Journal of Applied
Ecology 2007

Determinants of interspecific variation in population
declines of birds after exposure to radiation at Chernobyl

Blackwell Publishing Ltd

A. P. MØLLER* and T. A. MOUSSEAU†*Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7quai St Bernard, Case 237, F-75252 Paris Cedex 05, France; and †Department of Biological Sciences, University ofSouth Carolina, Columbia, SC 29208, USA

Summary
1. Radiation can reduce antioxidant levels dramatically because of the use of antioxidants to eliminate free radicals produced in the presence of radiation. Antioxidants are
crucial biochemicals for elimination of free radicals, which can cause permanent damage to DNA and other molecules. If antioxidants are a limiting resource, we would
expect individuals of species with a high expenditure of antioxidants to suffer the mostfrom radiation. We tested this hypothesis by investigating interspecific variation in therelationship between abundance and level of radiation in breeding birds inhabiting forests around Chernobyl, Ukraine. We used bird point counts to estimate abundance of
57 species of birds at 254 locations where background radiation levels were quantified.
2. Migratory birds use large amounts of antioxidants during their annual migrations toneutralize free radicals, and migrants have depleted antioxidant levels upon arrival attheir breeding grounds. Consistently, abundance decreased with increasing levels ofradiation in species that migrated the longest distances.
3. Bird species with long dispersal distances may experience deficiencies in antioxidant
levels because of physical activity but also because of exposure to novel antigens, implying that species with long dispersal distances should suffer the most from exposure toradiation. Indeed, the slope of the relationship between abundance and radiation
decreased with increasing dispersal distance.
4. Female birds deposit large amounts of antioxidants in their eggs, with the total
amount deposited often exceeding the total amount in a female’s. Accordingly, thedecrease in abundance with radiation level increased with relative egg size in different
species.
5. Many bird species have plumage that is coloured by carotenoids, which cannot berecovered once deposited in feathers. Therefore, bird species with carotenoid-based
plumage should show stronger declines with increasing levels of radiation than species
with melanin-based or structural coloration. In accordance with this prediction, thedecline in abundance with radiation was the strongest in species of birds with carotenoidbased plumage.
6. Synthesis and applications. These findings highlight the importance of antioxidants
for understanding the ecological consequences of radiation on the abundance of freeliving animals, showing that species using large amounts of antioxidants will be particularly susceptible to the effects of low-level radiation.
Key-words: carotenoids, dispersal, maternal effects, migration, sexual coloration
Journal of Applied Ecology (2007)
doi: 10.1111/j.1365-2664.2007.01353.x© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society

Correspondence: A. P. Møller, Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bât.
A, 7ème étage, 7 quai St Bernard, Case 237, F-75252 Paris Cedex 05, France (fax +33 1 44 27 35 16; e-mail amoller@snv.jussieu.fr).

2
A. P. Møller &T. A. Mousseau© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecology

Introduction
World-wide, thousands of square kilometres of land areradioactively contaminated, mainly as a result of theChernobyl disaster but also as a result of tests with nuclear
bombs. Furthermore, there is considerable natural variation in background radiation, with many areas reaching
non-negligible levels. Yet the ecological and evolutionary
consequences of human-induced and natural variation inradiation remain poorly known (Zakharov & Krysanov
1996; Møller & Mousseau 2006).
Radiation and antioxidants interact in a numberof different ways, making them key biochemicals forunderstanding the interactions between radiation on
one hand and ecology and evolution on the other.
First, a deficiency of antioxidants such as carotenoids
and vitamins A and E can increase the DNA damage
caused by free radicals (Ames 1983; Edge, McGarvey& Truscott 1997; Rice-Evans et al. 1997; Bast et al.
1998; Krinsky 1998; Møller et al. 2000), which might inparticular be the case in the presence of high levels ofradiation. Secondly, radiation produces free radicals
that are removed by antioxidants, resulting in depletionof antioxidants in the presence of high levels of radiation,leaving few reserves for scavenging the free radicals
produced by ordinary metabolic activity (Ben-Amotz
et al. 1998; Ivaniota, Dubchak & Tyshchenko 1998;
Neyfakh, Alimbekova & Ivanenko 1998a,b; Kumerova
et al. 2000). This reduction in antioxidants may be one
factor responsible for the increased levels of mutationin species in radioactively contaminated areas such an
those around Chernobyl in Ukraine, while the alternative factor is the direct effects of radiation on mutations(Ellegren et al. 1997; Møller & Mousseau 2003).
Antioxidants are important biochemicals that provide
protection against the damaging effects of free radicals
on DNA and other molecules (reviewed by Halliwell &Gutteridge 1990; Yu 1994; Møller et al. 2000; Surai
2002). Elevated levels of radiation, as experienced byrecovery workers and other people exposed to theChernobyl accident, are associated with a diminishedantioxidant defence as a result of the use of antioxidants for free radical scavenging (Ivaniota, Dubchak &Tyshchenko 1998; Neyfakh, Alimbekova & Ivanenko
1998a; Kumerova et al. 2000). Likewise, Møller, Surai& Mousseau (2005) showed various changes in barnswallows Hirundo rustica exposed to high levels ofradiation in Chernobyl. In particular, circulating plasma
levels of carotenoids and vitamins A and E were dramatically reduced, as were levels of these antioxidants
stored in the liver and eggs. However, such effects ofradiation on antioxidant levels are reversible because
supplementation with b-carotene and vitamins A andE can reduce the effects of the lipo-peroxidative cascade
among individuals subject to radiation (Clavere et al.
1996; Ben-Amotz et al. 1998; Neyfakh, Alimbekova &Ivanenko 1998b). Administration of antioxidants suchas vitamin E to subjects reduced the effects of radiation
on immunity (Rana & Malhotra 1995; Moriguchi et al.

