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Reduced abundance of insects and spiders linked to radiation
at Chernobyl 20 years after the accident
Anders Pape Møller and Timothy A Mousseau
Biol. Lett. published online 18 March 2009
doi: 10.1098/rsbl.2008.0778

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Biol. Lett.
doi:10.1098/rsbl.2008.0778
Published online

Global change biology

Reduced abundance ofinsects and spiders linkedto radiation at Chernobyl
20 years after the accident
Anders Pape Møller1,*and Timothy A. Mousseau2
1

Laboratoire d’Ecologie, Systématique et Evolution,Université Paris-Sud, CNRS UMR 8079, Bâtiment362, 91405 Orsay Cedex, France2
Department of Biological Sciences, University of South Carolina,
Columbia, SC 29208, USA*Author for correspondence (anders.moller@u-psud.fr).

Effects of low-level radiation on abundance ofanimals are poorly known. We conducted standardized point counts and line transects ofbumble-bees, butterflies, grasshoppers, dragonflies and spider webs at forest sites around
Chernobyl differing in background radiation byover four orders of magnitude. Abundance of
invertebrates decreased with increasing radiation, even after controlling for factors such as
soil type, habitat and height of vegetation. Theseeffects were stronger when comparing plots
differing in radiation within rather than amongsites, implying that the ecological effects ofradiation from Chernobyl on animals are
greater than previously assumed.
Keywords: dragonflies; ecosystem; grasshoppers;
pollinators; spiders

1. INTRODUCTION
The ecological consequences of radiation from Chernobyl are poorly known (Møller & Mousseau 2006).
Surprisingly, there are few data on the abundanceof animals in relation to radiation, and there havebeen no efforts to extensively census invertebrates inrelation to radiation. The few studies published aremainly based on sampling in a few locations, making it
difficult to generalize about the effects of radiation
when compared with other factors (Krivolutsky &Pokarshevsky 1992; Sokolov et al. 1994; Maksimova
2002; Jackson et al. 2005).
The objectives of this study were to assess theabundance of invertebrate taxa in relation to background radiation. These were insect pollinators(bumble-bees and butterflies), an important taxon ofherbivores (grasshoppers) and predators (dragonflies:and spiders). We conducted two kinds of census:
point counts covering more than 700 sites during
3 years and line transects. This is by far the mostextensive dataset on the abundance of animals from
Chernobyl. Abundance can be affected by environmental factors other than radiation, and, therefore,
we controlled statistically for potentially confounding
Electronic supplementary material is available at http://dx.doi.org/10.
1098/rsbl.2008.0778 or via http://rsbl.royalsocietypublishing.org.
Received 18 December 2008
Accepted 12 February 2009variables that could affect the relationship between
abundance and level of radiation. Line transects
provided a powerful within-site experimental design
controlling for many confounding variables because
neighbouring sites that differ in the level of radiation
by definition are similar in most respects, including
soil type, habitat and other features.
2. MATERIAL AND METHODS
A.P.M. conducted 731 standard point counts over the 3 years, lateMay–early June 2006–2008, within forested areas around Chernobyl, each count lasting 5 min during which all birds seen or heard,bumble-bees, butterflies, spider webs and dragonflies (dragonflies
were only censused in 2008) were recorded (Møller 1983; Bibby
et al. 2005). Points were located at 75 m intervals. Grasshoppers
were censused during early September 2007 at 374 points.
We conducted four line transects at 17 sites during earlyJuly 2008 within and just outside the southern border of theexclusion zone. At each site, we pre-selected plots with highand low radiation (high radiation: 0.60 mGy hK1 (s.e.Z1.29), lowradiation: 0.38 mGy hK1 (1.29)). At each plot, A.P.M. conducted
two line transects along roads in opposite directions, each of 50 m.
Walking speed was slow, each transect lasting 10 min. Half an hourlater, the same line transects were conducted once more without
reference to the first census results.
Invertebrate abundance estimates can be affected by habitat(agricultural habitats with grassland or shrub, deciduous forest or
coniferous forest estimated to the nearest 10% of ground coverage
within 50 m from each of the observation points), maximum height oftrees estimated to the nearest 5 m, soil type (loam/clay or sand),presence or absence of open water within 50 m from each point,
cloud cover at the start of each point count (to the nearest eighth),temperature (range 12–288C) and wind force (Beaufort, range 0–4).
For each point count, we recorded time of day (to the nearest minute).
Because the activity of many invertebrates is curvilinearly related
to time of day, with high levels of activity in the middle of the day(e.g. Barnes et al. 2001), we also included time squared in the analyses.
Once having finished a 5 min census, we measured a, b and gradiations two to three times at ground level using a hand-held
dosimeter (Model: Inspector, SE International, Inc., Summertown,TN, USA). Cross-validation against data from Shestopalov (1996)
revealed a strong positive relationship (linear regression on log–log
transformed data: FZ1546.49, d.f.Z1,252, r 2Z0.86, p!0.0001,
slope (s.e.)Z1.28 (0.10)), suggesting reliability of our estimates.
Abundance of invertebrates and radiation level were log transformed, while coverage with farmland and deciduous forest wassquare-root arcsine transformed. We developed best-fit models toassess the relationship between invertebrate abundance (dependentvariable) and radiation, after the inclusion of potentially confounding
environmental variables, as implemented in JMP (SAS Institute Inc.
2000). Model selection was based on Akaike’s information criterion(AIC), using the criterion of delta AIC!2.00 for exclusion ofvariables (Burnham & Anderson 2002). We analysed line transect
data by using abundance as the response variable and site, level ofradiation and their interaction as predictor variables. Frequency
distributions of invertebrate counts were skewed, with disproportionately many zeros. However, we obtained similar results withKendall rank-order correlation and partial rank-order correlation(controlling for confounding variables in table S2 in the electronic
supplementary material).

