Chapter 49

Biological Indicators of Ionizing Radiationin Nature
Anders Pape Møller and Timothy Alexander Mousseau
Abstract Ionizing radiation that consists of α, β and γ rays can directly damage
DNA and other molecules and as such result in somatic or germline mutations. The
consequences of ionizing radiation for living beings cannot be measured with aGeiger counter because it will depend on external dose, internal dose, and the extent
of DNA repair. In addition it will depend on the environmental conditions underwhich living organisms exist. We list environmental indicators of ionizing condition that reveal immediate and long-term consequences ranging from changes inDNA, over damaged cells and organs to altered gene function and development,
reduced fecundity and survival, and hence to negative population trends, andaltered communities and ecosystems and perturbed ecosystem functioning. We
test for consistency in biological indicator ability across spatial and temporal scales
relying on long-term field data collected at Chernobyl and Fukushima, and wetest for consistency in indicator ability among indicators. Finally, we address the
direct and indirect effects of ionizing radiation and we discuss the species or taxa
most susceptible to the effects of radiation.
Keywords Biological level of organization • Consistency across indicators •Direct vs. indirect effects of radiation • Environmental indicators • Spatial consistency • Temporal consistency

49.1

Introduction

Radiation is either non-ionizing (radio waves, visible light and heat) or ionizing
with sufficient energy to ionize an atom. Ionizing radiation consists of α particles
that cannot penetrate paper, β particles that can penetrate paper, but not an aluminium sheet, and γ rays that can penetrate paper, aluminium, and even layers of lead.
A.P. Møller (*)
Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud,
B^atiment 362, 91405 Orsay Cedex, France
e-mail: anders.moller@u-psud.fr
T.A. Mousseau
Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USAe-mail: mousseau@sc.edu© Springer Science+Business Media Dordrecht 2015
R.H. Armon, O. Hänninen (eds.), Environmental Indicators,
DOI 10.1007/978-94-017-9499-2_49

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A.P. Møller and T.A. Mousseau

Both ionizing and non-ionizing radiation can damage organisms, although only ionsproduced by ionizing radiation can directly damage DNA and other molecules.
Background radiation dose rates on Earth typically vary from 0.01 to 0.10 μSv/h,with the natural level in Chernobyl before the nuclear accident being only
0.01–0.02 μSv/h. However, some radiation hot spots have levels that exceed global
mean levels by three orders of magnitude. The negative effects of radiation havebeen documented since the first studies of radioactivity by Becquerel and Curie, andthe mutation effects of radiation were detected almost 90 years ago (Nadson andPhilippov 1925). Thus, the negative consequences of ionizing radiation for living
beings are a well-established fact. Still, very little is known about the biologicaleffects of radiation on free-living organisms.
Why not just measure radioactivity with a Geiger counter and use thesemeasures for predicting the consequences of radioactivity rather than investigate
how living beings respond to radiation? The main reason is that the consequences ofionizing radiation for living beings will depend on a number of factors, including
external dose, internal dose (the amount of radiation due to radionuclides that havebeen ingested or inhaled), and the extent of DNA repair. There are a large numberof radiation hotspots around the world where natural levels of radiation have beenshown to have negative effects on mutations, immunology, and disease, despite theopportunity for local adaptation to these conditions (Møller 2012).
A second major reason why the consequences of ionizing radiation cannot just be
measured with a Geiger counter is that animals and other organisms that live undernormal conditions commonly experience less benign environmental conditions thanin the lab. They usually do not have ad libitum access to food and essential nutrients,
making them experience trade-offs that are rare or non-existent in the lab. Likewise,
field populations commonly suffer from predation, parasitism, or other interspecificinteractions, while such effects are effectively controlled or eliminated in lab studies.
In fact, most humans also live under such constrained conditions, making it unlikelythat lab studies of the effects of ionizing radiation under benign environmental
conditions will apply to humans. Indeed, lab studies generally indicate benign effectsof low dose radiation, whereas field studies often show considerably increased
negative effects (Garnier-Laplace et al. 2012).
Radiation accidents are common, making it of significant importance to document
their effects on living beings. The number of radiation accidents runs into thehundreds, with 20 belonging to the grave categories on the International Nuclear
Event Scale (INES) 4–7 (Lelieveld et al. 2012). Only Chernobyl and Fukushima haveso far been designated as INES 7, which represents major accidents, with four
Category 7 events, because of the meltdown of three reactors at Fukushima. Despite
these events, there is only limited information available on the biological and healthconsequences of low dose radiation (reviews in Zakharov and Krysanov 1996; Møller
and Mousseau 2006; Yablokov et al. 2009).
The objective of this chapter is to assess biological indicators of ionizing
radiation under field conditions as a means of determining the extent to whichradiation accidents have immediate and long-term consequences for living beings.

