SOURCES AND EFFECTS OFIONIZING RADIATION
United Nations Scientific Committee on the
Effects of Atomic Radiation
UNSCEAR 2008
Report to the General Assemblywith Scientific Annexes

VOLUME II
Scientific Annexes C, D and E

UNITED NATIONSNew York, 2011

NOTE
The report of the Committee without its annexes appears as Official Records of the General
Assembly, Sixty-third Session, Supplement No. 46.
The designations employed and the presentation of material in this publication do not imply
the expression of any opinion whatsoever on the part of the Secretariat of the United Nations­
concerning the legal status of any country, territory, city or area, or of its authorities, or ­concerning
the delimitation of its frontiers or boundaries.
The country names used in this document are, in most cases, those that were in use at the time thedata were collected or the text prepared. In other cases, however, the names have been updated,
where this was possible and appropriate, to reflect political changes.

UNITED NATIONS PUBLICATION
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ISBN-13: 978-92-1-142280-1
e-ISBN-13: 978-92-1-054482-5© United Nations, April 2011. All rights reserved.
Publishing production: English, Publishing and Library Section, United Nations Officeat Vienna.

ANNEX E
effects of ionizing radiation
on non-human biota
Contents
Page

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Background. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Scope of annex. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 C. Effects of exposure to ionizing radiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. Individual level effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2.	Population and ecosystem level effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. Multiple stressors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
4. Commentary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 D. Observations from case studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 E. Structure of this annex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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I. ESTIMATING doseS to non-human biota. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Assessing exposures of biota. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. Choice of reference organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2. Radioecological models. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. Transfer of radionuclides in the environment and resulting exposures. . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Transfer of radionuclides in the terrestrial environment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. Dry deposition. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2. Interception of radionuclides deposited from the air. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. Weathering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
4. Distribution of radionuclides within plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
5. Uptake of radionuclides from soil. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
6. Migration in soil. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
7. Resuspension. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
8. Transfer to animals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 C. Transfer to freshwater organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 D. Transfer of radionuclides to marine organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 E. Evaluating doses to biota. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. Fraction of radiation absorbed by organism. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2.	Principal relationships for internal and external exposure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. Doses to non-human biota. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
4. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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II. Summary of dose–effects data from the UNSCEAR 1996 Report. . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Dosimetry for environmental exposures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Effects of radiation exposure on plants and animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. Terrestrial plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2. Terrestrial animals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. Aquatic organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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261

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		 C.
		 D.

Effects of radiation exposure on populations of plants and animals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
Effects of major accidents. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262

III. Summary of dose–effects data from the Chernobyl accident. . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Radiation exposure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Effects of radiation exposure on plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 C. Effects of radiation exposure on soil invertebrates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 D. Effects of radiation exposure on farm animals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 E. Effects of radiation exposure on other terrestrial animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 F. Effects of radiation exposure on aquatic organisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 G. Genetic effects in animals and plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 H. Overall observations on the effects of the Chernobyl accident. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

263
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IV. Effects of radiation EXPOSURE on NON-HUMAN BIOTA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Overall conclusions of the UNSCEAR 1996 Report . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Evaluations since 1996. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
1. United States Department of Energy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
2. Canada. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
3. FASSET . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
4. ERICA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
5. Observations from recent literature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
			
6. Effects on populations and ecosystems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

272
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273
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282
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V. summary and conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 A. Estimating dose to non-human biota. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 B. Summary of dose–effects data from the UNSCEAR 1996 Report. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 C. The current evaluation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
		 D. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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ACKNOWLEDGEMENTS. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297

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Introduction
A.

Backgroundharm. Furthermore, it also concluded that it was unlikely thatradiation exposures causing only minor effects on the most
exposed individual member of a population would have significant effects at the population level; that chronic exposures to low-LET radiation at dose rates of less than
100 mGy/h to the most highly exposed individuals would be
unlikely to have significant effects on most terrestrial animal
populations; and that maximum dose rates of 400 mGy/h toa small proportion of the individuals in aquatic populationsof organisms would not have any detrimental effects at the
population level.

1. The estimation of human exposure to ionizing radiationfrom radionuclides of natural and artificial origin is an important and ongoing function of the Committee. The Committee
has used simplified generic models of the dispersion andtransfer of radionuclides through the environment to estimate
the internal and external exposure of humans and the resulting doses. Owing to the complexity and interactions of theunderlying processes, special attention has been given toradionuclide transfer via human food chains and the assessment of ingestion doses. The underlying model assumptions
and parameters are kept under review and revised as necessary. The last revision was documented by the Committee inannex A, “Dose assessment methodologies” of the UNSCEAR
2000 Report [U3].

4. The International Commission on Radiological Protection (ICRP), the International Atomic Energy Agency(IAEA) and other international organizations have encouraged the exchange of information on the effects of radiation
exposure on non-human biota [I19, N6]. The IAEA’s action
plan on the protection of the environment was discussed atthe 2003 Stockholm Conference [I1], which concluded that
“While accepting that there remain significant gaps inknowledge and that there needs to be continuing research …
there was an adequate knowledge base to proceed and (theConference) strongly supported the development of a framework for environmental radiation protection”. It also foundthat “the time is ripe for launching a number of international
initiatives to consolidate the present approach to controllingradioactive discharges to the environment by taking explicit
account of the protection of species other than humans”.

2. In the past decades, scientific and regulatory activities
related to radiation protection focused on the radiation exposure of humans. The prevailing view has been that, if humans
were adequately protected, then “other living things are also
likely to be sufficiently protected” [I8] or “other species are
not put at risk” [I5]. Over time, the general validity of thisview has been questioned on occasion and therefore consider­ation has been given to the potential effects of exposure toionizing radiation of non-human biota. This has occurred, inpart, as a result of the increased worldwide concern over thesustainability of the environment, including the need to maintain biodiversity and protect habitats and endangered species[U22, U23]; in part, because it has increasingly been recognized that the exposure scenarios and pathways for assessing
human exposure may not apply to non-human biota; and, inpart, as a result of various efforts to assess the effects of exposure to ionizing radiation on plants and animals [C1, D1, F5,
I1, I2, I3, I4, I9, N6, P13, R9, T1, W16].

5. In 2000, the ICRP, recognizing that environmental protection is a global matter, set up a Task Group to examine
the issues. It considered that an approach to environmental
protection from ionizing radiation “should relate as closely
as possible to the current system for human radiologicalprotection, and that these joint objectives could therefore
best be met by the development of a limited number of Reference Animals and Plants” [I9]. Subsequently, the ICRP
decided to establish a new Committee (ICRP Committee 5)on the Protection of the Environment. The ICRP further
noted that “as radiation effects at the population level—or
higher—are mediated via effects on individuals of that population, it seems appropriate to focus on radiation effects on
the individual for the purpose of developing a framework ofradiological assessment that can be generally applied toenvironmental issues” [I10].

