Biol. Lett.
doi:10.1098/rsbl.2007.0136
Published online

Evolutionary biology

Elevated frequency
of abnormalities in barnswallows from Chernobyl
A. P. Møller1,*, T. A. Mousseau2, F. de Lope3
and N. Saino4
1
Laboratoire de Parasitologie Evolutive, CNRS UMR 7103,Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai StreetBernard, Case 237, 75252 Paris Cedex 05, France2
Department of Biological Sciences, University of South Carolina,
Columbia, SC 29208, USA
3
Departamento de Biologı́a Animal, Facultad de Ciencias,
Universidad de Extremadura, Avda. Elvas s/n, 06071 Badajoz, Spain
4Dipartimento di Biologia, Sez. Zoologia Scienze Naturali,Università degli Studi di Milano, via Celoria 26, 20133 Milano, Italy*Author for correspondence (amoller@snv.jussieu.fr).

Ever since the Chernobyl accident in 1986, that
contaminated vast areas in surrounding
countries with radiation, abnormalities and birthdefects have been reported in human populations. Recently, several studies suggested thatthe elevated frequency of such abnormalities canbe attributed to poverty and stress in affected
human populations. Here, we present long-term
results for a free-living population of barn swallows, Hirundo rustica, demonstrating thepresence of 11 morphological abnormalities in
populations around Chernobyl, but much lessfrequently in an uncontaminated Ukrainian control population and three more distant control
populations. The presence of these abnormalities
in barn swallows is associated with reduced
viability. These findings demonstrate a link
between morphological abnormalities and radiation in an animal population that cannot be
attributed to poverty and stress. The most parsimonious hypothesis for abnormalities in animaland human populations alike is that the effects
are caused by the same underlying cause, viz.
radiation derived from the Chernobyl accident.
Keywords: Hirundo rustica; mutation; radiation;
viability

1. INTRODUCTION
Free-living organisms with morphological abnormalities have a frequency of less than 1% (Campbell &Lack 1985), because natural selection removes individuals with aberrant phenotypes. Hence, we should
expect low frequencies of such aberrations in naturalpopulations, even when environmental perturbations
increase the frequency of abnormalities or birthdefects. Human populations exposed to radiationfrom the Chernobyl nuclear power plant haveelevated frequencies of abnormalities and birthdefects ( Feshchenko et al. 2002; UNDP/UNICEP
2002; Lazjuk et al. 2003; Scherb & Weigelt 2003;
Chernobyl Forum 2005a,b). However, recent studies
raised the possibility that such abnormalities may
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2007.0136 or via http://www.journals.royalsoc.ac.uk.
Received 8 March 2007
Accepted 27 March 2007

