Oecologia (2012) 170:1155–1165
DOI 10.1007/s00442-012-2374-0

GLOBAL CHANGE ECOLOGY - ORIGINAL RESEARCH

Ecosystems effects 25 years after Chernobyl: pollinators,
fruit set and recruitment
Anders Pape Møller • Florian Barnier •Timothy A. Mousseau

Received: 19 September 2011 / Accepted: 16 May 2012 / Published online: 17 June 2012
Ó Springer-Verlag 2012

Abstract Animals are assumed to play a key role inecosystem functioning through their effects on seed set,
seed consumption, seed dispersal, and maintenance of plantcommunities. However, there are no studies investigating
the consequences of animal scarcity on seed set, seed
consumption and seed dispersal at large geographicalscales. We exploited the unprecedented scarcity of pollinating bumblebees and butterflies in the vicinity of Chernobyl, Ukraine, linked to the effects of radiation onpollinator abundance, to test for effects of pollinatorabundance on the ecosystem. There were considerably
fewer pollinating insects in areas with high levels of radiation. Fruit trees and bushes (apple Malus domestica, pear
Pyrus communis, rowan Sorbus aucuparia, wild rose Rosarugosa, twistingwood Viburnum lantana, and European
cranberry bush Viburnum opulus) that are all pollinated by
insects produced fewer fruit in highly radioactively contaminated areas, partly linked to the local reduction inabundance of pollinators. This was the case even whencontrolling for the fact that fruit trees were generally

smaller in more contaminated areas. Fruit-eating birds likethrushes and warblers that are known seed dispersers wereless numerous in areas with lower fruit abundance, evenafter controlling for the effects of radiation, providing a
direct link between radiation, pollinator abundance, fruit
abundance and abundance of frugivores. Given that the
Chernobyl disaster happened 25 years ago, one would
predict reduced local recruitment of fruit trees if fruit set
has been persistently depressed during that period; indeed,
local recruitment was negatively related to the level ofradiation and positively to the local level of fruit set. The
patterns at the level of trees were replicated at the level ofvillages across the study site. This study provides the firstlarge-scale study of the effects of a suppressed pollinator
community on ecosystem functioning.
Keywords Chernobyl  Ecosystem functioning  Fruits 
Plant recruitment  Radiation

Introduction

Communicated by Jeff Karron.
A. P. Møller (&)
Laboratoire d’Ecologie, Systématique et Evolution,
CNRS UMR 8079, Université Paris-Sud, Bâtiment 362,
91405 Orsay Cedex, France
e-mail: anders.moller@u-psud.fr
F. BarnierCentre d’Etudes Biologiques de Chizé, CNRS,
79360 Villiers en Bois, France
T. A. Mousseau
Department of Biological Sciences, University of South
Carolina, Columbia, SC 29208, USA

The role of different taxa in the functioning of ecosystems
is currently of great scientific and practical interest, given
the looming extinction crisis due to human activity,
including climate change (review in Hooper et al. 2005).
The effects of key taxa on ecosystem functioning arewidely assumed, based on microcosm experiments andsmall-scale field experiments (review in Loreau et al.
2002), although there is little empirical evidence derived
from large-scale field studies.
Reduced abundance of pollinating insects like bumblebees and butterflies often impairs plant fertility and seed or
fruit set because plant fecundity is frequently pollen-limited (Faegri and van der Pijl 1966; Proctor 1996). For

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example, Knight et al. (2005) reviewed a large number ofstudies that showed evidence of pollen limitation. Burd
(1994) reported that 62 % of 258 species showed evidenceof pollen limitation. While pollen limitation may be
important for seed set, this may not have consequences forseedling production or recruitment. In fact, evidence suggesting effects of pollen limitation on population dynamics
of plants is meager at best (Ashman et al. 2004; Price et al.
2008; Waser et al. 2010). Because farming and forestry
rely on pollination for maintaining high levels of productivity, pollination has been considered one of the mostimportant ecosystem services (Costanza et al. 1997; Kearns
et al. 1998). It is not surprising that there are no studies thathave investigated these presumed effects of the absence or
reduction in abundance of pollinating insects at large spatial scales because large-scale experiments are rarely ifever possible.
The Chernobyl disaster on 26 April 1986, which released
vast amounts of radioactive material across large areas innorthern Ukraine, southwestern Russia and southern Belarus,
may provide such an example of the effects of absence ofpollinators at a large spatial scale on reproductive performance of plants including local recruitment. This disaster may
also have directly reduced the abundance of frugivores that areoften the main dispersers of plant seeds. The ecological consequences of radiation from the Chernobyl catastrophe arepoorly known because more than 20 years of research has so
far failed to conduct even the most basic types of censuses ofabundance and species richness (Zakharov and Krysanov
1996; Møller and Mousseau 2006; Yablokov et al. 2009).
Only very recently have we shown dramatic reductions in
species richness and abundance of breeding birds and major
invertebrate taxa such as bumblebees, butterflies, grasshoppers, dragonflies, and web-building spiders around Chernobyl(Møller and Mousseau 2006, 2007a, 2011).
The objectives of this study were to test for a supposed
effect of radiation on pollinator abundance at a large spatial
scale, under the assumption that a lack of pollinators would
have consequences for fruit production, abundance of frugivores, and recruitment by fruit trees and bushes. We did so byconducting extensive censuses of pollinators, frugivorous
birds, and fruiting trees and shrubs across 19 villages innorthern Ukraine differing in level of radiation by more thanfour orders of magnitude, with radiation varying by more than
one order of magnitude within most sites.

