Journal of Animal
Ecology 2005
74, 1102– 1111

Condition, reproduction and survival of barn swallows from
Chernobyl

Blackwell Publishing, Ltd.

A. P. MØLLER, T. A. MOUSSEAU*, G. MILINEVSKY†, A. PEKLO‡,
E. PYSANETS‡ and T. SZÉP§Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, 7 quai St Bernard, Case
237, F-75252 Paris Cedex 05, France; *Department of Biological Sciences, University of South Carolina, Columbia,
SC 29208, USA; †Ukrainian Antarctic Center, 16, blvd Tarasa Shevchenka, 01601 Kyiv, Ukraine; ‡ZoologicalMuseum, National Museum of the Natural History, National Academy of Sciences, 15 Bohdan Chmelnitsky St, 01030
Kyiv-30, Ukraine; and §Department of Environmental Science, College of Nyíregyháza, PO Box 166, H-4401
Nyíregyháza, Hungary

Summary
1. We investigated the relationship between radiation arising from the fall-out due tothe explosion of the nuclear reactor at Chernobyl, Ukraine, and body condition, rate of
reproduction and survival in a migratory passerine bird, the barn swallow Hirundo rusticaL., by comparing a contaminated region and a control region (Kanev) during 6 years
between 1991 and 2004.
2. The fraction of nonreproducing adults was on average 23% in Chernobyl comparedwith close to zero in Kanev and other European populations.
3. Body condition as estimated from body mass was similar in Chernobyl and Kanev.
Although laying date did not differ significantly between the two regions, clutch was
reduced by 7%, brood size by 14% and hatching success by 5% in the Chernobyl region
relative to the control area.
4. Annual adult survival, estimated from mark–recapture analyses, was on average 28%
in the Chernobyl region, but 40% in Kanev.
5. The relationships were generally confirmed in rank correlation analyses between
response variables and ambient radiation levels in different colonies.
6. The overall findings are consistent with the hypothesis that radioactive contamination in the Chernobyl region has significant negative impact on rates of reproduction
and survival of the barn swallow. We hypothesize that these effects are mediated by antioxidants and/or mutations.
Key-words: antioxidants, body condition, clutch size, hatching success, Hirundo rustica,
nonbreeding, population change, survival.
Journal of Animal Ecology (2005) 74, 1102–1111
doi: 10.1111/j.1365-2656.2005.01009.x

Introduction
Natural levels of radioactivity vary considerably, andeven naturally high levels may have biological consequences. For example, approximately 17 000 people diefrom radon-induced lung cancer in the USA each year

© 2005 British
Ecological Society

Correspondence: A. P. Møller, Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie
Curie, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05,
France. Tel.: +33 1 44 27 25 94; Fax: +33 1 44 27 35 16; Email: amoller@snv.jussieu.fr(Lubin & Boice 1997). The extent to which natural levelsof radiation affect wild animals and plants is almost
entirely unknown. Contamination arising from nuclear
weapons tests or accidents such as those at Three-mileIsland and Chernobyl has affected vast areas. In the caseof Chernobyl more than 5000 km2 have been contaminated in Ukraine and Belarus to the extent that theseareas have been completely depopulated (Anonymous
1996). Immediately following the explosion at the
Chernobyl reactor, the main source of radiation were I131,
Cs137 and Sr90 (Shestopalov 1996). Owing to its short halflife (8 days), I131 is no longer a significant concern. However,1103
Barn swallow
condition and life
history in
Chernobyl© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

Cs137 and Sr90 are both strong β-radiation emitters withhalf-lives on the order of 30 years (Shestopalov 1996),
and will thus be present in significant amounts for many
hundred years to come. Vast areas outside the exclusion zone are affected by lower levels of radiation that
greatly exceed natural background levels and suchcontamination may have consequences for survivaland reproduction of humans and other organisms.
For example, it has been shown that survival rates ofhumans and animals can be reduced in contaminatedareas (Robbins & Adams 1989; Kerber et al. 1993;
Ellegren et al. 1997; Jacob et al. 1998; Akleyev et al.
2002; Semjuk et al. 2002). Effects of low-level radiation
on reproductive success of free-living organisms have
only been examined to a very small extent (e.g. Fair &Myers 2002). Such effects of radiation on life history
may have consequences at the population level due toreductions in population size (Zakharov & Krysanov
1996; Ellegren et al. 1997). Given the size of the contaminated areas from the Chernobyl accident any
genetic or physiological effects will affect very large
populations of plants and animals, potentially withconsequences well beyond the directly affected areas
due to migration. These findings from Chernobyl contrast with the conclusions from the Hiroshima andNagasaki studies, which found no long-term effects on
reproduction or mutation (e.g. Awa et al. 1987; Neelet al. 1988). However, the amounts and the isotopes
involved differed dramatically, potentially accounting
for these differences.
The mechanisms resulting in reduced survivorshipand fecundity in populations living in contaminatedareas may be elevated mutation rates or physiologicalprocesses being affected by a reduction in levels of antioxidants. Genetic studies have reported increased
mutation rates in humans and barn swallows Hirundo
rustica L. from the radioactive contaminated areaaround Chernobyl in Ukraine (Dubrova et al. 1996;
Ellegren et al. 1997; Weinberg et al. 2001), and suchmutations may negatively affect a range of phenotypic
traits (Møller & Mousseau 2001, 2003). Second, antioxidants may be depleted in contaminated areas(Chaialo, Bereza & Chobot’ko 1991; Bazhan 1998;
Ben-Amotz et al. 1998; Ivaniota, Dubchak & Tyshchenko
1998; Neyfakh, Alimbekova & Ivanenko 1998a,b;
Lykholat & Chernaya 1999; Kumerova et al. 2000; Møller,
Mousseau & Surai 2005) and such reductions may
reduce clutch size (Blount et al. 2003) and affect otherlife-history traits.
The aims of this study of the barn swallow were toquantify: (1) the frequency of reproduction; (2) reproductive rates; and (3) survival rates in the radioactively
contaminated region around Chernobyl, Ukraine, andin a control region around Kanev more than 250 km to
the SE of the main contaminated area around Chernobyl. We further investigated these relationships bydetermining the association between our response variables and local levels of radiation measured in the fieldat each bird colony.