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Biological Indicators of Ionizing Radiation in Nature

49.2

873

Environmental Indicators of Ionizing Radiation

49.2.1 Identification of Environmental Indicatorsof Ionizing Radiation
Mutations are changes in the sequence of DNA caused by single or double strand
breakage of DNA. DNA repair can restore the original sequences of DNA, most
readily single-strand, but even double-strand breakage of DNA can be repaired
efficiently (Lehman 2006; von Sonntag 2010). Mutations are either somatic (i.e.,
occurring in ordinary body cells) or germ-line (i.e., occurring in gametes). Somatic
mutations are sometimes the source of genetic diseases including different types ofcancer, while germ-line mutations can be transferred to offspring and hence
accumulate across generations. Radiation is a powerful mutagen as shown byclassical laboratory experiments (Nadson and Philippov 1925; Muller 1954).
Even a natural variation in levels of background radiation is a significant causeof mutation (e.g., Forster et al. 2002) and cancer mortality (e.g., Lubin and Boice
1997; Zhang et al. 2012).
Ionizing radiation can damage DNA either directly by causing single or double
strand breakage, or indirectly by the production of free radicals that damage DNA,other molecules, and membranes. Indeed, barn swallows Hirundo rustica have germline mutation rates for neutral microsatellite markers increased by a factor 2–10
(Ellegren et al. 1997). Numerous other studies have shown increases in mutation rates
from bacteria (Ragon et al. 2011) to humans (Dubrova et al. 1996), with contaminated areas around Chernobyl having mutation rates that are increased 2–20-foldrelative to controls (Møller and Mousseau 2006). The effects of exposure to ionizing
radiation may be long lasting due to genomic instability, causing DNA to beparticularly susceptible to future environmental perturbations even after one ormore generations (Morgan et al. 1996). Germ-line mutations are not readily quantified under field conditions, mainly because it is difficult to sample DNA from bothparents and offspring. In addition, mutations may not have fitness consequences if
DNA is repaired, or if offspring carrying mutations are spontaneously aborted,
thereby preventing transmission to the next generation.
Mutations may result in the production of non-functional or damaged cells, asin sperm, pollen, red blood cells, and leukocytes. A large fraction of sperm cells
has abnormal morphology and behavior, preventing them from fertilization. The
frequency of such abnormal sperm is known to increase with the level of background radiation (Møller et al. 2005b), and such sperm cells have inferior swimming behavior, which may prevent fertilization (Møller et al. 2008; BonisoliAlquati et al. 2011). A similar production of abnormal germ cells occurs in pollen,
which likewise have high frequencies of abnormalities that prevent fertilization.
Indeed, the frequency of pollen abnormalities increases strongly with backgroundradiation level in many plant species (Kordium and Sidorenko 1997). Somatic cells
might likewise be affected by mutations, as shown for DNA damage to red blood
cells in birds (Bonisoli-Alquati et al. 2010).

