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Mutation Research 757 (2013) 52–59

Contents lists available at ScienceDirect

Mutation Research/Genetic Toxicology andEnvironmental Mutagenesis
journal homepage: www.elsevier.com/locate/gentox
Community address: www.elsevier.com/locate/mutresHigh frequency of albinism and tumours in free-living birds around
Chernobyl
A.P. Møller a,∗ , A. Bonisoli-Alquati b , T.A. Mousseau babLaboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, France
Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USAa r t i c l e

i n f oArticle history:
Received 10 September 2012
Received in revised form
22 December 2012
Accepted 15 April 2013
Available online 12 July 2013
Keywords:
Albinism
Chernobyl
Population decline
Radiation
Tumoursa b s t r a c t
The effects of radioactive contamination on the phenotype of free-living organisms are poorly understood,
mainly because of the difﬁculty of capturing the large numbers of individual specimens that are required
to quantify rare events such as albinism and tumour formation. We hypothesized that the frequency ofabnormalities like albinism and the frequency of radiation-induced diseases like cancer would increase
with the level of background radiation, that the two markers of radiation would be positively correlated,
and that the reduction in abundance of animals would be greater in species with a higher frequencyof albinism and tumour formation, if these markers reliably reﬂected poor viability. Here we analyzed
the frequency of albinistic feathers and tumours in a sample of 1669 birds captured during 2010–2012
at eight sites around Chernobyl that varied in level of background radiation from 0.02 to more than
200 ␮Sv/h. We recorded 111 cases of partial albinism and 25 cases of tumour formation. Nominal logistic
models were used to partition the variance into components due to species and background radiation.
Radiation was a strong predictor of the two markers in birds, with a small, but signiﬁcant effect of species
for albinism. The slope of the relationship between abundance and radiation in different bird species
was signiﬁcantly inversely correlated with the frequency of albinism and tumours, as was to be expected
if a common underlying cause (i.e. radiation) affects both variables. These ﬁndings are consistent withthe hypothesis that background radiation is a cause of albinism and tumours, that albinism and tumours
are biomarkers of radiation exposure, and that high frequencies of albinism and tumours were present
despite the low viability of birds with these conditions.
© 2013 Elsevier B.V. All rights reserved.

1. Introduction
Radioactive contamination is known to increase mutation rates
with signiﬁcant effects on phenotype [1,2]. A recent review suggests that natural populations may be almost an order of magnitude
more sensitive to ionizing radiation than previously predicted bylaboratory models [3], implying that natural variation in background radiation [4], but also low-dose radioactive contaminationfrom Chernobyl and other nuclear accidents may cause signiﬁcantchanges in the appearance of animals and other organisms [2].
Abnormalities are disproportionately frequent in radioactively contaminated areas [2,5–10]. For example, for barn swallows Hirundo
rustica from Chernobyl, Møller [7] reported abnormal barbs infeathers, which prevented these feathers from fusing normally. This
novel condition was associated with a signiﬁcant delay in reproduction, suggesting that the condition had signiﬁcant ﬁtness costs.
Likewise Hesse-Honegger and Walliman [10] observed elevated∗ Corresponding author. Tel.: +33 1 69 15 56 88; fax: +33 1 69 15 56 96.
E-mail address: anders.moller@u-psud.fr (A.P. Møller).
1383-5718/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.mrgentox.2013.04.019

levels of abnormalities in bugs from contaminated areas, including
the vicinity nuclear power plants. We have documented this abnormality in several bird species in 2012, more than 25 years after the
Chernobyl disaster. Furthermore, Møller et al. [8] reported elevatedfrequencies of ten different kinds of abnormalities in barn swallows
from Chernobyl compared with frequencies in four local and moredistant control populations. These abnormalities included changes
in patterns of colouration, morphology and shape of feathers, andmalformed or missing digits, beaks and eyes. Such abnormalities
were rare or completely absent in control populations despite verylarge sample sizes, nor have they been described in the extensive
literature on this species anywhere throughout its range [8,9].
Albinism, the result of absence of melanin pigments from tissue, occurs with a frequency that is typically extremely low infree-living organisms (e.g., [11,12]). In particular small and inbred
populations show an increased frequency of albinism in accordancewith the expectation that albinism is caused by a recessive allele[13–17]. Barn swallows from around Chernobyl show a highly elevated frequency of partial albinism reaching 13–15%. This albinism
is of germ-line origin as determined from a signiﬁcant parentoffspring resemblance, and barn swallows with this condition