Materials and methods 
The barn swallow is a c. 20-g aerial insectivorous
passerine bird with long-distance migration (Møller
1994). Populations in Europe winter south of the
Sahara, and adults have extremely low levels of storage
and circulating antioxidants upon arrival to the breeding grounds (Ninni et al. 2004). Males arrive before
females and attract females by aerial displays of their
red throat patches, long tails and elaborate song
(Møller 1994). Once a male is mated, the pair will build
a nest, where the female will lay eggs and incubate.
Females deposit significant amounts of carotenoids
and other antioxidants in eggs, resulting in a second
minimum in circulating antioxidants in females during
the laying period (Saino et al. 2002). Both males andfemales feed nestlings and often raise a second brood
before returning to Africa in September–October(Møller 1994).
Male barn swallows in Chernobyl have dramaticallyincreased asymmetry in their elongated outermost tailfeathers and much paler throat coloration comparedwith males from a control area and with males predating the Chernobyl accident (Møller 1993). Longtailed males in particular are very pale compared with
controls (Camplani, Saino & Møller 1999). These findings suggest that antioxidant availability is reduced inradioactively contaminated areas around Chernobyl.

 
We studied barn swallows in parts of the southern andwestern sector just outside the exclusion zone of theChernobyl area (Shestopalov 1996). We visited villages
and stopped to check collective farms for the presenceof barn swallows. We drove along all public roads tovisit villages and collective farms in areas with highlevels of radiation outside the exclusion zone near Chernobyl. We visited all such areas south of the exclusionzone. While visits to areas with high levels of radiation
is nonrandom, we see no reason why such a selection
should be associated with farming practice, soil quality
or abundance of insects, which are the main food forbarn swallows. If barn swallows were recorded, we
attempted to capture as many adults as possible atwindows and doors of farm buildings using mist nets.
The villages visited and used for the study included
Guda-Katyuzhanka, Kathyuskanka, Obukovichy,
Phenevichy, Ivankov, Vakhovka, Glybovka, Pribirsk,
Dytiatku, Pysky, Martynovichi, Bober, Vesniane
and Dymir (Fig. 1). As a control area we used Kanevc. 220 km south-west of Kiev that has a relatively low
level of contamination. The relatively low level of contamination was confirmed by our own measurementsof radioactivity. The control villages visited and used
for the study included Kanev, Stepatsy and Stepanetske (Fig. 1). In the control area around Kanev werelationship [linear regression on log-log transformed
data: F = 159·46, d.f. = 1,18, r2 = 0·89, P < 0·0001,
slope (SE) = 1·28 (0·10)], suggesting that our field estimates of radiation provided the same ranking of levelsof radiation among sites as did published estimates.
Similarly, the measurements by the Ministry of Emergencies were obtained by repeated standardized measurement of radiation at the ground level in a large
number of different localities in Ukraine.

1104
A. P. Møller et al.

    
Fig. 1. Location of study sites and levels of radiation in the
Chernobyl and Kanev regions. Shaded areas represent areas
where > 3 Curie of Cs137 per km2 were deposited in 1986 (CIA1996). The average radiation levels for sample sites located in
the contaminated areas were 0·390 mR h−1 (SE = 0·317) at 14
breeding sites in the Chernobyl region. In the control region
near Kanev (c. 150 km SSE of Chernobyl) radiation levels
were on average an order of magnitude lower [0·025 mR h−1(SE = 0·002)]. Approximate locations of field sites areindicated either as red stars (in contaminated areas) or green
stars (relatively uncontaminated control areas).

similarly visited all the nearest villages to check for thepresence of barn swallows on collective farms.
Several villages with barn swallows in the 1990s
held no or only very few barn swallows during the lasttwo visits, and these sites were therefore not included
during these later visits. Sites were selected based on thenumber of barn swallows present, and farms whereno or few barn swallows were left were omitted duringlater visits. Barn swallows commonly abandon breedingsites, and such abandonment is frequently associatedwith changes in farming practice (Møller & Mousseau2001).

 
We worked in the two study areas during 10–29 June
1991 (APM), 16 –24 June 1996 (APM), 6–12 June 2000
(APM, TAM), 4 –11 June 2002 (APM, TAM), 7–13
June 2003 (APM, TAM) and 23–28 June 2004 (APM,
TAM).

   

© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

We obtained radiation estimates from two sources;
our own field measurements or measurements by the
Ukrainian Ministry of Emergencies. We measured α,β and γ radiation levels at ground level directly in thefield using a hand-held dosimeter (Model: Inspector,
SE International, Inc., Summertown, TN, USA). We
measured levels several (two to 10) times at each site
and averaged the measurements. Our data were validated with correlation against data from the governmental measurements published by Shestopalov(1996), estimated as the mid-point of the ranges published. This analysis revealed a very strong positive

We captured barn swallows by placing mist nets acrossopen doors and windows in farm building. Thismethod is highly efficient during the main breeding
season, and we were able to catch more than 75% of all
adults, according to estimates of capture probability
based on the proportion of unbanded birds (see following section).