3. The Committee initially addressed the effects of radiation exposure on plant and animal communities in a scientific annex, “Effects of radiation on the environment”, of the
UNSCEAR 1996 Report [U4]. Prior to this, the Committee
had considered living organisms primarily as part of theenvironment in which radionuclides of natural or artificial
origin may be present and contribute to the internal exposureof humans via the food chain. Like man, however, organisms
are themselves exposed internally to radiation from radio­
nuclides that have been taken up from the environment andexternally to radiation in their habitat. In general terms, theCommittee, in its 1996 report, considered that populationlevel effects were of primary interest and, of those, that
reproductive effects were the most sensitive indicator of

6. Since the preparation of the UNSCEAR 1996 Report[U4], the approaches to evaluating radiation doses to nonhuman biota have been reviewed and improvements made[C1, E1, F1, F5, U26]. Information on the levels of radiation
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exposure below which biological effects are not expected or,alternatively, above which such effects might be expected,
has been developed. This has been obtained, in part, for the
projects on the Framework for Assessment of Environmental
Impact (FASSET) [F1] and the Environmental Risk from
Ionising Contaminants: Assessment and Management(ERICA) [E1], in particular, as part of the development of
the FASSET Radiation Effects Database (FRED) [F3]. This
information was subsequently integrated with the databaseon the effects of radiation exposure from the project on Environmental Protection from Ionising Contaminants in the
Arctic (EPIC) [B26] resulting in the so-called FREDERICA
database [F20].
B.

Scope of annex

7. The scientific information given in the FRED [F20]combined with that obtained in the subsequent ERICA programme [G11, J6] and that from more recent studies, especially those undertaken around the site of the Chernobyl
accident, provided the basis for the Committee’s review ofthe effects of exposure to ionizing radiation on non-humanbiota given in this annex. In particular, the Committee used
the information from its review to re-evaluate its recommendations on dose rates below which exposure to ionizing
radiation is unlikely to result in detrimental effects on populations of non-human biota, given in the UNSCEAR 1996
Report [U4].
8. This annex only provides the Committee’s overview of
the current data and methods to assess doses to non-humanbiota and a brief discussion of the nature of effects of­radiation exposure on individual organisms and populations.
Detailed discussion of these topics is beyond the scope of
this annex.
C.

metabolic impairment and changes in genetic diversity)
can be traced to events at the cellular or subcellular level in
specific tissues or organs.
1.

Individual level effects

11. Even though mutational events in somatic cells are primarily responsible for cellular transformation and tumour
formation, the occurrence of cancer in individual organisms
is normally of low relevance to the ecosystem as a whole,
except in the case of endangered or protected species [A13].
However, mutational effects in germ cells may lead to reproductive impairment [A14]. Genotoxic stressors, including
ionizing radiation, may alter reproductive success bydecreasing fertility via clastogenic and mutagenic effects ingerm cells resulting in a decrease of the number of gametes.
Such stressors may also increase the frequency of developmental abnormalities, e.g. when mutations are induced ingerm cells and the progeny of exposed parents develop
abnormally.
12. There are a number of weaknesses in the data on which
to base estimates of the dose rates below which effects on
non-human biota are not considered likely. In addition,
there are also issues in extrapolating from the effects
observed at cellular and subcellular levels to effects thatmight be observed in individual organisms, populations andeco­systems. Moreover, it is only under controlled conditions in the laboratory that organisms can be exposed to asingle stressor. This presents a further source of uncertainty
in extrapolating the results to real ecosystems where multiple stressors exist. Although beyond the scope of this annex,
the Committee acknowledges that improved understandingof the mechanisms of radiation damage, of how to extrapolate information from lower to higher trophic levels, and of
the possible consequences of multiple stressors is of great­interest and worthy of further study.

Effects of exposure to ionizing radiation

9. Since the preparation of the UNSCEAR 1996 Report[U4], a number of radiobiological phenomena have been
described, including genomic instability (genomic damage
expressed post irradiation after many cell cycles) and the
bystander effect (whereby non-irradiated cells in proximity
to irradiated cells exhibit effects similar to those seen in theirradiated cells). These phenomena were discussed inannex C, “Non-targeted and delayed effects of exposure toionizing radiation”, of the UNSCEAR 2006 Report [U1].
While such phenomena are relevant to understanding mechanisms for the development of effects on non-human biota
after exposure to ionizing radiation, a discussion of suchphenomena is beyond the scope of this annex.
10. The immediate effects of ionizing radiation exposure
may be seen at various levels of organization from the subcellular through individual organisms to populations andecosystems [G16]. Responses of various biological functions to radiation exposure (e.g. reproductive success,13. The scientific literature provides many examples ofadaptive responses to and hormetic effects of exposure toionizing radiation. Annex B of the UNSCEAR 1994 Report[U5] provided a comprehensive discussion of adaptive
responses. In that report, the Committee concluded that there
was evidence of an adaptive response in selected cellular
processes following exposure to low doses of low-LET
radia­tion but went on to suggest that it was premature to conclude that adaptive cellular responses had beneficial effects
that outweighed the harmful effects of exposure. Subsequent
to the UNSCEAR 1994 Report [U5], there have been numerous papers and considerable discussion concerning the­possibility of hormetic responses to low doses of gamma
radiation. For example, Boonstra et al. [B39] reported possible hormetic effects of gamma radiation exposure on populations of meadow voles. These authors suggested that
increases in glucocorticoid levels associated with chronic
gamma irradiation at a rate of about 1 mGy/d may be an
important factor in the increased longevity of exposed
meadow voles compared to non-exposed ones. Mitchel et al.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

[M9] found that a single dose of 10 mGy to radiation-­
sensitive mice (Trp53 heterozygous) reduced the risk of both
lymphoma and spinal osteosarcoma by greatly delaying theonset of malignancy. Further discussion of adaptive
responses and potential hormetic effects of low dose and low
dose-rate gamma radiation exposure is beyond the scope of
this annex.
14. The various life stages of organisms differ in their sensitivity to exposure to ionizing radiation. It is often assumed
that a population will be protected if the most sensitive
stage of the life cycle is protected. For a large number ofstressors, this assumption seems to be widely true [F9].
However, the most sensitive life stage is often difficult to
identify a priori. Consequently, if data on effects only exist
for one or two life stages, it may not be possible to know for
certain if these data represent information for the most sensitive life stage, even though most of the available infor­
mation indicates that gametogenesis and embryonicdevelopment are among the most radiosensitive stages ofthe life cycle [I4]. For example, Anderson and Harrison[A15] showed that the synchronous spawning in polychaete