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Fig. 1. Location of the eight study sites in relation to background radiation level (Cu/km2 ) around Chernobyl, Ukraine.

suffer from reduced survival prospects [18]. This was also foundin another study of birds [19]. A disproportionate fraction of partial
albinism in the barn swallow occurs in the facial red plumage, but
hardly any is seen in the dark blue plumage of the neck, back, wings
and tail [20,21]. Individual barn swallows with partially albinistic
plumage had on average lower mean phenotypic values than otherindividuals [21], as also reported for the hooded crow, another bird
species [19].
A fraction of invasive cancers in humans is caused by radiation
exposure, which includes non-ionizing radiation and in particular
ionizing radiation (e.g., [22,23]). Natural variation in backgroundradiation due to radon and other radioactive elements has a signiﬁcant impact on the incidence of cancer in humans [4,24]. The
incidence of all cancers caused by ionizing radiation increases witheffective dose [25]. Many kinds of cancer often take a long time todevelop (i.e. they have a long latency period), implying that longterm effects on cancer incidence from radioactive contaminationfrom Chernobyl are not yet detectable. Serdiuk et al. [26] and Cardis
and Hatch [27] reviewed the extensive evidence for other cancers being linked to radiation due to the Chernobyl catastrophe.
However, next to no information exists on cancers in free-living
vertebrates, although their short generation time would provide
insights into long-term effects that cannot yet be studied in humans(Fig. 1).

The objectives of this study were to determine (1) the relationship between the incidence of albinism and tumours, respectively,
and background radiation, using a large database of free-living birds
captured around Chernobyl during 2010–2012. In other words,
we intended to assess the reliability of the rate of albinism andthe incidence of tumours as biomarkers of species decline due toradiation exposure. Because the lifespan of most free-living animals with abnormalities is short [8,18,21] due to elevated risk of
predation, ﬁeld estimates of prevalence of abnormalities are by definition conservative. If mortality related to abnormalities tumours
were a major cause of disappearance of individual animals fromfree-living populations, we should expect that a smaller number ofindividuals remained in contaminated areas in species with a highfrequency of abnormalities. Therefore, the second objective of thisstudy was (2) to investigate the relationship between the slope ofthe relationship between abundance and background radiation fordifferent species of birds and the relative frequency of albinism andtumours.
2. Materials and methods
2.1. Study areas
We captured birds in mist nets at eight sites around Chernobyl in the period
25 May–5 June during the years 2010–2012 [28,29]. We used a total of 35–45 mist

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nets each 12 m long during two consecutive days at each of the study sites (i.e. one
evening and one morning capture session). All birds were marked with a numberedaluminium band for individual identiﬁcation, and they were subsequently sexed andaged according to standard criteria [30], measured, sampled for blood and released
after sperm collection. As a control sample from uncontaminated areas in Europe,
the ﬁrst author (APM) captured 35,578 birds in mist nets near Brønderslev, Denmark,during 1969–2012.

2.2. Frequency of albinism and tumours in birds
Upon capture all individual birds were examined by APM for the presence of
deviations from the normal phenotype by careful examination, while recording
twenty morphological measurements and three measures of abundance of parasites on each individual [31]. The overall procedure lasted 5–6 min per bird and was
similar at all study sites.
Partial albinism refers to the presence of single or a few white feathers in theotherwise reddish brown or dark blue plumage [21]. This trait is maintained acrossmoults in adults [21].
Tumours were recorded as externally clearly visible lumps of hard tissue (with adiameter of more than 0.5 cm) on the outside of the body. These structures included
papillomas on the legs as shown in Fig. 2.
APM likewise recorded cases of albinism and tumours in the sample of birds
from Denmark with exactly the same procedures. We provide summary statistics
for the frequency of abnormalities and tumours in each species, and the slopes of
the relationships between abundance and background radiation for each species isgiven in Electronic Supplementary Material Table S1.
Supplementary data associated with this article can be found, in the online
version, at http://dx.doi.org/10.1016/j.mrgentox.2013.04.019.

