Elevated Frequency of Cataracts in Birds from Chernobyl
Timothy Alexander Mousseau1, Anders Pape Møller2*
1 Department of Biological Sciences, University of South Carolina, Columbia, South Carolina, United States of America, 2 Laboratoire d’Ecologie, Systématique etEvolution, CNRS UMR 8079, Université Paris-Sud, Orsay, France

Abstract
Background: Radiation cataracts develop as a consequence of the effects of ionizing radiation on the development of thelens of the eye with an opaque lens reducing or eliminating the ability to see. Therefore, we would expect cataracts to be
associated with reduced fitness in free-living animals.
Methodology/Principal Findings: We investigated the incidence of lens opacities typical of cataracts in more than 1100
free-living birds in the Chernobyl region in relation to background radiation. The incidence of cataracts increased with levelof background radiation both in analyses based on a dichotomous score and in analyses of continuous scores of intensity ofcataracts. The odds ratio per unit change in the regressor was 0.722 (95% CI 0.648, 0.804), which was less than odds ratiosfrom investigations of radiation cataracts in humans. The relatively small odds ratio may be due to increased mortality inbirds with cataracts. We found a stronger negative relationship between bird abundance and background radiation when
the frequency of cataracts was higher, but also a direct effect of radiation on abundance, suggesting that radiation indirectly
affects abundance negatively through an increase in the frequency of cataracts in bird populations, but also through direct
effects of radiation on other diseases, food abundance and interactions with other species. There was no increase inincidence of cataracts with increasing age, suggesting that yearlings and older individuals were similarly affected as is
typical of radiation cataract.
Conclusions/Significance: These findings suggest that cataracts are an under-estimated cause of morbidity in free-living
birds and, by inference, other vertebrates in areas contaminated with radioactive materials.
Citation: Mousseau TA, Møller AP (2013) Elevated Frequency of Cataracts in Birds from Chernobyl. PLoS ONE 8(7): e66939. doi:10.1371/journal.pone.0066939
Editor: Jordi Moya-Larano, Estacion Experimental de Zonas Áridas (CSIC), Spain
Received December 10, 2012; Accepted May 11, 2013; Published July 30, 2013
Copyright: ß 2013 Møller, Mousseau. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Financial support was received from the US National Science Foundation, the University of South Carolina, the North Atlantic Treaty Organization
Collaborative Linkage Grant program, the Civilian Research and Development Foundation, the Fulbright Program, the National Geographic Society, and theSamuel Freeman Charitable Trust. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: anders.moller@u-psud.fr

up at the Chernobyl nuclear power plant showed a post-exposurelevel of dose of only 0.12 Gy, and despite the low level of dose
there was a statistically significant dose response for stage 1
cataract (the initial stage of cataracts) and posterior subcapsularcataracts (located in the subcapsular region of the ocular lens) [7].
Threshold exposure estimates showed that values greater than 700
mGy caused a significant risk of detectable opacities, which is amuch greater risk than what is recommended in radiation
protection guidelines [10]. Studies of atomic bomb survivors haveshown a clear linear dose-response for the frequency of cataracts
without a threshold and this is much lower than the threshold of
2–5 Gy usually assumed by the radiation protection community[11]. A similar conclusion was reached for a study of radiological
technologists [12]. Thus there is evidence consistent with low or no
thresholds [13], and this documented greater susceptibility toradiation than proposed by radiation protection authorities is
consistent with a recent assessment showing that to generally be
the case [14].
The eye lens is almost entirely composed of proteins whoseoxidation and subsequent aggregation and precipitation generate
the opacities characteristic of cataracts [15]. Some cases ofcataracts in humans have a genetic basis [16], although the maincauses of human cataracts are agents that produce oxidative stress(i.e., the imbalance between levels of reactive oxygen species andIntroduction
Cataract is a disease of the eye characterized by an opaque lensthat under normal conditions focus images on the retina to allow
perception of visual information. Such opacities result in a
reduction in vision and even complete loss of eyesight, andcataracts are the single-most common cause of blindness inhumans. The lens of the eye has for a long time been consideredsensitive to ionizing and non-ionizing radiation [1,2]. Cataracts
are a frequent outcome of exposure to radiation [e. g. 3–8]. The
underlying mechanism by which ionizing radiation causes
cataracts is the ionization of water and the production of free
radicals such as hydroxyl and hydrogen radicals. These free
radicals can damage DNA and cause damage or errors in lensprotein formation and hence contribute to cataract formation. The
lenses are almost entirely composed of proteins that can beoxidized with subsequent aggregation and precipitation causing
opacities in the lenses that form the basis of cataracts. Lens
proteins show little turnover throughout the life of an individual
thereby making them particularly susceptible to oxidative stress.
Dose thresholds of 0.5–2.0 Gy for acute exposure and 5.0 Gy for
protracted exposure for radiation cataract are assumed in theliterature [9]. However, to date the most extensive epidemiologicalstudy of 8607 Chernobyl Ukrainian liquidators involved in cleanPLOS ONE | www.plosone.org