arise from deteriorating living conditions in generaland not necessarily be due to radiation (ChernobylForum 2005a,b). In addition, worries about theeffects of exposure to radiation among humans havebeen suggested to result in elevated levels of stressthat potentially could cause an increase in thefrequency of birth defects (Chernobyl Forum 2005b;
Rosenthal 2005; Stephan 2005). In contrast, estimates of such abnormalities in animal populations
exposed to radiation from Chernobyl cannot be said
to suffer from these problems, and similarities inpatterns of abnormalities in animal and humanpopulations thus comprise a test of the effect ofstressful conditions on abnormalities. Therefore,studies of abnormal phenotypes among animals canbe used as a way to test for effects of radiation on thefrequency of abnormalities.
Here, we present results from long-term studies ofbarn swallows in Chernobyl and control areas in
Ukraine and in three other populations in Europe.
With over 7700 individuals examined for external
abnormalities, this provides the most extensive dataset on abnormalities in animals ever recorded.
2. MATERIAL AND METHODS
We captured adult barn swallows in a contaminated area (Chernobyl(518240 N, 30807 0 E), open farmland within the exclusion zone orwithin a distance of 1 km from the border of the zone) and a control
area (Kanev (49806 0 N, 33833 0 E), open farmland habitat similar tobut approx. 220 km southeast of the Chernobyl area) in Ukraine
during 1991, 1996, 2000 and 2002–2006. Additional control areas
include Spain 2002–2006, Italy 2001–2006 and Denmark 1984–2006 (see Møller et al. (2005a, 2006a) for details about procedures).
Upon capture, all individuals from Ukraine and Denmark wereexamined by APM, from Spain by FdL and Italy by NS, for thepresence of deviations from normal phenotype by careful examination while recording 20 morphological measurements and threemeasures of abundance of parasites on each individual (Mølleret al. 2006a). The total procedure lasted 5–6 min per bird, andprocedures were similar in all study sites because APM had
instructed FdL and NS. Similarity in procedure was reflected by ahigh degree of repeatability of measurements among measurers( Møller et al. 2006a). Furthermore, APM found a similarfrequency of partial albinos in Denmark during 1989–1990 and1991–1992 (c21Z0.04, pZ0.84), suggesting a similar search effort
for albinistic individuals before and after initiation of the study in
Chernobyl. Nestlings were inspected for abnormalities during
1996, 2000 and 2002–2006, restricted to individuals that were atleast 10 days old to allow a check of the plumage for the presenceof deviating coloration.
We identified the following 11 abnormalities that deviate from
common morphology, based on our extensive experience fromhandling more than 20 000 barn swallows (figure 1): (i) Partial
albinism refers to the presence of single or a few white feathers in theotherwise reddish brown or dark blue plumage (data for 1991, 1996and 2000 previously reported by Møller & Mousseau 2001). This
trait is maintained across moult in adults (Møller & Mousseau2001). (ii) Aberrant coloration of plumage refers to a mottled
plumage of the head (Møller & Mousseau 2001). (iii) Red colorationof chest refers to the presence of reddish brown coloration below theblue breast stripe. (iv) Blue coloration in the red face refers toblue spots in the normally reddish brown coloration of the head. (v)Deformed toes refer to crippled or malformed toes. (vi) Deformed
beak refers to beaks that cannot be closed due to bent edges ormalformed beaks. (vii) Tail feathers with non-fused barbs refer totips of the outermost tail feathers with brushy appearance due to theabsence of functional barbs. (viii) Bent tail feathers refer to lyreshaped outermost tail feathers. (ix) Tumours were externally clearlyvisible lumps of hard tissue (with a diameter of more than 1 cm) on
the outside of the body. (x) Deformed air sacks were observed in afemale barn swallow with a completely swollen breast. (xi) Deformedeyes were partly covered by swollen or irregularly shaped eyelids. No
individual had more than one abnormality.
We tested for deviations from a random distribution of abnormalities, using log-likelihood ratio tests (SAS 2000). Likewise, weused log-likelihood ratio tests to compare the frequency ofabnormalities in nestlings and adults, and the number of survivors
This journal is q 2007 The Royal Society2A. P. Møller et al.

Chernobyl abnormalities(b)(c)

(d )

(e)

(a)

(f)

(i)

(h)

(g)

Figure 1. Photographs of abnormalities in barn swallows. (a) Normal phenotype. (b –d ) Partially albinistic plumage. (e) and( f ) Deformed beak. ( g) Deformed air sacks. (h) and (i ) Bent tail feathers.
among individuals with and without abnormalities. We used logistic
regression to test for temporal trends in abnormalities (SAS 2000).

3. RESULTS
The 11 different categories of external malformations
in barn swallows from Chernobyl ranged in frequency from 0.09% malformed air sacks to 13.69%
partially albinistic plumage (table 1 in the electronic
supplementary material). Only partial albinism,
deformed toes and tumours were also found incontrol populations, albeit at a much lower frequency than in Chernobyl. If abnormalities wererandomly distributed among contaminated and control populations, we should expect the number ofabnormal individuals to reflect the number of individuals examined in each population. However, there
were many more conditions recorded in Chernobyl
than in the four control areas despite the opposite
being expected, suggesting that abnormalities werenon-randomly distributed among populations. Likewise, the frequency of individuals with abnormalities
was much greater in Chernobyl than expected bychance (log-likelihood ratio test, c21Z156.86, p!
0.0001), and that was the case for the frequency ofboth partial albinism (c21Z78.58, p!0.0001) andother abnormalities (c21Z140.39, p!0.0001).
Biol. Lett.

