man Resources. 2012. Plant and Enviromental Protection Sciences.
http://www.ctahr.hawaii.edu/peps/
University of Hawaii at Manoa, CTAHR Arnold H. Hara. 2011. http://
www.ctahr.hawaii.edu/haraa/
University of Hawaii at Manoa, CTAHR Hawaii County. 2010. http://
www.ctahr.hawaii.edu/hawaii/Programs.aspx.

Arnold H. Hara is an Entomologist and Extension Specialist in the Department of Plant and Environmental Protection Sciences, University of Hawaii
at Manoa in Hilo, Hawaii. Hara completed his doctorate in entomology in1982 at the University of California, Davis. He specializes in tropical ornamental pest management and in non-chemical postharvest disinfestation
treatments.

Instant symposiuM

Entomological Studies in Chernobyl and Fukushima
T. A. Mousseau and A. P. Møller

R

adioactive emissions can occur as a consequence of naturaldeposition in rocks, as a consequence of human release ofradioactive material such as during nuclear testing and theoperations of nuclear power plants (NAS 2012), and from nuclear
accidents such as those at the Three Mile Island, Chernobyl, and Fukushima Daiichi power plants. In some parts of the world (e.g. Ramsar,Iran), natural levels of radiation can be high, exceeding “normal” lowlevels by several hundred-fold (Ghiassi-Nejad et al. 2002), sometimes
resulting in significant rates of disease and associated mortality inhumans (e.g. Lubin and Boice 1997; Hendry et al. 2009) and, byinference, in other organisms. Much higher levels of radiation occur
as a consequence of nuclear accidents that have produced levels thatcan exceed normal background levels by a factor of 10,000 or more.
Radiation can have both short- and long-term effects on livingorganisms. Short-term physiological effects may include oxidativestress (e.g. Ben-Amotz et al. 1998; Møller et al. 2005b; BonisoliAlquati et al. 2010a), increased damage to DNA (e.g. Sakharov etal. 1996; Bonisoli-Alquati et al. 2010b), immunosuppression (e.g.
Camplani et al. 1999; Yablokov et al. 2009), and many other possibleeffects. Direct physiological effects can result in reproductive failureand even death. Reproductive failure associated with radiation oftenoccurs as a consequence of embryo mortality (Møller et al. 2005,2008; Yablokov et al. 2009). Reproductive failure has also been reported for birds such as barn swallows (Hirundo rustica), in whichmore than 25% of females living in contaminated areas may forego
reproduction altogether (Møller et al. 2005), and similarly reduced
fecundity has been reported for humans (Yablokov et al. 2009). Males
living in contaminated areas have shown a high degree of infertility,often producing few or mainly unviable sperm (Yablokov et al. 2009).
Short-term physiological effects of radiation may have negative
consequences for adult survival, especially in the sex that invests
the most in reproduction (Møller et al. 2005; Yablokov et al. 2009).
Radioactive contaminants have long been known to cause mutations (Nadson and Philippov 1925), although these are more difficult
to study due to their long-term nature that can extend across generations (Møller and Mousseau 2011a). Mutations arise from DNA
damage that is not repaired, thereby causing a reduction in fitness if148

the mutation occurs in a coding region and it affects gene expression(Eyre-Walker and Keightley 2007). Extensive studies of a diverse
array of plants, animals, and other organisms have shown increased
levels of mutations by a factor of two to 20 around Chernobyl (reviewin Møller and Mousseau 2006).

