Ecological Indicators 11 (2011) 424–430

Contents lists available at ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original article

Efﬁciency of bio-indicators for low-level radiation under ﬁeld conditions
Anders Pape Møller a,b,∗ , Timothy A. Mousseau caLaboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, FranceCenter for Advanced Study, Drammensveien 78, NO-0271 Oslo, Norwayc
Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USAba r t i c l e

i n f oArticle history:
Received 5 January 2010
Received in revised form 15 June 2010
Accepted 23 June 2010
Keywords:
Bio-indicators
Chernobyl
Low-level radiation
Radiation
Radioactive contaminationa b s t r a c t
Relatively little is known about biological consequences of natural variation in background radiation, andvariation in exposure due to nuclear accidents, or even the long term consequences to human health stemming from the over-use of nuclear medicine and imaging technologies (i.e. CAT scans). This realizationemphasizes the need for assessment and quantiﬁcation of biological effects of radiation on living organisms. Here we report the results of an environmental analysis based on extensive censuses of abundanceof nine animal taxa (spiders, dragonﬂies, grasshoppers, bumblebees, butterﬂies, amphibians, reptiles,
birds, mammals) around Chernobyl in Ukraine and Belarus during 2006–2009. Background levels of radiation explained 1.5–26.5% of the variance in abundance of these nine taxa, birds and mammals having
the strongest effects, accounting for a difference of a factor 18 among taxa. These effects were retainedin analyses that accounted for potentially confounding effects. Effect size estimated as the amount ofvariance in abundance explained by background level of radiation was highly consistent among years,
with weaker effects in years with low density. Effect sizes were greater in taxa with longer natal dispersal
distances and in taxa with higher population density. These results are consistent with the hypotheses
that costs of dispersal (i.e. survival) were accentuated under conditions of radioactive contamination, orthat high density allowed detection of radiation effects. This suggests that standard breeding bird censuses can be used as an informative bio-indicator for the effects of radiation on abundance of animals.
© 2010 Elsevier Ltd. All rights reserved.

1. Introduction
The biological consequences of natural variation in backgroundradiation levels remain largely unexplored. The average annual
worldwide radiation dose is around 2.4 mSv, with a typical range
of 1–10 mSv (IAEA, 2006), although variation in background radiation levels varies by more than a factor ten across depending on
composition of the underground rock. This variation is associatedwith signiﬁcant incidence of cancer and cancer-related mortality
in humans (e.g. Lubin and Boice, 1997), testifying to the fact that
there may be signiﬁcant impacts of natural variation in radiation
across living beings (e.g. Heidenreich et al., 2000; Moiseev et al.,
1973; Pimentel et al., 2003).
Numerous radiation accidents have taken place or beenreported, with the total number of radioactive releases worldwide
being counted in the hundreds. Although most of these incidents
have been minor, more than ten have released large amounts of∗ Corresponding author at: Laboratoire d’Ecologie, Systématique et Evolution,
CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, France.
Tel.: +33 1 69 15 56 88; fax: +33 1 69 15 56 96.
E-mail address: anders.moller@u-psud.fr (A.P. Møller).
1470-160X/$ – see front matter © 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecolind.2010.06.013

radioactive material. These include at least three in the former
Soviet Union, Three Mile Island in the US and nuclear test sites
in the US, Russia, Algeria, China, India, Australia, and the Paciﬁc. To
date, the single largest radiation accident is that at Chernobyl on
26 April 1986 that resulted in the emission of at least 9.35 × 103
to 1.25 × 104 peta-Becquerels to the environment (Yablokov et al.,2009). The most important isotopes and their half-lives were iodine(131 I, 8 days), strontium (90 Sr, 29 years), cesium (137 Cesium, 30
years) and plutonium (239 Pu, 24,110 years). Coincidentally, the soilsof northern Ukraine have some of the lowest levels of natural background radiation in the world at around 0.02–0.03 ␮Sv/h (Ramzaev
et al., 2006) making the Chernobyl fallout particularly apparent inthis part of the world, but also making the consequences particularly severe due to lack of adaptation to background radiation.
Given our generally poor knowledge of the effects of these twocauses of radiation on the biota there has been surprisingly little
study of the biological consequences (Møller and Mousseau, 2006,
2008, 2009). The notion that low-level radiation has an effect on
the abundance or performance of animals is controversial due tothe difﬁculty of extrapolating from high level to low-level exposure (e.g. Chadwick et al., 2003; Moss et al., 2006; Tubiana et al.,2006), as are the effects of low-level radiation on disease including
cancer (e.g. Brenner et al., 2003; Prasad et al., 2004). For example,