    
We estimated the size of the breeding population at different farms by inspecting all nests and investigatingthese for signs of reproduction. As we conducted fieldwork at a time when all reproducing individuals would
have started building nests (in Denmark 1000 km further north, no first clutch nests were initiated after 10
June during the study of more than 5000 clutches in
1970–2002, A. P. Møller, unpublished data), and astudy of barn swallows in nearby eastern Hungary during 4 years also revealed that all first clutch nests were
initiated by early June (P. Pap & A. P. Møller, unpublished data). All nests that were under construction, or
contained fresh eggs or nestlings, were considered torepresent cases of current year reproduction. We estimated the number of adult birds by means of mark–recapture analyses. When we had captured and banded
adults for several hours, we recorded during the lasthour of capture the number of banded and unbanded
birds. We estimated the size of the total population as
the total number of banded birds divided by the proportion of birds captured that were already banded
during the last hour.
In an independent estimate of local population size
we marked the white breast feathers of banded adultbarn swallows with a permanent red marker pen. During the last hour before capture was terminated wecounted the maximum number of adult barn swallows
with and without red colour markings, using a pair ofZeiss 10 × 30 binoculars. Population size was in thiscase estimated as the total number of banded birds
divided by the proportion of birds that were marked
with the red pen. In small breeding colonies with amaximum of 10 breeding pairs we counted the maximum number of adult birds seen as almost all foraging
usually takes place within a distance of 200 m from thebreeding site, with occasional observations at distancesof up to 500 m (Møller 1987; Ambrosini et al. 2002).

1105
Barn swallow
condition and life
history in
Chernobyl

We used the total number of birds divided by two as an
estimate of total breeding population size.
In 2004 we checked all females carefully for a fully
developed brood patch that is completely naked withno presence of feathers. Any adult female with featherson the brood patch was considered to be a nonbreeder.
The size of the nonbreeding population and hence
the number of nonbreeding females was the estimate of
total adult population size minus twice the number ofactive nests.

    
Body condition reflects the amount of stored resources
relative to the size of an individual, and body mass after
controlling statistically for body size thus provides anunbiased estimate of such storage. We took 10 measurements of different morphological characters andweighed each adult barn swallow upon capture to thenearest 0·1 g with a Pesola spring balance. The correlation between body mass and structural body size
measured as keel length was weak and not statisticallysignificant (linear regression: F = 1·86, d.f. = 1,629,
r2 = 0·001, P = 0·17). Hence, we used body mass inthe subsequent analyses as a measure of body condition, as body mass was not confounded by bodysize. Body mass is highly repeatable among captures(Møller 1994).


We visited all buildings at farms within the two study
regions. Each was inspected for nests in use and all new
nests (as evidenced from the absence of spider webs inthe nest cup) were checked for content. Laying date wascalculated for all nests with laying in progress (one, twoor three eggs) assuming that one egg is laid per day.
Similarly, for nests with nestlings we used size relative
to a standard growth curve to estimate age in days andthen back-calculated assuming an incubation period of
14 days (Møller 1994) and one egg being laid each day.
Clutch size was estimated as the total number of eggs innests with at least three eggs. Brood size was estimatedas the number of nestlings that were at least 2 days old,
thereby avoiding underestimates due to eggs that had
not yet hatched. Unhatched eggs remain undamaged innests, and hatching success was calculated as brood size
divided by clutch size.

 

© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

Survival analysis was based on data of 152 males and
151 females captured and recaptured in the Chernobyl
region and 103 males and 98 females captured andrecaptured at the Kanev region between 2000 and 2004.
We estimated annual survival rates using capture–mark–recapture methods (Lebreton et al. 1992). The
goodness-of-fit of the general Cormack–Jolly–Sebermodel (Clobert & Lebreton 1987) to the data was cal-culated using the program RELEASE (Burnham et al.
1987), and the bootstrap function of the program
MARK (White & Burnham 1999). Modelling and estimation of survival and recapture rates was made with
MARK (White & Burnham 1999). We considered theoverdispersion value (c-hat) during model selection(Lebreton et al. 1992). Model selection among thestudied models was based on the Akaike’s Information
Criterion by selecting the model with the lowest AICc
value (Anderson, Burnham & White 1994) and Akaike
weight (Anderson & Burnham 1999), and hierarchicallikelihood ratio tests (LRT) were made by comparing amodel with those nested within the model (Lebreton
et al. 1992).

 
We used two types of analyses to test for associations
between high levels of radiation and response variables.
In the first series of analyses we used one-way analysis
of variance to test for a difference between the
Chernobyl and the Kanev region, using region as a fixed
effect. In a second series of analyses we investigated therelationship between mean value for the response
variable and measured level of radiation for each site.
Sample sizes differ among analyses because all
variables could not be quantified for all nests.
We used parametric or nonparametric analyses
depending on whether the distribution of variables
deviated significantly from normal distributions. The
proportion of nonbreeders and hatching success weresquare-root-arcsine-transformed and colony size andradiation level estimates were log-transformed before
statistical analyses.
All values reported are means (± SE).