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Ionizing radiation has significant negative effects on the normal development oforgans, such as the brain and the lens of the eye. Birds at Chernobyl have brains thatare on average 5 % smaller than birds in control areas, and there is strong selection
against small brains (Møller et al. 2011). Likewise, the frequency of cataracts due toopacities of the lens is common in free-living birds in contaminated areas, but not incontrol populations (Mousseau and Møller 2013).
Mutations are a cause of altered DNA sequences that may have negative effects
on gene function and hence development of normal morphology. Indeed, thefrequency and the extent of abnormalities in plants and animals are elevated in
Chernobyl as compared to control areas (Møller 1993, 1998; Zakharov andKrysanov 1996; Møller and Mousseau 2001, 2003). Detailed studies of barnswallows have shown high frequencies of abnormalities in populations in contaminated areas as compared to control populations (Møller et al. 2007). Abnormalities
are rare under natural conditions because predators differentially eliminate individuals with aberrant phenotypes. Frequencies of aberrations and hard tumors in adiverse array of bird species reached levels that were many times higher than incontrol areas (Møller et al. 2013a). Similarly high frequencies of abnormalities
have recently been reported for butterflies from Fukushima (Hiyama et al. 2012).
If ionizing radiation affects fertility, this may have negative effects on fecundity.
Møller et al. (2005a, 2008) reported significantly elevated hatching failure in birds
near Chernobyl compared to control populations, possibly due to embryo mortality
caused by either damaged sperm and/or eggs, and hatching failure was also reported
for butterflies at Fukushima (Hiyama et al. 2012). The main factors determining
fecundity is whether an individual survives to the age of first reproduction and thenumber of subsequent years of reproduction. Detailed lifetime studies of barnswallows revealed annual adult survival rates reduced to 28 % in contaminatedareas compared to 40 % in control populations (Møller et al. 2005a). Across16 species of birds, adult survival rate was reduced by 21 % in contaminated ascompared to control areas (Møller et al. 2012), and it was reduced in butterflies inFukushima (Hiyama et al. 2012).
If fecundity and survival are reduced in contaminated areas, this translates into
reduced abundance and species richness because uncommon species disappear due
to random elimination of a few individuals. The underlying mechanisms are poorly
understood, although individual birds are know to avoid nesting in the mostcontaminated areas (Møller and Mousseau 2007b), although contaminated areasthat are partly empty due to the negative effects of radiation may be replenishedthrough differential immigration (Møller et al. 2006). Surprisingly, the first standardized counts assessing the relationship between abundance and radiation were
not conducted until 2007, more than 20 years after the Chernobyl accident. This is
all the more surprising given that such research is inexpensive and does not require
special equipment or training. We have made censuses of birds and other organisms(i.e., biotic inventories) at more than 1,000 census points in contaminated areas in
Ukraine, Belarus, and Japan using standard procedures (Bibby et al. 2005). Indeed,
species richness and abundance of birds (Møller and Mousseau 2007a, b, 2009), butalso spiders, dragonflies, grasshoppers, bumblebees, butterflies, amphibians,

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Biological Indicators of Ionizing Radiation in Nature875

reptiles, birds, and mammals, are reduced in more contaminated areas in Chernobyl(Møller and Mousseau 2007a, b, 2009, 2011b, 2013) and Fukushima (Hiyama
et al. 2012; Møller et al. 2012, 2013b). We have controlled for the potentiallyconfounding effects of habitat, soil, weather, and time of day, but still found highly
consistent results (Møller and Mousseau 2011b).
Species and higher taxa differ in their susceptibility to radiation (Møller andMousseau 2011; Galván et al. 2011). Bird species that have long dispersal andmigration distances, pheo-melanin and carotenoid-based plumage, and high fecundity are the most strongly negatively affected by radiation, apparently due to theeffects of radiation on the production of free radicals and hence on depletionof antioxidants. Interspecific interactions between species may be affected byradiation if one of the interacting parties is particularly susceptible to radiation.
For example, plant-pollinator and prey–predator interactions are affected by radiation if the abundance of pollinators or predators changes. Indeed, mammalian prey
were strongly aggregated in the least contaminated sites around Chernobyl, andpredators were disproportionately common in those sites, presumably resulting inover-exploitation of prey (Møller and Mousseau 2013).
The effects of ionizing radiation on the abundance and diversity of species may
affect interspecific interactions that constitute an integral part of ecosystem functioning. Chernobyl and other areas affected by radiation have perturbed ecosystems(Møller et al. 2012). Radiation reduces the abundance of pollinating insects, such as
bumblebees and butterflies, with subsequent negative effects on fruit set of apples,
pears, and other fruit bearing plants. In turn, frugivorous birds are less abundant insuch areas with few fruit, which negatively affects seed dispersal and hence
recruitment. Indeed, the recruitment rate of apples and pears was severely reduced
in study plots with elevated background radiation.

