Since 1990, we have collected information suggestinga reduced and continuously declining abundance ofbirds in the most contaminated areas. This prompted
us to conduct standard censuses in relation to local
levels of radiation.
During May to June 2006, we censused breeding
birds using standard point count census (Møller 1983;
Bibby et al. 2005), while simultaneously recordinglevels of background radiation at these forest sites.
Species richness and abundance of animals can beaffected by numerous environmental factors otherthan radiation, and, therefore, we controlled statistically for a range of potentially confounding variables
that could affect our assessment of the relationshipbetween species richness and abundance of animals
and the level of background radiation by including
variables reflecting habitat, soil type, weather andseveral other factors in the statistical models. Most
radiation around Chernobyl is currently in the topmost layer of the soil (Shestopalov 1996; EuropeanUnion 1998), where soil invertebrates are abundant.
Therefore, we predicted that the abundance of bird
species eating soil invertebrates would be particularly
depressed in the most contaminated areas.

Biol. Lett. (2007) 3, 483–486
doi:10.1098/rsbl.2007.0226
Published online 14 August 2007

Community ecology

Species richness andabundance of forest birds
in relation to radiation
at Chernobyl
A. P. Møller1,* and T. A. Mousseau2
1
Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université
Pierre et Marie Curie, Bâtiment A, 7ème étage, 7 quai St Bernard,
Case 237, 75252 Paris Cedex 05, France2
Department of Biological Sciences, University of South Carolina,
Columbia, SC 29208, USA*Author for correspondence (amoller@snv.jussieu.fr).

The effects of low-level radiation on the abundance of animals are poorly known, as are theeffects on ecosystems and their functioning.
Recent conclusions from the UN Chernobyl
forum and reports in the popular media concerning the effects of radiation from Chernobylon animals have left the impression that theChernobyl exclusion zone is a thriving ecosystem, filled with an increasing number of rarespecies. Surprisingly, there are no standardized
censuses of common animals in relation toradiation, leaving the question about the ecological effects of radiation unresolved. We conducted standardized point counts of breeding
birds at forest sites around Chernobyl differingin level of background radiation by over threeorders of magnitude. Species richness, abundance and population density of breeding birds
decreased with increasing level of radiation,even after controlling statistically for the effects
of potentially confounding factors such as soil
type, habitat and height of the vegetation. Thiseffect was differential for birds eating soil invertebrates living in the most contaminated top soil
layer. These results imply that the ecologicaleffects of Chernobyl on animals are considerably
greater than previously assumed.

2. MATERIAL AND METHODSAPM (wearing a radiation protection suit) conducted standard
point counts during 29 May to 9 June 2006, with each countlasting 5 min during which all bird species seen or heard wererecorded (Møller 1983; Bibby et al. 2005). The census was
conducted within the Chernobyl exclusion zone with a permit fromthe Ukrainian authorities. Two hundred and fifty-four points werelocated at a distance of approximately 100 m intervals within
forested areas (excluding successional stages of secondary forest
due to abandoned farming (these areas are still almost exclusively
open grassland)) of the Chernobyl exclusion zone or in areas
adjacent to the southern and western borders.
Point counts of birds provide highly reliable estimates of species
richness and abundance (Møller 1983; Bibby et al. 2005). We
directly tested the reliability of our counts for a sample of 10 points
where two persons performed the counts. The second person
performing the counts was unaware of the purpose of his counts.
The Pearson product–moment correlation between species richness
in these two series of counts was rZ0.99, tZ42.06, d.f.Z8,
p!0.0001, and for abundance it was equally high: rZ0.99,tZ12.47, d.f.Z8, p!0.0001. Species eating soil invertebrates weredistinguished from all other species (table 1 in the electronic
supplementary material).

Keywords: census; ecosystem effects;
population density; radiation at Chernobyl;
species richness(a) Confounding variables
Bird abundance estimates can be affected by numerous potentiallyconfounding variables (Møller 1983; Bibby et al. 2005), and,
therefore, it is crucial to control such variables statistically to assessthe underlying relationship between radiation and animal species
richness or abundance. We quantified habitat (agricultural habitats
with grassland or shrub (either currently or previously cultivated),
deciduous forest or coniferous forest estimated to the nearest 10%of ground coverage within a distance of 50 m from the observation
point). Agricultural habitat thus also controlled statistically for any
effects of edge habitat. Maximum height of trees was estimated to
the nearest 5 m, and soil type was recorded as loam/clay or sand.
The presence of open water within a distance of 50 m was also
recorded. Weather conditions can affect animal activity and hence
census results (Møller 1983; Bibby et al. 2005), and we recorded
cloud cover at the start of each point count (to the nearest eighth,range 0–1 during the censuses), temperature (degree Celsius, range12–22oC) and wind force (Beaufort, range 0–4 during the censuses). For each point count, we recorded time of day when thecount was started (to the nearest minute). Since bird activity may
show a curvilinear relationship with time of day, with high levels ofactivity in the morning and to a lesser extent in the evening (Møller1983; Bibby et al. 2005), we also included time squared as anadditional variable.