1996) and the intestine (Empey et al. 1992; Felemovicius
et al. 1995). While these studies provide important
information regarding the links between radiation
exposure and antioxidant defence, there has been no
study that links the effects of radiation on population
size of different species to antioxidant defence. We havecarried out a preliminary test of the links between effectsof radiation on population density and antioxidant use,by studying a community of free-living birds in areas in
Ukraine varying by three orders of magnitude in levelsof radioactive contamination (0·04–135·89 mR h–1).
All organisms must cope with the detrimental effects
of free radicals in order to transfer undamaged DNA tooffspring, and a number of different defence mechanisms have evolved to cope with such effects. Although
all species must cope with the potentially detrimental
effects of free radicals, because of their use of antioxidants,
certain species are predisposed to suffer particularly
from these negative effects. We hypothesized that, while
all species of higher organisms use antioxidants to copewith free radicals, some species use disproportionate
amounts but also have to maintain disproportionately
large margins to ensure survival. A migratory species,
with individuals weighing 10 g, annually travelling
10 000 km, would produce vast amounts of free radicals(Costantini, Cardinale & Carere 2007). These free radicals
have to be neutralized, thereby reducing antioxidant
stores during and after migration (Ninni et al. 2004).
The amounts of antioxidants needed for free radical
scavenging should exceed, by a large margin, what isavailable in favourable years, because poor environmental
conditions before the start of migration, head winds
and other factors may increase the need for antioxidants
considerably. This argument is based on geometric rather
than arithmetic means, emphasizing the importance of
selection arising from rare events of adverse conditions,thus implying that, on average, migratory species will
suffer from low levels of antioxidants more often thanresident species. We argue that four different activities
account for reductions in antioxidant levels in freeliving organisms, and that each of these factors will
increase the susceptibility of a species to the negative
effects of radiation. These factors are (i) extreme physical activity, such as that associated with long-distancemigration; (ii) dispersal; (iii) deposition of antioxidants
in eggs; and (iv) deposition of antioxidants in signals
used for social or sexual communication.
We will briefly review the empirical basis for considering these four factors as sinks for antioxidants. First,
twice annually long-distance migration constitutes alevel of extreme physical activity (Berthold 2001) thatmay deplete antioxidant levels. Direct physiologicalevidence suggests that migrants arrive at their breeding
grounds with depleted levels of antioxidants, withearly-arriving migrants differing in levels of carotenoid
depletion from late-arriving individuals (Ninni et al.
2004). Similarly, there is experimental evidence from
salmon showing that oxidative stress is an important
cost of migration (Welker & Congleton 2005). This