Impacts on Wildlife in Chernobyl

We have been studying the impacts of nuclear accidents on
wildlife for more than 12 years (APM since 1991; TAM since 2000).
Initially, our studies were descriptive and aimed primarily at
documenting whether or not there were measurable impacts on themorphology and life histories of organisms (mostly birds) living in
the contaminated areas of Chernobyl (Møller and Mousseau 2001,2003). Our efforts expanded to include Fukushima in July 2011
(Møller et al 2012, 2013). Largely in response to some untested
assertions published in the 2005 Chernobyl Forum reports thatsuggested that plants and animals were thriving inside the exclusionzone, our efforts expanded to include detailed analyses of mutation
rates, developmental abnormalities (e.g. visible mutations, tumors),
fertility and reproductive capacity, longevity, population abundances,and biodiversity, as well as measures of ecosystem functioning inbirds, insects, spiders, plants, and microbes (Møller and Mousseau
2006, 2007a, 2007b, 2007c, 2008, 2009, 2011a, 2011b; Møller et al.
2005a, 2005b, 2006, 2008). Here, we briefly summarize a few of ourmore interesting findings related to insects.
Our first efforts to study insects in Chernobyl focused on Drosophila melanogaster. Initially, in 2004, these studies were largely
unsuccessful as it proved unexpectedly difficult to find Drosophila,
even in the abandoned villages where fruit trees were abundant. Anecdotally, it appeared that fruit set was very low, possibly as a result oflow pollinator numbers in the areas of high contamination. However,at the time, we noted that fruit trees in the town of Chernobyl itself
were overladen with fruit, despite moderate radiation levels, and Drosophila were correspondingly abundant, thus calling into question
our pollinator abundance hypothesis. We subsequently learned thatseveral experimental beehives had been brought to Chernobyl, likely
accounting for the high fruit set and large numbers of Drosophila

American Entomologist • Fall 2012

Fig.1. Locationof census areas
around (A) Chernobyl(Ukraine and Belarus)and (B) Fukushima
Prefecture (Japan).

in this area, despite significant radiation levels. As a consequenceof these insights and discoveries, we initiated a series of ecologicalcensuses during 2006-2009 inside and out of the Chernobyl Exclusion Zone of Ukraine, as well as in several regions of southeastern
Belarus, where contamination levels also varied considerably. Insectand spider censuses were performed at a total of 254 points in 2006,
235 points in 2007, 237 points in 2008, and 159 points in 2009 andwere located at ≈100 m intervals within forested areas (excludingsuccessional stages of secondary forest due to abandoned farming,
which are still almost exclusively open grassland). We conduced
similar censuses at a total of 300 sampling points in forested areas
west of the exclusion zone around the Fukushima Daiichi power
plants in 2011 (Møller et al. 2012a, 2013).
Our statistical analyses of abundance included many potentiallyconfounding variables in addition to background radiation levels andanimal abundance. These other factors included ground coveragewith farmland, deciduous and coniferous forest, grass, bush, andtrees; temperature, cloud cover, and wind; time of day, and time ofday squared. We also included radiation level squared to accountfor non-linear relationships between species richness and abundance, respectively, and radiation. We developed statistical models
to assess the relationship between abundance (response variables)and radiation, assuming a Poisson distribution of abundance, afterinclusion of the potentially confounding variables, as implemented
in the statistical software JMP (SAS Institute 2000). Further details
concerning locations, methods, statistical analyses and results canbe found in Møller and Mousseau (2007a, 2009, 2011b).

Results and Discussion

Radioactive contamination may affect the abundance of animals
through direct effects on physiology or through indirect effects of mutations that can have deleterious consequences for reproduction andviability. Previous studies of animals at Chernobyl have shown negative effects of radiation on immunity, antioxidant status, reproductive
failure by females, and sperm production. Likewise, mutation rates
at Chernobyl have increased by up to a factor of twenty relative tothe normal background mutation rates (Møller and Mousseau 2006).
In Chernobyl, the abundance of all investigated taxa decreased
with the level of background radiation (Mousseau and Møller 2011)

