Ecological Indicators 52 (2015) 128–133

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

Heterogeneous relationships between abundance of soil surface
invertebrates and radiation from Chernobyl
Vladimir Bezrukov a , Anders Pape Møller b,∗ , Gennadi Milinevsky c , Stanislav Rushkovsky a ,Maria Sobol a , Timothy A. Mousseau daDepartment of General and Molecular Genetics, Taras Shevchenko National University of Kyiv, Volodymyrska St. 64, 01601 Kyiv, Ukraine
Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405 Orsay Cedex, FrancecSpace Physics Laboratory, Taras Shevchenko National University of Kyiv, Volodymyrska St. 64, 01601 Kyiv, UkrainedDepartment of Biological Sciences, University of South Carolina, Columbia, SC 29208, USAba r t i c l e

i n f oArticle history:
Received 5 October 2014
Received in revised form
10 November 2014
Accepted 13 November 2014
Keywords:
Abundance
Chernobyl
Interspeciﬁc differences
Radiation
Susceptibility to radiationa b s t r a c t
Although pollution due to nuclear accidents constitutes some of the largest environmental disasters,
there is surprisingly little information available on the relationship between abundance of animals andbackground radiation. We sampled invertebrates with pit-fall traps at Chernobyl in areas differing inbackground radiation level by more than four orders of magnitude. We obtained samples from 58 traps
for 19 taxa of which ﬁve showed positive associations (Acari, Araneae, Formica sp., Homoptera), whilefour showed negative associations (Coleoptera, Collembola, Vespa, Insecta). These relationships wereindependent of other environmental factors such as habitat, humidity and ecotype. Estimates of therelationship between abundance and background radiation from the pitfall trap study were similar to
those from an independent study based on invertebrates found under slices of wood placed on the ground.
The differences in relationship between abundance and radiation among taxa may arise from direct
effects of radiation. The ﬁndings reported here have implications for choice of animal taxa for efﬁcientmonitoring of the biological impact of radiation on animals.
© 2014 Elsevier Ltd. All rights reserved.

1. Introduction
Radioactive material occurs under natural conditions due tothe radionuclides contained in rocks and from cosmic rays andsuch radioactive hotspots show signiﬁcant negative effects onplants and animals (review in Møller and Mousseau, 2013a,b).
Radioactive contamination due to release from nuclear disasters
has affected hundreds of thousands of square kilometers across theglobe with particularly strong effects having been documented at
Chernobyl and Fukushima. Studies have shown that the abundanceof organisms is affected by radioactive contaminants. This applies tosoil invertebrates (Krivolutski and Pokarzhevsky, 1992; Krivolutski
et al., 1999; Maksimova, 2005), bacteria (Zymenko et al., 1995;
Romanovskaya et al., 1998; Ragon et al., 2011), spiders (Møller andMousseau, 2009, 2011; Møller et al., 2012b,c), insects (Møller andMousseau, 2009, 2011; Møller et al., 2012b,c), birds (Møller andMousseau, 2007a,b; Møller et al., 2012b,c) and mammals (Møller
and Mousseau, 2013a). Such effects of radiation on abundance are∗ Corresponding author. 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).
http://dx.doi.org/10.1016/j.ecolind.2014.11.014
1470-160X/© 2014 Elsevier Ltd. All rights reserved.

consistent among years and geographical locations (Møller et al.,2011, 2012b), but differ among taxa.
There are signiﬁcant differences among bird species in susceptibility to radiation in Chernobyl with species on average being
negatively affected in terms of abundance, while a few species show
no or even a positive effect (Møller and Mousseau, 2007b). Similar
heterogeneity has been documented for the relationship between
abundance and level of background radiation in Fukushima (Møller
et al., 2012b,c). While such heterogeneity in effects of radiation
on abundance may be expected simply for sampling reasons, statistically signiﬁcant heterogeneity beyond sampling suggests thatthese are inherent species-speciﬁc characteristics. Indeed, interspeciﬁc differences for birds in frequency of cataracts (Mousseau
et al., 2013), reductions in brain size (Møller et al., 2013), frequencyof tumors and abnormalities (Møller et al., 2013), aspermy andsperm behavior (Møller et al., 2008, 2014) and levels of antioxidants (Bonisoli-Alquati et al., 2011; Galván et al., 2014) suggest that
underlying physiological processes account for such heterogeneity.
Although soil invertebrates, arachnids and insects constitutesigniﬁcant parts of biodiversity, and although small invertebrates
are readily sampled in standard pitfall traps, there are so far no
pitfall trap studies conducted in Chernobyl or Fukushima. WhileV. Bezrukov et al. / Ecological Indicators 52 (2015) 128–133