3
Population declines
and radiation© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecology

implies that migrants will differ from residents in antioxidant levels, but also that long-distance migrants will
differ from short-distance migrants in antioxidant levels.
Secondly, migrants disperse over long distances but
there is also movement to areas with novel parasite
strains that have not previously been encountered by ahost. This raises the prospect of induction of immune
responses (Møller & Erritzøe 2001), which are known
to be potent sources of free radicals (Costantini &Dell’Omo 2006) because of rapid cell proliferation(Roitt, Brostoff & Male 1998; Møller et al. 2000).
Immune cells use free radicals as a powerful weapon tokill bacteria and other infections by stimulating free
radical production by macrophages (Chapple 1997).
Enhanced immune cell activity can overproduce free
radicals, and antioxidant protection in this case could
be vital in avoiding damage to DNA and other molecules(Gille & Sigler 1995; Jaeschke 1995). Given that there
are interspecific differences in dispersal propensity (Paradis
et al. 1998), we suggest that there are interspecific differences in the use of antioxidants associated with dispersal, causing a negative relationship between dispersal
distance and population decline caused by radiation.
Thirdly, females of invertebrates, fish and birds deposit
large amounts of antioxidants in their eggs, providing an important source of maternal effects (Blount,
Houston & Møller 2000). Antioxidants play a central role
in reproduction during embryo development and athatching (reviewed by Surai, Speake & Sparks 2001). In
particular, this period of intense growth is associatedwith increased oxidative stress, to which embryos arevery susceptible (Surai et al. 1999; Surai 2002). Female
birds allocate large amounts of lipid-soluble antioxidants,
such as carotenoids and vitamin A and E, to their eggs
compared with their circulating levels and body stores(Blount, Houston & Møller 2000), and experimental
provisioning with carotenoids has shown that the egglaying ability of female gulls is limited by carotenoid
availability (Blount et al. 2003). Finally, an extensive
study of dose rates of free-living birds in Chernobyl has
shown that residual dose rate, after accounting forbackground radiation level, is significantly explained by
the relative size of an egg (A. P. Møller, S. Gaschak & T. A.
Mousseau, unpublished data). This implies that femalesof bird species with relatively large eggs for their body size
suffer proportionately more from radiation exposure.
Fourthly, the colour of many sexual signals is basedon carotenoids. Because carotenoids can only be synthesized by algae, bacteria, fungi and plants (Fox 1979;
Brush 1981; Goodwin 1984; Latscha 1990; Stradi 1998),
higher animals must ingest them in order to produce
carotenoid-based sexual signals. Animals differ in theirrate of carotenoid absorption (Scheidt 1989) and rateof carotenoid deposition in signals (Brush & Power
1976; Hudon 1991) but also in their ability to convert
ingested carotenoids into other pigments (Fox 1979;
Goodwin 1984; Putnam 1992; Stradi 1998). Furthermore,availability of one kind of antioxidants can reduce theuse of other kinds (Møller et al. 2000; Surai 2002) andconversion between different kinds of antioxidants may
depend on the relative availability of one or more kinds(Møller et al. 2000; Surai 2002). Given that a relatively
large amount of the total body content of carotenoids
can be deposited in the plumage, we hypothesized thatcarotenoid-based plumage can affect the scarcity ofcarotenoids and other antioxidants.
The objective of this study was to investigate interspecific variation in response to spatial variation in background radiation around Chernobyl and the ecologicalfactors accounting for such interspecific variation. Morespecifically, we tested whether (i) bird species withlonger distance migrations suffer stronger declines in
population size with radiation because of the reductionsin levels of antioxidants caused by annual migrations;(ii) dispersal is associated with greater reductions inabundance during exposure to radiation; (iii) species
that produce relatively large eggs for their body size suffer
stronger declines in population size with radiation becauseof the reductions in levels of antioxidants caused bymaternal allocation to eggs; (iv) species with carotenoidbased plumage, and hence allocation of carotenoids tofeather coloration suffer greater declines in population
size with radiation because of the reductions in levels ofantioxidants caused by production of carotenoid-richplumage.
We tested these four predictions by determining
whether declines in abundance estimates of breeding
birds in relation to radiation based on results fromstandardized point counts could be accounted for by
migration distance, dispersal, relative egg mass andpresence of carotenoid-based plumage, using a data setof 57 species of birds. Finally, different species may show
similar responses to radiation as a result of the effectsof common descent rather than convergent evolution,
and we controlled for such effects by analysing the datausing standardized linear contrasts.

Materials and methods 
We used standardized point counts to census birds(Møller 1983; Bibby et al. 2005). Standard point countsof breeding birds were conducted from 29 May to 9
June 2006, with each count lasting 5 min, during whichtime all individual birds seen or heard were recorded.
Only one person performed the counts, to avoid problems of interobserver variability. The points werelocated at 100-m intervals within the Chernobyl exclusion zone, or in areas adjacent to the exclusion zone on
the southern and western borders. A total of 254 point
counts was positioned in forested areas across a range ofradiation levels spanning more than three orders ofmagnitude. Census points were not selected based onradiation level, because this was recorded when the census had already been made. The high degree of spatial
heterogeneity in background radiation level (Fig. 1;
Shestopalov 1996) ensured that the census points

4
A. P. Møller &T. A. Mousseau

Fig. 1. Locations of sampling areas in the Chernobyl area of northern Ukraine. Modified from Shestopalov (1996).

varied by more than three orders of magnitude in radiation level.
The point count method to census birds provides
highly reliable estimates of species richness and abundance, as shown by numerous methodological studies(Møller 1983; Bibby et al. 2005). We tested the reliability of our counts directly for a sample of 10 points,
with two people independently performing the counts.
To strengthen the power of this test and to ensure thatthe outcome would not be determined by greater carefulness or dedication, the second person performing
the counts was unaware of the purpose of the task andthat the counts would be used for assessing the qualityof the census. The Pearson product–moment correlation
between species richness in these two series of counts was
0·99, t = 42·06, d.f. = 8, P < 0·0001, and for abundance
it was equally high, r = 0·99, t = 12·47, d.f. = 8, P < 0·0001.