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

exposure to chronic and acute radiation has different effects (e.g.
Wickliffe et al., 2003). Numerous laboratory studies have investigated effects of radiation on model systems including cell cultures(e.g. Chadwick et al., 2003; Liang et al., 2007; Sykes et al., 2006).
Laboratory model systems traditionally utilize controlled environmental conditions, but also providing benign and ad libitum
access to food and other resources. In contrast, ﬁeld assessmentof biological effects of low-level radiation relies on the fact thatenvironmental conditions in the ﬁeld typically are sub-optimal interms of food, predation risk, and risk of parasitism, and animals
typically have to work hard to meet their requirements (review in
Møller et al., 1998). For example, carotenoids and other antioxidants are typically limiting under ﬁeld conditions (e.g. Møller etal., 2000), with important consequences for free radical scavenging
and ultimately for damage to DNA and other biologically signiﬁcantmolecules (e.g. Halliwell and Gutteridge, 1999; Lefﬂer, 1993). Radiation increases the level of oxidative stress (e.g. Bonisoli-Alquati etal., 2010a,b; Bazhan, 1998; Ben-Amotz et al., 1998; Chaialo et al.,
1991; Ivaniota et al., 1998; Kumerova et al., 2000; Lykholat andChernaya, 1999; Neyfakh et al., 1998a,b). Thus, species that use
antioxidants for biological needs other than free radical scavenging caused by radiation such as deposition in eggs and plumage
and use during migration and dispersal have been found to suffer
the most from elevated levels of background radiation (Møller andMousseau, 2007b). Several studies have indicated that the presenceof high levels of carotenoids may reduce mutation rates (reviews in
Ferguson, 1994; Krinsky and Denek, 1982; Møller et al., 2000; Sies,
1993; Valko et al., 2004). We might also consider that mildly deleterious mutations will have benign effects under lab conditions,but more serious consequences under adverse environmental conditions. This line of argument suggests that biologically relevant
estimates of effects of low-level radiation are best obtained fromfree-living organisms under natural environmental conditions. This
also raises the possibility of using standard census techniques (e.g.
Voříšek et al., 2010) for assessment of effects of low-level radiation
on free-living organisms.
The primary objective of this study was to identify biological indicator(s) of background radiation level. To this end we
conducted extensive ﬁeld censuses of nine different animal taxa
in the surroundings of Chernobyl in Belarus and Ukraine during
2006–2009, with some of these results already having been published. Because many different biotic and abiotic environmental
factors can affect census results, we also recorded biotic and abiotic
factors known to potentially inﬂuence census results and enteredthese into statistical models describing the relationship between
abundance and level of background radiation. A second objective
was to test the repeatability of radiation effects on abundance
among years. A third objective was to test the extent to which natal
dispersal and mean population density affected the relationshipbetween radiation and abundance. Three possible scenarios were
set out a priori for dispersal: Either dispersal may bring immigrants
to suitable habitat with low population density thereby obscuring
any relationship between radiation and abundance or, dispersal
may permit individuals to escape locally deleterious conditions.
Alternatively, dispersal may be costly in terms of production offree radicals from physical activity and/or from immune response
to novel antigens (Møller and Mousseau, 2007b). Similar effects
have been reported in many other taxa (Møller et al., 2000). Given
that antioxidants used for neutralizing free radicals may be used
to eliminate the negative effects of radiation on general healthand on mutations in particular (e.g. Bazhan, 1998; Ben-Amotz etal., 1998; Chaialo et al., 1991; Ivaniota et al., 1998; Kumerova etal., 2000; Lykholat and Chernaya, 1999; Neyfakh et al., 1998a,b;
Bonisoli-Alquati et al., 2010b), taxa with long-distance dispersal are
predicted to suffer more from such costs (i.e. antioxidant limitation)
than taxa with short dispersal distances. Low levels of abundance

425

Fig. 1. Location of census areas and levels of background radiation around Chernobyl. Partly developed from European Union (1998).

will invariably prevent detection of strong effects for statisticalreasons because small mean values generally are associated withsmall variances. Therefore, it is crucial to include data for several
years to ensure that the abundance estimates exceed low meanabundances.
2. Methods
2.1. Study sites
APM (wearing a radiation protection suit in the most contaminated areas) conducted standard point counts during 29 May–9
June 2006, 1–11 June 2007, 29 May–5 June 2008 and 1–6 June
2009, with each count lasting 5 min during which the number of
spider webs, and the number of individual grasshoppers, dragonﬂies, bumblebees, butterﬂies, amphibians, reptiles and birds seenor heard were recorded (Møller, 1983; Bibby et al., 2005). The
census was conducted within the Chernobyl Exclusion Zone or inareas adjacent on the southern and western borders with a permit from the Ukrainian authorities and in areas in southern Belarus
around Gomel (breeding seasons 2006–2009) (Fig. 1). A total of
254 points (breeding season 2006), 235 points (breeding season
2007), 237 points (breeding season 2008) and 159 points (breeding season 2009) were located at ca. 100 m intervals within forested
areas (excluding successional stages of secondary forest due toabandoned farming (these areas are still almost exclusively open
grassland)). All sampling sites were identiﬁed using GPS coordinates, and samples for 159 sites were recorded in all four years.
We censused birds at the end of May and the beginning of June
when most individuals reach their annual maximum of singing
activity, making censuses of breeding birds highly reliable (Voříšek
et al., 2010). We directly tested the reliability of our counts byletting two persons independently perform counts. The degree