2.3. Breeding bird censuses
The point-count census method provides reliable information on relative abundance of birds [32–35]. It consists of counts over a 5-min period during which thenumber of birds seen or heard is recorded. APM conducted these standard pointcounts during May–June in the years 2006–2009 in the Chernobyl area. The fact thatone person made all counts eliminates any variance in results due to inter-observer
variability. The counts were made approximately on the same dates and at the sametime of the day during each of the four years. Møller and Mousseau [34] provide further information on the methods and potentially confounding variables that weretaken into account in the analyses. We have previously tested the reliability of ourcounts by having two persons independently perform the counts, and the degree ofconsistency was high, both for species richness and abundance (details are reported
by Møller and Mousseau [34]).

2.4. Background radiation
We measured radiation in the ﬁeld and cross-validated these measurementswith those reported by the Ukrainian Ministry of Emergencies. Once having ﬁnishedthe 5-min point-count we measured radiation levels with a hand-held dosimeter(Model: Inspector, SE International, Inc., Summertown, TN, USA), directly in theﬁeld at ground level at each point where we censused birds. We measured the radiation 2–3 times at each site and averaged the measurements. We cross-validated
our measurements against governmental measurements published by Shestopalov[36], estimated as the mid-point of the ranges published. This analysis revealed avery strong positive relationship (linear regression on log-log transformed data:
F = 1546.49, d.f. = 1,252, r2 = 0.86, P < 0.0001, slope (SE) = 1.28 (0.10)), suggesting that
our ﬁeld estimates of radiation provided reliable measurements of levels of radiation
among sites.
Handheld Geiger-counters are likely to provide reliable measures of backgroundcontamination levels of radionuclides for gamma sources, and to a lesser degree forbeta emitters when the Geiger detector is in close proximity to the source. However,characterization of alpha emitters usually requires more complex methods that areusually only tractable in a laboratory setting due to the short transmission distanceof alpha particles in air.
Given the different characteristics of radionuclides in the environment around
Chernobyl, ﬁeld measurements of contaminant levels are likely to underestimate
biologically relevant radiation levels when the main exposure pathway is via
ingestion. Similarly, measurements of background radiation in the areas around
Chernobyl closest to the reactor (e.g., the Red Forest) very likely underestimate
biologically relevant doses, given the abundance of alpha-emitting actinides (e.g.,
plutonium isotopes) that were differentially deposited in this area. That said,
Gashchak et al. [37] previously reported that the internal dose of small birds
captured in Chernobyl is strongly positively correlated with the external dose,
accounting for more than 50% of the variance in internal dose. This would suggestthat measurements of the gamma radiation are a reasonable proxy for total exposure, at least for the type of comparative analysis reported here, and that results will
be conservative with respect to any reported association with radiation levels.

2.5. Statistical analyses
Using Generalized Linear Models, we previously estimated the slope of therelationship between abundance and background radiation with log10 -transformed
abundance for each species at each observation point and log10 -transformed radiation level for each species [38]. We used nominal logistic regression to relate
the incidence of albinism and tumours to background radiation level after inclusion of species as a factor. These two models showed no signiﬁcant lack of ﬁt. We
subsequently related the slope of the relationship between abundance and background radiation to the squareroot-arcsine-transformed prevalence of albinism andtumours in different species of birds, weighing each species estimate by sample size.
Models were weighed by sample size (the number of individuals) to account for
the fact that sample sizes differed and hence the precision of the estimate differedamong species. Most statistical analyses assume that data points provide equally
precise information about the deterministic part of total process variation, i.e. thestandard deviation of the error term is constant over all values of the predictor variable [39]. Garamszegi and Møller [40] showed that bias due to variation in sample
size is a serious problem in comparative analyses, similar to considering species asstatistically independent observation. If this assumption of even sampling effort isviolated, weighing each observation by sampling effort allows the use of all data,
giving each data point a weight that reﬂects its degree of precision due to the sampling effort [40–42]. This procedure will also allow both rare and common species tobe included and hence avoid any bias in sampling due to rarity. All analyses weremade with JMP version 10.0 [43].