Materials and methods
Study areas and censuses
This study was based on extensive censuses of pollinatinginsects, fruit set, and birds eating fruit within and just

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outside the Chernobyl Exclusion Zone in Ukraine with allvillages used for sampling indicated in Fig. 1.
We censused pollinating insects during May–June
2006–2009, abundance of fruits and recruits of plants
during September 2007, and birds eating fruit likewiseduring September 2007. Censuses were conducted at 19
villages separated by distances of up to 15 km (each village
having been evacuated after the Chernobyl disaster in1986). In each of these villages, we censused all fruit trees
in all gardens, with most gardens in 2007 still holding atleast one live apple and one live pear tree planted before1986). At each village, we conducted point censuses, wherean observation point constituted a location with 5 min ofrecordings of individual plants, their fruit, pollinators, andfrugivorous birds.
Censuses of pollinating insects
A.P.M. conducted standard point counts during late May–
early June 2006–2009 (a total of 898 counts widely distributed across forested areas), with each point being
censused once during 5 min during which all bumblebees,
butterflies, and birds seen or heard were recorded (Møller
1983; Bibby et al. 2005; Møller and Mousseau 2007a,2009). We did not census other taxa such as Diptera
because inclusion of additional taxa would have extended
the duration of the study and hence increased exposure toradiation. Inclusion of Diptera and other insect orders
would also have caused problems of distinguishing
between pollinating and non-pollinating taxa. The bumblebees and butterflies recorded were all pollinators asshown by observations of these insects visiting flowers andhaving contact with reproductive parts of flowers during
such visits. Honeybees Apis mellifera are now extremelyrare in the Chernobyl Exclusion Zone, leaving insect pollination to species of wild bees, bumblebees, and butterflies. Indeed, our attempts to collect Drosophila from the
Exclusion Zone in late summer 2002 were largely unsuccessful due to an almost complete lack of fruit, with the
only exception being the town of Chernobyl where a studyof honeybees using introduced bee-hives was locallyassociated with high fruit set for both apples and pears, but
not in neighboring villages (our own unpublished observations). Møller and Mousseau (2009) report the identity of
bumblebee and butterfly species for the first 3 years of thecensus of these insects. Census points were located at aninterval of at least 100 m within forested areas around
Chernobyl (Fig. 1). Forested areas were selected because
censuses were conducted in order to study the effects ofradiation in the main habitat in the Chernobyl Exclusion
Zone, and because secondary growth in villages has now
essentially turned these into secondary forest separated byopen fields. The point counts were made across a range ofOecologia (2012) 170:1155–1165

1157

Fig. 1 The distribution ofvillages used for sampling in
relation to radiation levels(darker areas have higher
radiation levels) around
Chernobyl Nuclear Power Plant(NPP) in Ukraine. The 19
villages used for the fruit census
indicated by filled circles. Map
redrawn from European Union(1998)

background radiation levels spanning over four orders ofmagnitude (Fig. 1; Møller and Mousseau 2007a, 2009).
Census of fruit bushes and trees
At each of the census points in September 2007m all fruit
bushes and trees with a height larger than 1 m within adistance of 50 m from the location of the point wererecorded using a pair of binoculars and inspection of allsites that were invisible from the census point. This
amounted to a total of 1,329 bushes and trees of apple
Malus domestica, wild pear Pyrus communis, wild rose
Rosa rugosa, rowan Sorbus aucuparia, twistingwood
Viburnum lantanam and European cranberry bush V. opulus across the same 374 census points that were used for
censusing insects and birds. These six plant species constitute the majority of all widely distributed bird-dispersed
plants, occurring commonly and widely across all study
sites. All six species are generally self-incompatible andsexually reproducing with no vegetative or asexual propagation. These species are frequently visited by pollinators,
and at least apple is known to require pollinators for
maximum reproductive success (Mouton 2011). Althoughhoneybees Apis mellifera are the most common pollinatorsof apples and pears (McGregor 1976; Stern et al. 2004;
Mouton 2011), available data derive almost entirely frommanaged orchards with next to no information on pollinators under natural conditions. We used a height thresholdof 1 m for inclusion because inclusion of shorter individuals would have required considerably more search effort