  
   
© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecology

We obtained radiation estimates from our own fieldmeasurements and cross-validated these with measurements made by the Ministry of Emergencies. We
measured α, β and γ radiation levels at ground level
directly in the field at each point where birds were censused, using a hand-held dosimeter (Model Inspector,

SE International Inc., Summertown, TN). We measured
levels two to three times at each site and averaged themeasurements. Our data were validated by correlation
with data from the government measurements publishedby Shestopalov (1996), estimated as the mid-point of
the ranges published. This analysis revealed a very 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 ourfield estimates of radiation provided the same rankingof levels of radiation among sites as the published estimates. The measurements by the Ministry of Emergencies
were obtained by repeated standardized measurementof radiation at the ground level in a large number ofdifferent localities in Ukraine. Radiation levels varyconsiderably at very short geographical distances becauseof the heterogeneity in the deposition of radiation after
the Chernobyl accident (Fig. 1; Shestopalov 1996) andour measurements at the census points ranged from0·04 to >135 mR h–1.

  
 
Bird abundance estimates can be affected by numerous
potentially confounding variables other than the actual
number of individual birds present (Møller 1983;

5
Population declines
and radiation

Bibby et al. 2005). Therefore it is crucial to control suchvariables statistically to assess the underlying relationship between radiation and abundance. We quantified
three aspects of habitat directly at each of the points(agricultural habitats with grassland or shrub, deciduous
forest, and coniferous forest estimated to the nearest
10% of ground coverage within a distance of 50 m from theobservation point). Furthermore, the maximum height oftrees was estimated to the nearest 5 m, while soil type wasrecorded as loam/clay or sand. Finally, the presence ofopen water within a distance of 50 m was recorded because
access to water can increase abund-ance of birds.
A second category of variables with an important
impact on bird censuses is weather conditions, which
can affect animal activity and hence census results(Møller 1983; Bibby et al. 2005). Therefore we recorded
three different aspects of weather at each point: (i) cloud
cover at the start of each point count (to the nearest
eighth, range 0–1 during the censuses), (ii) temperature(degrees Celsius, range 12–22 °C during the censuses)and (iii) wind force (Beaufort, range 0–4 during thecensuses). For each point count we recorded the time of
day when the count was started (to the nearest minute).
Because bird activity may show a curvilinear relationship with time of day, with high levels of activity in themorning and lower levels in the evening (Møller 1983;
Bibby et al. 2005), we also included time squared as anadditional variable.

 

a permanent breeding population, using informationin Cramp & Perrins (1977–1994). We achieved this byconsidering the distance from the mainland to allislands closer than the furthest island from the mainland,
including those that did not hold permanent populations. Therefore, the estimate of maximum dispersal
distance was a minimum estimate because many
populations on islands are not likely to have taken the
shortest route from the mainland to an island, andislands may have been colonized directly rather than byusing intermediate islands as stepping-stones.
Life history
We recorded egg mass (g), age at first reproduction,
clutch size, maximum number of clutches per season andadult survival rate from Cramp & Perrins (1977–1994).
If multiple estimates were provided, we extracted theinformation from the UK data because those estimates
were generally based on the largest sample sizes.
Body mass
We extracted mean body mass of males and females
during the breeding season from Cramp & Perrins(1977–1994), again generally preferring estimates fromthe UK because of larger sample sizes. Body mass
was estimated as the mean value of the means for males
and females.
The entire data set is reported in Appendix S1 in the
Supplementary material.

Plumage coloration
We scored the breeding plumage of all species as sexually monochromatic if males and females did not differ
in coloration according to information provided by thedescriptions in Cramp & Perrins 1977–1994), and otherwise as sexually dichromatic, separately for carotenoidand melanin-based coloration. We considered sexuallydichromatic colours that were yellow, orange and red
to be caused by carotenoids (Tella et al. 2004; Olson &Owens 2005). For melanin-based coloration we included
all colours that were brown, black or reddish brown as
typical for coloration based on phaeo- and eu-melanin(Gray 1996; Tella et al. 2004; Olson & Owens 2005).
Migration distance© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecology

We recorded the northernmost and southernmost
breeding and wintering latitude to the nearest 0·1
degrees latitude based on the distribution maps in
Cramp & Perrins (1977–1994). Migration distance was
the obvious difference in the mean of the two breeding
latitudes and the mean of the two wintering latitudes.
Dispersal distance
We estimated maximum dispersal distance as theminimum distance from the mainland to an island with  
Because of common ancestry, comparative analyses
based on species-specific data overestimate the numberof independent observations, thus increasing the risk ofstatistical type I errors (Harvey & Pagel 1991). In order
to identify evolutionary independent comparisons, weused the method of independent contrasts (Felsenstein1985) as implemented in the Macintosh-based software CAIC, using the CRUNCH algorithm (Purvis &Rambaut 1995). To do this we constructed a composite
phylogeny of all species in our database (see Fig. S1 in the
supplementary material), based on Sibley & Ahlquist(1990) and updated with recent phylogenies of a more
limited range of taxa (Blondel, Catzeflis & Perret 1996;
Slikas, Sheldon & Gill 1996; Badyaev 1997; Barker,
Barrowclough & Groth 2001). All branches were assigned
the same length, and analyses performed assuming
uneven branch lengths produced similar results. Deleting
contrasts with extreme residuals to test the robustnessof the analysis did not change the results (Purvis &Rambaut 1995). Contrasts were analysed by forcing
regressions through the origin, because the dependent
variable is expected not to have changed if there is nochange in the independent variable (Harvey & Pagel
1991). In order to weight regressions for sample size inthe analysis of contrasts, we calculated weights for each

6
A. P. Møller &T. A. Mousseau

contrast by calculating the mean sample size for the
taxa immediately subtended by that node, and logtransforming this value to achieve normality.


All analyses were made with the statistical software
JMP (SAS 2000). Radiation level, migration distance,
dispersal distance, egg mass and body mass were log10transformed, while coverage with farmland, deciduous
forest and coniferous forest was square root arcsinetransformed before analysis. For each species we used
the number of individuals at each of the 254 points as
the dependent variable and the habitat variables, weather
variables, time of day, time of day squared and radiationlevel as independent variables, using a Poisson distribution. We extracted the slope of the relationship between
abundance and radiation level from the partial regression,
and we subsequently used these slope estimates for the
57 species for further analyses. First, we estimated meanslope weighted by sample size and tested whether themean differed significantly from the null expectation ofa slope of zero (under the assumption that radiation had
no effect on abundance). Secondly, we used stepwise
regression analyses weighted by sample size to assess
whether interspecific differences in slope could be
accounted for by the potential explanatory variables.
We used stepwise regression models with a backwardelimination procedure to assess the relationship between
slope (dependent variable) and the potential predictor
variables. We used a probability of P < 0·25 for variables
to enter and P > 0·10 for variables to leave the model,
as implemented in the statistical software JMP (SAS2000). The models developed were later confirmed inforward stepwise regression models, and in no case did
the forward and backward models differ.

Table 2. Best-fit stepwise regression model weighted by sample size of the relationshipbetween slope of the relationship between abundance and background radiation level(dependent variable) and presence of carotenoid-based plumage, migration distance,
dispersal distance, egg mass and body mass. The model for species had the statistics F= 9·67, d.f. = 5, 51, r2 = 0·49, P < 0·0001, while the model for contrasts had the statistics
F = 7·77, d.f. = 4, 52, r2 = 0·12, P < 0·0001
Variable

Sum of squares

F

P

Slope (SE)Species
Carotenoid-based plumage
Migration distance
Dispersal distance
Egg mass
Body mass
Error

1·12
1·20
0·50
1·65
1·17
4·77

12·02
12·87
5·31
17·64
12·52

0·00110·00070·025
0·00010·0009–0·077 (0·022)–0·060 (0·017)–0·032 (0·014)–0·295 (0·070)
0·169 (0·048)© 2007 The Authors.
Contrasts
Journalcompilation
Carotenoid-based
plumage©
2007 British
Dispersal distance
Ecological Society,
Egg mass
Journal of Applied
Body mass
Ecology
Error

0·011
0·011
0·003
0·004
0·052

11·39
11·23
3·27
4·28

0·00140·00150·077
0·044–0·069 (0·021)–0·040 (0·012)–0·172 (0·095)
0·145 (0·070)

Fig. 2. Slopes of the relationship between abundance andbackground radiation level for 57 breeding bird species near
Chernobyl, Ukraine.