decomposition of leaf litter is reduced in contaminated areas
around Chernobyl (Mousseau et al., 2014), these effects are notreadily interpreted because we do not know to which extent different soil-inhabiting taxa are affected.
The main objective of this study was to assess to what extent theabundance of soil surface invertebrates was affected by radioactive
contamination from Chernobyl. First, we sampled invertebrates
with pitfall traps to test for differences in susceptibility to radiation
among taxa. Second, we identiﬁed the taxa that provide the mostsensitive indicators of radiation. Third, we cross-validated our estimates of effects of radiation on abundance by comparing our pitfall
trap results with those obtained from invertebrates found underslices of pine wood placed across a radiation gradient.
2. Methods
2.1. Sampling sites
We chose six sites that were ecologically similar ranging in levelof contamination from 0.013 to 36 mrem/h (Fig. 1). The coordinatesof the sites and their characteristics are listed in the electronic supplementary material (Table S1). We report characteristics of thesesix study sites in Table S1 in terms of radioactivity, soil type, amountof dead organic matter, amount of surface covered with open water
as in ponds, and dominant vegetation.
Soil at the traps was classiﬁed as sand or ash (ash derived fromforest ﬁres) within a radius of 10 m from each of the trap sites. The
amount of litter was classiﬁed on a three-point scale from 1 – little, over 2 – common to 3 – abundant within a radius of 10 m fromthe traps. We recorded if there was open water (ponds or puddles) within a distance of 50 m from the traps. Finally, we recorded
whether the dominant vegetation was grass, deciduous trees orconiferous trees within a distance of 10 m from the traps.
We considered three different ecotypes based on soil, abundance of litter and other features of habitats (Ingegnoli, 2002;
Bastian et al., 2003).
2.2. Cross validation
We cut 5 cm slices from the trunks of four Scots pine (two froman uncontaminated area and two from a highly contaminated area)that were approximately 60 years old. At each of 20 sites varying
in radioactive contamination by more than four orders of magnitude we put our one slice of each of the four trees in early June 2013.
Each slice was identiﬁable from a unique numbered metal tag. During early June 2014 we re-visited all 20 sites and recorded on thelower surface facing toward the soil the number of fungi and theanimal taxa used in the present study and counted these animals
before turning over the slice again for future study. We recorded
background radiation at the site of each slice when this was originally put out and one year later as described above. For the ﬁve taxa
with animals common in the two datasets we estimated the abundance of animals in relation to background radiation using Poisson
regression as described below.
2.3. Measuring background radiation levels
We measured radiation levels in the ﬁeld at ground level at
each location where a pitfall trap was deposited using a hand-held
dosimeter (Model: Inspector, SE International, Inc., Summertown,
TN, USA). We measured levels 2–3 times at each of these locations
and averaged the measurements for each location. Such data werecorrelated with data from governmental measurements at groundlevel published by Shestopalov (1996), estimated as the mid-pointof the ranges in the published maps. These analyses showed ahigh degree of consistency between the two methods (Møller and129