due to tall grass and shrub. We recorded height of all
bushes and trees to the nearest meter because larger bushes
and trees are expected to have more fruit, and radiation
may reduce growth of bushes and trees. For a sub-sample
of 30 bushes and treesm we subsequently measured actual
tree heights with a measuring tape to the nearest meter. The
two estimates were strongly positively correlated (Pearsonr = 0.98, t = 39.68, P \ 0.001), and did not differ significantly from each other (paired t test: t = 0.57, df = 29,
P = 0.57). This provides evidence of our estimates ofheight of bushes and trees being reliable.
We also estimated the number of fruits on each bush ortree to the nearest multiple of ten. Again, for the same subsample of 30 bushes and trees mentioned above, we subsequently counted the exact number of fruits. The two
estimates were strongly positively correlated (Pearsonr = 0.99, t = 221.73, P \ 0.001), and did not differ significantly from each other (paired t test: t = 0.18, df = 29,
P = 0.86). This provides evidence of our estimates of theabundance of fruits being reliable.
Finally, we classified all apple and pear trees as recent
recruits or older trees based on the clearly bimodal distribution of tree heights caused by recruitment from before
1986 having been prevented by human harvest of fruit. We
set the height threshold for recent recruits that have entered
the population since 1986 at 5 m. Among the 298 individuals 5 m or shorter, there were only two apple trees thatwere clearly older than the Chernobyl disaster, as judged
from the diameter of their trunks, and that had recently had
broken trunks causing these trees to be shorter than 5 m.

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These two individuals were subsequently categorized as
old trees pre-dating 1986, leaving 296 recruits. The results
reported on recruitment rate were qualitatively similar, if
we used a threshold of 4 or 6 m instead of 5 m.

species consists of fruit during fall and winter. Our
observations of frugivory by these species fit well withwhat is reported in the ornithological literature (Cramp andPerrins 1988–1994).

Censuses of birds

Measuring background radiation levels

A.P.M. censused birds including fruit-eating birds during
September 2007 (a total of 374 points) using the same point
census method as described above. Bird abundance estimates can be affected by many different potentially confounding variables (Møller 1983; Bibby et al. 2005), and,
therefore, it is crucial to statistically control for the effectsof such variables on abundance estimates. That must also
be the case for the abundance of insects such as bumblebees and butterflies. We quantified habitat (agricultural
habitats with grassland or shrub, deciduous forest, or
coniferous forest estimated to the nearest 10 % of groundcoverage within a distance of 50 m from each of theobservation points). Maximum height of trees was estimated to the nearest 5 m, and soil type was classified aseither loam/clay or sand. The presence or absence of open
water within a distance of 50 m from each point was also
recorded. Weather conditions can affect bird activity andhence census results (Møller 1983; Bibby et al. 2005), and
it is well known that many bird are more active during
sunny and warm weather than during cold and rainy conditions. Thus, we recorded cloud cover at the start of eachpoint count (to the nearest eighth, range 0–1 during thecensuses), temperature (degrees Celsius, range 12–28 °C),
and wind force (Beaufort, range 0–4 during the censuses).
For each point count we recorded time of day when the
count was started (to the nearest minute). Because theactivity of many birds shows a U-shaped relationship withtime of day, with high levels of activity in the morning andless so in the evening (Møller 1983; Bibby et al. 2005), we
also included time squared as an additional variable in theinitial models. These environmental variables were enteredinto the initial statistical models to control for the potentially confounding effects of these variables (see ‘‘Statistical methods’’).
We considered the following bird species to be frugivores, based on our own observations in the field during thestudy (with the main fruits eaten mentioned in parentheses): blackbird Turdus merula (all species), song thrush
Turdus philomelos (all species), fieldfare Turdus pilaris (allspecies), mistle thrush Turdus viscivorus (all species),
robin Erithacus rubecula (Viburnum), redstart Phoenicurus
phoenicurus (Viburnum), black redstart Phoenicurus ochruros (Viburnum), bullfinch Pyrrhula pyrrhula (Sorbus,
Viburnum), blackcap Sylvia atricapilla (Viburnum), garden
warbler Sylvia borin (Viburnum), and greenfinch Carduelis
chloris (Rosa rugosa). A large fraction of the diet of theseWe measured radiation in the field and cross-validated
these measurements with those reported by the Ministry of
Emergencies. Once having finished the 5-min census, wemeasured a, b, and c radiation levels at ground level
directly in the field at each point using a hand-held
dosimeter (Model: Inspector; SE International, Summertown, TN, USA). We measured levels 2–3 times at eachsite and averaged the results. We cross-validated ourmeasurements against data from the governmental measurements published by 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 = 1,546.49, df =1,252, r2 = 0.86, P \ 0.0001, slope (SE) = 1.28 (0.10)],suggesting that our field estimates of radiation provided
reliable measurements of levels of radiation among sites.
The measurements by the Ministry of Emergencies wereobtained by repeated standardized measurement of radiation at the ground level in a large number of different
localities in Ukraine. Radiation levels vary considerably
at geographical distances of hundreds of meters due toheterogeneity in the deposition of radiation after the
Chernobyl accident (Fig. 1; Shestopalov 1996), and ourmeasurements at the census points ranged from 0.01 to
379.70 lSv/h, or more than four orders of magnitude.
Among the 19 villages, radiation levels varied by morethan an order of magnitude in 12 of them. Thus, radiationlevel was a continuous variable in the analyses. The
abundance of census points at different radiation levels isshown in the figures in Møller and Mousseau (2009).