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Cataracts in Birds from Chernobyl

although some larger birds (e.g. hawfinches Coccothraustes coccothraustes) were inspected at 206magnification because of the larger
eye and the need for longer examination distances. Examinations
were conducted under a black, lightproof hood to induce iris
dilation and reduce interference from background lighting. Eacheye was scored to the nearest 0.5 on a scale from 0 to 4 with 0
indicating total clarity and scores 1, 2, 3 and 4 denoting increasing
extent of opacity reaching complete opacity at a score of 4. Such a
discrete five-point scale is similar to what has been used in studiesof radiation cataracts in humans [7]. There was considerable
variation among individuals in opacification (Fig. 2) with mosteyes falling between 1 and 2. A lens was scored as 1 if there wasany suggestion of cloudiness in the cornea or lens, 2 if thecloudiness extended across most of the cornea or lens, and 3 if
the cloudiness was sufficiently opaque to obscure details in theiris. A score of 4 indicated the presence of a partial or complete
cataract. Occasionally birds, most noticeably smaller species,
would close one or both their eyes in response to being placed
inside the darkened environment, preventing inspection of one
or both eyes for such individuals. In this case we used the score
for the open eye as an estimate of the mean cataract score forthe two eyes. Although this method requires a period offamiliarization and internal calibration for the observer, scores
were highly repeatable when observations of the same individuals were taken independently by TAM and APM (cataract
score: R = 0.93 (SE = 0.04), F = 27.56, d.f. = 19, 20, r2 = 0.96,
P,0.0001; dichotomous score: R = 0.81 (SE = 0.11), F = 9.47,
d.f. = 19, 20, r2 = 0.90, P,0.0001), as has been reported forsimilar approaches used for human subjects [21]. The overall
procedure lasted 1–2 minutes per bird and was similar in all
study sites.
A selection of photos of the eye is provided in Figure 1. All
photos were captured using an EyeQuick Digital Ophthalmoscopecamera on loan from EyeQuick, LLC. Unfortunately, because of
the constraints of working under field conditions and theoperator’s insufficient training, it was not possible to consistently
and reliably capture images from all birds using this technique.
The images presented here serve only to illustrate the range ofvariation in eye shape and opacity and cannot at present be used
for quantitative analyses of variability.

state of the antioxidant and repair machinery) such as ultraviolet
radiation and smoking, as well as accumulation of effects of free
radicals with aging [15,17]. Accordingly, Galván et al. [18]showed elevated levels of cataracts in wild birds with pheomelaninbased plumage coloration, apparently linked to the effects ofoxidative stress. Cataracts are a rare phenomenon in wild animals[19] because any deterioration in vision will likely very soon befollowed by death due to predation or lack of ability to findadequate and sufficient food for survival.
The objectives of this study were to determine (1) the
relationship between the incidence of cataract and backgroundradiation, using a large database of more than 1100 free-living
birds captured at Chernobyl during 2011–2012. In other words,
we assessed the reliability of the rate of cataracts as a biomarker ofradiation exposure. Because the lifespan of most free-living
animals with impaired vision is bound to be short due to elevatedrisk of predation and inability to find sufficient amounts of food,field estimates of prevalence of cataracts are by definition
conservative. Therefore, the second objective of this study was(2) to determine whether the abundance of different species ofbirds decreased the most in species that showed a stronger impact
of radiation on the incidence of cataracts. Finally, we tested (3) if
the frequency of cataracts increased with age as expected fromhuman studies showing accumulation of free radicals with age [3–8]. Because many birds can be aged reliably as either yearlings orolder individuals [20], we included a categorical age variable andthe interaction between level of background radiation and age as
predictors of the extent of cataracts.

