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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. (amoller@snv.jussieu.fr) 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

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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

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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

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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

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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

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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

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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

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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

correlate with Chernobyl radiation loads of their mothers. 500

Biochemistry 63, 1138-1143 501

7 Ivaniota, L. et al. (1998) [Free radical oxidation of lipids and antioxidant 502

system of blood in infertile women in a radioactive environment]. 503

Ukrainski Biokhim. Zhurnal 70, 132-135 504

8 Ben-Amotz, A. et al. (1998) Effect of natural beta-carotene 505

supplementation in children exposed to radiation from the Chernobyl 506

accident. Radiation Env. Biophys. 37, 187-193 507

9 Møller, A.P. et al. (2005) Antioxidants, radiation and mutation in barn 508

swallows from Chernobyl. Proc. R. Soc. B 272, 247-53 509

10 Møller, A.P. et al. (2000) Carotenoid-dependent signals: indicators of 510

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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27

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