426

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

of consistency was high for both species richness and abundance(details reported by Møller and Mousseau, 2007a).
Mammal censuses were conducted using 161 line transects eachwith a length of 100 m along roads in a large number of areas in
the Chernobyl exclusion zone and just outside the zone during
3–4 February 2009. Mammals were identiﬁed from footprints infresh snow using a standard ﬁeld guide (Bang et al., 2007). To avoid
counting the same individual repeatedly we only counted the minimum number of individuals recorded simultaneously. For example,
if the tracks of a fox Vulpes vulpes crossed the transect to the right,
and 30 m later the tracks of a fox crossed to the left, this was only
counted as a single individual, although two individuals may havebeen involved on some such occasions. In contrast, if the tracks of
two foxes crossed to the left, while none crossed to the right, thiswas counted as two foxes.
2.2. Confounding habitat and weather variables
Abundance estimates can be affected by numerous confounding
variables (Voříšek et al., 2010), and, therefore, it is crucial to control such variables statistically to assess the underlying relationshipbetween radiation and species richness and abundance. We classiﬁed habitats (agricultural habitats with grassland or shrub [either
currently or previously cultivated], deciduous forest, or coniferous
forest) and estimated to the nearest 10% ground coverage by thesedifferent habitat types within a distance of 50 m from the observation point. Agricultural habitat included edges between forest andopen areas, and the agricultural habitat variable thus also reﬂected
the amount of edge habitat between forest and open areas. Maximum height of trees was estimated to the nearest 5 m and soil typewas 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 (Voříšek et al.,2010), and we recorded cloud cover at the start of each point count(to the nearest eighth, range 0–1 during the censuses), temperature(degrees Celsius, range 12–25 ◦ C), and wind force (Beaufort, range
0–4 during the censuses). For each census point we recorded timeof day when the count was started (to the nearest minute). Because
activity may show a curvilinear relationship with time of day, forexample, with high levels of activity in the morning and to a lesser
extent in the evening for bird (Voříšek et al., 2010), and higher levels of activity for thermo-philic vertebrates and invertebrates, we
also included time squared as an explanatory variable.
2.3. Measuring background radiation levels
We measured radiation levels in the ﬁeld and cross-validated
these with measurements by the Ministry of Emergencies andShestopalov (1996). We measured ␣, ␤, and ␥ radiation at groundlevel at each census point after having conducted the census (thusmaking the census blindly with respect to radiation level) using ahand-held dosimeter (Model: Inspector, SE International, Inc., Summertown, TN, USA). We measured levels several (2–3) times at eachsite and averaged the measurements. Our data were validated withcorrelation against data from the governmental measurements
published by Shestopalov (1996), estimated as the mid-point of theranges published, with analyses showing a high degree of consistency between methods (Møller and Mousseau, 2007a). Radiationlevels vary greatly at a local scale due to heterogeneity in deposition of radioactive material after the Chernobyl accident (Fig. 1;
Shestopalov, 1996). Our measurements at the census points ranged
from 0.01 to 135.89 ␮Sv/h.
2.4. Dispersal distance
We do not have comparable estimates of dispersal distances fordifferent taxa. Therefore, we asked 12 biologists to score the natal