Table 1. Model of the relationship between abundance at 254
points in relation to background level of radiation, species
and radiation by species interaction. The model had thestatistics F = 60·47, d.f. = 113, 14364, r2 = 0·32, P < 0·0001
VariableF

P

Slope (SE)Radiation
SpeciesRadiation × species

151·61107·7011·63< 0·0001< 0·0001< 0·0001–0·028 (0·002)

Results
We recorded a total of 1570 individuals of 57 species
during the censuses of the forested areas around
Chernobyl (and thus no species was excluded fromthe subsequent analyses). The slope of abundance inrelation to radiation ranged from –0·25 to 0·11, with amean weighted by sample size of –0·022 (SE = 0·008)
that differed significantly from zero (one-sample t-test,
t = 2·90, d.f. = 56, P < 0·0001). Eighteen of the 57 slopes
were statistically significant, compared with the 2·85 thatwould be expected by chance. Thirteen of these significant slopes were negative, while only five were positive.
There was considerable variation among species in slopeof the relationship between abundance and radiationlevel (Fig. 2). In fact, a model revealed a significant
relationship between abundance and radiation, an
important effect of species and significant heterogeneity
in response to radiation among species (Table 1). The
significant heterogeneity implied that species responded
differently in terms of abundance to radiation.
Interspecific variation in the effect of radiation onabundance was further analysed in a stepwise modelthat weighted the slope of each species by sample size toaccount for differences in sampling effort. The best-fit
stepwise overall model included five variables andaccounted for almost half of the variance (Table 2).
First, species with carotenoid-based plumage coloration had stronger decreases in abundance as a result ofradiation than other species (Fig. 3a and Table 2). Thisfactor accounted for 10% of the variance. Secondly,
migratory bird species showed stronger decreases inabundance with radiation than resident species (Fig. 3b
and Table 2), accounting for 11% of the variance. Thirdly,
dispersal distance accounted for 4% of the variance inslope of the relationship between abundance and radiation (Fig. 3c and Table 2), implying that species withlong dispersal distances suffered the strongest declines
associated with radiation. Fourthly, large relative egg
mass was associated with stronger declines in abundanceassociated with radiation (Fig. 3d and Table 2), accounting for 15% of the variance. Finally, bird species withlarge body mass suffered less from the effects of radiation on abundance (Fig. 3c and Table 2), accountingfor 10% of the variance. Melanin-based plumage and arange of other life-history traits, such as adult survivalrate, age at first reproduction, clutch size, number ofclutches, incubation period, nestling period and annual
fecundity, did not enter the model. An analysis ofstandardized linear contrasts revealed a model that
included carotenoid-based plumage, dispersal distanceand body mass as significant predictors of slope(Table 2). The effects for egg mass and migration
distance did not reach statistical significance, implyingthat the relationships for these two variables in theanalyses of species-specific data were the result ofsimilarity in response among species because of theeffects of common descent.

7
Population declines
and radiation

Discussion© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
EcologyFig. 3. Population trends of different species of breeding
birds near Chernobyl, Ukraine, in relation to (a) presence orabsence of carotenoid-based plumage, (b) migration distance(degree latitude), (c) dispersal distance (km) and (d) relative
egg mass (g), after adjusting for body mass. All relationships
are based on species-specific data, while the phylogeneticallycontrolled analyses are reported in Table 2. All independent
variables were expressed as residuals after adjusting for thethree other independent variables, although this was only
done for illustrative purposes. The full analysis is reported inTable 2.

The main findings of this study were that (i) bird species
differed in their response to radiation from Chernobyl
but with, on average, a decrease in population densitywith increasing level of background radiation, and(ii) the strongest declines in population density withradiation level were documented for species withcarotenoid-based plumage, long-distance migrationand dispersal, and large eggs for their body size. Allfour of these factors are associated with antioxidant
levels, suggesting that reduced antioxidant levels may
precipitate population declines when species are exposed
to radiation. A phylogenetic analysis of standardized
linear contrasts confirmed the significant effects ofcarotenoid-based plumage and dispersal distance. We will
briefly discuss the evidence linking these four factors toantioxidants and radiation.
Point counts provide robust estimates of abundanceof birds because of their clearly defined procedures,simple assumptions and ability to record a wide rangeof species (Møller 1983; Bibby et al. 2005). All 254 points
used for the censuses were assessed for the presence andabundance of all 57 species of birds, making comparisons among species feasible. Although it is well known
that bird species differ in their detection probability
because of differences in behaviour and conspicuousness(Møller 1983; Bibby et al. 2005), such differences
should be similar among census locations, rendering
estimates of the relationship between abundance andradiation unbiased. The overall abundance of species
across all 254 points ranged from one to 369 individuals,