225

worms rendered the organisms susceptible to low-level
cumulative impact of ionizing radiation exposure. Because
they spawned synchronously and died, oocytes were formed
all at once, and damaged gametes could not be replaced.
15. The propagation of effects on individuals to the population as a whole depends greatly on the characteristics of thespecific life history. The relative importance of each stage inthe life history also varies between species, depending on thespecific reproductive characteristics (short generation time
versus long generation time, iteroparous versus semelparous, sexual versus asexual reproduction, etc.). Changes inthe value of an individual parameter such as age of reproduction (i.e. generation time) often have much stronger consequences for species with fast population growth rates (i.e.
with short generation time and high fecundity rate) than for
those with slow population growth rates [G3]. On the other
hand, the National Council of Radiation Protection andMeasurements (NCRP) [N8] noted that when natural causesof deaths are considered collectively on a biologically comparable time scale, natural mortality occurs at a biologicallycomparable age, as illustrated in figure I.

Figure I. Cumulative survival curves of the mouse, beagle and human for natural causes of death

CUMULATIVE SURVIVAL

1.0
Human

0.8
Beagle

0.6
0.4
0.2

Mouse

0
100

300

1 000

500
1 100
700
900
AGE AT DEATH (mouse days)

1 300

1 500

5 000

6 000

7 000

2 000

3 000

4 000

AGE AT DEATH (dog days)
20

40

60

80

100

120

AGE AT DEATH (human years)

2. Population and ecosystem level effects
16. Whatever the stressor considered, population-level
effects are valuable indicators of ecological hazard (e.g.
[F9]). However, because of experimental constraints, mostavailable data describe the effects on the individual traits ofirradiated organisms. Many studies have documented theeffects of radiation exposure at the cellular, tissue and individual levels. The consequences have been found to be

increases in morbidity and mortality, decreases in fertility
and fecundity, and increases in mutation rate [W10]. Thesetypes of effect, observed at the individual level, may haveconsequences for a population of a species.
17. Matson et al. [M12] and Baker et al. [B29] investigatedthe possible genetic and population effects resulting fromthe chronic radiation exposure of bank voles, Clethrionomys
glareolus, inhabiting contaminated sites near Chernobyl.

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UNSCEAR 2008 REPORT: VOLUME II

Both groups reported that genetic diversity was elevated in
the contaminated sites when compared to relatively uncontaminated sites but were unable to attribute any significant
detrimental effects among the bank vole populations to­radiation exposure.
18. Ionizing radiation does not appear to have any direct
effects at the population or higher ecological levels (i.e.
community or structure and function of ecosystems). At
present, it appears that all such effects are mediated byeffects at the individual or lower levels. In addition, indirect effects through food-web mediated processes may
occur [G16]. One approach to extrapolating from theeffects on individuals to effects at the population level is tointegrate the effects on survival and reproduction in termsof population growth rate. Population growth rate is one of
the most important characteristics of a population and isdefined as the population increase per unit time divided by
the number of individuals in the population. Population
models are used to extrapolate from the toxic effects on
individuals, expressed as modifications to values of lifecycle parameters, to effects at the population level. Thismethod has been used, for example, by Woodhead [W10]in a theoretical way and was implemented through experiments within the ERICA project for the chronic exposureof two invertebrates exhibiting contrasting life cycles: theearthworm and the daphnid [A26, G3].
19. An ecosystem has complex interactions between biotic
and abiotic components and among biotic components. The
latter are called interspecific interactions and include competition, predation and association. These interactions contribute to the flow or cycle of energy, materials and informationin the ecosystem, and thus provide the ecosystem with its
fundamental property of self-organization. It is possible that
if one species is directly damaged by a toxic agent, anotherspecies more resistant to that agent is also indirectly affectedby the depletion of interactions with the directly damaged
species. As a result, the entire ecosystem can be affected in
extreme cases. These indirect effects have been observed inecosystems exposed to ultraviolet radiation [B37] and somechemicals [C23, H24, M24, T24, W20]. Similarly, someindirect effects through inter-species interactions have been
observed in irradiated ecosystems, as reviewed in the
UNSCEAR 1996 Report [U4]. Given this backdrop, theimportance of indirect effects has been considered in reviewsof the effects of exposure to ionizing radiation on ecosystems [B38, C21, I2, I3, I4, N1, U4]. Since these indirect
effects cannot necessarily be deduced from effects on individuals and populations, ecosystem-level effects are evaluated using mathematical modelling, model ecosystem
experiments and field irradiation experiments.
3.

Multiple stressors

20. In general terms, the modifying effects of multiple
stressors can be considered in one of two broad categories,
namely (a) the modification by the other stressors of theorganism’s uptake of radioactive material and the distribution of radioactive material within the organism, and (b) the
influence of the other stressors on the radiosensitivity of thespecies [A18, B28, F5, G18, L8, P9, R19, S17, S18].
21. Metabolic manifestations of exposure to ionizing radiation include impairment in enzyme function, altered protein
turnover, impairment in general metabolism and inhibitionof growth. Sugg et al. [S17] showed that the body conditionof largemouth bass exposed to mercury and 137Cs in different
lakes near the Savannah River site could be related to DNA
damage. Changes in lipid metabolism in fish liver and astimulation of the ventilation rate of a lamellibranch species
have also been shown to occur at low doses in this mixed
exposure scenario [P22, P23].
22. Experiments involving multiple exposures to metals(cadmium and zinc), organic pollutants, such as polychlorinated biphenyl (PCB), polycyclic aromatic hydrocarbon(PAH), endocrine disruptors, and radionuclides (radioactive
isotopes of cobalt, caesium, and silver) have been conductedboth under controlled conditions and in the field [G17].
Experiments using a freshwater bivalve (Dreissena polymorpha) and a carnivorous fish (Oncorhynchus mykiss)
exposed under chronic conditions to water containing concentrations of 1–4 µg/L of cadmium and/or 170–250 µg/L ofzinc showed a 60% decrease in the bioaccumulation of theisotopes of silver and caesium in the bivalve and a 30%
decrease in the fish. However, no effect was observed forother radionuclide/organism pairs (such as cobalt for thefish). On the other hand, prior exposure to organic micro­
pollutants enhanced both the uptake and retention of 57Co
and 134Cs in the fish. Several possible explanations, linked toa modification of the health status of the animal by the presence of stable pollutants, were advanced by the authors andsupported by biomarker measurements: an increase in respiratory activity by alteration of the global metabolism; adecrease in the Na+/K+-ATPase in gills and therefore modification of the ionic flux; or an alteration of the epithelium
permeability [A16, A17, F15].
23. Genotoxic/cytotoxic damages are not specific to ionizing radiation and may also be initiated by other toxins [S18].
Indeed, most biochemical techniques for detecting DNA
damage at the molecular or cellular level lack specificity forradiation-induced DNA damage [T9]. However, Tsytsugina[T8] and Tsytsugina and Polikarpov [T6] analysed the distribution of chromosome aberrations in cells and the frequencyof the different types of aberrations in order to discriminate
between the contributions of radiation and chemical factors
to the total damage to natural populations in aquatic organisms. These studies showed that the chromosome damage
observed in aquatic worm populations exposed to dose ratesof 10 µGy/h or more in lakes located in the vicinity of the siteof the Chernobyl accident was mainly caused by radioactive
contamination. Hinton and Bréchignac [H20], however, cautioned that, while there is a great potential value in using
biomarkers for assessing risks to non-human biota, there
remain many challenges in linking changes in biomarkers at