49.2.2 Testing for Consistency of Indicator Ability
Across Spatial Scales
Large-scale radiation accidents affect hundreds if not thousands ofsquare-kilometers. Still, there have been few attempts to test whether there isconsistency in responses to radiation across spatial scales. Møller and Mousseau(2011b) compared breeding bird census data obtained from the same years in
Ukraine and Belarus and found highly consistent effects of radiation on theabundance of birds.
We have taken this analysis one step further by analyzing the slope of abundanceof different taxa of animals in relation to radiation at Chernobyl and Fukushima(Møller and Mousseau 2013; Fig. 49.1). There was no significant interaction
between radiation and area for species richness of birds, number of birds, andnumber of bumblebees, implying that the effect of radiation was similar in the
two areas. In contrast, there were significant interactions for butterflies, dragonflies,876

A.P. Møller and T.A. Mousseau

Fig. 49.1 Box plots of the slope of the relationship between abundance and level of backgroundradiation for 80 species of birds at Chernobyl and 56 species of birds at Fukushima. The box plotsshow the median, quartiles, 5- and 95-percentiles, and extreme values. Note that slopes weregenerally negative, implying reduced population sizes at higher radiation levels, and slopes at
Chernobyl were more negative than at Fukushima

grasshoppers, and spider webs, implying different effects in the two areas. We
should not necessarily expect similarity because Chernobyl has been subject tochronic radiation for 27 years, whereas Fukushima has been exposed only for
2 years, and thus the composition of radionuclides differs.
Interestingly, many species occur both at Chernobyl and Fukushima, allowing atest of similarity in the effect of radiation on abundance at the two sites (Møller
et al. 2012). The relationship between abundance and radiation in birds was on
average 0.063 (SE ¼ 0.007), N ¼ 80 species in Chernobyl and 0.040 (0.008),
N ¼ 45 species in Fukushima. However, among the 14 species occurring at bothsites there was a significant interaction between radiation, area, and species,
implying that the abundance varied among areas and species, with radiation having
different effects. The slope of the relationship between abundance and radiation for
the 14 common species was 0.008 (0.001) at Chernobyl, but at 0.067 (0.011)
much stronger at Fukushima (Møller et al. 2012).

49.2.3 Testing for Consistency of Indicator Ability over TimeWe have conducted censuses of animals at both Chernobyl and Fukushima for morethan 1 year, allowing for tests of relationships between abundance and radiation

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877

Fig. 49.2 Slope of therelationship between
abundance and level ofbackground radiation in2012 in relation to 2011 for
35 species of breeding birds
near Fukushima. The size ofthe circles reflects sample
size. The slopes weregenerally more negative in2012 than in 2011

among years. Indeed, we have documented temporal consistency for different taxa
at Chernobyl and Fukushima (Møller and Mousseau 2011b; Fig. 49.2).
Laboratory experiments on the effects of radiation on living beings are usuallybased on acute radiation treatment, while the situation in the wild consists ofchronic exposure with an accumulation of mutational effects over time. While
such accumulation effects have not been demonstrated in Chernobyl because noor few studies were conducted immediately after the accident, Fukushima allows
tests of whether there are increasingly detrimental effects over time. While theslope of the relationship between abundance of birds and radiation was 0.006(SE ¼ 0.005) for 45 species in 2011, it was 0.015 (SE ¼ 0.005) in 2012 for thesame species. Thus, the effects of radiation on abundance became much more
severe 1 year later as compared to immediately after the accident. If many individuals with abnormalities die, as suggested by studies at Chernobyl (Ellegren
et al. 1997; Møller et al. 2013a), we might expect a slight temporal trend toward
fewer abnormalities over time due to radioactive decay. Indeed, Møller et al. (2007)
showed that there was a trend toward reduced frequency of abnormalities over timein barn swallows, although this reduction could also be due in part to lower
radiation doses in some areas following two decades of radioactive decay.
Exposure to radiation may result in adaptive responses to ionizing radiation if
there is genetic variation in the underlying mechanisms (i.e., the mechanism(s) ofadaptation are heritable), if there is selection against inefficient mechanisms, and if
selection occurs for a sufficient number of generations. Recent studies of plants
have suggested that DNA repair and specific proteomic patterns provide evidenceof such adaptation (Boubriak et al. 2008; Danchenko et al. 2009; Klubicová
et al. 2010). However, these experiments are based only on a single sample froma contaminated area and a second from a control area, providing no proper
replication, thereby preventing firm conclusions about the underlying cause.