Results
    
We estimated the number of active nests and thenumber of adults present at a number of different sites(Table 1). The estimation of population size based on
captures of individuals will only be reliable if captured
individuals do not become trap shy. We tested for thiseffect by determining whether estimates based on capturesdiffered from estimates based on sightings of birds thatwere dyed on their breast feathers after capture. Estimates
based on different methods were highly consistent,with almost all variance occurring among sites rather
than between methods (Table 1, F = 640·24, d.f. = 11,12,
P < 0·0001). In 2004 we checked all females for thepresence of a brood patch, and this method gave very
similar results to estimates based on dyed birds(F = 102·40, d.f. = 3,4, P < 0·0001). There was considerable variation in the proportion of nonbreedingpairs, ranging from 0 to 67% across sites (Table 1). The
frequency of nonbreeding pairs in the Kanev region
was significantly lower than in the Chernobyl region

1106
A. P. Møller et al.

Table 1. Estimates of number of active nests and number of adult barn swallows in Chernobyl and Kanev regions 1996–2004

Site
1996
Glybovka
Guda-Katyushanka
Ivankov
Obukhovchi
Phenevichy
Rudya-Dymerskaya
Kanev Reserve
Stepanetske
Stepantsy
Kanev Chicken Farm
2000
Bobor
Pribirsk
Vesniane
Kanev
2002
Bobor
Dytiatku
Pisky
Pribirsk
Vesniane
Kanev
2003
Dytiatku
Pisky
Vesniane
Kanev
2004
Dytiatku
Pisky
Vesniane
Kanev© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

No. active
nests

No. birds fromrecaptures

No. birds fromsightings ofdyed birds

7
5
1
3
2
5
7
10
10
10
3
15
5
45

No. of birds
countedNonbreeding
birds (%)

16
11
2
7
4
12
14
22
21
20

12·5
9·1
0·0
14·3
0·0
16·7
0·0
9·1
4·8
0·0

14

57·1
11·8
44·4
0·0

34
18
90

1
18
36
4
19
45

38
100
8
55
90

23
26
8
35
25
30
9
15

90
6

62
90

66·7
5·3
28·7
0·0
35·0
0·0

56
54
12
70

56
55
12
70

21·7
3·9
50·0
0·0

59
69
26
30

60
69
26
30

18·0
15·0
45·0
0·0

(Fig. 2a; Mann–Whitney U-test, z = 3·18, P = 0·002).
However, the frequency of 1·7% (SE = 1·2) in Kanev did
not differ significantly from the value of 0% recorded inwestern Europe (one-sample t-test, t = 1·42, d.f. = 26,
P = 0·37). There was a significant positive relationshipbetween the frequency of nonbreeding pairs and local
levels of radiation [Fig. 3; linear regression: F = 35·07,
d.f. = 1,26, r 2 = 0·57, P < 0·0001, slope (SE) = 0·31 (0·05)].
Previous studies have shown that nonbreeding males
aggregate in large colonies, while nonbreeding females
have never previously been recorded (Møller 1988).
There is usually a small excess of males among adultbarn swallows (9·4%; SE = 1·0) in Denmark (Møller
1994; A. P. Møller, unpublished data). This was also thecase in Ukraine with 52·85% of 932 adults captured
being males. Colony size could have confounded therelationship between frequency of nonbreeders andlevel of radiation. However, colony size was not related
to levels of radiation (linear regression based on logtransformed data: F = 0·12, d.f. = 1,26, r2 = 0·00,
P = 0·73). Also, the relationship between the frequency
of nonbreeding pairs and local levels of radiation was
not confounded by colony size measured as the total
number of adult birds present [multiple linear regres-102
8sion: F = 16·87, d.f. = 2,25, r2 = 0·57, P < 0·0001, slope(SE) for radiation = 0·31 (0·05), t = 5·79, P < 0·0001;
slope (SE) for log-transformed colony size = −0·01(0·10), t = 0·12, P = 0·91].
The sex ratio among adults was 53·42% (n = 556) in
Chernobyl and 52·13% (n = 376) in Kanev, with no significant difference between areas (G = 2·76, d.f. = 1,
P = 0·10). Thus, there were no clear differences in sex
ratio among areas in Ukraine.

    
Adult barn swallows differed in body mass in relation
to level of contamination. Barn swallows from the
Chernobyl region were slightly lighter than conspecifics from the Kanev region (Fig. 2b). There was a sex
difference in body mass, but this effect was similar in
the two regions as evidenced by a nonsignificant interaction term between sex and region (F = 0·42, d.f. = 1,903,
P = 0·52). Adults from Chernobyl weighed on average
1·1% less than adults from Kanev. Individuals withlarger structural body size, as estimated by keel length,
did not weigh more in Kanev (linear regression: males:
F = 0·76, d.f. = 1,179, P = 0·38; females: F = 0·86,1107
Barn swallow
condition and life
history in
Chernobyl

Fig. 2. Difference in (a) percentage nonbreeders (%), (b) body mass (g), (c) laying date (day 1 = 1 May), (d) clutch size, (e) broodsize and (f ) hatching success (%) between Chernobyl and Kanev regions. Values are means (±SE).

and region by sex as factors and keel length as acovariate did not reveal a significant effect of region on
body mass (F = 2·54, d.f. = 1,887, P = 0·11). The relationship between mean body mass per colony and levelof radiation was not statistically significant (Spearman
rank correlation: rS = 0·05, z = 0·25, n = 31, P = 0·81).

 

Fig. 3. Relationship between abundance of nonbreeding
adult barn swallows (%) and level of radiation (mR h−1) in
Chernobyl and Kanev regions.

© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

d.f. = 1,169, P = 0·35), but did so in the Chernobyl
region, particularly for females [linear regression: males:
F = 14·53, d.f. = 1,283, r2 = 0·05, slope (SE) = 0·03
(0·008), P = 0·002; females: F = 24·21, d.f. = 1,253,
r2 = 0·09, slope (SE) = 0·05 (0·01), P < 0·0001]. Barnswallows had slightly shorter keels in Chernobyl thanin Kanev (mean difference of 1·0%), and this difference
between areas was similar in the two sexes (F = 0·18,
d.f. = 1,888, P = 0·68). An analysis of covariance withbody mass as the dependent variable and region, sex,