dispersal distance of the different taxa on a scale from 0 to 100, with
100 being given to birds. This was done blindly without any priorinformation on the purpose of the study. There was a highly significant repeatability of these scores (F = 4.19, d.f. = 11,96, P < 0.0001),
implying that different persons ranked the animal taxa similarly
with respect to perceived natal dispersal ability. Thus we used themean scores in the subsequent analyses. Means (SE) are reported
in Appendix A.
2.5. Mean population density
We used the mean number of individuals recorded per census
point as an estimate of population density. We do not consider point
counts to provide reliable information on absolute abundance.
However, they should provide information on relative abundance
because different taxa should be similarly detectable across sites(Voříšek et al., 2010). Such relative abundance would sufﬁce for our
purposes. We note that such information is unavailable for most of
the taxa investigated here.
2.6. Statistical analyses
Radiation level and abundance were log10 -transformed, while
ground coverage with farmland and deciduous forest was squareroot arcsine-transformed (coniferous forest was not included as an
explanatory variable, because it simply represents the ground coverage not attributed to farmland and deciduous forest). We also
included radiation level squared to account for non-linear relationships between species richness and abundance, respectively,
and radiation. We developed statistical models to assess the relationship between abundance (response variables) and radiation,
assuming a Poisson distribution of abundance, after inclusion of thepotentially confounding variables, as implemented in the statisticalsoftware JMP (SAS Institute, 2000).
We quantiﬁed the relationship between abundance of different
taxa and level of radiation by estimating the coefﬁcient of determination and by calculating the slope of the relationship between
abundance and log10 -transformed radiation. These slopes wereused for subsequent analyses.
As a measure of effect size we used R2 because it directly
reﬂects the amount of variance explained. We square root arcsinetransformed R2 to obtain an approximately normal distribution.
We tested for consistency in results by testing the relationshipbetween effect sizes before and after accounting for the potentiallyconfounding variables. Likewise, we tested for consistency in effectsize among years in a one-way ANOVA with taxon as a factor.
3. Results
Effects of background radiation on nine animal taxa are reported
in Table 1. All effects were statistically signiﬁcant. R2 ranged from0.015 in amphibians to 0.265 in mammals with considerable scatteraround the regression lines (Fig. 2).
In a second series of models we entered potentially confounding factors such as time of day, time of day squared, cloud cover,temperature, soil type, cover with grassland and shrub, cover with
forest, height of trees, and presence of water. Effect sizes differed little from the ﬁrst series of analyses with values ranging from 0.006
in butterﬂies to 0.196 in mammals (Table 2). There was a strong
positive correlation between R2 values for the two sets of analyses (F = 17.02, d.f. = 1,7, R2 = 0.71, P = 0.0044, slope (SE) = 0.79 (0.19)),with mean values not signiﬁcantly different (paired t-test, t = 2.02,
d.f. = 8, P = 0.08). Effect sizes tended to be stronger when the relationships were controlled for potentially confounding variables.
There was signiﬁcant consistency in R2 among years, with taxon
accounting for 61% of the variance in effect size (Table 2; F = 4.91,
d.f. = 6,19, R2 = 0.61, P = 0.0035). Differences in effect size among

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

427

Fig. 2. Abundance of nine taxa of animals in relation to levels of background radiation (␮Sv/h) around Chernobyl. (a) Spider webs, (b) grasshoppers, (c) dragonﬂies, (d)bumblebees, (e) butterﬂies, (f) amphibians, (g) reptiles, (h) birds and (i) mammals.

428

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

Table 1Models relating abundance of different animal taxa to background radiation levels. Slope (SE) reﬂects the relationship between log10 -transformed abundance (+1) and
log10 -transformed radiation level (␮Sv/h).
Taxon

F

d.f.

R2

P

Slope

SE

Spiderwebs
Grasshoppers
Dragonﬂies
Bumblebees
Butterﬂies
Amphibians
Reptiles
Birds
Mammals

81.94
13.58
34.58
55.71
57.63
14.22
24.13
258.21
57.27

1,896
1,372
1,402
1,896
1,896
1,896
1,896
1,896
1,159

0.084
0.035
0.079
0.059
0.060
0.015
0.026
0.224
0.265

<0.0001<0.0001<0.0001<0.0001<0.0001
0.0002<0.0001<0.0001<0.0001−0.162−0.071−0.112−0.085−0.099−0.005−0.021−0.094−0.182

0.018
0.019
0.019
0.011
0.013
0.001
0.004
0.006
0.024

Table 2Models relating abundance of different animal taxa to background radiation levels after accounting for the confounding effects of time of day, weather, and habitat. Slope(SE) reﬂects the relationship between log10 -transformed abundance (+1) and log10 -transformed radiation level (␮Sv/h).
Taxon

F

d.f.

R2

P

Slope

SE

Spiderwebs
Grasshoppers
Dragonﬂies
Bumblebees
Butterﬂies
Amphibians
Reptiles
Birds
Mammals

98.45
21.42
10.47
70.30
5.59
6.66
13.02
131.98
37.32

1,886
1,364
1,393
1,886
1,886
1,886
1,886
1,883
1,153

0.100
0.056
0.026
0.074
0.006
0.007
0.014
0.130
0.196

<0.0001<0.0001
0.0013<0.0001
0.018
0.010
0.0003<0.0001<0.0001−0.070−0.098−0.038−0.051−0.016−0.004−0.009−0.083−0.192