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

the molecular or cellular levels to effects on individual­organisms and populations of organisms.
24. The antioxidant status modified by exposure to various
stressors may influence the radiosensitivity of organisms.
The cellular damage due to radiation exposure is mainly
associated with oxidation. This oxidative stress may also be
caused by other stressors, such as chemical pollutants, andcellular defence mechanisms against reactive oxidative­species (ROS) that may be solicited are not stressor specific[S27]. Therefore, the interaction of heavy metals and radionuclides, and the resulting modification of radiosensitivity,
may depend on the capability of the antioxidant defence­systems of the organism [C13, C14, C15, S27, V1].
25. The potential effects of exposure to uranium in theenvironment may arise from the chemical toxicity of themetal and its radiotoxicity (arising from the uranium alphaparticles) and thus, such situations can be regarded as being
due to a mixture of stressors coming from a single element[B30, C19, P24]. Thus, while an evaluation of the chemical
toxicity of uranium to non-human biota is beyond the scopeof this annex, it is important to recognize that the chemical
toxicity and the radiological effects of uranium occur concurrently, and that both may need to be considered in apractical assessment of risks to non-human biota.
4.

Commentary

26. Most of the data on the effects of exposure to ionizing
radiation on non-human biota are from observations made on
individual organisms. Radiation effects on populations occur
as a result of the exposure of individual organisms. The
propa­gation of effects from individual organisms to populations is complex and depends on a number of factors. However, as suggested in the UNSCEAR 1996 Report [U4], themost important effects appear to be those on reproduction

Table 1.

227

and reproductive success. Many questions remain withrespect to the following: the mechanisms whereby radiation
exposure can cause harm; inter-species extrapolation; propagation of harm from nuclear DNA to the population; and theeffects of multiple stressors. Moreover the possibility ofhormetic effects at low doses and dose rates of gamma radiation, the relation between changes in biomarkers at themolecular and cellular level and the effects on individualorganisms or populations of organisms, and the effects ofmultiple stressors continue to be of ­considerable interest.
D. Observations from case studies
27. Ecological risk assessments (ERAs) have been conducted for a wide variety of situations where non-humanbiota are exposed to enhanced levels of radiation or radio­
active material. ERA studies are available for a wide varietyof nuclear fuel cycle activities from uranium mining to waste
management, as well as for sites with enhanced levels ofnaturally occurring radioactive materials, and for sites contaminated as a result of accidents. Table 1 outlines the key
elements of an ERA framework for assessing the effects of
exposure to ionizing radiation on non-human biota. Various
approaches for performing ERAs have been outlined including those of the IAEA [I2, I3, I4], NCRP [N1], the UnitedStates Department of Energy (DOE) [U26], Jones et al. [J1],
Environment Canada and Health Canada [E2], FASSET [F1,L4] and ERICA [B17]. All of the approaches necessarily
involve simplifications of the knowledge about the actual
environment. A common approach to the assessment of theeffects of radiation exposure on non-human biota involves
the use of a screening index (SI), where SI is simply a dimensionless ratio of the estimated dose rate (to an individualorganism) to the reference radiation dose rate, viz.:SI =estimated dose rate
reference dose rate

(1)

Key elements of a framework for the assessment of the effects of radiation exposure on non-human biota
Element

Considerations

Exposure of biota• Spatial and temporal patterns of radionuclide concentrations in environmental material• Uptake by organism• Non-uniform distribution within organism

Reference biota• Not possible to evaluate all biota• Need to select reference biota or indicator species appropriate for area of interest and desirable basis for selection• Possible need to consider individual biota per se when species are endangered

Dosimetry model for (reference) biota• Absorbed dose (to whole body or to tissue/organ)• Geometry corrections• Relative biological effectiveness (RBE): the effects of different qualities of radiation on biota

Endpoints in radiological assessment• Selection of appropriate population-level (deterministic) “umbrella” effects such as mortality or reproductive capacity and­corresponding reference doses

Effects on biota• Connection between radiation effects on “umbrella” endpoint in individual, and consequent “possible” effects on population• Role of background radiation levels• Natural population variability

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UNSCEAR 2008 REPORT: VOLUME II

28. The reference dose rate refers to the chronic dose rate(commonly expressed in milligray per day) below which
potential effects on populations of organisms are notexpected. The ratio, SI, assumes that the estimated dose rate
and the reference dose rate relate to the same endpoint (e.g.
mortality, reproductive capacity). The estimation of dose
rate to an individual organism is discussed in section I of thisannex. As there are many complex factors involved, caution
is needed in extrapolating from the effects of radiation exposure on an individual organism to those on a population oforganisms [B17].
29. The reference radiation dose rates for particular endpoints developed by the Committee in the UNSCEAR 1996
Report [U4] have been the most commonly used for thedenominator of the SI calculation. However, other guidance
has also been developed [C1, E1, E2, F5, I4, N1] and, more
recently, the concept of species sensitivity distributions(SSDs) has been introduced [B17, G3]. These developments
may necessitate a re-evaluation of the reference dose rates
obtained in the ERA case studies.
30. Because of the sparsity of peer-reviewed literature, allof the various sources of information on reference dose rates(e.g. various reports and supporting environmental assessments in Canada, technical reports of government agencies
in various countries and conference proceedings) have been
considered in this annex.
31. Of the numerous reports [A24, A25, B17, C1, C2, C20,
C22, E2, E3, E5, E22, E23, F2, G2, G3, G27, J2, S10, S11,
S32, S33, U26, W19], only a few provide studies of the radia­
tion exposure of non-human biota arising from radio­active
waste management activities or accidents involving dose
rates close to or exceeding the reference dose rates [A25, E8,E22]. For example, one study [S39] which involved investigation of the risks to biota from exposure to ionizing radiation from nuclear fuel cycle activities in Canada concluded
that the largest risk is associated with past uranium mining
activities; that discharges of radioactive material from powerreactors under normal operating conditions are not expected
to cause environmental harm; that organisms within one of
the waste management areas examined may be harmed byexposure to ionizing radiation; and that current radioactive
discharges from uranium refineries and conversion plants are
not expected to cause environmental harm. Similar results
can be derived from a consideration of the case studies
reported in ERICA [B17] of a wide ­variety of nuclear fuelcycle and other activities.
32. One study in which the estimated dose rates to biota
exceeded the reference dose rates, at least over a limited area,
was of the radioactive waste management site at the ChalkRiver Laboratories (CRL) located on the shore of the Ottawa
River, 160 km north-west of Ottawa, Ontario, Canada [E23].
The CRL site was established in the mid-1940s and has a history of various nuclear operations and facilities, primarily
related to research. An ERA was conducted to assess thedoses to biota arising from elevated levels of tritium, 14C,