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Table 49.1 Environmental indicators of ionizing radiation and their properties in terms of ease ofuse, consistency in response over space and time, reliability, and information content
Biological level oforganization
Mutations, DNA
and othermolecules
Germ cells
OrgansPopulations
SpeciesInteractions
among species
Ecosystems

CosteffectivenessConsistency
over space andtime

Reliability

Informative

Relatively
easy

High

?

?

Weakly

Easy
Easy
Time
consumingTime
consumingTime
consumingTime
consuming

High
High
High

Yes
Yes
Yes

Yes
Yes
Yes

Yes
Yes
Yes

High

Yes

Yes

Yes

Medium

Yes

Yes

Yes

Low

Yes

Yes

Yes

Feasibility

49.2.4 Testing for Consistency of Indicator Ability
Among Indicators
Environmental indicators of the effects of radiation on different levels of biologicalorganization have shown strong effects of chronic exposure at Chernobyl more than
27 years after the accident, and on-going studies at Fukushima show increasingly
negative effects of radiation with time. Studies of the effects of ionizing radiation at
different organizational levels differ in feasibility, cost effectiveness, consistency overspace and time, reliability, and information content (Table 49.1). Thus, studies ofmutations are relatively easy to conduct, although there are no studies showing
consistency in response over space and time. More ecologically oriented studies
focusing on populations, species, interactions among species, and ecosystems aretime consuming with low cost effectiveness. However, if we require knowledge
concerning the effects of radiation at different organizational levels for the characterization of direct and indirect effects and estimation of risks and injuries to individuals,
populations, and ecosystems, we must conduct studies at these different levels.

49.3

General Discussion

We have briefly reviewed the literature on indicators of ionizing radiation at
different levels of biological organization from molecules and cells, to individuals,
populations, species, multi-species interactions, and ecosystems. There are many
parallels between the effects observed in natural animal and plant systems and those49

Biological Indicators of Ionizing Radiation in Nature879

documented for humans (review in Serdiuk et al. 2011). We have documented
consistency in response to radiation over time and space, implying that our findings
are not chance relationships, but rather consistent patterns of a pervasive impact ofradiation on living systems. This raises two questions: First, what are the direct
versus the indirect effects of radiation? Second, at which organizational level is theimpact of radiation most efficiently and readily measured? Concerning the firstquestion, there are so far no assessments of the relative direct effects of radiationand the indirect effects of radiation through food availability and interactions withconspecifics, predators, parasites, or pollinators. Clearly, such an assessment isurgently needed.
The second question concerns which species or taxa are most susceptible toradiation and hence most reliable as biological indicators of the effects of radiation(i.e., the canary in the coal-mine analogy). We have previously demonstrated thatanimal taxa with large mean population density and long natal dispersal distanceare most strongly negatively affected by radiation (Møller and Mousseau 2011a).
Rare bird species are more strongly negatively affected by radiation, and rare
species are disproportionally found in the least contaminated sites around Chernobyl (Møller and Mousseau 2011b). Common species generally have long dispersal
distances and occur at high average background radiation levels (Møller andMousseau 2011b). This effect of dispersal may interact with mutation rate because
species that disperse the farthest have the lowest frequency of mutations making it
unlikely that mutations spread to uncontaminated areas through dispersal.

49.4

Future Prospects

It has been predicted that another nuclear accident at the INES 7 scale is likely tooccur during the next 50 years in a heavily populated area affecting c. 30 million
people (Lelieveld et al. 2012). Hence, there is great urgency to learn from past
accidents to mitigate future effects. We consider this chapter to constitute a firstnecessary step toward the production of a tool kit for the assessment of theconsequences of future nuclear accidents. Given the poor level of knowledge ofthe effects of radiation accidents on wild organisms, it is essential to retrieve
information at a number of different scales. It is also essential to involve manydifferent people, including citizen scientists, because knowledgeable citizens are
numerous and dedicated.
We would like to emphasize the general lack of replication of most studies oflow dose radiation. A second major problem is the general lack of proper experimentation with appropriate levels of replication, thus preventing inferences aboutcausation. This precarious situation is mainly due to poor scientific methodology
and a chronic lack of funding for research on the effects of low dose radiation.
Construction and maintenance of nuclear power plants is hugely expensive, andallocation of even 0.1 per mille would represent a huge boost to research concerning
the consequences of radiation accidents.

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