1. INTRODUCTION
The ecological consequences of radiation from theChernobyl catastrophe are poorly known (Zakharov &Krysanov 1996; Møller & Mousseau 2006). Without
scientific justification, the Chernobyl exclusion zone
has been promoted as a thriving ecosystem with anumber of uncommon species having appeared inincreasing numbers in recent years (Chernobyl Forum2005a,b; Mycio 2005; Rosenthal 2005; Stephan 2005;
UN Chernobyl Forum Expert Group 2005).
Surprisingly, there are little data on how theabundance of animals varies with levels of radiation,and there has been no effort to census animals in
relation to local levels of radiation around Chernobyl.
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2007.0226 or via http://www.journals.royalsoc.ac.uk.
Received 26 April 2007
Accepted 2 July 2007

483

This journal is q 2007 The Royal Society

484

A. P. Møller & T. A. Mousseau

Birds in Chernobyl

78291
635kBq m–2 1Cikm–22410 2010 km

40 100 185 555 1480

0.027 0.054 0.1 0.27 0.54 1.08 2.7515404Figure 1. Locations of census areas in the Chernobyl area of northern Ukraine: (1) Bobor, (2) Chernobyl, (3) Dytiaku, (4)Ivankov, (5) Mikhivshchyna, (6) Pisky, (7) Red Forest, (8) Vesniane and (9) Yasen. Adapted from Shestopalov (1996).
(b) Measuring background radiation levels
We obtained radiation estimates from our measurements and crossvalidated these with measurements by the Ministry of Emergencies.
We measured a, b and g radiation at ground level directly at eachpoint where we censused birds using a handheld dosimeter (Model:Inspector, SE International, Inc., Summertown, TN, USA). We
measured levels several (2–3) times at each site and averaged themeasurements. Our data were validated with correlation against datafrom the governmental measurements published by Shestopalov(1996), estimated as the midpoint of the ranges published. This
analysis revealed a strong positive relationship (linear regression onlog–log transformed data: F1,252Z1546.49, r2Z0.86, p!0.0001,
slope (s.e.)Z1.28 (0.10)), suggesting that our estimates of radiation
provided the same ranking of levels of radiation as did publishedestimates. The measurements by the Ministry of Emergencies wereobtained by repeated standardized measurement of radiation at theground level in a large number of different localities in Ukraine.
Radiation levels vary considerably at very short geographicaldistances due to heterogeneity in the deposition of radiation after theChernobyl accident (figure 1; Shestopalov 1996). Our measurements at the census points ranged from 0.04 to 135.89 mR hK1.
(c) Statistical methods
Radiation level was log10-transformed, while coverage with farmland, deciduous forest and coniferous forest was square-root
arcsine-transformed. We also included radiation level squared toaccount for nonlinear relationships between species richness andabundance and radiation. We developed best-fit statistical models
to assess the relationship between species richness and abundance(dependent variables) and radiation, assuming a Poisson distribution, after inclusion of the potentially confounding variables, as
implemented in the statistical software JMP (SAS Institute 2000).
Population density was analysed using abundance as the dependent
variable, with species richness as an additional independentvariable. Model selection was based on Akaike’s information
criterion (AIC), using the criterion of delta AIC!2.00 for theexclusion of variables (Burnham & Anderson 2002).
The frequency distribution of the counts of birds was skewed,
with a disproportionate number of zeros. Therefore, we repeatedthe analyses using Kendall rank–order correlation and partial
Biol. Lett. (2007)

rank–order correlation (controlling for the confounding variables intable 2 in the electronic supplementary material), and the conclusions remained unchanged (electronic supplementary material).