American Entomologist • Volume 58, Number 3(Table 1). The mean of the slopes describing the relationship between
abundance and level of background radiation for different taxa wasstatistically significant (mean (SE) = -0.059 (0.015), N = 10, P =0.0041), and the significance of this relationship remained strong evenafter adjusting for potentially confounding environmental variables(F = 33.98, d.f. = 1, 6, r2 = 0.85, P = 0.0011, slope (SE) = 1.668 (0.286)).
Analyses of invertebrate abundances at Fukushima revealed adifferent pattern of variation (Møller et al. 2013). Butterflies andcicadas showed a drop in abundances with increasing contamination levels, while there was no pattern of change for bumblebees,
dragonflies, or grasshoppers. Spiders, on the other hand, showed astatistically significant increase at the most contaminated sites, possibly reflecting the decreased abundance of birds found in these areas(Møller et al. 2013). Another possible explanation for the differencesobserved between Chernobyl and Fukushima could relate to theimportance of mutation accumulation over multiple generations that
we have previously suggested as an important factor impacting on

Table 1: Abundance of different animal taxa in Fukushima and Chernobyl in relation to radiation level. See Møller et al. 2012 and 2013 forfurther details.

Fukushima

Sum ofsquares

No. bumblebees

0.001

No. cicadas

0.208

No. butterflies

No. dragonflies

No. grasshoppers

d.f.
1, 298FP

0.16

0.69

Estimate (SE)4.553

1, 29837.18 <0.0001 −0.254 (0.042)

0.127

1, 2980.87

0.35

0.0002

1, 29819.24 <0.0001 −0.054 (0.012)

0.004

1, 2981, 298

14.12

No. bumblebees

1.595

1, 89655.71 <0.0001 −0.037 (0.005)

No. dragonflies

1.195

1, 40234.58 <0.0001 −0.049 (0.008)

No. spiders

Chernobyl

No. butterflies

No. grasshoppers
No. spiders

0.636
2.153
0.891

5.738

1, 896
1, 372

1, 8960.22

0.64

0.095 (0.025)

57.63 <0.0001 −0.043 (0.006)
13.58

0.0003 −0.071 (0.019)

81.94 <0.0001 −0.071 (0.008)
149

Acknowledgments

We gratefully acknowledge logistic support and help in Ukraine byI. Chizhevsky and G. Milinevski. We gratefully acknowledge support
from the U.S. National Science Foundation, the University of South
Carolina School of the Environment, the NATO CLG program, theCRDF, the Fulbright Program, the National Geographic Society, and theSamuel Freeman Charitable Trust for research in Chernobyl, and theUniversity of South Carolina and Qiagen GmbH for research in Japan.

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Timothy Mousseau is a Professor of Biological Sciences at the University ofSouth Carolina. Anders Møller is a Director of Research for the CNRS (France)at the University of Paris-Sud.

What is it? answer.
This is a leafhopper (Cicadellidae: Deltocephalinae) abdomenwith an adult female strepsipteran (Halictophagidae) headprotruding from the side. The strepsipteran’s body is filled withfirst instar larvae. The leafhopper, Alocoelidia fulva Evans, wascollected in Madagascar.
This photo was submitted by James N. Zahniser, Illinois
Natural History Survey, Prairie Research Institute, Universityof Illinois at Urbana-Champaign, 1816 S. Oak St., Champaign,IL 61820, zahniser@illinois.edu.
If you have a color photograph of an insect, insect part, orentomological apparatus that you would like to submit for the“What is it?” feature, please e-mail a 300-dpi TIFF and a description of the image to the editor at cdarwin@aol.com.

populations in the Chernobyl region where radioactive contaminants
have shaped populations for 25 generations for most insect species(Møller and Mousseau 2011a). Alternatively, differences could relate
to the many contrasts between Fukushima and Chernobyl events,especially with regard to the composition of contaminants that weredispersed. In Fukushima, cesium-134 and cesium-137 predominate,while in Chernobyl, cesium-137, strontium-90, plutonium-239 andamericium-241 are found at significant levels across the landscape,and differential sensitivity to these mixtures could perhaps accountfor some of the differences between locales. Clearly, significant research effort should be directed towards a clear understanding of themechanisms underlying differences and similarities of the impacts
resulting from these two catastrophes.

American Entomologist • Fall 2012