Methods
Ethics Statement
The research complied with requirements for research on birds
in Ukraine, and permission was given by the administration of theChernobyl Excclusion Zone. All sampling was approved in an
ethical review by the University of South Carolina Institutional
Animal Care and Use Committee. All birds were handled shortly,and none died or showed signs of suffering during the shortexamination. All individuals flew upon release.

Study Areas
The research complied with requirements for research on birds
in Ukraine, and permission was given by the administration of
the Chernobyl Exclusion Zone. All birds were handled shortly,and none died or showed signs of suffering during the shortexamination. All individuals flew upon release. We captured
birds in mist nets at eight sites within and just outside theChernobyl Exclusion Zone on 25 May–5 June 2011–2012 fromfour pairs of relatively uncontaminated and contaminated sites(Figure 1). We used 35–45 mist nets each 12 m long for two
consecutive days at each of the study sites (i.e. one evening andone morning capture session at each site). All birds were bandedwith a unique aluminum band for individual identification, andthey were subsequently sexed and aged according to standard
criteria [20], measured, sampled for blood and sperm, andreleased.

Breeding Bird Censuses
We assessed the relationship between abundance and radiation
during the breeding season using point census counts. The point
count census method provides reliable information on relative
abundance of birds [22–25]. It consists of counts lasting 5 minutes
during which the number of birds seen or heard was recorded with
the next census point being located at a distance of more than
100 m. APM conducted these standard point counts during May–
June 2006–2009 in sites around Chernobyl. The fact that one
person made all counts eliminates any variance in results due tointer-observer variability. The counts were made approximately
the same dates and at the same time of the day each of the four
years. Møller & Mousseau [24] provide additional information on
the methods and potentially confounding variables that were taken
into account in the analyses. We have previously tested thereliability of our counts by letting two persons independently
perform counts, and the degree of consistency was high for both
species richness and abundance (details reported by Møller &Mousseau [24]). Relationships between abundance and radiation
are repeatable among years [26]. We provide summary statistics
for the frequency of cataracts in each species and the slope of therelationship between abundance and background radiation level inTable S1.

Frequency of Cataracts
Upon capture all individuals were examined by TAM for thepresence of cataracts or minor opacities in the eyes. This was done
without prior knowledge of the level of background radiation,
thereby making the assessment blind with respect to radiationlevels. Eyes were visually inspected using a standard medical
ophthalmoscope (model ADC 5215) usually at 406 magnification
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Figure 1. Location of the eight study sites in relation to background radiation level (Ci/km2) around Chernobyl, Ukraine. Adaptedfrom Shestopalov (1996).
doi:10.1371/journal.pone.0066939.g001

P,0.0001, slope (SE) = 1.28 (0.10)), suggesting that our field
estimates of radiation provided reliable measurements of levels ofradiation among sites.
In Chernobyl, cesium-137, strontium-90, various isotopes of
plutonium, and americium-241 are found at biologically significant levels across the landscape [28]. Cesium-137, with a half-lifeof about 30 years, decays by beta emission primarily to a metastable isomer of barium-137, which is responsible for the gamma
emissions of this isotope [29]. Thus if ingested, cesium-137 will
generate both beta and gamma doses for living organisms.
Cesium-134 that has a half-life of about 2 years is exclusively abeta emitter and is thus mainly a concern if ingested. Strontium90, with a half-life of about 29 years, is almost a pure beta emitter[29]. Most isotopes of plutonium are alpha emitters and are thus
primarily of concern if ingested, due to the short travel distance ofalpha particles. However, plutonium-241, which is present to asignificant degree in the Chernobyl region, has a half-life of about
14 years, and decays via beta emissions to americium-241 (half lifeof 432 years), which in turn decays via alpha emissions toneptunium-237, with gamma emissions as an additional byproduct.