Laying date did not differ significantly between the tworegions (Fig. 2d; F = 0·23, d.f. = 1,181, P = 0·64). Thisfinding was independent of year effects (F = 0·14,
d.f. = 1,177, P = 0·71). Thus differences for clutch andbrood size, and for hatching success, were independentof laying date effects. The relationship between mean
laying date and radiation level was not statisticallysignificant (Spearman rank correlation: rS = 0·05, z =0·22, n = 23, P = 0·83).
Clutch size was 7·0% smaller in the Chernobyl region
than in the Kanev region (Fig. 2e; F = 6·83, d.f. = 1,217,
P = 0·01). This effect remained significant after accounting for year effects (F = 5·33, d.f. = 1,213, P = 0·02).
Overall, the relationship between mean clutch size andradiation level was significantly negative (Spearman
rank correlation: rS = −0·49, z = 2·28, n = 23, P = 0·02).
Brood size at hatching also was smaller in Chernobyl
than in Kanev (Fig. 2f; F = 17·04, d.f. = 1,176, P < 0·0001),
with a mean difference of 13·5%. This effect was independent of year (F = 39·95, d.f. = 1,171, P < 0·0001).
The relationship between mean brood size and radiationlevel was also significantly negative (Spearman rankcorrelation: rS = −0·59, z = 2·79, n = 23, P = 0·005).

1108
A. P. Møller et al.

Hatching success was significantly higher in Kanev
than in Chernobyl (Fig. 2g; F = 6·42, d.f. = 1,175,
P = 0·01) with a mean difference between regions of
4·6%. This effect was independent of year (F = 7·13,
d.f. = 1,171, P = 0·008). There was also a significant
negative relationship between mean hatching successand radiation level (Spearman rank correlation: rS =−0·52, z = 2·69, n = 23, P = 0·007).
One of our study sites (Vesniane) was within the
exclusion zone, where farming ceased completely in
1986. Exclusion of this site from the analyses revealed
very similar results, and none of the differences reported
above changed after exclusion of data from Vesniane.

     © 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

The basic Cormack–Jolly–Seber model (Sg*t, Pg*t) wasused to fit the survival data (χ2 = 0·28, d.f. = 2, P = 0·87;
RELEASE; P = 0·23; 100 repetitions, deviance-based
bootstrap goodness-of-fit (GOF) test by MARK). The
overdispersion value (c-hat), estimated on the basis of thebootstrapped GOF, was slightly less than 1 (c-hat = 0·99),
and a c-hat = 1-value was used during model selection.
In the global model we examined annual survival (S)and recapture rates (P) for four groups (g; males andfemales in Chernobyl and Kanev), and their interaction
with study period (g * t).
The two most parsimonious models differed little intheir AICc scores (632·4, 632·64). Both models foundsignificant differences between Chernobyl and control
populations in recapture rates. The first model alsosuggested differences in recapture rates between males
and females in the Chernobyl populations but notfor the control regions. However, a LRT of these twomodels suggested there was no significant difference
between the sexes in recapture rate in Chernobyl during
the study period, although the power of this test waslow (χ2 = 2·33, d.f. = 1, P = 0·13; LRT).
Recapture rate differed significantly among thestudied groups, being lower for Kanev birds whencompared with males and females in the Chernobyl
area (χ2 = 7·58, d.f. = 2, P = 0·02; LRT).
Recapture rate also varied significantly among years(χ2 = 13·13, d.f. = 2, P = 0·001; LRT). There was no
significant interaction among groups and years, causing the recapture rate to vary in parallel over the study
period (χ2 = 3·72, d.f. = 6, P = 0·72; LRT).
On the basis of the LRTs of nested models we foundthat annual survival rates varied greatly among study
groups and sexes [Chernobyl males: 0·327 (SE = 0·085);
Chernobyl females: 0·233 (SE = 0·028); Kanev males:
0·431 (SE = 0·100); Kanev females: 0·542 (SE = 0·170);
χ2 = 18·44, d.f. = 2, P < 0·001; LRT ]. However, althoughdifferences between male and female survival rates
were significant in the Kanev populations (χ2 = 5·56,
d.f. = 1, P = 0·02; LRT), this was not the case for Chernobyl (χ2 = 0·12, d.f. = 1, P = 0·73; LRT).
Observed survival rates varied significantly among
years in both regions in parallel (year effect: χ2 = 14·59,

d.f. = 2, P < 0·001; in a parallel fashion: interaction
between year and location: χ2 = 2·40, d.f. = 6, P = 0·88;
LRT).

Discussion
Barn swallows in the Chernobyl region only differedslightly in body mass from barn swallows from the control area. Surprisingly, we found different patternsof body mass–body size relationships between the
Chernobyl and Kanev regions. While body mass was
independent of skeletal size (as estimated from keel
length) in Kanev, as has been found in Denmark (Møller
1994), there were clear positive relationships in Chernobyl. This difference was particularly pronounced infemales, while the difference for males was less clear.
We hypothesize that this difference may partly be theresult of effects of radiation on mutation. Small individuals in Chernobyl may be more likely to be mutants,
which because of deleterious effects of mutations also
have a small body mass (Møller & Mousseau 2001). In
contrast, small individuals in Kanev are likely to besmall for reasons other than deleterious mutations, andtheir body mass is therefore not likely to be reduced incomparison with the body mass of large individuals.
In the Chernobyl region a large fraction of the adultfemales were nonbreeders. Nonbreeding in the barnswallow has previously been recorded only in males, asa slightly skewed sex ratio results in on average 9·4%of males remaining unmated in a Danish population(Møller 1988, 1994; A. P. Møller, unpublished data).
The large proportion of nonbreeding females recorded
in several colonies in the Chernobyl region is unprecedented in the numerous studies of barn swallows
in Europe (e.g. Møller 1994). Thus, the observed frequency of 22·8% (SE = 4·5) nonbreeding females in
Chernobyl is well above the level recorded in the control area in Kanev of 1·7% (SE = 1·2) (Fig. 2a). It isalso well above the null expectation of 0% nonbreeding
females based on data from three long-term studies ofbarn swallows in Denmark, Italy and Spain of eachmore than 3000 individually banded adult barn swallows (A. P. Møller, F. de Lope & N. Saino, unpublisheddata). However, the estimate from Kanev did not deviate significantly from the value recorded in the west
European populations. This suggests that nonbreeding
among females was markedly higher in Chernobyl thanin Kanev. In contrast, the adult sex ratio in Chernobyl
did not differ from that recorded in Denmark (Møller
1994), or from that recorded in Kanev. Thus, elevatedlevels of radiation in Chernobyl were not associatedwith a difference in adult sex ratio.
Among the barn swallows that bred, clutch size andin particular brood size were small, with a smaller
fraction of eggs hatching in Chernobyl than in Kanev.
There was no significant difference in laying date
between the two regions, suggesting that this variable
was not a confounding factor for differences in clutchsize, brood size or hatching success.