Ar, 90Sr, 131I, 137Cs and 239Pu and from radionuclides that are
naturally present in the environment, for example, the uranium series radionuclides, using standard methods for evaluating the uptake of these radionuclides by biota from theaffected aquatic and terrestrial environments [B12]. A reference dose rate of 1 mGy/d was used for all organisms [B36].
Dose rates to some aquatic organisms such as frogs, small
fish, snails and aquatic plants within the on-site waste management areas were estimated to be above the reference dose
rate of 1 mGy/d; however, outside of the actual waste management areas, dose rates were estimated to be below the reference dose rate. The main contributor to the estimated dose
rates to invertebrates and terrestrial plants was 90Sr in surface
soil, while that to the woodchuck (estimated at 51 mGy/d)was inhalation in the burrow of 222Rn decay products frombackground levels of 226Ra in the soil. A few individual invertebrates and terrestrial plants actually within the confines ofsmall on-site waste management facilities were also estimated to have been subjected to dose rates above 1 mGy/d.
Based on the limited spatial extent of the estimated dose rates
that exceeded the reference dose rate and environmental
observations, the authors considered that significant effects at
the population level were unlikely.
41

33. Much of the new information on the effects of exposure
to ionizing radiation on organisms has arisen from studies in
the area surrounding the site of the Chernobyl accident,
where dose rates to organisms were above the reference dose
rate suggested in the UNSCEAR 1996 Report [U4]. A summary of the results of these studies up to 1996 is provided inthis annex. Section III of this annex provides a comprehensive review of the more recent data from studies of nonhuman biota in the area surrounding the site of the Chernobyl
accident.
E. Structure of this annex
34. The prime purpose of this annex is to build on theinformation reported in the UNSCEAR 1996 Report [U4];to compile data that has since become available on theeffects of exposure to ionizing radiation on non-humanbiota; and to determine if the reference dose rates need to be
updated. However, it is necessary first to provide some general information on the relationships between the levels ofradiation in the environment in which the biota live and theconsequent dose (or dose rate) to biota as a whole or selected
tissues and organs. Table 1 provides a summary of five key
elements that form the basis for assessing the effects of
exposure to ionizing radiation on non-human biota.
35. The relationships between the levels of radiation exposure and the activity concentration of radioactive material in
the environment and the dose to an organism living in thatenvironment is the subject of section I.
36. Section II provides a summary of the information considered in the UNSCEAR 1996 Report [U4] and the key
observations from that report.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

37. Section III provides an overview of the findings of thestudies of non-human biota in the area surrounding the siteof the Chernobyl accident. It includes the work of the­Chernobyl Forum [E8].
38. Section IV provides a summary of the effects of
exposure to ionizing radiation on non-human biota derived
from the material given in earlier sections and reviews
carried out by other scientific organizations and groups,
namely, the IAEA [I4], Bird et al. [B1], the DOE [J1,U26], Environment Canada and Health Canada [E2],I.

Canada’s former Advisory Committee on RadiologicalProtection (ACRP) [A1], the UK Environment Agency[C1], the FASSET group [F1, F5, L1, L4], and the ERICA
group [E1, G11, G15]. The published literature was also
reviewed.
39. Section V provides an overall summary of the data
reviewed and, based on these data, the Committee’s evaluation of the dose rates below which effects on non-humanbiota are not considered likely. A few important areas forpotential future study are also noted.

ESTIMATING doseS to non-human biota

40. Data on the effects of radiation exposure on non-humanbiota have been obtained from experimental studies carriedout in the laboratory and in the field. Additional data havebeen obtained from the results of studies on environmentswith elevated levels of radiation or of radioactive material
resulting from normal operations of nuclear facilities, waste
management activities, or accidents. The interpretation of
the results of these studies requires an understanding of therelationship between the levels of radiation and the activity
concentrations of radionuclides in the various environmental
media in which the organism resides, the consequent dose
rate to an organism (or a tissue or organ of the organism) thatlives in the environment, and the biological effect of interest.
For example, radionuclides in the ambient environment may
lead to external irradiation and internal irradiation as a resultof radionuclides being taken into the organism via inhalation, ingestion, or uptake through its skin or membrane.
Empirically determined concentration factors and transfer
factors are commonly used to estimate contaminant concentrations in the organism (e.g. expressed for wet or dry weightin units of Bq/kg) from concentrations in the ambient environment (e.g. expressed in units of Bq/kg for sediment orsoil, or Bq/L for water). Dosimetric models can then be used
to derive, for selected organisms, dose conversion coefficients (DCCs) that relate ambient concentrations to internalor external exposure, as appropriate, and hence to dose.
A.