Mousseau, 2007a). Radiation levels vary by several orders of magnitude at a scale of 1 km due to heterogeneity in deposition ofradioactive material after the Chernobyl accident (Shestopalov,1996).
2.4. Pitfall traps and handling
We used 500 ml plastic containers with an inner diameter of
90 mm and 25% ethylene glycol as a preservative. They were placedin the ground so the top of the container was at the level of the soil
surface and covered with CDs (compact discs) for protection fromrain and solar light. The distance from the soil surface to the CD
was about 2 cm. The distance among traps was 2 m, and a total of
20 traps per site we used in this survey. The traps were placed along
two intersecting transects to form a “+” and oriented toward north,south, east and west. The traps were placed on 25 August 2007 andcontents were collected on 8 September 2007.
2.5. Identiﬁcation
Container contents were sorted under a stereo binocular microscope and transferred to 1.5 ml eppendorf tubes with 96% ethanol.
The organisms were identiﬁed to order using Chinery (1993, 2007),
Gibbons (1995), Gilarov (1964) and a mite identiﬁcation web(http://www.lucidcentral.org/keys/v3/mites/Invasive Mite
site
Identiﬁcation/).
Some samples were excluded from the analysis because they
were destroyed by wild animals (the containers were dry or
removed). One trap (site RF03) was excluded because it contained
an enormous number of ants (667) and collembolas (26,922) thatexceeded the general sample by more than three standard deviations. This aberrant trap was situated very close to an ants’ nest
hence explaining the abundance of ants.
2.6. Statistics
Because observations of animals in pitfall traps basically arecount data, they have to be treated as having a Poisson distribution. Therefore, we used generalized linear mixed models withthe abundance of animals as the response variable and background radiation and the ﬁrst two principal component scores
reﬂecting environmental variables (Table S2). None of these components were statistically signiﬁcant predictors and hence they
were excluded from the ﬁnal statistical models.
We reduced the ﬁve environmental variables using principal
component analysis. This analysis was based on the correlation
matrix for the ﬁve environmental variables using varimax rotation. The principal component analysis revealed two factors witheigenvalues above one accounting for 60% and 25% of the variance,
respectively. The ﬁrst factor was strongly positively correlated withsoil and ash, dead organic matter, presence of water and ecotype. The second factor showed a positive loading for presence oftrees and ecotype. We subsequently extracted principal componentscores for the 58 pitfall trap sites and used these scores as additional predictor variables in the analyses. All analyses were madewith JMP (SAS, 2012). We report means ± 1 SE.
3. Results
3.1. Summary statistics
We found animals of three orders of the class Arachnida, elevenorders (ten orders and one genus – Collembola) of Insecta and oneorder (Myriapoda) of the class Chilopoda (Table 1). In total, thisstudy was based on 12,049 animals (Table 1) ranging in abundance

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V. Bezrukov et al. / Ecological Indicators 52 (2015) 128–133

Fig. 1. Location of the six sampling sites for pitfall traps in the neighborhood of Chernobyl with background radiation indicated with increasing intensity of coloration(kBq/m2 ). The large arrow shows the location of the Chernobyl Nuclear Power Plants.
Adapted from Shestopalov (1996). Further information on sites can be found in Table S1.

Table 1
Mean abundance, SE and total abundance of animals collected in 58 pitfall traps at
Chernobyl.
Taxon

Taxon

Mean abundanceSE

Total abundance

Order
Order
Order
Class
Order
Order
Order
Order
Order
Order
Order
Genera
Order
Order
Order
Class
Order
Class
PhylumAraneae
Opiliones
Acari
Arachnida
DipteraHomoptera
Orthoptera
Hemiptera
Lepidoptera
Coleoptera
Hymenoptera
Collembola
Thysanoptera
Psocoptera
Dermaptera
Insecta
Myriapoda
Chilopoda
Arthropoda

3.71
0.16
48.81
52.67
3.26
0.33
0.43
4.67
0.05
3.28
13.29
129.43
0.17
0.12
0.02
155.050.02
0.02
207.74

0.34
0.06
3.70
3.69
0.51
0.15
0.10
0.67
0.03
0.81
1.52
23.71
0.06
0.09
0.02
24.41
0.02
0.02
25.79

215
9
2831
3055
189
19
25
271
3
190
771
7507
10
7
1
8993
1
1
12,049from Chilopoda, Dermaptera and Myriapoda each with one individual to Collembola with 7507 and Acari with 2138 individuals.
3.2. Abundance and radiation
The abundance of animals depended on taxon, radiation andtheir interaction (Table 2). While there was no overall main effectof the relationship between abundance and radiation, the abundance of different taxa differed, and the interaction between taxon
and radiation was highly signiﬁcant (Table 2). This implies that atleast one taxon differed from all others in relationship between
abundance and radiation. Inspection of the data revealed that therelationship was negative for some taxa, positive for others and not
signiﬁcant for yet others (Fig. 2).
Five taxa showed an increase in abundance with radiation:
Acari, Araneae, Arachnida, Formica sp. and Homoptera (Table 3 andFig. 2). Three taxa showed a decrease with increasing radiation:
Coleoptera, Collembola and Vespa sp. (Table 3 and Fig. 2). There
was also an overall negative relationship for insects (Table 3).