1109
Barn swallow
condition and life
history in
Chernobyl© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

Adult survival in the Chernobyl region was also low
compared with the control area in Ukraine and to estimates from western Europe (Møller 1994; Møller &Szép 2002; A. P. Møller, T. Szép, N. Saino & F. de Lope,
unpublished data). The population in the Chernobyl
area therefore decreased considerably, while that was
not the case in the control area near Kanev. Numerous
studies of the breeding biology of European barnswallows have revealed clear geographical patterns withlaying being later and clutch sizes larger towards thenorth (Møller 1984, 1994). As the Chernobyl region isc. 250 km further north than the Kanev region, theresults are conservative as we would expect a priori thatlaying would be later and clutches larger in the Chernobyl region. They clearly were not.
The recorded survival rates and reproductive rates in
the Chernobyl region are not sufficient to maintain astable population size. If we assume that the populationin the Kanev region is self-sustaining, then the population in Chernobyl clearly cannot be sustained without immigration. Adult survival rate in Chernobyl
was only 43% of that in the Kanev region for females
and 76% for males. While 23% of adult females werenonbreeders in the Chernobyl region, less than 2%
were nonbreeders in the Kanev region. In addition,brood size was more than 24% lower in Chernobyl
than in Kanev. A study of a decreasing Danish barnswallow population with an adult survival rate of 35%
revealed that the population was not sustainable eventhough the reproductive rate was higher than thatrecorded in the Chernobyl region (Engen, Sæther &Møller 2001). Thus, the Chernobyl population cannot
possibly be sustainable and must be acting as a sink
population.
We can only speculate about the possible mechanisms generating the observed patterns described here.
Here we propose two different, but not necessarily
mutually exclusive explanations: (1) deleterious effects
of mutations, and (2) negative effects of radiation on
antioxidants. This study did not provide analyses thatallow us to assess the relative role of mutations and useof antioxidants as a cause of the reduction in reproductive rate and annual adult survival. Also, alternativeinterpretations exist. The observations reported here
may be accounted for if there were differences in abundance or composition of food between the two regions.
Barn swallows mainly feed on Diptera, particularly
Muscidae, Syrphidae and Tabanidae, but also aphids,
beetles and butterflies (Møller 1994). Barn swallows
must ingest all antioxidants, and carotenoids are particularly common in insects that feed on pollen such as
Syrphidae and Lepidoptera, but also in insects thatfeed on leaves such as aphids and caterpillars. As mostradionuclides (mainly Cs137 and Sr90) are in the upper
soil (Shestopalov 1996), we might expect Diptera to be
more affected by radiation than aphids or Lepidoptera.
Hence, there is no reason to expect differences in carotenoid availability due to differences in the abundanceof insects to account for the reported findings.

A second alternative is that changes in farming practice differ between the two regions. Modern farming has
collapsed in the large collective farms and the numberof dairy cows have been reduced dramatically. For
example, the number of dairy cows in two large farms
in the Chernobyl and Kanev regions has decreased
from 250 and 230 in 1991, respectively, to 30 and 38
cows in 2002. Clutch size of barn swallows in Denmarkis slightly smaller (on average 4·9%) on farms without
than with cows, while there are no effects of abandonment of dairy farming on adult body mass, frequency
of nonbreeding, hatching success, brood size or adultsurvival (Møller 2001). Changes in farming practice
are very similar across Ukraine and thus cannot
account for the regional differences or the patterns
observed within the regions described here. Althoughlarge areas in the Chernobyl region have been depopulated and farming has ceased completely as an official
measure to reduce transfer of radioactive material tohumans through food, this cannot have affected our
results because we almost exclusively worked outside
the exclusion zone. Only one of our study sites waswithin the exclusion zone, and our general findings did
not change after exclusion of this single observation.
Hence, it is unlikely that environmental changes canaccount for the observations reported here, aschanges in agricultural practice have been similar across
Ukraine. Finally, both alternative explanations would
suggest large differences in body condition of adults
between areas, which was clearly not the case.
Why are the associations between radiation, condition, reproduction and survival so clear in the barnswallow? First, we do not know whether similar patterns will be found in other avian species, as no otherstudies have been made to date. Second, if the patterns
reported for the barn swallow turn out to be unique, wesuggest that antioxidants may be the cause. Migratory
birds that fly thousands of kilometres produce large
amounts of free radicals that must be neutralized byantioxidants (Ninni et al. 2004). In addition, females
allocate considerable amounts of antioxidants to eggs
(Blount, Houston & Møller 2000; Blount et al. 2003),
resulting in a second minimum in body antioxidants
during a short period of time. Given that large amountsof antioxidants are used for coping with the physiological consequences of radiation in the Chernobyl region(Chaialo et al. 1991; Bazhan 1998; Ben-Amotz et al.
1998; Ivaniota et al. 1998; Neyfakh et al. 1998a,b;
Lykholat & Chernaya 1999; Kumerova et al. 2000;
Møller et al. 2005), there may be trade-offs between
allocation to competing demands such as those causedby migration and reproduction.