0.007
0.021
0.012
0.006
0.007
0.002
0.002
0.007
0.031

years were signiﬁcantly accounted for by density, with effect sizes
being lower in years with lower density (effect of density withintaxon, nested ANOVA: F = 3.06, d.f. = 7,12, R2 = 0.86, P = 0.043), as
expected for least squares statistical procedures (Table 3).
There was a strong positive relationship between mean
population size and the efﬁciency of abundance of different taxa as an indicator of radiation levels (i.e. effect size)(Fig. 3a; F = 14.64, d.f. = 1,7, R2 = 0.67, P = 0.00065, slope (SE) = 0.0526(0.0138)). In addition, there was a strong negative relationship between mean dispersal distance score and effect size
among taxa (Fig. 3b; F = 16.55, d.f. = 1,7, R2 = 0.70, P = 0.0048,
slope (SE) = −0.0825 (0.0203)). Mean density and dispersal score

were strongly positively correlated (F = 42.35, d.f. = 1,7, R2 = 0.86,
P = 0.0003, slope (SE) = 1.425 (0.219)). This implies that we could notinvestigate the independent effect of the two predictors because ofcollinearity.
4. Discussion
The main ﬁndings of this study of animal taxa as bio-indicatorsof low-level radiation in Ukraine and Belarus were that taxa differed considerably in suitability, with effect size varying by morethan two orders of magnitude, birds and mammals showing thestrongest effects of radiation on abundance. Potentially confound-

Table 3
Consistency in relationships between abundance of different animal taxa and background radiation level in different years. Slope (SE) reﬂects the relationship between
log10 -transformed abundance (+1) and log10 -transformed radiation level (␮Sv/h).
Taxon

Year

F

d.f.

R2

P

Slope

SE

Spiderwebs
Spiderwebs
Spiderwebs
Spiderwebs
Dragonﬂies
Dragonﬂies
Bumblebees
Bumblebees
Bumblebees
Bumblebees
Butterﬂies
Butterﬂies
Butterﬂies
Butterﬂies
Amphibians
Amphibians
Amphibians
Amphibians
ReptilesReptilesReptilesReptiles
Birds
Birds
Birds
Birds

2006
2007
2008
2009
2008
2009
2006
2007
2008
2009
2006
2007
2008
2009
2006
2007
2008
2009
2006
2007
2008
2009
2006
2007
2008
2009

27.06
4.24
0.06
1.60
14.74
20.70
89.76
7.53
0.37
0.11
54.27
5.07
5.13
6.54
4.73
4.77
1.42
4.15
9.63
4.00
5.73
5.14
144.43176.71102.36
25.62

1,252
1,238
1,235
1,165
1,235
1,165
1,252
1,238
1,235
1,165
1,252
1,238
1,235
1,165
1,252
1,238
1,235
1,165
1,252
1,238
1,235
1,165
1,252
1,238
1,235
1,163

0.10
0.02
0.00
0.01
0.06
0.11
0.26
0.03
0.00
0.00
0.18
0.02
0.02
0.04
0.02
0.02
0.01
0.02
0.04
0.02
0.02
0.03
0.36
0.43
0.28
0.14

<0.0001
0.041
0.81
0.21
0.0002<0.0001<0.0001
0.00650.54
0.74<0.0001
0.025
0.024
0.011
0.031
0.030
0.23
0.043
0.0021
0.047
0.017
0.025
<0.0001<0.0001<0.0001<0.0001−0.022−0.024−0.0020.009−0.046−0.051−0.096−0.025−0.005−0.003−0.076−0.029−0.026−0.026−0.006−0.006−0.002−0.005−0.012−0.006−0.010−0.008−0.130−0.141−0.103−0.064

0.003
0.012
0.008
0.007
0.012
0.011
0.010
0.009
0.008
0.009
0.010
0.013
0.012
0.010
0.003
0.003
0.002
0.003
0.004
0.003
0.004
0.004
0.011
0.011
0.012
0.013

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

Fig. 3. Effect size of the relationship between abundance and background radiationlevel in different animal taxa in relation to (a) their natal dispersal ability (arbitrary
units) and (b) mean population density (number of individuals per census point).
The lines are the linear regression lines.

ing variables did not qualitatively affect the results. Finally, taxa
with long natal dispersal distances and high population densities
showed stronger negative relationships with radiation than taxa
with short dispersal and smaller densities.
The strength of the association between abundance of different taxa of animals and background radiation level varied by morethan a factor ten. These ﬁndings are consistent with the hypothesis that low-level radiation has signiﬁcant negative impact on
population of animals. This is a signiﬁcant ﬁnding because negative impacts of radiation on physiology or reproductive success, asreported repeatedly (e.g. Heidenreich et al., 2000; Moiseev et al.,
1973; Pimentel et al., 2003), will not necessarily have populationconsequences. Clearly, there were signiﬁcant differences amongtaxa in effects of radiation on abundance, and these differenceswere consistent among years, suggesting that even a census basedon a single year will provide reliable information on effects of radiation on abundance. The different amounts of variance explainedsuggest that mammals and birds are particularly susceptible toradiation and hence particularly suitable for censusing the effectsof radiation on animals, followed by spiderwebs, bumblebees andgrasshoppers. Because mammals are difﬁcult and time consuming to census, with the only exception being censuses of tracks insnow, birds appear to be the most efﬁcient indicator of low-level
radiation. Because birds are generally abundant, distributed everywhere, and relatively easy to identify and count, they potentiallyprovide an effective tool for censuses directed towards understanding effects of radiation on abundance of animals. Dragonﬂies,
butterﬂies, amphibians and reptiles were the least efﬁcient bioindicators of low-level radiation. The reason for such differencesin susceptibility to radiation among taxa remains poorly under-429