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Statistical methods
Abundance of fruit, tree height, abundance of pollinatorsand frugivores, and radiation level were log10-transformed
and the local abundance of recently recruited trees and oldtrees was square-root transformed to normalize data. Therewas still significant heterogeneity in variances among
villages after these transformations, thereby violating
assumptions for parametric tests. We assumed that these
violations would not have major consequences due to thelarge number of observations included in each analysis. We
explicitly tested for effects of these violations of assumptions by re-doing all analyses using ranked variables. Noneof the conclusions changed qualitatively following thisapproach (results not shown). We included all main effects

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and two- and three-way interactions in maximal models,eliminating terms using the F test for model selection(Crawley 2002). The final best-fit model was reached when
all variables had a significant effect at P \ 0.05.
We developed best-fit statistical models to assess therelationship between fruit set (response variable) andplant species, radiation, village as a random factor toaccount for multiple measurements within villages, andplant height (because large plants are expected to produce
more fruit, and size may be affected by radiation) andtheir interactions, as implemented in the statistical software JMP (SAS Institute 2012). These models were
subsequently modified by inclusion of abundance of
bumblebees and butterflies as two additional predictor
variables in order to test for an effect of pollinators on
fruit set. Although the abundance of pollinators varies
among years, Møller and Mousseau (2011) have shownconsistent negative relationships between abundance ofbutterflies and bumblebees, respectively, and level ofbackground radiation.
At the next trophic level in the food chain, we tested
whether the abundance of frugivorous birds could be predicted by abundance of fruit, level of radiation, village as arandom factor to account for multiple measurements within
villages, environmental variables that could affect theabundance of birds such as time of the day, and weather
variables and their interactions.
We developed statistical models for recruitment rate(the local abundance of recruits at a given census point) byrelating this to the abundance of older trees, radiation level,and village as a random factor to account for multiple
measurements within villages and their interaction. In asecond model, we also included current fruit set as anadditional predictor variable, and its interactions with
abundance of older trees and radiation level to test foreffects of fruit set on recruitment rate. This set of models
assumes that the relative level of current fruit set of individual trees is representative in terms of relative abundance
for fruit set in recent years. Although untested, it seems
likely that this assumption is fulfilled because different
sites have trees of approximately the same height, the samesoil, the same radiation level, and the same pollinator
community in different years.
In a final series of analyses, we used means per village
to test if the effects found at the level of fruit tree individuals or census points could be extended to the largescale level of villages.
We estimated effect sizes as a reflection of the strengthof relationships, using Pearson product-moment correlation
coefficients as our metric. We used the guideline by Cohen(1988) that correlation coefficients of 0.10, 0.30, and 0.50,
respectively, explaining 1, 9, and 25 % of the variance, areweak, intermediate, and strong effects.

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Results
Abundance of pollinators in relation to radiation
We recorded 345 bumblebees and 439 butterflies during
the 898 point counts, mean 0.38 bumblebees (SE = 0.03)
and 0.49 butterflies (SE = 0.03) per census point. The
most common species of bumblebees were Bombus terrestris (74.3 %), B. agrorum (13.7 %), and B. lapidarius(6.9 %). The most common species of butterflies were
Aporia crataegi (36.6 %), Pararge aegeria (13.8 %), andCoenonympha pamphilus (11.0 %). The abundance of
bumblebees and butterflies decreased with increasing levelof background radiation [Fig. 2a; bumblebees: F = 3.61,
df = 15,868, P \ 0.0001, slope (SE) = -0.057 (0.006);
Fig. 2b; butterflies: F = 3.52, df = 15,868, P \ 0.0001,
slope (SE) = -0.027 (0.007)]. The decrease in abundanceacross the more than four orders of magnitude range inbackground radiation levels amounted to 72 % for bumblebees and 40 % for butterflies, leaving the most contaminated areas with few insect pollinators.
Abundance of fruit in relation to radiationand pollinators
We recorded fruit set by 1,329 bushes and trees during thestudy. The number of apple trees per observation point
ranged from 0 to 17, mean (SE) = 1.53 (0.12), n = 374,
while the number of pear trees per observation point ranged
from zero to 18, mean (SE) = 1.71 (0.13), n = 374. The
number of fruits per census point was 107 (SE = 16) forapple, 91 (15) for pear, 10 (2) for rose, 0.9 (0.7) for rowan,
8 (2) for twistingwood and 76 (18) for European cranberry
bush. The abundance of fruit per tree decreased withincreasing level of background radiation, as shown forapples in Fig. 2c.
First, we analyzed abundance of fruit in relation to plant
species, radiation, plant height, site, and their interactions(Table 1). Fruit set was explained by three predictor variables and three two-way interactions in a model that
accounted for 42 % of the variance, while the three-way
interaction was not included (Table 1). The abundance offruit per individual plant varied among plant species, and,unsurprisingly, larger plants produced more fruit (Table 1).
The effect of radiation on fruit set varied significantly
among plant species as shown by the interaction between
species and radiation (Table 1), showing that species differed in susceptibility to effects of radiation. There was a
weak effect of species by height interaction, implying thatfruit set depended on height in different ways among
species (Table 1). Finally, there was a significant interaction between radiation and height, implying that radiation
reduced fruit set for a given height (Table 1).