Acknowledgements
We are most grateful to N. Szczerbak and A. A. Tokarfor logistic help provided during our visits to Ukraine
over the years. We received funding from the CNRS(France), the University of South Carolina School of1110
A. P. Møller et al.

the Environment, the Samuel Freeman Charitable Trust,the National Science Foundation, National Geographic
Society and U.S. Civilian Research Development
Foundation to conduct this research. TSz was supported
by OTKA T29853 and T42879. This is gratefully
acknowledged.

References© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

Akleyev, A.V., Grosche, B., Gusev, B.I., Kiselev, V.I.,
Kisselev, M.F., Kolyado, I.B., Romanov, S., Shoikhet, Y.N.
& Neta, R. (2002) Developing additional resources. Radiation and Environmental Biophysics, 41, 13 –18.
Ambrosini, R., Bolzern, A.M., Canova, L., Arieni, S., Møller,
A.P. & Saino, N. (2002) The distribution and colony size ofbarn swallows in relation to agricultural land use. Journal ofApplied Ecology, 39, 524 –534.
Anderson, D.R. & Burnham, K.P. (1999) Understanding
information criteria for selection among capture-recaptureor ring recovery models. Bird Study, 46, S14 –S21.
Anderson, D.R., Burnham, K.P. & White, G.C. (1994) AIC
model selection in overdispersed capture-recapture data.
Ecology, 75, 1780 –1793.
Anonymous (1996) Chernobyl. Ten years on. Radiologicaland Health Impact. OECD, Paris.
Awa, A.A., Honda, T., Neriishi, S., Sufuni, T., Shimba, H.,
Ohtaki, K., Nakano, M., Kodama, Y., Itoh, M. &Hamilton, H.B. (1987) Cytogenetic study of the offspringof atomic bomb survivors, Hiroshima and Nagasaki.
Cytogenetics (eds G. Obe & A. Basler), pp. 116 –130.
Springer-Verlag, Berlin.
Bazhan, K.V. (1998) [Lipid peroxidation and the antioxidant
system in subjects exposed to the influence of extreme
factors]. Lik Sprava, 8, 47–50.
Ben-Amotz, A., Yatziv, S., Sela, M., Greenberg, S.,
Rachmilevich, B., Shwarzman, M. & Weshler, Z. (1998)
Effect of natural beta-carotene supplementation in children
exposed to radiation from the Chernobyl accident. Radiationand Environmental Biophysics, 37, 187–193.
Blount, J.D., Houston, D.C. & Møller, A.P. (2000) Why egg
yolk is yellow. Trends in Ecology and Evolution, 17, 47– 49.
Blount, J.D., Houston, D.C., Surai, P.F. & Møller, A.P. (2003)
Egg-laying capacity is limited by carotenoid pigment availability in wild gulls Larus fuscus. Proceedings of the Royal
Society of London B (Biology Letters), 271, S79–S81.
Burnham, K.P., Anderson, D.R., White, G.C., Brownie, C. &Pollock, K.H. (1987) Design and Analysis Methods for Fish
Survival Experiments Based on Release-Recapture. American Fisheries Society Monographs, 5. Bethesda, Maryland.
Camplani, C., Saino, N. & Møller, A.P. (1999) Carotenoids,
sexual signals and immune function in barn swallows from
Chernobyl. Proceedings of the Royal Society of London B,
266, 1111–1116.
Chaialo, P.P., Bereza, V.I. & Chobot’ko, G.M. (1991) [Freeradical processes and blood antioxidant systems in the lateperiod following acute radiation sickness]. Medical Radiology(Moscow), 36, 20 –21.
CIA (1996) Handbook of International Economic Statistics.
Directorate of Intelligence, Washington.
Clobert, J. & Lebreton, J.-D. (1987) Recent models for
mark–recapture and mark resighting data: a response to
C. Brownie. Biometrics, 43, 1019–1022.
Dubrova, Y.E., Nesterov, V.N., Krouchinsky, N.G.,
Ostapenko, V.A., Neumann, R., Neil, D.L. & Jeffreys, A.J.
(1996) Human minisatellite mutation rate after the Chernobyl accident. Nature, 380, 683 – 686.
Ellegren, H., Lindgren, G., Primmer, C.R. & Møller, A.P.
(1997) Fitness loss and germline mutations in barn swallows breeding in Chernobyl. Nature, 389, 593 –596.