3. Results
We recorded in total 111 cases of albinism and 25 cases oftumours in 1669 birds captured in the surroundings of Chernobyl,
or 66.5 cases of albinism and 15.0 cases of tumours per 1000
birds. This compared with rates of 8.9 cases of albinism and nocases of tumours per 1000 birds in Denmark (N = 35,578 individual
birds). The mean relative frequency of albinism across all species
in Chernobyl was 0.066 (SE = 0.008), N = 63 species, while mean
relative frequency of albinism was 0.102 (SE = 0.014) when only
considering the 13 species with at least one case of albinism. Likewise, the relative frequency of tumours was 0.015 (SE = 0.003) forall species, but 0.025 (0.008) in the 10 species with at least one
case. A Kendall rank-order correlation analysis showed a weak, but
signiﬁcant positive correlation between the presence of albinism
and tumours in the 1669 individual birds from Chernobyl (Kendall
 = 0.086, P = 0.0005). There was also a signiﬁcant, positive relationship between prevalence of albinism and prevalence of tumours
across species of birds in an analysis with species as observations
weighed by sample size (F = 34.42, d.f. = 1.61, r2 = 0.36, P < 0.0001,
slope (SE) = 1.153 (0.197)).
Therefore, we proceeded by investigating the relationshipbetween each of the two kinds of abnormality and backgroundradiation, while taking the non-independence of individuals among
species into account by including species as a factor. There was asigniﬁcant positive effect of radiation on the occurrence of bothalbinism and tumours (Fig. 2(A and B) and Table 1). In addition,
there was a signiﬁcant species effect in the analysis of albinism(Table 1). Odds ratios and their 95% conﬁdence intervals arereported in Table 1. Unit odds ratios per unit change in radiation
were 0.738 (95% CI 0.624, 0.867) for partial albinism and 0.486 (95%
CI 0.310, 0.713) for tumours.
If background radiation were the underlying cause of theincrease in abnormalities and the reduction in abundance, weshould expect a negative relationship between the slope describing
the intra-speciﬁc relationship between abundance and radiationand the relative frequency of the two kinds of abnormality (i.e.
the species most affected by radiation are also more prone toabnormality and cancer). The mean slope for the 63 species was-0.062 (0.010), differing signiﬁcantly from zero (one-sample ttest, t = −6.21, d.f. = 62, P < 0.0001). Indeed, the slopes for different
species were negatively related to relative frequency of albinism
in a model weighed by sample size (Fig. 3A; F = 11.13, d.f. = 1.61,
r2 = 0.15, P = 0.0015, slope (SE) = −0.124 (0.037)). Likewise, slopes
for different species were negatively related to relative frequency

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Fig. 2. Birds with albinistic feathers and tumours from around Chernobyl as indicated by the arrows. (a) barn swallow Hirundo rustica with a normal plumage and no tumours;(b) barn swallow with albinistic feathers, (c)–(h) are different species of birds with albinistic feathers, while (i)–(x) are different species of birds with solid tumours clearlyvisible from the outside.

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Table 1
Nominal logistic regression models of albinism and tumours in relation to background radiation and species. R2 was 0.20 and 0.06 for the two models. Odds ratios and their
95% conﬁdence interval are also shown.
Variable

Chi-square

d.f.