3. RESULTS
The abundance of invertebrates decreased withincreasing radiation (figure 1). We recorded 298
bumble-bees with Bombus terrestris accounting for72.6 per cent of all observations (see table S1 in theelectronic supplementary material). Abundance ofbumble-bees decreased between normal backgroundradiation levels and the most contaminated areas(figure 1a). In addition, there were effects of year,temperature, wind and habitat on the abundance ofbumble-bees (see table S2 in the electronic supplementary material). We recorded 389 butterflies with
Aporia crataegi accounting for 36.6 per cent (see table
S3 in the electronic supplementary material). Again,
abundance decreased significantly between sites withThis journal is q 2009 The Royal Society

Downloaded from rsbl.royalsocietypublishing.org on 19 March 2009(a) 10(b) 10

no. of butterflies

Radiation and invertebrate abundance

no. of bumble-bees

A. P. Møller & T. A. Mousseau

110 –1

10 –1(c) 10(d) 10
no. of dragonflies

1

no. of grasshoppers2

1

10 –1 –2
1010–1

1
10radiation (µGy h–1)

102

103

1

10 –1 –2
1010–1

1
10radiation (µGy h–1)

102

103

102

103

no. of spider webs(e) 102101

10 –1 –2
1010–1

1
10radiation (µGy h–1)

Figure 1. Abundance of (a) bumble-bees, (b) butterflies, (c) grasshoppers, (d ) dragonflies and (e) spider webs estimatedduring point counts in 2006–2008 in relation to background radiation (mGy hK1) for forested locations around Chernobyl,
Ukraine and Belarus. (The lines are the linear regression lines.)level of contamination (figure 1b). Abundance ofbutterflies was additionally explained by time of day,wind and habitat (see table S2 in the electronic
supplementary material).
We recorded 305 grasshoppers during our point
counts. Abundance decreased significantly with radiation (figure 1c), with additional effects of date, timeof day, temperature, cloud cover and habitat (seetable S2 in the electronic supplementary material).
The total number of dragonflies was 105 during point
counts, with abundance decreasing significantly withradiation (figure 1d ), time of day and habitat (seetable 1D in the electronic supplementary material).
Finally, we recorded 775 spider webs, with abundance declining with radiation (figure 1e), year,
temperature and wind (see table S2 in the electronic
supplementary material).
The census results from repeated line transects
were consistent (see table S4 in the electronicBiol. Lett.

