, H. and Nichols, R. (1999) Evaluation of the impact of Chernobyl 403
on the prevalence of congenital anomalies in 16 regions of Europe. 404
Int. J. Epidemiol. 28, 941-948 405
2 Chernobyl Forum (2005) Chernobyl: The True Scale of the Accident. 20 406
Years Later a UN Report Provides Definitive Answers and Ways to 407
Repair Lives, IAEA, WHO, UNDP 408
3 Jacob, P. et al. (1998) Thyroid cancer risk to children calculated. Nature 409
392, 31-32 410
411
Figure 1. Increased frequency of (a) spontaneous abortion (red bars, x 0.1) 412
and congenital malformation (clear bars) before and after the accident in 413
Gomel and Mogilev, Belarus. Values are means (SD). (b) Increased 414
frequency of thyroid cancer in children in relation to radiation in Belarus 415
(circles) and Ukraine (squares). Adapted with permission from [2,3]. 416
417
17
0
5
10
15
20
Before After
Time relative to Chernobyl accident
(a)
418
419
0
2
4
6
8
10
1985 1990 1995 2000 2005
Year
(b)
420
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Box 4. Problems of analyzing effects when there is one event 421
422 The Chernobyl disaster provides an unrivalled opportunity to test 423
effects of radiation on biological phenomena under large-scale field 424
conditions, given that it is not straightforward to extrapolate from the 425
laboratory to the field. However, this also raises philosophical 426
considerations about how to use a single observation to make rigorous tests 427
of scientific hypotheses. We can imagine three different solutions to this 428
problem, of which two have been adopted so far. First, investigations that 429
simultaneously use temporal and spatial patterns of a phenomenon can 430
compare the situation before and after the disaster in contaminated and 431
control areas. Such an approach has been used to study partial albinism and 432
asymmetry in feathers of the barn swallow Hirundo rustica before and after 433
the Chernobyl disaster (Figure 1; [1]). Partial albinism is caused by 434
mutations that are rare among all animals, but the frequency in swallows 435
has increased in the Chernobyl region by five-tenfold since 1986, but not in 436
control areas (Figure 1). Similarly, the degree of asymmetry in the length of 437
outermost tail feathers of barn swallows has increased fivefold in 438
Chernobyl, but not in control areas [1]. 439
Second, whereas a given pattern might arise for random reasons with 440
a sample of two, a pattern that occurs repeatedly is unlikely to arise by 441
chance. This approach was used for studies of bilateral asymmetry (e.g. 442
differences in perfect symmetry between the length of right and left 443
characters such as wings) in plants and animals in radioactively 444
contaminated areas near Chernobyl and in control areas for a total of 15 445
species (four plants, four insects, two fish, one amphibian, one bird and 446
three mammals [2-4]). All revealed higher frequencies of asymmetry in 447
representatives from Chernobyl, deviating significantly from the binomial 448
null expectation [5]. 449
19
Third, the heterogeneous spatial distribution of radiation implies that 450
it is highly unlikely that a similar spatial distribution of phenotype will 451
occur by chance. Thus, an analysis of spatial auto-correlation or a Mantel 452
test is unlikely to provide a significant relationship between radiation and 453
phenotype unless there is an effect of radiation on the phenotypic trait in 454
question, especially if geographic distance is controlled statistically. This 455
approach has yet to be used. 456
457
1 Møller, A.P. (1993) Morphology and sexual selection in the barn swallow 458
Hirundo rustica in Chernobyl, Ukraine. Proc. R. Soc. B 252, 51-57 459
2 Møller, A.P. (1998) Developmental instability of plants and radiation 460
from Chernobyl. Oikos 81, 444-448 461
3 Medvedev, L.N. (1996) Chrysomelidae and radiation. In Chrysomelidae 462
Biology (Jolivet, P.H.A. and Cox, M.L., eds), pp. 403-410, SPB 463
Academic Publishing 464
4 Zakharov, V.M. and Krysanov, E.Y., eds (1996) Consequences of the 465
Chernobyl Catastrophe: Environmental Health, Center for Russian 466
Environmental Policy 467
5 Møller, A.P. (2002) Developmental instability and sexual selection in 468
stag beetles from Chernobyl and a control area. Ethology 108, 193-469
204 470
6 Møller, A.P. and Mousseau, T.A. (2001) Albinism and phenotype of barn 471
swallows Hirundo rustica from Chernobyl. Evolution 55, 2097-2104 472
473
Figure 1. (a) Barn swallows Hirundo rustica with (left) and without (right) 474
partial albinism. (b) Frequency of partial albinism in barn swallows 475
Hirundo rustica in Chernobyl (red bars) and control areas (clear bars) 476
before and after the disaster in 1986. Adapted with permission from [6]. 477
20
478 479
480
0
5
10
15
20
Year
(b)
481 482
483
21
References 484
485
1 Chernobyl Forum (2005) Chernobyl: The True Scale of the Accident. 20 486