P

Estimate (SE)Odds ratio

95% CI for odds ratio

Albinism
SpeciesRadiation

146.9733.82

61
1<0.0001<0.0001

0.660 (0.120)

0.309

0.162, 0.577

Tumours
Radiation

15.06

1

0.00010.722 (0.210)

0.061

0.011, 0.271

of tumours in a model weighed by sample size (Fig. 3B; F = 10.92,
d.f. = 1.61, r2 = 0.15, P = 0.0016, slope (SE) = −0.923 (0.279)). Exclusion of the single species with an extremely high estimate of
frequency of tumours (hoopoe Upupa epops) did not change
the conclusion (F = 14.75, d.f. = 1.60, r2 = 0.20, P = 0.0003, slope(SE) = −0.274 (0.071)).

4. Discussion
The main ﬁndings of this study of albinism and tumours in freeliving birds in the Chernobyl region were that (1) albinism andtumours were more common than previously reported, (2) the frequency differed among species, (3) the frequency increased with

Fig. 3. Occurrence of (A) albinism and (B) tumours in individual birds in relation to background radiation level (␮Sv/h). The individual observations are shown with regression
lines and 95% conﬁdence intervals.

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the level of background radiation, and (4) species with the most
severely depressed populations in contaminated areas were also
the species that had the highest frequency of albinism and tumours.
These ﬁndings have important implications for estimation of thefrequency of abnormalities, but also for their consequences at the
population level.
Albinism is a rare condition in free-living animals [14], the highest frequencies being reported for island or marginal populations[16,17]. Because it is likely that albinism has a recessive genetic
basis, we should expect to ﬁnd more cases in populations with signiﬁcant inbreeding. Here we have shown that the high frequency
of ca. 15% albinism previously reported in populations of barnswallows around Chernobyl [21] can be generalized to other bird
species. The mean frequency was 6.6% of all individuals across all
species of birds, in comparison with a frequency of 0.9% in birds
from uncontaminated areas in Denmark. For the barn swallow wehave previously shown, by use of historical records, that the prevalence of partial albinism was lower before the Chernobyl accident[21]. Several studies have suggested that albinism is associatedwith signiﬁcantly reduced viability [18,19,21]. Therefore, albinism
is likely to be under-represented in our study because albinistic
animals are more prone to mortality before being captured thanbirds with normal plumage. We have also shown that the prevalence of albinism in different bird species is a signiﬁcant predictorof the impact of background radiation on population size in the surroundings of Chernobyl. Møller et al. [29] reported for contaminedareas around Chernobyl severely reduced survival rates of the same
bird species that we have studied here (Fig. 4).
Ionizing radiation is a signiﬁcant cause of cancer in humans(see, e.g., [22,23,27]), and even natural variation in backgroundradiation due to radon and other isotopes has a signiﬁcant impact
on the incidence of human cancer [4,24]. Cancer often takes longtime to develop, implying that long-term radiation effects of Chernobyl in terms of cancer may not yet be detectable. An exception
is thyroid cancer, because it appeared early after the Chernobyl
accident in 1986 due to exposure to radioactive iodine that was
released in large amounts, but only has a short half-life of lessthan ten days [27]. There is almost no information available onradiation-induced cancers in free-living organisms, although theirshort generation time would provide insights into long-term effects
that are not yet detectable for humans. Tumours need less time
to reach a detectable or a lethal size in smaller organisms [44].
Here we have shown a frequency of 1.5% of birds having tumoursin the neighbourhood of Chernobyl, while not one single tumourcase was recorded in a much larger sample of birds captured in
uncontaminated areas in Denmark. Thus the frequency of tumoursin birds is elevated in Chernobyl. The true frequency in the population will depend on the viability cost of the tumours. If we assume
that tumours result in premature death in wild birds, then the true
prevalence must be signiﬁcantly higher than the 1.5% recorded inour study. We can also expect that the relationship between theslope of the relation between abundance and radiation in different species of birds and the prevalence of tumours constitutes anunder-estimate of the true relationship due to differential mortality of individual birds with tumours. Finally, we have shown thatthe frequency of albinism and the frequency of tumours were positively correlated across individual animals but also across species.
Again, this is what would be expected if the two conditions have acommon underlying cause.
There was evidence of an increase in the frequency of albinism
and tumours with increasing background radiation in birds. We
have previously reported that the prevalence of albinism in thebarn swallow increases with the level of background radiation,and that uncontaminated control populations of birds in Ukraine
and elsewhere in Europe have low frequencies of albinism [7,8,18].
The frequency of tumours increased with the level of background57