stood. However, Møller and Mousseau (2007b) showed for birds
that interspeciﬁc differences in availability and/or use of antioxidants may play an important role in determining effects of radiation
on abundance. Such analyses may also be feasible for insects orother taxa with high metabolic rates for their body size.
Many potentially confounding variables may inﬂuence census
results (reviews in Voříšek et al., 2010). Here we explicitly tested
the effect of time of day, weather and several habitat variableson the abundance of nine animal taxa. Effect sizes, quantiﬁed as
R2 , were consistent between estimates that accounted or did notaccount for potentially confounding variables. Hence, the biologicalsignal in abundance data is so strong that potentially confounding
variables only marginally affected effect size estimates, although
there was a weak, but non-signiﬁcant reduction in effect size when
confounding variables were not considered.
Dispersal may be an important factor affecting the association
between abundance of animals and level of background radiation. We hypothesized two different scenarios: A ﬁrst possibility
is that dispersal is costly in terms of production of free radicals
from physical activity due to actual dispersal and/or from immune
response to novel antigens encountered in the new environments
during dispersal (Møller and Mousseau, 2007b). A second possibility is that dispersal obscures any relationship between abundance
and low-level radiation due to immigration from elsewhere. The
relationship that we found is consistent with the ﬁrst hypothesis
because effect size was strongly negatively related to dispersal distance (Fig. 3a). Thus, taxa with long dispersal distances showed
the strongest effect sizes, while taxa with smaller dispersal abilities only showed weak effects. However, we also found that taxa
with high mean densities showed stronger effects than taxa withlow densities (Fig. 3b). This relationship is expected because smallmean values generally are associated with small variances.
This paper describes patterns of abundance of different animal taxa in relation to radiation, but does not directly investigate
the underlying mechanisms. Radioactive fallout from Chernobyl
is associated with reduced and suppressed reproduction, reduced
reproductive success and reduced nestling and adult survival rate
(Møller and Mousseau, 2007b; Møller et al., 2008; Yablokov et al.,2009). Such negative effects will across generations tend to suppress local population densities in the most contaminated areas
unless balanced by immigration. Previous studies of dispersal andradiation have shown that avian species with long-distance dispersal are the most sensitive to radiation (Møller and Mousseau,
2007b). Thus immigration is an unlikely factor maintaining local
population density in the most contaminated areas. Source-sink
dynamics may stabilize population densities in radioactively contaminated areas if radioactive population sinks receive immigrants
from non-radioactive population sources that have a net production of emigrants. While such dynamics have been described for
Chernobyl (Møller et al., 2006), we consider immigration from population sources as inadequate for maintaining stable populations incontaminated areas.
In conclusion, extensive census data for nine taxa of animals
vary considerably in efﬁciency as predictors of background radiation levels. Furthermore, taxa with long dispersal distances showedstronger relationships with radiation than taxa with short dispersal
distances. Finally, the most abundant taxa showed the largest effectsizes. We recommend that these results be validated by precise
data on individual internal doses. Our ﬁndings have implications forchoice of organisms for estimating the effects of low-level radiationon the abundance of free-living organisms.
Acknowledgments
We are grateful for logistic help during our visits to Ukraine
and Belarus from O. Bondarenko, M. Bondarkov, I. Chizhevsky, S.

430

A.P. Møller, T.A. Mousseau / Ecological Indicators 11 (2011) 424–430

Gaschak, E. Konoplya, A. Litvinchuk, G. Milinevski, A.M. Peklo, E.
Pysanets, E. Konoplya, V. Kudryashov and N. Saino. The following
colleagues kindly helped provide scores for natal dispersal distance of different animal taxa: A. Antonov, A. Badyaev, J.A. Endler,
F. Fossøy, J.R. Gold, A. Moksnes, E. Røskaft, M. Soler, B.G. Stokke, F.
Takasu, and J. Waldron. We received funding from the Universityof South Carolina School of the Environment, Bill Murray and theSamuel Freeman Charitable Trust, the National Science Foundation,
NATO, the Fulbright Program, CRDF and the National Geographic
Society to conduct our research.
Appendix A.
Natal dispersal scores for different animal taxa based on scoresprovided by 12 scientists. The value for birds was set to 100.
Taxon

Mean natal
dispersal

SE nataldispersal

Mean population density
per census point

Birds
Mammals
Spiders
Grasshoppers
Dragonﬂies
Bumblebees
ReptilesButterﬂies
Amphibians