Background Radiation
We measured the level of background radiation in the field andcross-validated these measurements with those reported by the
Ukrainian Ministry of Emergencies. Once having finished the
5 minute point count we measured radiation levels at ground level
directly in the field at each point where we censused birds using ahand-held dosimeter (Model: Inspector, SE International, Inc.,
Summertown, TN, USA). Likewise, we measured radiation at theexact capture spot for each individual bird. This was done 2–3
times at each site and the measurements were averaged. We havecaptured more than 1200 individual birds in the surroundings ofChernobyl during 2010–2012, and the radiation levels at which
individuals were recaptured the same breeding season, but also thefollowing season were highly repeatable, suggesting that a single
measure of background radiation provide a reliable estimate of
future exposure (T. A. Mousseau et al. unpublished data). We
cross-validated our measurements against governmental measurements published by Shestopalov [27], estimated as the mid-pointof the ranges published in the Chernobyl atlas. This analysis
revealed a very strong positive relationship (linear regression on
log-log transformed data: F = 1546.49, d.f. = 1, 252, r2 = 0.86,
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We assessed the relationship between cataracts and backgroundradiation in three different ways. First, we related our cataract
score of all individuals to background radiation entering species asa random factor to account for the non-independence of multiple
observations of different species. Second, we used nominal logistic
regression to relate the incidence of cataracts to backgroundradiation level after inclusion of species as a factor. Third, we usedordinal logistic regression to relate the incidence of cataracts (anordinal variable) to background radiation level after inclusion of
species as a factor. These three models showed no significant lackof fit. We subsequently related the slope of the relationshipbetween abundance and background radiation to the score ofcataracts in different species of birds, weighting each species
estimate by sample size. Using GLM, we previously estimated theslope of the relationship between abundance and backgroundradiation using log10-transformed abundance for each species at
each observation point and log10-transformed radiation level foreach species [26]. Models were weighted by sample size (thenumber of individuals assessed for cataracts) to account for the factthat sample sizes differed and hence the precision of the estimate
differed among species. Most statistical analyses assume that data
points provide equally precise information about the deterministic
part of total process variation, i.e. the standard deviation of theerror term is constant over all values of the predictor variable [31].
Garamszegi & Møller [32] showed that bias due to variation insample size is a major problem in comparative analyses. If thisassumption of even sampling effort is violated, weighting eachobservation by sampling effort allows the use of all data, giving
each datum a weight that reflects its degree of precision due tosampling effort [31,33,34]. This procedure also allows both rare
and common species to be included and hence avoids any bias insampling due to rarity [35]. All analyses were made with JMP
version 10.0 [36].
We tested if there were phylogenetic patterns in the cataracts
data by means of nested analyses with species nested within genus,
genera nested within families and families nested within orders.
We performed a path analysis [38] of the relationship between
background radiation, cataracts and population trends in relation
to background radiation. Basically, we estimated the partial
regression coefficients for the paths between background radiation,
cataracts and abundance.
We estimated effect sizes by relying on Cohen’s [37] guidelines
for the magnitude of effects, proposing explicit criteria for judging
whether effects are small (Pearson r = 0.10, explaining 1% of thevariance), intermediate (r = 0.30, explaining 9% of the variance) orlarge (r = 0.50, explaining 25% of the variance).

Figure 2. Photographs of selected eyes from Chernobyl birds.
(a) Blackcap (Sylvia atricapilla), normal – score 0; (b) barred warbler(Sylvia nisoria), normal – score 0; (c) blackcap (Sylvia atricapilla), slighthaze in cornea – score 1; (d) barn swallow (Hirundo rustica), significant
haze on cornea – score 2; (e) chiffchaff (Phylloscopus collybita), slighthaze on cornea – score 1; (f) chiffchaff (Phylloscopus collybita),
significant haze on cornea – score 1; (g) barn swallow (Hirundo rustica),
significant haze on cornea – score 3; (h) chaffinch (Fringilla coelebs),
slight haze on cornea – score 1; (i) chaffinch (Fringilla coelebs), clear eye
but deformed eye lids – score 0; (j) tree pipit (Anthus trivialis), significant
opacity of cornea – score 2; (k) robin (Erithacus rubecula), significant
haze on cornea – score; (l) chiffchaff (Phylloscopus collybita), deformed
eye lids, haze on cornea – score 2. All photos captured using an
EyeQuick Digital Ophthalmoscope Camera.
doi:10.1371/journal.pone.0066939.g002