229

Assessing exposures of biota

1. Choice of reference organisms
41. In view of the enormous variety of living organisms, itwould be impossible to consider all species of flora andfauna as part of an environmental impact assessment evenfor a limited area. Instead, a concept has been developed
involving the selection of reference organisms that are representative of large components of common ecosystems andfor which models are adopted for the purpose of deriving
doses and dose rates to organisms, tissues, or organs fromradionuclides in the environment. The results of such dose
assessments for these predefined reference organisms willallow a basic assessment to be made concerning the possible
biological effects. This approach provides a strategy thatallows the modelling effort to be reduced to a manageablelevel. It further provides information on the exposures of different organisms under varying exposure conditions, whichallows the estimation of the impacts on those components ofthe environment for which data may be sparse or absent.
42. The reference organism approach of the ICRP had its
genesis in some earlier publications [P6, P13]. In the framework of the FASSET project [F20, L4], reference organisms
were defined as “a series of entities that provide a basis forthe estimation of radiation dose rate”. The idea was that theseorganisms would provide a basis for assessing the doses toorganisms and consequential effects in general due to radionuclides in the environment. The main criterion for the selection of reference organisms within the FASSET project wasthat the habitats and feeding habits should be such that theexternal and internal exposures are maximized.
43. The ICRP is assembling databases that relate to a limited
number of “reference animals and plants”. These are defined
as “hypothetical entities with the assumed basic charac­teristics
of a specific type of animal or plant, as described to the generality of the taxonomic level of family, with defined anatomical, physiological, and life-history properties that can be used
for the purposes of relating exposure to dose, and dose toeffects, for that type of living organism” [I12].
44. Both the FASSET and the ICRP approaches wereintended to simplify the process of estimation and evaluationof exposures to ionizing radiation of non-human biota.
Whereas reference organisms in FASSET were specificallyselected for different ecosystems (e.g. agricultural, semi-­
natural, freshwater, and marine), ICRP [I10] described thereference animals and plants in groups (family or taxonomic
level). The reference organisms selected cover a range of ecosystems and taxonomic families (table 2). The generic (reference) organisms that are explicitly considered in this annex
are summarized in table 2. Organisms similar to those adopted
by the ICRP were selected for consistency. The features ofthe selected organisms are described in reference [I10].

230

Table 2.

UNSCEAR 2008 REPORT: VOLUME II

Comparison of reference organisms defined by different international bodies
Defined by

Reference organisms

FASSET
Terrestrial ecosystems [L1]

Soil microorganisms
Soil invertebrates
Plants and fungi
Bryophytes
Grasses, herbs and crops
ShrubsAbove ground invertebrate
Burrowing mammal
Herbivorous mammals
Carnivorous mammals
ReptileVertebrate eggs
Amphibians
Birds
Trees

FASSET
Aquatic ecosystems [L1]

Benthic bacteria
Benthic invertebrates
Molluscs
Crustaceans
Vascular plants
Amphibians
Fish
Fish eggs
Wading birds
Sea mammals
Phytoplankton
Zooplankton
Macroalgae

ICRP
Proposal on Reference Animals and Plants [I10]This annex

2. Radioecological models
45. Three classes of radioecological model can be distinguished and are presented here in terms of increasing complexity—equilibrium models, dynamic models and researchmodels.

Deer
Rat
Duck
Frog
Trout
FlatfishBee
CrabEarthworm
Pine tree
Wild grass
Brown seaweed
Earthworm/soil invertebrate
Rat/burrowing mammal
Bee/above ground invertebrate
Wild grass/grasses, herbs and crops
Pine tree/tree
Deer/herbivorous mammal
Duck/bird
Frog/amphibian
Brown seaweed/macroalgae
Trout/pelagic fish
Flatfish/benthic fish
Crab/crustaceans

46. Equilibrium models are primarily intended for theassessment of exposures due to routine discharges of radio­
active material into air or water. They are based on two fundamental assumptions: (a) the emission rates of the radionuclides
are constant in time; and (b) the duration of the discharges islong compared to the time needed for radionuclide transfer

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

along the environmental pathways considered. With theseassumptions, the radionuclide concentrations reach equilibrium within each of the compartments into which the environment is subdivided for modelling purposes, and the transfers
between compartments are easily characterized by time-­
invariant ratios of concentrations between the acceptor anddonor compartments.
47. Since equilibrium radionuclide concentrations in theenvironment are typically attained after considerably long
operational times of a nuclear facility, the equilibrium­models are likely to give conservative exposure estimates.
This type of radioecological model has been used to determine compliance of routine discharges from nuclear ­facilities
with authorized limits [H4, I11, N3, U3].
48. Ciffroy et al. [C22] tested the influence of the timedependence assumption frequently used in radioecologicalmodels in a case study conducted on the Loire River inFrance. For routine discharges of radionuclides from
nuclear power plants, their main conclusions were that:(a) attention must be paid to the temporal variations in the
discharges, and gaps between actual instantaneous discharges and maximum discharges on a yearly time scalemust be analysed; (b) the equilibrium assumption at thewater-suspended matter interface must be justified andeventually corrected when equilibrium conditions are notexpected; and (c) for organisms showing slow uptake/elimination rates, a kinetic approach to the bioaccumulation
process can avoid some overestimation of radionuclide
concentrations. The assumption of equilibrium led to overestimations of one to two orders of magnitude in predicting60
Co concentrations in invertebrates.
49. A number of inherent advantages have contributed tothe proliferation of equilibrium models. The model structure
can be kept simple, but there is flexibility to allow moredetailed structure, if necessary. Under equilibrium conditions, dispersion of trace amounts of radionuclides in theatmosphere or rivers is adequately represented by analyticalsolutions of more general physical models; transfer via foodchains is represented by simple multiplicative chains of­concentration ratios.
50. A major conceptual limitation of radioecologicalmodels is that many of the parameters involved (e.g. concentration ratios) have to be established empirically.
Experience gained during recent decades has amply demonstrated that numerical values of many of these parameters may vary by several orders of magnitude; this has
been well documented, for example, for plant–soil relationships of radiocaesium and radiostrontium concentrations [F7, F8, N4]. While for the purposes of screening or
environmental protection as may be established by the
ICRP or required by a national regulator, representative
parameter values can be selected that ensure that themodel assessments are conservative, obvious difficulties
exist if a realistic assessment of exposures in specific­ecosystems is needed.

231

51. Dynamic radioecological models [M4, S13, W3] areapplied if the time dependence of exposures that result fromvarying or instantaneous releases has to be taken into
account. Examples of their use include the assessment of
the time-dependent radionuclide concentrations in the environment, such as those resulting from accidental radio­
nuclide releases varying over time, and the simulation ofseasonal effects, which are of major importance in terrestrial environments during the first year following depositionof radionuclides after an accidental release [M7].
52. Research models are characterized by a high degree ofcomplexity and longer computation times, and presently are
limited to simulating a few of the important processes inanalyses of environmental pathways for radionuclides [C7,P9]. Currently, therefore, they do not offer an alternative toequilibrium and dynamic radioecological models for environmental assessments, although they do constitute animportant tool for improving understanding of the sources ofvariability observed empirically.
53. The scope of this annex is limited to providing a broad
overview of the approach to estimating radiation exposureand subsequent doses to non-human biota. The reader interested in these topics is referred to the extensive literature.
Exposure assessments are generally based on equilibrium
models. However, for case studies at specific locations contaminated by accidental releases of radionuclides, information on the levels of exposure of local biota taken from theliterature is sometimes based on simulations using dynamic
radioecological models.

3.