100.0
89.1
75.4
62.2
44.1
32.3
32.1
30.5
22.7

–
11.7
25.8
18.2
16.1
8.5
9.0
6.9
6.5

7.010
2.764
0.885
0.816
0.399
0.489
0.046
0.489
0.022

References
Bang, P., Dahlstrøm, P., Mears, R., 2007. Animal Tracks and Signs. Oxford University
Press, Oxford, UK.
Bazhan, K.V., 1998. Lipid peroxidation and the antioxidant system in subjects exposed to the inﬂuence of extreme factors. Lik Sprava 1998 (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. Radiation and Environmental
Biophysics 37, 187–193.
Bibby, C.J., Hill, D.A., Burgess, N.D., Mustoe, S., 2005. Bird census techniques. Academic Press, London.
Bonisoli-Alquati, A., Mousseau, T.A., Møller, A.P., Caprioli, M., Saino, N., 2010a.
Increased oxidative stress in barn swallows from the Chernobyl region. Comparative Biochemistry and Physiology A 155, 205–210.
Bonisoli-Alquati, A., Voris, A., Mousseau, T.A., Møller, A.P., Saino, N., Wyatt, M., 2010b.
DNA damage in barn swallows (Hirundo rustica) from the Chernobyl region
detected by use of the Comet assay. Comparative Biochemistry and Physiology
C 151, 271–277.
Brenner, D.J., Doll, R., Goodhead, D.T., Hall, E.J., Land, C.E., Little, J.B., Lubin, J.H., Preston, D.L., Preston, R.J., Puskin, J.S., Ron, E., Sachs, R.K., Samet, J.M., Setlow, R.B.,
Zaider, M., 2003. Cancer risks attributable to low doses of ionizing radiation:
Assessing what we really know. Proceedings of the National Academy of Sciencesof the United States of America 100, 13761–13766.
Chadwick, K.H., Leenhouts, H.P., Brugmans, M.J.P., 2003. A contribution to the linear
no-threshold discussion. Journal of Radiological Protection 23, 53–77.
Chaialo, P.P., Bereza, V.I., Chobot’ko, G.M., 1991. Free-radical processes and blood
antioxidant systems in the late period following acute radiation sickness. Medical Radiology (Moscow) 36, 20–21.
European Union, 1998. Atlas of Caesium Deposition on Europe after the Chernobyl
Accident. EU Publication EUR 16733, Bruxelles, Belgium.
Ferguson, L.R., 1994. Antimutagens as cancer chemopreventive agents in the diet.
Mutation Research 307, 395–410.
Halliwell, B.H., Gutteridge, J.M.C., 1999. Free radicals in Biology and Medicine, Third
edition. Oxford University Press, Oxford, UK.
Heidenreich, W.F., Brugmans, M.J.P., Little, M.P., Leenhouts, H.P., Paretzke, H.G.,
Morin, M., Lafuma, J., 2000. Analysis of lung tumour risk in radon-exposed
rats: an intercomparison of multi-step modelling. Radiation and Environmental
Biophysics 39, 253–264.
IAE, 2006. Environmental Consequences of the Chernobyl Accident and their Remediation: Twenty Years of Experience. International Atomic Energy Agency,
Vienna, Austria.
Ivaniota, L., Dubchak, A.S., Tyshchenko, V.K., 1998. Free radical oxidation of lipids andantioxidant system of blood in infertile women in a radioactive environment.
Ukrainski Biokhimskie Zhurnal 70, 132–135.
Krinsky, N.I., Denek, S.M., 1982. Interaction of oxygen and oxy-radicals withcarotenoids. Journal of the National Cancer Institute 69, 205–210.
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.
Lefﬂer, J.E., 1993. An Introduction to Free Radicals. John Wiley and Sons, New York,NY.
Liang, L., Deng, L., Mendonca, M.S., Chen, Y., Zheng, B., Stambrook, P.J., Shao, C., Tischﬁeld, J.A., 2007. X-rays induce distinct patterns of somatic mutation in fetal
versus adult hematopoietic cells. DNA Repair 6, 1380–1385.
Lubin, J., Boice Jr., J., 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 liquidators of Chernobyl accident consequences. Ukrainski
Biokhimskie Zhurnal 71, 82–85.
Moiseev, A.A., Maslov, V.I., Testov, B.V., Ovchenkov, V.Ya., 1973. Doses to Mouse-Type
Rodents Inhabiting Sites of Elevated Natural Radioactivity. State Committee on
the Use of Atomic Energy of the USSR, Moscow (in Russian).
Møller, A.P., 1983. Methods for monitoring bird populations in the Nordic countries.
Nordic Council of Ministers, Oslo.
Møller, A.P., Hobson, K.A., Mousseau, T.A., Peklo, A.M., 2006. Chernobyl as a population sink for barn swallows: tracking dispersal using stable isotope proﬁles.