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intermediate effect size (Table 2). In addition, there was asignificant positive effect of abundance of butterflies (Fig. 3),
with a small effect size, while the effect of bumblebees on fruit
set was small and non-significant (Table 2). Unsurprisingly,
fruit set varied among plant species, and the effect of radiation
on fruit set varied among plant species (Table 2), as shown by
the species by radiation interaction. There was a significant
interaction between radiation and abundance of butterflies on
fruit set (Table 2). The negative sign of this interaction
implies that for a given abundance of butterflies fruit set
decreased with increasing level of radiation. Finally, there wasa significant interaction between abundance of butterflies andbumblebees, suggesting that fruit set for a given abundance ofbutterflies increased even more when bumblebees wereabundant (Table 2). In the remainder of the paper we analyze
apples and pears in more detail.
Abundance of frugivorous birds in relation
to abundance of fruit and radiation
We recorded between 0 and 34 frugivorous birds at each of
the 374 census points, mean (SE) = 0.93 (0.13). The mostabundant species was the blackbird with 117 individuals,
followed by fieldfare (114 individuals), song thrush (51individuals), robin (37 individuals), black redstart (12individuals), blackcap (6 individuals), mistle thrush (5individuals), and redstart, bullfinch, greenfinch, and garden
warbler, each accounting for a single individual.
The abundance of frugivores was explained by a modelthat included only four predictor variables, accounting for
6 % of the variance (Table 3). The abundance of frugivores
increased significantly with local abundance of apples, witha small effect size (Fig. 4; Table 3). Furthermore, theabundance of frugivores decreased weakly with radiationlevel, and there were small but significant effects of timeof day and cloud cover on recorded abundance of frugivores (Table 3). No interaction effect reached statisticalsignificance.
Recruitment by fruit-producing bushes and trees
in relation to radiation and abundance of fruit
Fig. 2 Mean (±SE) abundance of a bumblebees and b butterflies per
census point, and c mean (SE) number of apples per tree in relation to
background level of radiation (lSv h-1) around Chernobyl NPP

In a subsequent model we added the abundance of bumblebees and butterflies to the model in Table 1 to test if theabundance of pollinating insects explained variation in fruit
set (Table 2). In this model, fruit set was explained by four
predictor variables and three two-way interactions that
accounted for 27 % of the variance, while the remaining
interactions did not reach statistical significance (Table 2).
Radiation was significantly negatively related fruit set, with an123

We recorded 100 recent recruits and 322 old apple trees,giving rise to a ratio of 0.31 for recruits relative torecruiting trees, while for pears the comparable numbers
were 196, 305 and 0.64. Plant individuals considered recent
recruits were 3.8 m tall (SE = 0.1, n = 100) for apples,while old apple trees were 9.3 m tall (SE = 0.2, n = 322).
Similar numbers for pears were for recent recruits 3.1 m(SE = 0.1, n = 196) for recent recruits, while old pear
trees were on average 10.7 m tall (SE = 0.3, n = 305).
The best-fit models relating number of recruits at eachplot to the number of trees, radiation and their interaction

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Table 1 Relationship between fruit set and plant species, radiation level, height, and their interactions for 1,329 fruit bushes and trees around
Chernobyl
Variable

Sum of squares

df

F

P

Species (S)192.04

5

Radiation (R)47.11

Height (H)

94.31

S9R

37.69

Slope (SE)64.18

\0.0001

1

78.72\0.0001-0.463 (0.052)

1

157.59\0.00011.510 (0.120)

5

12.60

\0.0001

S9H

17.81

5

5.95

\0.0001

R9H

15.74

1

26.30

\0.0001

Error

783.971,310

Effect size
0.22
0.24
0.33
0.10
0.07

-0.657 (0.128)

0.14

Effect size is the Pearson product-moment correlation coefficient. The model had the statistics F = 51.98, df = 18, 1,310, r2 = 0.42,
P \ 0.0001. The three-way interaction did not reach statistical significance
Table 2 Relationship between fruit set and plant species, radiation level, abundance of pollinators and their interactions for 1,329 fruit bushes
and trees around Chernobyl
Variable

Sum of squares

Species (S)Radiation (R)127.97
55.15

Butterflies (L)

19.52

df

F

P

Slope (SE)