Transfer of radionuclides in the environmentand resulting exposures

54. The major pathways of radiation exposure of biota
in the environment are summarized in figure II. In thisschematic representation, the physical components of theterrestrial environment are air, soil and sediment; the­biological components include plants, invertebrates, andvertebrates (mammals, birds, reptiles, and land-based
amphibians). The physical components of the freshwateraquatic environment include streams, rivers, lakes andsediments; the biological components are phytoplankton,
zooplankton, macroinvertebrates, sessile aquatic plants
and vertebrates (fish, water-based amphibians and someaquatic mammals). In a marine environment, the physicalcomponents include tidal zones, coastal waters andmarine sediments; and the biological components include
phytoplankton, zooplankton, macroinvertebrates, sessile
aquatic plants, and vertebrates (fish and marine mammals), molluscs, crustaceans and marine birds. The terrestrial and aquatic environments are not totally separate.
Some birds and terrestrial mammals eat fish and shellfish; moose and waterfowl feed on aquatic plants; andterrestrial animals ingest drinking water from the aquatic
environment.

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UNSCEAR 2008 REPORT: VOLUME II

Figure II. Major environmental transfer routes for evaluating radiation exposure of biota
Activity in air and rain

Activity in water/sediment

PlantsSoil/sediment

Biota
External
exposureInternal
exposure

External
exposure

Radiation exposure of biota

55. The total radiation dose received by an organism (orsome organ or tissue of the organism) is the sum of the contributions from both external and internal exposure. External
exposure results from complex non-linear interactions ofvarious factors, such as the levels of the radionuclides in the
habitat, the geometrical relationships between the radiation
source and the target, the shielding properties of the materials in the environment, the size of the organism and theradio­nuclide-specific decay properties (characterized by thetype and energy of the radiations emitted and their emission
probabilities).
56. Internal exposure is determined by the activity concentrations of the radionuclides in the organism, the size of theorganism, the radionuclide distributions within the organism
and the specific decay properties of the radionuclides. In
addition, the relative biological effectivenesses (RBE) ofalpha, beta and gamma radiation need to be taken into
account in assessing the consequences of the exposure.

B.

Transfer of radionuclides in the terrestrial environment

57. Radioactive material released into the atmosphere isdispersed and transported by the wind. Exposures ofbiota are calculated from the activity concentrations ofradionuclides in the environmental media, such as air,soils and vegetation, and in the organisms under consideration. The principal processes involved in the transportof radionuclides in the terrestrial environment include
dry deposition, wet deposition, interception by vegetation, loss of radionuclides from plants due to weathering,
resuspension, the systemic transport of radionuclides
within plants, uptake from soil, run-off to water bodies
and the transfer to animals. This section discusses thefactors that affect the behaviour of radionuclides in a terrestrial environment and the uptake of radionuclides
from the environment to plants and animals.

1.

Dry deposition

58. Dry deposition per unit time is proportional to the nearsurface concentration of the material in air. Usually, the dry
deposition of a radionuclide from the atmosphere to soil andvegetation is expressed in terms of the deposition velocity,vg (m/s), which is defined as the ratio of the activity deposition rate per unit area and the local activity concentration in
air of the radionuclide at a reference height. This empiricalquantity depends on a variety of factors such as the size of
any associated particles, the characteristics of the surface–air
interface, the meteorological conditions and the chemical
form of the radionuclide.
59. Typical estimates of deposition velocities for grass andforests are summarized in table 3. These values are used forthe calculation of the exposures of biota resulting from theatmospheric release of radionuclides.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

Table 3.

233

Typical estimates of deposition velocities for grass and forest [P14, R11]
Chemical/physical form

Deposition velocity (m/s)
Foresta

Grass

Particles, 0.1–1 µm
Elemental iodine
Methyl iodide

0.001
0.01
0.000 1

Crown

Trunk

Soil

0.005
0.05
0.000 50.000 50.005
0.000 05

0.000 8–0.003
0.006–0.02
0.000 08–0.000 3

a Coniferous trees and deciduous trees with fully developed foliage.

2.

3.

Interception of radionuclides deposited from the air

Weathering

60. Interception defines the fraction of radioactivity deposited by wet and dry deposition processes that is initiallyretained by the plant. There are several possible ways toquantify the interception of deposited radionuclides. The
simplest is the interception fraction, f, which is defined as theratio of the activity initially retained by the standing vegetation, Ai, immediately subsequent to the deposition event to
the total activity deposited. A full description of the interception process is beyond the scope of this annex and the reader
interested in this topic is referred to the extensive literature(e.g. see reference [H26]).

63. Following deposition on vegetation, radionuclides are
removed by wind and rain. In addition, the increase of biomass
during growth leads to a reduction in the activity concentration.
Since growth is subject to seasonal variations, the post-­
deposition reduction of the activity concentration of radio­
nuclides in plants depends on the season. These processes of
reduction in the activity concentration of radionuclides in plants
occur simultaneously after deposition. As it is difficult to quantify the exact contribution of each process, the net reduction in
the activity concentration with time is usually called “weathering” and expressed by the empirical weathering half-time, Tw.

61. Radioactive material in air can be washed out by rain
and snow. A fraction of the radionuclides deposited with
precipitation is retained by the vegetation, and the rest
falls through the canopy to the ground. Although theradio­active material retained eventually transfers to soil
through weathering and is retained only temporarily byvegetation, the fraction initially intercepted is important
owing to the fact that the concentration of radioactive
material will be at its highest at this time. Interception of
wet deposits is the result of a complex interaction of theamount of rainfall, the chemical and physical form of thedeposit and the actual stage of development of the plant[M4] and thus, interception fractions for a single event
may vary from 0 to 1.

64. The chemical form of the contaminant seems to be ofminor importance in weathering. After the Chernobyl accident, the median weathering half-times observed for iodine
and caesium on grass were approximately 8 and 10 days,
respectively [K5]. Shorter half-times were observed primarily in regions with fast growing vegetation, while longer
half-times were found in Scandinavia, where the growth
rates were lower because of the later spring in the area [K5].
In general, longer weathering half-times are observed forslowly growing or dormant vegetation [M8].

62. To account for its dependence on biomass in somemodels, the interception of wet deposited activity is model­
led as a function of the biomass density, according to theapproach of Chamberlain [C8]. The chemical form is a key
factor; since the plant surface is negatively charged, theabsorption of anions is less effective than that of cations [H6,H7, K4, M4, P11]. Differences between plants seem to be ofminor importance compared to those between radionuclides,
e.g. the interception of polyvalent cations is higher than thatfor anions by as much as a factor of 8 [H5]. However, ingeneral, for the estimation of interception following the routine discharge of radioactive material, very simple approaches
are used in the models [P10]. Anspaugh [A22] suggested adefault value for the interception fraction of the order of 0.3
for all elements, plants and precipitation events for routinedischarges of radionuclides.