Fig. 4. Slope of the relationship between abundance and radiation (␮Sv/h) and frequency of (A) albinism and (B) tumours in different species of birds. The estimatesfor different species are shown with circles proportional to the sample size.

radiation, accounting for a small, but signiﬁcant amount of variance. Small birds typically have a generation time of two years or
less, implying that the 26 years since the Chernobyl disaster equals
13 generations or more. In contrast, this period only equals a single generation in humans. The high frequencies of albinism andtumours reported here for birds may be attributed to accumulationof mutations over time, high metabolic rates resulting in high rates
of ingestion of radionuclides, genomic instability or a combinationof these factors. Mutations may accumulate across generations withconsequences for the development of diseases, including cancer[26,45]. Likewise, genomic instability caused by radiation can render genomes unstable across generations with accumulating effects[45–47]. Either way, the ﬁndings reported in this study suggest thatthe accumulation of effects of radiation recorded in birds is signiﬁcant, and they suggest that similar accumulation across generations
may cause an increase in the frequency of tumours and other medical conditions in other classes of animals including humans.
Ellegren et al. [18] reported that the survival prospects of barnswallows with albinism were severely reduced compared withthose of birds with normal plumage. If it turned out that the probability of survival is linked to albinism in birds in general, thenwe may consider the ﬁeld estimates of albinism to be conservative. Greater risk of mortality in albinistic birds should translate
into an under-estimation of the prevalence of albinism. It should
also imply that the reduction in abundance of birds at high levels of background radiation should be greater in species with ahigher prevalence of albinism (and tumours). Indeed, slopes of theAuthor's personal copy
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relationship between abundance and level of background radiation
were signiﬁcantly negative, as previously reported for birds breeding around Chernobyl [34,38]. Interestingly, the slopes for different
species were inversely related to the relative frequency of albinism
and tumours. These relationships must be considered conservative due to the disappearance of individual birds with albinism andtumours.
Biological indicators of radioactive contamination under ﬁeld
conditions include the abundance of many different taxa of animals[48], the frequency of albinism [5,8,21] and other abnormalities[8,49], the amount of genetic damage [50], the frequency of abnormal sperm [51], impaired sperm movement [52] and reduced
reproductive variables and survival rate of birds [53]. It is important to cross-validate such indicators as a test of their reliability, as
already provided for censuses of different animal taxa [48]. Here wehave shown that the occurrence of albinism and tumours in birds
are weakly positively correlated among individuals, but also among
species. In addition, we have shown that the frequency of albinism
and tumours in different bird species is inversely correlated withthe reduction in abundance of different species of birds at high levels of radiation. These ﬁndings provide important cross-validation
for different indicators of radioactive contamination. Future studies
will investigate whether particular ecological and life-history traits
predict variation across species in frequency of tumours underconditions of radioactive contamination, similarly to what has previously been done for data on population trends of different bird
species [34]. For example, rapid growth rate and large body size canpositively predict cancer incidence, and selection of the capacity toﬁght cancer – also called cancer selection – may well vary with thelife history of different animal species [44].
In conclusion, we have shown that albinism and tumour formation are frequent in many bird species in the surroundings ofChernobyl; that the frequency increases with background radiation level; and that species showing the most severe decrease inabundance are also the species with higher frequency of albinism
and tumours. These estimates exceed the frequencies reported forhumans and suggest that albinism and tumours may accumulate
in frequency over time.
Conﬂict of interest statement
The authors declare that there is no conﬂict of interest.
Acknowledgements
We gratefully acknowledge logistic support and help in Ukraine
by I. Chizhevsky and G. Milinevski. We gratefully acknowledge support from the US National Science Foundation, the University ofSouth Carolina, the NATO CLG Program, the CRDF, the Fullbright
Program, the National Geographic Society, and the Samuel Freeman
Charitable Trust for research in Chernobyl.
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