Handheld Geiger counters provide reliable measures ofbackground contamination levels of radionuclides for gamma
sources, and to a lesser degree for beta emitters if the Geiger
detector is in close proximity to the source. However,characterization of alpha emitters usually requires more
complex measurement methods that are usually only tractable
in a laboratory setting due to the short transmission distance ofalpha particles in air.
Given the different characteristics of radionuclides in theenvironment at Chernobyl, field measurements of contaminantlevels are likely to underestimate biologically relevant radiationlevels when the main exposure pathway is via ingestion.
Similarly, background radiation measures in the areas ofChernobyl closest to the reactor (e.g. the Red Forest) very
likely underestimate biologically relevant doses given theabundance of alpha emitting actinides (e.g. plutonium isotopes)that were differentially deposited in this area. That said,
Gashchak et al. [30] have previously reported that internal
dose of small birds captured in Chernobyl is strongly positively
correlated with external dose, accounting for more than 50% of
the variance in internal dose. This result suggests that gamma
radiation measurements are a reasonable proxy for total
exposure at least for the sorts of comparative analyses reported
here, and that results will be conservative with respect to any
reported associations with radiation levels.

Results
There was a highly significant Kendall rank order correlation
between cataract scores for the two eyes (Kendall t = 0.48,
P,0.0001), this score was significantly repeatable (R = 0.72
(SE = 0.02), F = 6.09, d.f. = 1077, 1144, r2 = 0.85, P,0.0001),
and, we used the mean score in subsequent analyses. In
Chernobyl, 391 out of 1111 individual birds or 35.2% had acataract score of 1 or more.
A mixed model with mean cataract score as the response
variable, species as a random effect and radiation as a continuous
predictor accounted for 13% of the variance (Table 1; Figure 3).
However, the residuals from this model were not normally
distributed (Shapiro-Wilk W test, W = 0.88, P,0.0001). The
random species effect accounted for 7% of the variance with therest attributed to radiation. A second model that used cataract
score for both eyes as the response variable and background

Statistical Analyses
We quantified the incidence and the score of intensity ofcataracts using the mist netted sample of birds. As a way of testingfor consistency in cataract scores, we calculated the rank ordercorrelation between cataract score for the left and the right eye.
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Table 1. Mixed model of cataracts in relation to species(random factor) and radiation.

F

Variabled.f.

Intercept

48.66, 1074

log Radiation

1, 1074P

Estimate (SE),0.0001
89.63,0.0001

0.131 (0.014)

The random species effect accounted for a variance ratio of 0.0955 and 8.71% of
the total variance.
doi:10.1371/journal.pone.0066939.t001