supplementary material). All five invertebrate taxa
decreased significantly in abundance with increased
radiation (figure 2), with intermediate to large effects(sensu Cohen 1988) accounting for 14–38 per cent of
the variance (see table S4 in the electronic supplementary material). There were also significant site
effects, with the exception of spider webs (see table
S4 in the electronic supplementary material).
Grasshoppers and butterflies showed significant
interactions between radiation and site (see table S4in the electronic supplementary material).
4. DISCUSSION
We found declining abundance of invertebrates withradiation near Chernobyl, especially in line transects
that controlled for confounding environmental variables
through within-site comparisons. The only comparable
data for abundance and diversity of birds in Chernobyl
show similar patterns (Møller & Mousseau 2007).

Downloaded from rsbl.royalsocietypublishing.org on 19 March 2009(a) 102(b) 102

no. of bumble-bees

no. of butterflies

Radiation and invertebrate abundance11(c) 103(d ) 102
no. of dragonflies

102

101
10–2

10–1

1
radiation (µGy h–1)

102

103

10

no. of grasshoppers

10A. P. Møller & T. A. Mousseau

101
10–2

10–1

1radiation (µGy h–1)

10102

no. of spider webs(e) 102

101
10–2

10–1

1
radiation (µGy h–1)

10102

Figure 2. Abundance of (a) bumble-bees, (b) butterflies, (c) grasshoppers, (d ) dragonflies and (e) spider webs estimatedduring line transects in July 2008 in relation to background radiation (mGy hK1) around Chernobyl, Ukraine and Belarus.
(The lines are the linear regression lines.)

The negative relationship extended to the range
0.01–1 mGy hK1 (figures 1 and 2), suggesting that
invertebrates are affected even at levels of contamination below one hundred times normal levels.
Most radiation around Chernobyl is currently inthe topmost soil (Shestopalov 1996), where mostinvertebrates live. For example, butterfly eggs, larvaeor pupae spend time in the soil layer or the vegetation
just above. This could negatively affect survival
and fecundity, and hence abundance. Alternatively,
indirect effects of radiation on prey could potentiallyexplain the reduced abundance of spiders anddragonflies, but not the reduced abundance of bumblebees, butterflies and grasshoppers.
Point counts covered many different sites, implyingthat factors other than radiation varied among sites. Notsurprisingly, we, on average, explained only 6 per centof the variance. The second kind of census based on awithin-site design better controlled for confounding
Biol. Lett.

variables. On average, the relationship between abundance and radiation explained 22 per cent of thevariance based on transects.
These results have implications for ecosystems andoverall ecosystem functioning. Reduced abundance ofpollinators generally affects plant fecundity and seed
set, when plant fecundity is pollen limited (Proctor
1996). Likewise, spiders are important predators(Wise 1993), and reductions in abundance can haveimportant consequences for abundance of otherinvertebrate taxa (e.g. Snyder & Wise 2001).
Pollination and predation are considered important
ecosystem services (Costanza et al. 1997), and disruption may affect the overall ecosystem functioning,suggesting that the Chernobyl region and its surroundings is a perturbed ecosystem.
We acknowledge help from I. Chizhevsky, G. Milinevski, G.
Rudolfsen, S. Rushkovsky and N. Saino. We gratefullyDownloaded from rsbl.royalsocietypublishing.org on 19 March 2009

4A. P. Møller & T. A. Mousseau

Radiation and invertebrate abundance

acknowledge support from US National Science Foundation, Samuel Freeman Charitable Trust, CRDF, NATO
CLG program, Fulbright Program and National Geographic Society.

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