If deteriorating conditions in Ukrainian agriculture
were the cause of an elevated frequency of abnormalities in humans and animals alike, we would expectan increase in the frequency after 1990 associatedwith the breakdown of collective farming. However,the frequency of abnormalities among adult barnswallows from Chernobyl decreased significantly from1991 to 2006 both for partial albinism and otherabnormalities (figure 2; partial albinism: c21Z5.45,pZ0.020; other abnormalities: c21Z5.62, pZ0.018).
We should expect survival prospects of individuals
with and without abnormalities in Chernobyl to be
similar, if abnormalities were benign. We foundevidence of natural selection against abnormalities inboth nestlings and adults. First, a total of 33.5% of
248 nestlings from Chernobyl had abnormalities,
while only 17.8% of 841 adults had any abnormalities(c21Z24.65, p!0.0001). Second, survival prospects
for adults with and without abnormalities were estimated based on recaptures in subsequent years in thesame sites. With capture probabilities above 90% andsite philopatry of more than 99.9% (NO10 000 adultsfrom Ukraine, Spain, Italy and Denmark; Møller et al.
2006a), we determined whether the probability ofrecapture in a subsequent year differed between
individuals with and without abnormalities captured

Chernobyl abnormalities

A. P. Møller et al.

3Figure 2. Frequency of partial albinism and other abnormalities in barn swallows in Chernobyl during 1991–2006.

dispersal into the Chernobyl area than the control
area (Møller et al. 2006b).
We can think of no alternative explanations otherthan exposure to radiation that can have caused theobserved patterns. There has been a general deterioration of farming in Ukraine since 1990. This shouldhave negative effects in both control and contaminatedareas, predicting increases in the frequency of abnormalities. We demonstrated a significant decrease, asexpected from decreased levels of radiation during
1991–2006 due to natural decay of isotopes. Estimatesof the frequency of abnormalities in birds could
potentially have been overestimated if individuals withabnormalities are more likely to be caught. However,
we can exclude the possibility of biased sampling
because capture probability has been consistently highboth in Ukraine and the non-Ukrainian control populations (Møller et al. 2005a, 2006a).

during 2002–2005. The survival probability of 48
birds with abnormalities from Chernobyl was estimated from recaptures. While the survival probabilityof 368 non-albino adults from Chernobyl was 0.279(Møller et al. 2005a), the survival probability of birds
with abnormalities was 0.063 (c21Z13.42, pZ0.0002).

We gratefully acknowledge the help from I. Chizhevsky,G. Milinevski, A. Peklo, G. Rudolfsen and S. Rushkovsky,
and the support from the National Geographic Society, theUS National Science Foundation, the University of South
Carolina Environmental Research Initiative Committee(ERIC), the University of South Carolina School of theEnvironment and the Samuel Freeman Charitable Trust.

4. DISCUSSION
This study showed an elevated diversity and frequency of abnormalities in barn swallows from
Chernobyl compared with control populations in
Ukraine and elsewhere. Furthermore, we found lower
survival prospects for both nestlings and adults withabnormalities than for the average individual. Thus,
the presence of abnormalities is associated with severe
fitness costs. This is the first study showing that
abnormalities in free-living animals are elevated incontaminated areas just as documented for humans(Feshchenko et al. 2002; Lazjuk et al. 2003; Scherb &Weigelt 2003). The cause of these effects is likely to
be a combination of mutation rates having increased
by up to more than a factor of 10 (Ellegren et al.
1997; Møller & Mousseau 2006) and elevated teratogenic effects of radioactive isotopes in the environment, possibly caused by depletion of antioxidants byradiation (Møller et al. 2005b; Møller & Mousseau2006). We can exclude that the effects arose from
non-radioactive pollution because all study areas wererural without any exposure to industrial pollution.
Radiation levels in the study areas in Chernobyl
were one to two orders of magnitude above thebackground level (data reported in Møller et al.
2005a). Birds from Chernobyl are likely to have
hatched at farms with elevated radiation levels,
because mean natal dispersal distance is only 3 km
per generation (Møller & Mousseau 2001). Likewise,
birds from the Ukrainian control region are unlikely
to have originated from the same areas as birds fromthe Chernobyl region, because the distance separatingthese two regions is 220 km, or more than 70 times
the annual natal dispersal distance. If anything, theestimates of effects reported here are likely to beconservative, because there is more long distance

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