Effect size

5
1

34.41
74.15

\0.0001\0.0001-0.447 (0.052)

0.16
0.23

1

26.24

\0.0001

0.613 (0.120)

0.14

0.188 (0.139)

Bumblebees (B)

1.36

1

1.83

0.18

S9R

14.23

5

3.83

0.0019

0.04
0.05

R9L

12.39

1

16.65

\0.0001-0.693 (0.170)

0.11

L9B

8.74

1

11.75

0.00061.762 (0.514)

0.09

Error

975.831,312

Effect size is the Pearson product-moment correlation coefficient. The model had the statistics F = 32.97, df = 15, 1,312, r2 = 0.27,
P \ 0.0001. The three-way interactions did not reach statistical significanceFig. 3 Number of apples per tree in relation to abundance ofbutterflies per census point in areas around Chernobyl NPP

included the number of trees, radiationn and number oftrees by radiation interaction for both tree species(Table 4). For applesn the relationship accounted for 42 %of the variance in recruitment, while for pearsn this was
51 %. Unsurprisingly, the number of recruits increased
strongly with the number of trees for both species,

accounting for large effect sizes (Table 4). There was asignificant negative relationship between recruitment rate
and radiation (Fig. 5; Table 4). Finally, the significant
negative interaction between number of trees and radiation
implied that for a given number of trees recruitment
decreased even more than linearly with increasing levels ofradiation (Table 4).
In a final model, we also included current fruit set as anadditional predictor to those listed for the model inTable 4, under the assumption that relative local fruit set isrepeatable among years and hence should correlate positively with recruitment rate. The two models explained asimilar amount of variance with the same predictor variables having similar effect sizes as the previous models(Table 5). In addition, fruit set also entered with a weak but
significant effect size, showing that local recruitment
indeed increased with increasing fruit set (Table 5).
Large-scale effects
The abundance of both butterflies and bumblebees
decreased with increasing level of radiation among the 19
villages [butterflies: F = 10.89, df = 1,17, P = 0.004,
slope (SE) = -0.139 (0.042); bumblebees: F = 8.51,

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Table 3 Relationship between abundance of frugivorous birds and fruit set, radiation level, environmental variables including weather and timeof day around Chernobyl
Variable

Sum of squares

No. apples

0.27

Radiation
Time
Cloud cover
Error

df

F

P

Slope (SE)

Effect size

1

4.28

0.039

0.027 (0.013)

0.11

0.27

1

4.39

0.037

-0.040 (0.019)

0.11

0.61

1

9.84

0.0018-0.016 (0.005)

0.16

0.43

1

6.94

0.0088-0.088 (0.033)

0.13

22.87

374

Effect size is the Pearson product-moment correlation coefficient. The model had the statistics F = 5.84, df = 4, 369, r2 = 0.06, P \ 0.0001

with the abundance of butterflies [butterflies: F = 8.44,
df = 1,17, P = 0.010, slope (SE) = 2.808 (0.967); bumblebees: F = 9.11, df = 1,17, P = 0.008, slope (SE) =2.040 (0.676)], while there were no significant effects forbumblebees. The abundance of frugivores increased with theabundance of apples [F = 8.66, df = 1,17, P = 0.009,
slope (SE) = 0.136 (0.046)], while there were no significant
effects for pears or radiation. Finally, the abundance ofrecruits increased with the abundance of fruit [apples:F = 10.12, df = 1,17, P = 0.006, slope (SE) = 0.298(0.094); pears: F = 17.60, df = 1,17, P = 0.0006, slope(SE) = 0.500 (0.119)] independent of radiation. There wasan independent positive association between number of
recruits and the abundance of frugivores for pear [F = 6.62,
df = 1,16, P = 0.021, slope (SE) = 0.857 (0.333)].
Fig. 4 The abundance of frugivorous birds per census point inrelation to abundance of apples per tree in areas around Chernobyl
NPP

Discussion

df = 1,17, P = 0.010, slope (SE) = -0.100 (0.034)]. The
amount of fruit per tree decreased with increasing level ofradiation across the 19 villages [apples: F = 18.71,
df = 1,17, P = 0.0005, slope (SE) = -0.783 (0.181);
pears: F = 10.63, df = 1,17, P = 0.0046, slope (SE) =-0.475 (0.146)]. The amount of fruit per tree increased

We found a severe reduction in the abundance of pollinating insects in the most contaminated areas around
Chernobyl compared to nearby uncontaminated areas in thesame neighborhood (Fig. 2). This reduced abundance ofpollinators was negatively related to fruit production bybushes and trees. The abundance of frugivorous birds

Table 4 Relationship between number of recently recruited trees and number of trees, radiation level, and their interaction; effect size is thePearson product-moment correlation coefficient
Variable

Sum of squares

df

F

P

Slope (SE)

Effect sizeApplesNo. trees (T)

38.89

1

142.58\0.0001

0.438 (0.037)

0.53

Radiation (R)