Ecological Applications 16, 1696–1705.
Møller, A.P., Karadas, F., Mousseau, T.A., 2008. Antioxidants in eggs of great tits Parus
major from Chernobyl and hatching success. Journal of Comparative Physiology
B 178, 735–743.
Møller, A.P., Milinski, M., Slater, P.J.B. (Eds.), 1998. Stress and Behavior. Advances in
the Study of Behaviour, p. 27.
Møller, A.P., Mousseau, T.A., 2006. Biological consequences of Chernobyl: 20 years
after the disaster. Trends in Ecology and Evolution 21, 200–207.
Møller, A.P., Mousseau, T.A., 2007a. Birds prefer to breed in sites with low
radioactivity in Chernobyl. Proceedings of the Royal Society of London B 274,
1443–1448.
Møller, A.P., Mousseau, T.A., 2007b. Determinants of interspeciﬁc variation in population declines of birds from exposure to radiation at Chernobyl. Journal ofApplied Ecology 44, 909–919.
Møller, A.P., Mousseau, T.A., 2008. Reduced abundance of raptors in radioactively contaminated areas near Chernobyl. Journal of Ornithology 150,
239–246.
Møller, A.P., Mousseau, T.A., 2009. Reduced abundance of insects and spiders linked
to radiation at Chernobyl 20 years after the accident. Biological Letters 5,
356–359.
Møller, A.P., Biard, C., Blount, J.D., Houston, D.C., Ninni, P., Saino, N., Surai, P.F.,
2000. Carotenoid-dependent signals: Indicators of foraging efﬁciency, immunocompetence or detoxiﬁcation ability? Poultry and Avian Biology Reviews 11,
137–159.
Moss, I.B., Mikhailova, M.E., Glushkova, I.V., Kasinskaia, S.I., Anoshenko, I.P., Aktiutik, T.V., Tikhanovich, N.I., Kamysh, N.A., 2006. Genetic monitoring of natural
Drosophila populations in radiation contaminated regions of Belarus. Radiation
Biology and Radioecology 46, 287–295.
Neyfakh, E.A., Alimbekova, A.I., Ivanenko, G.F., 1998a. Vitamin E and A deﬁciencies inchildren correlate with Chernobyl 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.
Pimentel, E., Tavera, L., Cruces, M.P., Balcazar, M., de la Rosa, M.E., 2003. Low radondose effect on fecundity and egg-to-adult viability of Drosophila. Radiation
Measurements 36 (Special Issue), 511–516.
Prasad, K.N., Cole, W.C., Hasse, G.M., 2004. Health risks of low dose ionizing radiationin humans: a review. Experimental and Biological Medicine 229, 378–382.
Ramzaev, V., Yonehara, H., Hille, R., Barkovsky, A., Mishine, A., Sahoo, S.K., Kurotaki, K., Uchiyama, M., 2006. Gamma-dose rates from terrestrial and Chernobyl
radionuclies inside and outside settlements in the Bryansk Region, Russia in
1996–2003. Journal of Environmental Radioactivity 85, 205–227.
SAS Institute Inc., 2000. JMP. SAS Institute Inc., Cary, NC.
Shestopalov, V.M., 1996. Atlas of Chernobyl Exclusion Zone. Ukrainian Academy of
Science, Kiev, Ukraine.
Sies, H., 1993. Strategies of antioxidant defense. European Journal of Biochemistry
215, 213–219.
Sykes, P.J., Morley, A.A., Hooker, A.M., 2006. The PKZ1 recombination mutation assay:
a sensitive assay for low dose studies. Dose–Response 4, 91–105.
Tubiana, M., Aurengo, A., Averbeck, D., Masse, R., 2006. Recent reports on the effectof low doses of ionizing radiation and its dose–effect relationship. Radiation andEnvironmental Biophysics 44, 245–251.
Valko, M., Izakovic, M., Mazur, M., Rhodes, C.J., Telser, J., 2004. Role of oxygen radicals
in DNA damage and cancer incidence. Molecular and Cellular Biochemistry 266,
37–56.
Voříšek, P., Klvanova, A., Wotton, S., Gregory, R.D., 2010. A Best Practice Guide forWild Bird Monitoring Schemes. European Union, Bruxelles, Belgium.
Wickliffe, J.K., Bickham, A.M., Rodgers, B.E., Chesser, R.K., Philips, C.J., Gaschak, S.P.,
Goryanaya, J.A., Chizhevsky, I., Baker, R.J., 2003. Exposure to chronic, low-dose
rate ␥-radiation at Chornobyl does not induce point mutations in Big Blue® mice.
Environmental and Molecular Mutagenesis 42, 11–18.
Yablokov, A.V., Nesterenko, V.B., Nesterenko, A.V., 2009. Chernobyl: Consequencesof the Catastrophe for People and Nature. New York Academy of Sciences, New
York, NY.