3.3. Cross-validation of the relationship between abundance andradiation
We cross-validated the method used to estimate the relationship between abundance and radiation according to pitfall traps
by comparing the estimates with an independent study based on
invertebrates found under wood. The estimates of the relationship between abundance and radiation derived from the tree slice
experiment were signiﬁcantly positively related to the estimates
based on pitfall traps for Acari, Chilopoda, Coleoptera, Collembola
and Formica sp. (F = 11.15, r2 = 0.72, d.f. = 1, 3, P = 0.044, estimate(SE) = 0.097 (0.029)). Likewise a non-parametric Kendall rank ordercorrelation showed a signiﬁcant positive relationship (Kendall
 = 1.00, P = 0.014). Hence we conclude that the estimates of therelationship between abundance and radiation in different taxa
were independent of the study method.

4. Discussion
The invertebrate taxa investigated here differed in their abundance relative to background radiation level with some taxa
showing signiﬁcant positive relationships, others signiﬁcant negative relations and yet others no signiﬁcant relationships. We could
exclude the possibility that the ﬁndings were biased because therelationship between abundance and radiation was consistent in acomparison between estimates based on pitfall traps and estimates
based on animals found under slices of pine wood deposited at 20
sites across a radiation gradient at Chernobyl. These ﬁndings imply
that careful choice of speciﬁc taxa with a strong negative relationship between abundance and level of background radiation will
provide the most sensitive assessment of the biological effects ofradiation.

V. Bezrukov et al. / Ecological Indicators 52 (2015) 128–133

131

Table 2
Generalized linear mixed model of the relationship between abundance of animals and taxon, background radiation and their interaction. Values are 2 and associatedP-values, estimates (SE) and 95% lower and upper conﬁdence limits.
Term

2

P

Estimate

SE

Lower CL

Upper CLIntercept
Taxon
Radiation
Taxon × Radiation

6.89
42457.64
0.72
271.760.009<0.0001
0.40<0.0001

−0.69

0.56

−2.36

−0.10

−0.21

0.31

−1.10

0.16

There is a surprising deﬁcit of census data from areas contaminated with radionuclides, and studies of soil invertebrates are
restricted to only a handful (Krivolutski and Pokarzhevsky, 1992;
Krivolutski et al., 1999; Maksimova, 2005; Møller and Mousseau,
2009, 2011; Møller et al., 2012b,c) despite the importance of thesetaxa for ecological processes. Here we have shown differences in therelationship between abundance of soil surface invertebrates andradiation, with Coleoptera, Collembola, Vespa sp. and insects showing signiﬁcant negative relationships, Acari, Araneae, Formica sp.

and Homoptera showing positive relationships and the remaining
taxa showing no signiﬁcant relationship. We can exclude the possibility that these differences were due to sampling alone because
we were able to cross-validate our ﬁndings for ﬁve taxa (Acari,
Chilopoda, Coleoptera, Collembola and Formica sp.) with data fromanother study that used a different methodology. Some of therelationships that we have documented here differed from thosepreviously reported elsewhere. Thus Møller and Mousseau (2011)
showed negative relationships between abundance and level ofFig. 2. Abundance of invertebrates in relation to background radiation (mR/h) at 58 sites near Chernobyl with pitfall traps. (A) Acari, (B) Araneae, (C) Formica sp., (D)Coleoptera, (E) Collembola and (F) Vespa sp.

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V. Bezrukov et al. / Ecological Indicators 52 (2015) 128–133

Table 3Results for the relationship between abundance and log-transformed background radiation from generalized linear mixed models with a Poisson distribution and log-link
function for different taxa of animals at Chernobyl. Values are 2 and associated P-values, estimates (SE) and 95% lower and upper conﬁdence limits.
Taxon

2

P

EstimateSE

Acari
Arachnida
Araneae
Chilopoda
Coleoptera
Collembola
Dermaptera
DipteraFormica sp.
Hemiptera
HomopteraHymnoptera
Lepidoptera
Myriapoda
Opiliones
Orthoptera
Psocoptera
Thysanoptera
Vespa sp.
Insecta