12.62

1

46.26

\0.0001-0.279 (0.041)

0.33

68.46

\0.0001-0.509 (0.061)

0.40

T9R

18.68

1

Error

100.93370

Pears
No. trees (T)

67.16

1

243.66\0.0001

0.586 (0.038)

0.63

Radiation (R)

19.65

1

71.28

\0.0001-0.336 (0.040)

0.40

97.45

\0.0001-0.549 (0.056)

0.46

T9R

26.86

1

Error

101.99370

The models had the statistics F = 90.22, df = 3, 370, r2 = 0.42, P \ 0.0001 and F = 126.04, df = 3, 370, r2 = 0.51, P \ 0.0001 for apple
trees and pear trees, respectively

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Oecologia (2012) 170:1155–1165

1163

of heavy metals and other pollutants (Kevan 1999). Radiation effects on the abundance of pollinators at Chernobyl
were indicated by negative relationships between counts ofbumblebees and butterflies and local levels of backgroundradiation, with small to intermediate effect sizes. There areat least two potential underlying mechanisms; direct andindirect effects of radiation on abundance of pollinators.
Most radiation around Chernobyl is currently in the topmost 10 cm layer of the soil (Shestopalov 1996; European
Union 1998; Yablokov et al. 2009), where most invertebrates live some or most of their annual cycle. Most butterflies lay their eggs in herbs just above the soil, where
their larvae subsequently feed. Many larvae pupate in thesoil. Adult butterflies spend significant amounts of time in
the herb layer. For bumblebees, nests are usually located in
the soil or the herb layer, where eggs, larvae, and pupae areexposed to radiation from the soil. Adult bumblebees
mainly feed in the herb layer and spend the remaining timein their nests. Thus, there are ample opportunities for
exposure to soil layer radiation for these two major taxa ofpollinating insects. Therefore, direct effects of radiation on
the abundance of bumblebees and butterflies cannot be
ruled out. It is also fully possible that pollinators areaffected indirectly through contamination of nectar andpollen by radionuclides, as reported for honeybees inGermany exposed to the effects of the Chernobyl disaster(Bunzl et al. 1988). Bumblebees directly feed pollen andnectar to their larvae that then may experience increased
doses with consequences for mutations and subsequentviability of their descendants. Likewise, butterflies thattypically feed on nectar and pollen may in this way becomecontaminated and transfer radionuclides to their eggs thatthen suffer reduced viability.

Fig. 5 Mean (SE) recruitment rate of a apples and b pears in relation
to background level of radiation (lSv h-1) around Chernobyl NPP.
Values are the number of recent recruits per tree. The value at100–1,000 lSv h-1 is zerodecreased with decreasing abundance of fruit. Finally,
recruitment by fruit-producing trees decreased withincreasing level of radiation, possibly mediated by areduction in the abundance of pollinating insects and theamount of fruit. These effects at a local scale were replicated at the large-scale level among villages.
Before discussing our findings in detail, we mustemphasize that this study is based on correlational evidence
that does not necessarily imply causal relationships. It isalso important to note that the effect sizes that we reporttypically account for 1–10 % of the variance, which iscommon for ecological studies in any research domain(Møller and Jennions 2002). Pollinators are important bioindicators of the state of the environment including levels

Table 5 Relationship between number of recently recruited trees and number of trees, radiation level, number of fruits and their interaction
Variable

Sum of squares

df

F

P

Slope (SE)

Effect sizeApplesNo. trees (T)

9.35

1

34.74

\0.0001

0.332 (0.056)

0.29

Radiation (R)

10.24

1

38.04

\0.0001-0.257 (0.042)

0.31

No. fruits
T9R

1.65
15.47

1
1

6.13
57.50

0.014
\0.0001

0.102 (0.041)-0.475 (0.063)

0.13
0.37

Error

99.28

369

Pears
No. trees (T)

38.00

1

139.34\0.00010.530 (0.045)

0.52

Radiation (R)

18.05

1

66.19

\0.0001-0.325 (0.040)

0.39

No. fruits

1.36

1

5.00

0.026

0.073 (0.033)

0.12

T9R

24.11

1

88.43

\0.0001-0.528 (0.056)

0.44

Error

100.62369

The other two-way interactions and the three-way interaction did not reach statistical significance. Effect size is the Pearson product-moment
correlation coefficient. The models had the statistics F = 70.14, df = 4, 369, r2 = 0.43, P \ 0.0001 and F = 96.80, df = 4, 369, r2 = 0.51,
P \ 0.0001 for apple trees and pear trees, respectively