8
A. P. Møller &T. A. Mousseau© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecologycausing heterogeneity in sampling effort among species.
We took that fact into account by weighting the slopeof the relationship between abundance and radiation
by number of individuals recorded, thereby placing
more weight on species with many individuals. We believethat this provided a sound, stringent and coherent
way of analysing the effect of radiation on abundanceof different species of birds.
Carotenoid-based coloration is common in numerous
animals, including birds. Because animals cannot synthesize carotenoids, any carotenoids used for coloration or
physiological processes must be ingested (Fox 1979;
Brush 1981; Goodwin 1984; Latscha 1990; Stradi 1998).
In contrast, animals can produce other kinds of colour,
such as those based on melanins and structure (Fox
1979; Brush 1981; Goodwin 1984; Stradi 1998). Birds
with carotenoid-based plumage allocate large amountsof carotenoids to coloration, potentially facing a tradeoff with other uses of carotenoids (reviewed by Møller
et al. 2000). We found that bird species with carotenoidbased plumage colour, but not those with melanin-based
colour, suffered the strongest declines in abundancewith increasing levels of radiation. This finding suggeststhat something specific to carotenoids accounts for thedifference in relationships between the two kinds ofcoloration and the effect of radiation on abundance.
We have suggested that the simplest explanation is thatbirds in highly contaminated areas suffer from a deficiency of antioxidants, including carotenoids. Use of
carotenoids for plumage coloration may further reducelevels of antioxidants, with the consequence that suchspecies experience the strongest declines in abundance.
Previous studies of barn swallows from Chernobyl haveshown circulating and stored levels of antioxidants,
including carotenoids, to be suppressed by up to morethan half of their levels in uncontaminated control
areas (Møller, Surai & Mousseau 2005), and this hasconsequences for the plumage coloration of migratorybarn swallows developed several months after leaving
the breeding grounds (Camplani, Saino & Møller 1999).
A difference in antioxidant levels between contaminatedand control areas may arise from a difference in use ofantioxidants, availability or both. Given that there wasa sex difference in liver carotenoid levels, but not in levelsof other antioxidants, between Chernobyl and control
areas (Møller, Surai & Mousseau 2005), we suggest that thealternative explanation, that availability differs amongareas, is less likely. If availability had differed, we would
expect a difference in antioxidant levels of both sexes.
Both migration distance and dispersal distance independently explained variation in population size of
breeding birds with level of radiation, although only
dispersal distance remained a significant predictor inanalyses of standardized linear contrasts. Møller et al.
(2006) analysed source–sink dynamics of barn swallows
in Ukraine before and after the Chernobyl disaster.
Because rates of reproduction and adult survival ofbarn swallows in contaminated areas do not allow themaintenance of a stable population (Møller et al. 2005),

the population can only be maintained by immigrationfrom source populations from neighbouring areas thatare not contaminated. Consistent with this scenario,
Møller et al. (2006) found that the variance in stable
isotope profiles increased significantly for birds from
Chernobyl after the disaster in 1986, while there was nodifference between Chernobyl and the control areas
before 1986. These findings suggest that Chernobyl
populations after 1986 contain more individuals thathave immigrated from far away than the same population before 1986. Such a difference is not present inuncontaminated control populations. These differences
may arise from the source–sink dynamics of the populations, as suggested by Møller et al. (2006). Dispersal
may be costly for different reasons, but first and foremost because an individual enters a novel site where
enemies including parasites are unknown. The ability
to fend off parasites will depend on the ability to produce efficient immune responses to novel antigens(Møller & Erritzøe 2001), and this ability will dependon the availability of immunostimulants such as carotenoids (Møller et al. 2000) but also antioxidants suchas carotenoids and vitamins A and E (Møller et al.
2000). Such biochemicals are in short supply in the
Chernobyl region (Møller, Surai & Mousseau 2005;
A. P. Møller et al., unpublished data), suggesting that
any individual from Chernobyl will be at a selective disadvantage during dispersal. The negative relationshipbetween susceptibility to radiation and dispersal distance
may arise as a consequence of this effect.
Bird eggs contain large amounts of antioxidants
such as vitamin A and E, but also carotenoids that giveegg yolks their characteristic colour (Blount, Houston& Møller 2000). Such antioxidants of maternal origin
provide important protection against free radicals ofdeveloping embryos before, during and after hatching(Surai, Speake & Sparks 2001; Surai 2002). We foundthat the relative egg mass of different bird species
accounted for a significant amount of interspecific variation in the relationship between abundance and levelof radiation, although that effect did not reach the levelof statistical significance in a phylogenetic analysis ofstandardized linear contrasts. In contrast, there was no
similar effect observed for age at first reproduction,
clutch size, maximum number of clutches per year or
adult survival rate. Therefore something specific about
relative egg mass, reflecting the rate of production ofeggs, rather than the total production of eggs, as reflectedby clutch size or the total number of clutches produced
per year, accounts for this observation. Birds typicallyinvest large amounts of antioxidants into egg production, with the total amount of antioxidants allocated tothe eggs of a clutch exceeding the total body store ofthese biochemicals several times (Blount et al. 2003;
Biard, Surai & Møller 2006). Thus females have to ingest
sufficient amounts of high-quality food to be able toproduce eggs with normal levels of antioxidants. Iflevels of circulating and stored antioxidants are severely
depressed in birds exposed to radiation, as shown for9Population declines
and radiation© 2007 The Authors.
Journal compilation© 2007 British
Ecological Society,
Journal of Applied
Ecology