9.28
11.99
4.50
0.31
10.64
8.44
2.65
0.71
115.43
0.25
5.61
1.31
2.95
0.31
0.00
0.27
0.19
0.03
5.94
11.89

0.00230.00050.034
0.580
0.00110.00370.103
0.400<0.0001
0.610
0.018
0.253
0.086
0.579
0.995
0.604
0.668
0.861
0.015
0.0006

0.332
0.365
0.907
4.570
−1.289−0.16171.000−0.327
1.951
0.154
5.278
−0.202
10.3494.568−0.012−0.6140.928−0.370−1.579−0.176

0.110
0.106
0.441
8.740
0.391
0.055
106.100
0.385
0.190
0.308
2.326
0.176
7.529
8.739
1.792
1.171
2.216
2.099
0.627
0.051

background radiation for spiderwebs, butterﬂies and grasshoppers,
while here we did not ﬁnd signiﬁcant relationships for these taxa.
The data are not comparable for Araneae because the previous
study was based on web-building spiders, while most of the spiders in the present study were ground dwelling jumping spiders.
Likewise, Møller and Mousseau (2011) analyzed diurnal butterﬂies
while those analyzed here were mainly noctuid moths. Similarly,
the Orthoptera analyzed by Møller and Mousseau (2011) were true
grasshoppers, while those analyzed here were mainly crickets. Thus
these data are not comparable.
Interpretation of the ﬁndings reported here will require detailed
physiological and genetic analyses. The ﬁndings reported here mayarise from differences in susceptibility to radiation, mutation rates,
DNA repair or direct and indirect impact of radiation. For example,
direct impact of radiation due to the toxic effects of radionuclides
may result in damage to DNA or normal processes of physiological homeostasis. In contrast, indirect effects of radiation may
act through effects on abundance of food, parasites, predators orcompetitors. There is currently very little empirical informationon these possible mechanisms. For example, Beasley et al. (2012)
showed for grasshoppers Chorthippus albomarginatus from Chernobyl in a common garden experiment that parental radiation
exposure had little measurable effect on developmental instability in morphology, fecundity or survival. More studies of this sortare required for a better understanding of the underlying mechanisms responsible for differences in abundance of invertebrates
related to differences in background radiation.
We measured background radiation using a handheld dosimeter. This approach rests on the assumption that the invertebrates
investigated here are exposed to a similar level of radiation
throughout their lives, and that their movements do not result inaltered radiation exposure. This assumption seems likely for invertebrate taxa that do not move long distances, while it may apply
less to taxa that disperse far such as spiders and butterﬂies. We
have previously shown for different animal taxa and for birds that
population density was more negatively affected by radiation when
natal dispersal distance was long (Møller and Mousseau, 2011).
This study allows for a ranking of taxa with respect to theirindicator ability of the biological effects of ionizing radiation in asimilar way as Møller and Mousseau (2011) have done previously
for a smaller number of invertebrates and for vertebrate taxa. The
strongest positive effect was documented for ants of the genus
Formica and Arachnida, while the strongest negative effect was
documented for Coleoptera and Collembola.

Lower CL
0.118
0.157
0.067
−10.510−2.056−0.270−5.750−1.0681.583−0.4390.887−0.544−1.053−10.510−3.477−2.878−3.080−4.524−2.789−0.276Upper CL
0.549
0.575
1.797
26.734−0.518−0.053655.736
0.443
2.326
0.768
10.0640.146
30.45726.735
3.923
1.797
5.992
3.965
−0.318−0.076

In conclusion, invertebrate taxa sampled in pitfall traps differed in their susceptibility to background radiation with sometaxa showing positive relationships between abundance and radiation, while others showed negative effects. Further experimental
studies will be needed to unravel to mechanisms underlying thisheterogeneity in population responses to environmental radiation
exposures.
Acknowledgements
We thank Ihor Chizhevsky (Chornobyl Ecocenter) for help during ﬁeldwork. We thank the Samuel Freeman Charitable Trust, theUniversity of South Carolina College of Arts & Sciences, and theCentre National de la Recherche Scientiﬁque for ﬁnancial support.
Appendix A. Supplementary data
Supplementary data associated with this article can befound, in the online version, at http://dx.doi.org/10.1016/j.ecolind.
2014.11.014.
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