radiation and individual as a random factor likewise showed aneffect of radiation (F = 6.31, d.f. = 1, 1108, P = 0.012, estimate(SE) = 0.038 (0.015)) and species (variance ratio = 0.92, 95%
CI = 0.054, 0.274). A third model based on logistic regression
was significant (X2 = 232.75, d.f. = 57, P,0.0001) with no significant lack of fit (X2 = 1822.53, d.f. = 6630, P = 1.00). The effect ofspecies was significant (X2 = 204.52, d.f. = 56, P,0.0001) as was
the effect of radiation (X2 = 101.77, d.f. = 1, P,0.0001). Finally, a
Kendall rank order correlation between cataract scores andbackground radiation was also significant (Kendall t = 0.13,
P,0.0001). When we added age to the random effects model,
the partial effect of age was small and far from significant(F = 0.19, d.f. = 1, 382, P = 0.66), and the same applied to theradiation by age interaction (F = 0.0007, d.f. = 1, 382, P = 0.97).
Thus all analyses supported a hypothetical effect of radiation on
the frequency of cataracts independent of species effects.
A nominal logistic regression model with a dichotomous
cataract variable as the response variable and species andradiation as predictors explained 21% of the variance (Table 2).
There was an intermediate effect of radiation with an odds ratio of
0.284 (95% CI 0.186, 0.431), implying that the incidence of
cataracts increased with level of background radiation. The odds
ratio per unit change in the regressor was 0.722 (0.648, 0.804).
There were weak, but significant phylogenetic signals in thecataracts data as evidenced by nested analyses. That was the casefor genera nested within families (F = 2,42 d.f. = 14, 22, P = 0.031)
and for families nested within orders (F = 56.17, d.f. = 16, 35,
P,0.0001), but not for orders within super-orders (F = 0.00,
d.f. = 3, 51, P = 0.99).
The slope of the relationship between abundance and radiation
was negatively related to the mean level of cataracts with anintermediate effect size (Figure 4; F = 4.91, d.f. = 1, 55, r2 = 0.08,
P = 0.031, estimate (SE) = 20.222 (0.100)). A path analysis showedthat there was a weak positive effect of radiation on cataracts and astronger negative effect on abundance of birds (Figure 5). In
addition there was a negative effect of cataracts on abundance ofbirds (Figure 5). The indirect effect of radiation through cataracts
on abundance was 0.14060.286 = 0.040, while the direct effect
was 0.484. While cataracts accounted for 4.0% (0.28660.140) of
the variance in abundance, radiation accounted for 23.4%(20.484620.484). This implies that the effect of cataracts on

Figure 3. Mean cataracts in birds from Chernobyl in relation to
background radiation level (mSv/h). The linear fit with confidence
intervals is shown.
doi:10.1371/journal.pone.0066939.g003

abundance was a sixth of the effect of radiation per se. The
unexplained variance was 61%.

Discussion
The main findings of this study of cataracts in free-living birds in
the Chernobyl region were that (1) the intensity and the incidenceof cataracts increased with level of background radiation, (2) theslope of the relationship between abundance of breeding birds andbackground radiation decreased with increasing incidence of
cataracts, but also through direct effects due to other diseases, foodabundance or interspecific interactions in different species of birds,
and (3) there was no increase in incidence of cataracts withincreasing age.
Radiation cataracts are a frequent outcome of exposure toionizing radiation [3–8]. While many studies have shown thatatomic bomb survivors, workers in radiation facilities and people
exposed to radiation following nuclear accidents suffer fromelevated risk of developing cataracts [7,11,12], there are to the bestof our knowledge no previous studies of animals. Cataracts in freeliving birds in this study increased in a dose-dependent mannerwith level of background radiation with no evidence of a threshold.
Individuals with opacities in one lens were much more likely toalso develop opacities in the lens of the other eye, thereby
increasing the risk of death for the individual. Here we have shownthat radiation level in a mixed model accounted for anintermediate effect of 0.28, while a logistic regression based on
dichotomous data showed an effect of a similar magnitude (0.30).
The odds ratio for birds was 0.284 (95% CI 0.186, 0.431). This
odds ratio is low compared to estimates for humans ranging from1.25 (1.06–1.47) [12] over 1.30 (1.24–1.55) [11] to 1.54 (1.11–
2.14) [7]. The odds ratio estimated for birds is bound to be

Table 2. Nominal logistic regression model of cataracts in relation to species and background radiation.

VariableP

Chi-squared.f.

Species

182.1256,0.0001

Radiation

98.29

1

0.0001

Estimate (SE)Odds ratio

95% CI for odds ratio

0.759 (0.084)

0.284

0.186, 0.431

2

R was 0.21. The odds ratio and its 95% confidence interval is also reported.
doi:10.1371/journal.pone.0066939.t002