Years Later a UN Report Provides Definitive Answers and Ways to 487
Repair Lives, IAEA, WHO, UNDP 488
2 Stephan, V. (2005) Chernobyl: Poverty and stress pose ‘bigger threat’ 489
than radiation. Nature 437, 181. 490
3 Rosenthal, E. (2005) Chernobyl’s dangers called far exaggerated. 491
International Herald Tribune 6 September 2005. 492
4 Kumerova, A.O. et al. (2000) Antioxidant defense and trace element 493
imbalance in patients with postradiation syndrome: first report on 494
phase I studies. Biol. Trace Element Res. 77, 1-12 495
5 Neyfakh, E.A. et al. (1998) Radiation-induced lipoperoxidative stress in 496
children coupled with deficit of essential antioxidants. Biochemistry 497
63, 977-987 498
6 Neyfakh, E.A. et al. (1998) Vitamin E and A deficiencies in children 499
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Ukrainski Biokhim. Zhurnal 70, 132-135 504
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supplementation in children exposed to radiation from the Chernobyl 506
accident. Radiation Env. Biophys. 37, 187-193 507
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swallows from Chernobyl. Proc. R. Soc. B 272, 247-53 509
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foraging efficiency, immunocompetence or detoxification ability? 511
Poultry Avian Biol. Rev. 11, 137-159 512
22
11 Chumak, A. et al. (2001) Monohydroxylated fatty acid content in 513
peripheral blood mononuclear cells and immune status of people at 514
long times after the Chernobyl accident. Radiation Res. 156, 476-487 515
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Figure 1. Distribution of radiation in Europe in May 1986 from the 653
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28
Fig. 1 655
656
657 658
29
659
Table 1. Studies investigating the effects of radiation in Chernobyl on cytogenetics, genetic variability and mutations Species Genetic marker Effect Comments Refs
Chromosome aberrations: Homo sapiens Lymphocytes with chromosomal
aberrations Increased 2–10 times Women of Gomel and Mogilev, Belarus [33]
Lymphocytes with chromosomal aberrations
Increased rate of 10–20 times Clean–up workers [34]
Lymphocytes with chromosomal aberrations
Increased 3–7 times Children of Belarus [34]
Apodemus flavicollis Chromosomal aberrations Increased 3–7 times [34]Mus musculus Number of reciprocal translocations Increase by a factor 15 [35,3Ictalurus punctatus, Carassius carassius, Cyprinus carpio, Tinca tinca
Frequency of aneuploidy Increased aneuploidy in contaminated areas [37]
Dero obtuse, Nais pseudobtusa, Nais pardalis (Oligochaeta)
Chromosomal aberrations About 2 times Natural populations [38]
Pinus sylvestris Chromosomal aberrations Increased by a factor 3 Field populations [39]Somatic mutations: Homo sapiens Minisatellites Increased rate [40] Minisatellites Increased rate [41] Minisatellites No significant increase [42] Minisatellites and microsatellites No significant increase [43] Microsatellites No significant increase [44]Clethrionomys glareolus Mutations No significant increase [45] Substitutions in cytochrome b Multiple substitutions and transversions were
restricted to samples from Chernobyl [46]
Mutations and heteroplasmy Increase by 19% in mutations and by 5% in heteroplasmy, although not significant
[47]
Mus musculus Point mutations No significant increase Transplant experiment with exposure during 90 days
[48–5
Mitochondrial cytochrome b heteroplasmy No significant increase Short-term transplant experiment [51]Ictalurus punctatus Breakage in DNA Increased rate of breakage [52]Carassius carassius DNA content based on flow cytometry Changes in DNA content, but unrelated to
known measures of contamination [53]
Drosophila melanogaster Sex-linked recessive lethal mutations Increase [54]Triticum sativum Micro–satellites Increase rate by a factor 10 The only transplant experiment [55]Arabidopsis thaliana Lethal mutations Increase by a factor 2–4 Greenhouse and natural populations [56] Lethal mutations Rate 4–8 times higher than in controls in 1992 [57]Pinus sylvestris Mutation rate at enzyme loci Increase by a factor 20 Field populations [56] Protein-coding genes Increased by 4–17 times Field populations [56]Germline mutations: Homo sapiens Minisatellites Increased rate [18] RAPDs Increased rate of germline mutations [20,5 Minisatellites Increased rate by a factor 1.6 in men, but not
in women [21]
Hirundo rustica Microsatellites Increase rate by a factor 2–10 Only two of three microsatellites showed an increase
[19]
Other effects: Mus musculus Lethality, embryo mortality and sterility Increase Mating with laboratory animals [59]Triticum sativum, Secale cereale
Aberrant cells Increase in a dose-dependent manner [60]
Pinus sylvestris Hypermethylation of genomic DNA Dramatic increases; probably stress response Experimental populations [61]
660 661