the barn swallow (Møller, Surai & Mousseau 2005),
production of relatively large eggs for a given body size
will impose even greater restrictions on antioxidant
availability. For example, Blount et al. (2003) showed thataccess to carotenoids by gulls, even in uncontaminatedareas, improved egg-laying ability and, by implication,
female birds in heavily contaminated areas will suffer
even greater carotenoid depletion, especially if laying
relatively large eggs for their body size.
Body mass predicted decline in abundance as a resultof radiation, with large-sized species showing smaller
declines than small species. Small species of birds haverelatively higher rates of metabolism than large species(Schmidt-Nielsen 1984), implying greater productionof free radicals during ordinary metabolism. Relatively
smaller storage of antioxidants by small species willrender such species more susceptible to the effects ofantioxidant shortage, particularly if encountering radiation levels that will increase the use of antioxidants.
Furthermore, large species generally have much greater
home ranges than smaller species, and this implies thatlarge species will encounter a greater heterogeneity inlevels of radiation than small species. Given that there
is enormous heterogeneity in levels of radiation around
Chernobyl (Shestopalov 1996), large species will more
often have relatively uncontaminated areas within theirhome range than small species.
The slight differences in conclusions from analysesof species-specific data and standardized linear contrasts
merit some discussion. For example, we found that
migration distance explained interspecific variation in
the relationship between abundance and backgroundradiation level, while that was not the case in an analysis of contrasts (Table 2). This implies that migratory
birds, in particular long-distance migrants, showed thestrongest declines in abundance with increasing levelsof radiation. However, the analysis of contrasts revealed
that this relationship was not caused by evolutionary
differences in migration distance among taxa, but by
specific clades having long-distance migration anddeclines in population size with increasing level ofradiation. This implies that migration distance is indeed
a predictor of susceptibility to radiation, albeit not an
evolutionary one.
There are several implications of this study. First, we
would expect individuals of bird species with carotenoidbased plumage to have paler plumage colour in Chernobyl
than individuals from control sites in Ukraine. Secondly,
we would predict species of birds with long-distancedispersal to have severely depleted antioxidant levels in
Chernobyl, but not in control sites, after the period
when antioxidant levels are usually replenished for
migrants. Thirdly, we would expect antioxidant levelsof eggs laid by birds in Chernobyl to be reduced compared with eggs from control sites. Indeed, Møller,
Surai & Mousseau (2005) found dramatically reduced
antioxidant levels in barn swallow eggs from Chernobyl.
Alternatively, because antioxidant availability can limit
egg production in birds (Blount et al. 2003), we suggestthat a reduction in egg size is one way by which birds
from highly contaminated areas can maintain clutch
size at a lower availability of antioxidants. Another way
is to reduce clutch size, as already reported for the barnswallow from Chernobyl (Møller et al. 2005).
While the present study has implications for the
study of animals living in radioactively contaminatedareas such as Chernobyl and several test sites used for
exploding nuclear bombs, it may also have important
implications for animals elsewhere. There is large
variation in natural levels of radioactivity as a result ofvariation in abundance of radioactive isotopes, mainly
in mountain regions where the underlying rock reaches
the surface. There are no studies of the biological consequences of such variation in natural levels of radioactivity, but we suggest that some of the consequences
can be predicted from the present study.
In conclusion, we have shown that bird species areaffected by radiation to a different extent, as reflectedby their relationship between abundance and the levelof radiation. Different characteristics of birds linked tothe use of antioxidants accounted for this variation:
carotenoid-based plumage, dispersal distance and, tosome extent, egg mass. These findings suggest that antioxidants play a key role in determining interspecificvariation in the ecological consequences of radiation.

Acknowledgements
We gratefully acknowledge logistic support and help in
Ukraine by I. Chizhevsky, G. Milinevski, G. Rudolfsen,
S. Rushkovsky and N. Saino. A. Peklo kindly provided
information on birds. We gratefully acknowledge
support from the National Geographic Society, the US
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.

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Supplementary material
The following supplementary material is available forthis article.
Appendix S1. Information on slope of the relationshipbetween abundance and radiation, total abundance,
dispersal distance, migration distance, carotenoid- andmelanin-based coloration, egg mass, and body mass of
57 species of breeding birds from forests near Chernobyl.
Fig. S1. Phylogenetic relationships among species
breeding in the Chernobyl region and used for analyses
of factors predicting the association between abundance and level of background radiation.
This material is available as part of the online article from:http://www.blackwell-synergy.com/doi/full/
10.1111/j.1365-2656.2007.01353.x.
Please note: Blackwell Publishing is not responsible forthe content or functionality of any supplementarymaterials supplied by the authors. Any queries (otherthan missing material) should be directed to the corresponding author for the article.