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1164

Fruit set increased significantly with the abundance ofbutterflies, with a small effect size, while surprisingly there
was no significant relationship for bumblebees. Even after
controlling for abundance of pollinators, there was still anegative relationship between radiation and fruit set, with asmall effect size. We suggest that this apparent direct effectof radiation is caused by elevated pollen abnormality(Kordium and Sidorenko 1997) giving rise to embryo
abnormalities and endosperm abortion, as already shown inradiation experiments on domestic apples (Malus domestica; Nicoll et al. 1987). However, the relationship between
pollen viability and radiation is not consistently negative,
with some species showing no relationship and others
showing strong negative effects (Kordium and Sidorenko
1997). Two statistically significant interactions predicting
fruit set are well worth discussing. First, we found that therelationship between radiation and fruit set differed significantly among plant species. Such interspecific variationin susceptibility to radiation has already been reported forbirds which have been found to vary considerably in thegenerally negative relationship between abundance andradiation (Møller and Mousseau 2007b). Similarly, thefrequency of pollen abnormalities can be related to radiation exposure, and also vary significantly among plant
species (Kordium and Sidorenko 1997). Second, for agiven abundance of butterflies, fruit set was disproportionately reduced at high levels of radiation. This finding
implies that an absence of pollinators and radiation act in a
multiplicative way to reduce fruit set, the two factors incombination being worse that either on their own. There
are no previous studies assessing whether such effects ofradiation are additive or multiplicative. Finally, we cannot
exclude the possibility that other mechanisms that have notbeen studied here could account for the observed patterns.
All taxa studied so far at Chernobyl have shown negative
relationships between abundance and level of radiation,although to varying degrees (Møller and Mousseau 2011).
Therefore, it is unlikely that reduced fruit set and recruitment rate at high radiation sites would be caused byincreased abundance of flower and fruit predators andphytophagous pests such as insects compared to low radiation sites. Likewise, it seems unlikely that generalist
pollinators may have profited from the reduced abundanceof specialist pollinators such as bumblebees and butterflies
because all taxa investigated so far have shown negative
relationships between abundance and radiation (Møller andMousseau 2011).
Ten different species of frugivorous birds were recorded
during our study, with a very heterogeneous spatial distribution. Local abundance of frugivores increased with theabundance of apples. There was an additional intermediateand negative effect of radiation, implying that the abundance of frugivores decreased with increasing level of123

Oecologia (2012) 170:1155–1165

background radiation. We have previously shown thatthrushes, that typically eat considerable amounts of soil
invertebrates, are particularly negatively affected by radiation because most radionuclides are currently located in
the top soil layer (Shestopalov 1996; European Union
1998; Yablokov et al. 2009) where their prey species live
(Møller and Mousseau 2007a). However, we could only
account for 29 % of the variance in local abundance offrugivores, leaving most variance unexplained. Therefore,
we must conclude that seed dispersal by frugivores is at
most weakly negatively affected by level of radiation,suggesting that relatively few seeds disperse from the mostcontaminated areas.
Recruitment rate of trees depends on abundance ofseeds, the quality of these seeds, their growth conditions,and subsequent survival of saplings. There is hardly any
empirical evidence suggesting that pollen limitation
has consequences for population dynamics of plants(Ashman et al. 2004; Knight et al. 2005). These negative
effects of radiation in conjunction with number of trees
could act through reduced pollen viability (Kordium andSidorenko 1997), reduced fruit set (this study), elevatedlevel of embryo abortion (Nicoll et al. 1987), reduced
rates of germination, or elevated risk of mortality during
the first years after germination. We could show
explicitly for the second of these mechanisms acting
through a reduced fruit set that indeed fewer recruits
were recorded when local production of fruits was
reduced, although this was only a weak effect accounting
for slightly more than 1 % of the variance. Despite theweak effect, and the fact that we only estimated fruit set
in a single year, we were still able to document such aneffect on recruitment rate.
We analyzed relationships at the local level of individual plants or census points and found evidence consistent
with the expectation that radiation had negative cascading
effects on the ecosystem. We extended these analyses to alarge geographical scale by investigating relationships
among variables at the scale of mean estimates for the 19
villages within and just outside the Chernobyl Exclusion
Zone. Interestingly, local scale patterns at the level ofindividual plants were replicated at the large geographic
scale, implying that the patterns reported here may extend
to the thousands of square kilometers contaminated withradioactive material in the surroundings of Chernobyl(Fig. 1).
In conclusion, we have shown negative cascading
effects of radiation at Chernobyl from pollinating insects
over fruit set and frugivory to recruitment of fruit-producing plants. These patterns were extended from local
effects at the level of individual plants to the level of villages, showing that radiation from Chernobyl has largescale effects on ecosystem functioning.

Oecologia (2012) 170:1155–1165
Acknowledgments We gratefully acknowledge logistic support andhelp in Ukraine by I. Chizhevsky, G. Milinevski, G. Rudolfsen,
S. Rushkovsky, and N. Saino. N. Waser and three anonymous reviewers
provided constructive comments. We gratefully acknowledge support
from the US National Science Foundation, the University of South
Carolina Environmental Research Initiative Committee (ERIC), theUniversity of South Carolina School of the Environment, the NATO
CLG program, the CRDF, the Fulbright Program, the National Geographic Society, and the Samuel Freeman Charitable Trust. The
research was conducted with all required permissions in Ukraine.

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