Engen, S., Sæther, B.-E. & Møller, A.P. (2001) Stochastic
population dynamics and time to extinction of a declining
population of barn swallows. Journal of Animal Ecology,
70, 789–797.
Fair, J.M. & Myers, O.B. (2002) Early reproductive success ofwestern bluebirds and ash-throated flycatchers: a landscapecontaminant perspective. Environmental Pollution, 118,
321–330.
Ivaniota, L., Dubchak, A.S. & Tyshchenko, V.K. (1998) [Freeradical oxidation of lipids and antioxidant system of bloodin infertile women in a radioactive environment]. Ukrainski
Biokhim Zhurnal, 70, 132–135.
Jacob, P., Goulko, G., Heidenreich, W., Likhtarev, I., Kairo, I.,
Tronko, N.D., Bogdanova, T.I., Kenigsberg, J., Buglova, E.,
Drozdovitch, V., Golevneva, E., Demididchick, E.D.,
Balonov, M., Zvonova, I. & Beral, V. (1998) Thyroid cancer
risk to children calculated. Nature, 392, 31–32.
Kerber, R.A., Till, J.E., Simon, S.L., Lyon, J.L., Thomas, D.C.,
Preston Martin, S., Rallison, M.L., Lloyd, R.D. & Stevens, W.
(1993) A cohort study of thyroid disease in relation to fallout
from nuclear weapons testing. JAMA, 270, 2076–2082.
Kumerova, A.O., Lece, A.G., Skesters, A.P., Orlikov, G.A.,
Seleznev, J.V. & Rainsford, K.D. (2000) Antioxidant
defense and trace element imbalance in patients withpostradiation syndrome: first report on phase I studies.
Biological Trace Element Research, 77, 1–12.
Lebreton, J.-D., Burnham, K.P., Clobert, J. & Anderson,
D.R. (1992) Modeling survival and testing biologicalhypotheses using marked animals: a unified approach withcase studies. Ecological Monographs, 62, 67–118.
Lubin, J. & Boice, J. Jr (1997) Lung cancer risk from residential radon: meta-analysis of eight epidemiologic studies.
Journal of the National Cancer Institute, 89, 49–57.
Lykholat, E.A. & Chernaya, V.I. (1999) Parameters of peroxidation and proteolysis in the organism of the liquidatorsof Chernobyl accident consequences. Ukrainski Biokhim
Zhurnal, 71, 82–85.
Møller, A.P. (1984) Geographical variation in breeding
parameters of two hirundines. Ornis Scandinavica, 15, 43–54.
Møller, A.P. (1987) Advantages and disadvantages of coloniality in the swallow Hirundo rustica. Animal Behaviour, 35,
819–832.
Møller, A.P. (1988) Infanticidal and anti-infanticidal strategies in the swallow Hirundo rustica. Behavioral Ecology andSociobiology, 22, 365–371.
Møller, A.P. (1993) Morphology and sexual selection in thebarn swallow Hirundo rustica in Chernobyl, Ukraine. Proceedings of the Royal Society of London B, 252, 51–57.
Møller, A.P. (1994) Sexual Selection and the Barn Swallow.
Oxford University Press, Oxford.
Møller, A.P. (2001) The effect of dairy farming on barn swallow
Hirundo rustica abundance, distribution and reproduction.
Journal of Applied Ecology, 38, 378 – 389.
Møller, A.P. & Mousseau, T.A. (2001) Albinism and phenotype of barn swallows Hirundo rustica from Chernobyl.
Evolution, 55, 2097–2104.
Møller, A.P. & Mousseau, T.A. (2003) Mutation and sexual
selection: a test using barn swallows from Chernobyl. Evolution, 57, 2139–2146.
Møller, A.P. & Szép, T. (2002) Survival rate of adult barnswallows Hirundo rustica in relation to sexual selection
and reproduction. Ecology, 83, 2220 –2228.
Møller, A.P., Surai, P.F. & Mousseau, T.A. (2005) Antioxidants,
radiation and mutation in barn swallows from Chernobyl.
Proceedings of the Royal Society of London B, 272, 247–252.
Neel, J.V., Satoh, C., Goriki, K., Asakawa, J., Fujita, M.,
Takahashi, N., Kageoka, T. & Hazama, R. (1988) Search
for mutations altering protein change and /or function inchildren of atomic bomb survivors: final report. American
Journal of Human Genetics, 42, 663 – 676.

1111
Barn swallow
condition and life
history in
Chernobyl© 2005 British
Ecological Society,
Journal of Animal
Ecology, 74,1102–1111

Neyfakh, E.A., Alimbekova, A.I. & Ivanenko, G.F. (1998a)
Vitamin E and A deficiencies in children correlate withChernobyl radiation loads of their mothers. Biochemistry(Moscow), 63, 1138 –1143.
Neyfakh, E.A., Alimbekova, A.I. & Ivanenko, G.F. (1998b)
Radiation-induced lipoperoxidative stress in children
coupled with deficit of essential antioxidants. Biochemistry(Moscow), 63, 977–987.
Ninni, P., de Lope, F., Saino, N., Haussy, C. & Møller, A.P.
(2004) Antioxidants and condition-dependence of arrival
date in a migratory passerine. Oikos, 105, 55 – 64.
Robbins, J. & Adams, W. (1989) Radiation effects in the Marshall Islands. Radiation and the Thyroid (ed. S. Nagasaki),pp. 11–24. Kluwer, Amsterdam.
Saino, N.V., Bertacche, V., Ferrari, R., Martinelli, R., Møller,
A.P. & Stradi, R. (2002) Carotenoid concentration in barnswallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal
Society of London B, 269, 1729–1734.

Semjuk, O.F., Kavsan, V.M., Muller, W.E.G. & Schroder, H.C.
(2002) Long-term effects of low-dose radiation on humanhealth. Cellular and Molecular Biology, 48, 393–409.
Shestopalov, V.M. (1996) Atlas of Chernobyl Exclusion Zone.
Ukrainian Academy of Science, Kiev.
Weinberg, H.S., Korol, A.B., Kirzhner, V.M., Avivi, A.,
Fahima, T., Nero, E., Shapiro, S., Rennert, G., Piatak, O.,
Stepanova, E.I. & Skvarskaja, E. (2001) Very high mutation rate in offspring of chernobyl accident liquidators.
Proceedings of the Royal Society of London, B, 268, 1001–
1005.
White, G.C. & Burnham, K.P. (1999) Program MARK:
Survival estimation from populations of marked animals.
Bird Study, 46, S120 –S138.
Zakharov, V.M. & Krysanov, E.Y., eds (1996) Consequencesof the Chernobyl catastrophe. Environmental Health. Center
for Russian Environmental Policy, Moscow, Russia.
Received 13 December 2004; accepted 1 June 2005