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Figure 5. Path analysis of the direct and indirect relationships
between cataracts and radiation, respectively, and abundanceof breeding birds. U represents the unexplained variance. P-values
for path coefficients are * P,0.05 and *** P,0.001.
doi:10.1371/journal.pone.0066939.g005

effect is bound to be an under-estimate given the likely elevatedprobability of mortality among individuals with cataracts. Possible
direct effects of radiation on abundance include effects on otherdiseases [44], abundance of food [45] and interspecific interactions[46,47].
Most human cases of cataracts are reported in people older than
40 years [3–8]. However, radiation cataracts can affect even young
children, as shown in a study of people exposed to radiation from
Chernobyl in Belarus [3] and studies of children treated withradiation therapy for cancer [48–50]. In addition, recent reports
indicated that health care technicians who use radiation for
medical treatment are at much higher risk of cataract irrespectiveof sex or age [51]. Here we were able to age more than half of all
birds as either yearlings or older individuals using well-establishedexternal age criteria [20]. When entering age as a categoricalpredictor of cataracts in our statistical models together with thelevel of background radiation and species, we found only weak andnon-significant effects of age on the incidence and the severity ofcataracts. Hence radiation exposure rather than age was the main
predictor of cataract. This conclusion must be drawn cautiously
because high mortality rates among individuals with cataracts may
have significantly reduced the fraction of old individuals that are
more likely to develop cataracts.
In conclusion, we have shown increased incidence of cataracts
in free-living birds inhabiting areas with elevated levels of
background radiation around Chernobyl. Cataracts were associated with depressed breeding population sizes in contaminatedareas.

Figure 4. Relationship between slopes for the relationshipbetween abundance and background radiation and thefrequency of cataracts in different species of birds. The size ofsymbols reflects variation in sample size.
doi:10.1371/journal.pone.0066939.g004

conservative given the elevated risk of death experienced byindividuals with cataracts. Although it may seem intuitively
obvious that individual birds with cataracts suffer from reduced
fitness, the magnitude of that cost has so far never been quantified
in birds or other taxa.
Population size of birds can be assessed from point counts[22,23] and mist net captures [39]. Birds and other organisms
have severely depressed breeding population sizes in the mostcontaminated areas surrounding Chernobyl both in Ukraine andin Belarus [24,26,40]. Some of these effects may arise because ofantioxidant deficiency [40], or because of excess mortality due to avariety of health reasons [41]. Studies of humans have shown thata great diversity of disease conditions has developed as aconsequence of exposure to radiation from Chernobyl [8,42]. If
that was also the case in birds, as our data suggests, we should
expect that the species with the strongest negative effects ofradiation on abundance of breeding birds were the species with thehighest frequency of disease. Thus we predicted a negative
relationship between slope of the relationship between abundance
and radiation and incidence of cataracts. This was indeed therelationship that we found. Obviously, we cannot ascertain thatcataracts are the direct cause of these population declines, nor can
we estimate the exact contribution of cataracts to this reduction.
However, given that cataracts are associated with a dramaticincrease in risk of mortality in birds, it seems likely that species
with high frequencies and degree of cataracts will suffer fromelevated levels of mortality. Furthermore, Galván et al. [18] haveshown that bird species with pheomelanic coloration are more
likely to develop cataracts than species without such coloration,and such species also show much stronger population declines
from background radiation than expected [43], consistent with our
predictions. We estimated the direct effects of backgroundradiation, but also the indirect effects through cataracts, relying
on path analysis (Figure 5). This resulted in an estimated indirectcontribution of cataracts by 4.0% and a direct contribution ofradiation by 23.4% to population levels. Therefore, radiation had
a direct effect that was six-fold greater than the indirect effect of
cataracts. However, again, we must emphasize that the indirect

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Supporting Information
Table S1 Frequency of cataract, slope of the relationship between abundance and level of backgroundradiation, and sample size. See Methods for further details.
(DOC)

Acknowledgments
We gratefully acknowledge logistic support and help in Ukraine by A.
Bonisoli-Alquati, I. Chizhevsky, G. Milinevski and the Chernobyl
EcoCenter. Thanks to Dr. M. Ellman for the loan of the EyeQuick
Digitial Ophthalmoscope camera to capture images of bird eyes.

Author Contributions
Conceived and designed the experiments: TAM APM. Performed theexperiments: TAM APM. Analyzed the data: APM. Contributed reagents/
materials/analysis tools: TAM. Wrote the paper: APM TAM. Acquired
grant funding: TAM APM.

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Cataracts in Birds from Chernobyl

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