3. RESULTS
We recorded 1570 individuals representing 57 speciesof birds (see table 1 in the electronic supplementarymaterial). Species richness of birds was reduced bymore than half when comparing sites with the highest
and normal background level of radiation within thestudy areas (figure 2a). In addition, there wereindependent effects of time of day and habitat on thenumber of species recorded (table 2 in the electronic
supplementary material). Total abundance of all
species decreased by almost two-thirds between sites
with the highest levels and the normal backgroundlevels of radiation within the study areas (figure 2b;table 2 in the electronic supplementary material).
The effect of radiation level remained after controlling
statistically for the effects of time of day, weather andfarmland habitat (table 2 in the electronic supplementary material). Finally, population density ofbirds, defined as total abundance of all species
divided by species richness, decreased significantlywith increasing radiation level (figure 2c; table 2 inthe electronic supplementary material).
The abundance of bird species eating soil invertebrates decreased considerably with radiation level(figure 2b; F1,252Z115.76, r2Z0.31, p!0.0001, slope(s.e.)ZK0.114 (0.011)). In contrast, there was no
significant relationship between the abundance of theBirds in Chernobyl(a)8

no. of species

64

20(b) 10soil invertebrates

abundance

8others

64
20

population density(c) 1.8
1.6
1.4
1.2
1.0
0.005 0.05 0.5 5.0 50
radiation (mR h–1)

500

Figure 2. (a) Mean species richness (s.e.) of birds, (b) meanabundance (s.e.) of birds and (c) mean (s.e.) population
density of birds in relation to background radiation level(mR hK1) for forested locations around Chernobyl. The
partial effects for radiation were (a) F1,249Z55.63, r 2Z
0.18, p!0.0001, (b) F1,247Z62.07, r 2Z0.20, p!0.0001
and (c) F1,246Z51.88, r 2Z0.17, p!0.0001.

remaining species and radiation (F1,252Z1.53, r 2Z
0.006, pZ0.22, slope (s.e.)ZK0.014 (0.013)). A
similar conclusion was reached when the potentiallyconfounding variables reflecting weather, habitat andtime of day were included.

4. DISCUSSION
Species richness of birds in forests around Chernobyl
decreased by more than 50% with increasing level ofradiation, and this effect was independent of potentially confounding factors such as time of day, weather,soil type, age of tree stands and habitat. Abundance ofbirds decreased by 66% between the most contaminated sites and sites with normal background radiation(within the study areas). These results are the first
census data reported from Chernobyl, and they
indicate dramatic effects on species richness andBiol. Lett. (2007)

A. P. Møller & T. A. Mousseau

485

abundance of birds that play important roles inecosystem functioning.
We found strong declines in species richness,abundance and population density of birds associatedwith elevated levels of background radiation near
Chernobyl. The conclusions were similar when basedon parametric or non-parametric analyses, controllingfor potentially confounding variables. We had relatively few observations in the range of 1–10 mR hK1(figure 2). However, the negative relationships wereprominent both among data points with a radiationlevel below and above 5 mR hK1 (figure 2), showingthat even radiation levels below 5 mR hK1 were associated with reduced abundance. Most radiation around
Chernobyl is currently in the topmost layer of the soil
(Shestopalov 1996; European Union 1998), where soil
invertebrates live. Bird species consuming soil invertebrates decreased in abundance more strongly thanother species, suggesting that radiation had differential
effects on specific functional ecological groups.
We suggest three mechanisms underlying theseobserved patterns of species richness and abundance ofbirds in relation to level of radiation. First, radiation
may directly reduce survival rates and fecundity,
thereby causing extinction or reducing population sizes,
as shown previously for the barn swallow Hirundo
rustica (Møller et al. 2005). Second, birds may avoid
radioactively contaminated areas because such areas aresuboptimal habitats for birds (Møller & Mousseau2007). Third, birds may be less abundant and species
richness may be reduced in contaminated areas owing
to reduced abundance of invertebrates that constitutethe most common food of many species.
We have previously demonstrated significant
negative impacts of Chernobyl-related fallout on barnswallow mutation rates, survival and reproduction(Møller 1983; Ellegren et al. 1997; Møller et al. 2005).
Here, we extend our observations to document extensive reductions in the species richness, abundance andpopulation density of birds in general with increasinglevels of radiation around Chernobyl. These effects arelikely to have important implications for other parts ofthe ecosystem and for overall ecosystem functioning.
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 University ofSouth Carolina Environmental Research Initiative Committee(ERIC), the University of South Carolina School of theEnvironment, the National Geographic Society and theSamuel Freeman Charitable Trust.

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