65. In forests, weathering is more complex because of the
canopy structure, which comprises several vegetation layers, such as crown, trunk and understorey vegetation. Radio­
nuclides lost from the crown may be retained by theunderstorey vegetation, thus reducing the overall loss rate ofradionuclides from vegetation to soil.
4.

Distribution of radionuclides within plants

66. The currently available dosimetric models for theassessment of the exposure of biota do not take into accountheterogeneous radionuclide distributions within plants.
Hence, any information on these distributions cannot­currently be used in the assessment.
5.

Uptake of radionuclides from soil

67. Soil is the main reservoir for long-lived radionuclides deposited on terrestrial ecosystems. The behaviour of radionuclides in234

UNSCEAR 2008 REPORT: VOLUME II

soils controls their migration in soil, the possible transport togroundwater, and the long-term radionuclide concentration invegetation and thus the exposure of soil organisms. As for all
minerals, the uptake of radionuclides by plants mainly takes
place via dissolution from soil. The concentration of radio­
nuclides in soil solutions is the result of complex physical–
chemical interactions with the soil matrix, with ion exchange
being the dominant mechanism. Ion exchange by its very
nature is a competitive mechanism. The concentrations andcomposition of the major competing elements present in soil
thus are of primary importance in determining the distributionof radio­nuclides between soil, soil solution and plant roots(which are able to influence the microspace in their vicinity inorder to provide and maintain conditions that favour the uptakeof nutrients) [E6].
68. The physical chemistry of sorption and desorption ofradionuclides in the soil–soil solution system and their possible uptake by plants are the result of complex interactions
between soil type, pH, redox potential, sorption capacity,
clay content, content of organic matter and soil management practice. Although these factors are qualitatively
known, they are difficult either to quantify or to integrate
into a universal model applicable to a wide range of soil
conditions. Consequently, the approaches used include
classifying the transfer according to soil types (e.g. peat,sand, loam and clay) and other physical and chemicalparameters. In addition, various biological factors should
be considered, especially whether or not the radionuclide isan essential element.
69. For the quantification of the root uptake of radio­
nuclides, empirically derived (aggregated and greatly simplified) parameters—soil–plant transfer factors or concentration

Table 4.

ratios—are usually applied despite their inherent limitations[E6]. In this case, these parameters are the ratios of theactivity concentrations in the plant to those in the soil within
the uppermost layer of a standardized thickness. Transfer
factors were originally defined for agricultural ecosystems
within which radionuclides are distributed homogeneously
within the rooting depth of agricultural plants because ofploughing.
70. The aggregated transfer factor is defined as the activity
concentration of a radionuclide in a material (Bq/kg) divided
by the total deposition—activity per unit area (Bq/m2)—atequilibrium. The concept of aggregated transfer factors wasdeveloped as a simplification of detailed physical and chemical processes to a single value, inter alia, to avoid difficulties
with determining radionuclide concentrations in soils with amulti-layered structure, such as in forests.
71. Alternatively, concentration ratios that relate to theactivity concentrations of radionuclides in specific soil horizons exploited by the mycelium or the root system were proposed in the late 1980s and proved to be useful, especially inconnection with the prediction of the transfer of 137Cs tofungi [G4, R8, Y1, Y4, Y5].
72. Illustrative ranges of soil–plant transfer factors for anumber of elements are summarized in table 4 [T11]. This
table shows that the uptake of caesium from soil usually
does not result in a simple proportional accumulation inplants. Radiocaesium is effectively sorbed by micaceous
clay minerals that are present in almost all soils in varying
amounts. A detailed compilation of soil–plant transfer factors including data for specific plant groups, plant organs
and soil types can be found elsewhere [I14].

Typical ranges of soil–plant transfer factors [T11]
Element

Concentration ratio
Bq/kg plant (d.m.) per Bq/kg soil (d.m.)

Aggregated transfer factora
Bq/kg plant (d.m.) per Bq/m2 soil

Sr
Cs
Csb
I
Tc
Pb
Ra
U
Np
Pu
Am
Cm

0.01–10.001–0.1
0.1–100.001–1
0.1–100.001–0.01
0.001–0.1
0.001–0.1
0.001–0.1
10‑5–10‑3
10‑5–10‑3
10‑5–10‑3

4 × 10‑5–4 × 10‑3
4 × 10‑6–4 × 10‑4
4 × 10‑4–4 × 10‑2
4 × 10‑6–4 × 10‑3
4 × 10‑4–4 × 10‑2
4 × 10‑6–4 × 10‑5
4 × 10‑6–4 × 10‑4
4 × 10‑6–4 × 10‑4
4 × 10‑6–4 × 10‑4
4 × 10‑8–4 × 10‑6
4 × 10‑8–4 × 10‑6
4 × 10‑8–4 × 10‑6

a Calculated from the concentration ratio assuming a mass density for dry matter (d.m.) in the soil rooting zone of 280 kg/m2 taking account of the mass of the soil within therooting zone.
b Observed range in natural and semi-natural ecosystems on acid sandy soils poor in potassium.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

73. Caesium uptake is particularly high from organic soils
with a low pH and pronounced potassium deficits [F11].
Such soils are frequently found in the Russian Federation,
Belarus and Ukraine, as well as in Scandinavia, the uplandareas of the UK and the alpine areas of Europe. For organic
matter, the cation exchange capacity decreases with increasing acidity owing to the saturation of carboxyl groups withhydrogen ions. Furthermore, the availability of caesium for
uptake is enhanced in soils that are poor in potassium. Additionally, the clay content of organic soils is low and this prevents strong sorption and leads to persistently high caesium
levels in plants [A7, F12, F13, K6]. Another important aspectis that the bioavailability of radionuclides and their uptake
after deposition may change with time. This was observed inareas close to the site of the Chernobyl accident and wascaused by the degradation of fuel particles, the fixation of
caesium within the soil and changes in the sorption strengthof the soil for caesium [N5, S14, S15].
74. In recent years, a number of experiments have been
performed to determine soil–plant transfer factors for tropical and subtropical environments [C9, F11, R6, T12, T13,

235

U24, U25, W12, W13]. The anaerobic soil conditions inflooded paddy fields change the solubility of some elements,
such as I and Tc, and thus possibly their soil–plant transfer
factors [M25, T26, Y3]. In general, however, the results do
not indicate any systematic impact of climatic conditions on
the transfer of radionuclides from soil to plants, although thenumbers of data are still small. Further data on the tropicaland subtropical environments are therefore needed [M25].
75. In forest ecosystems, the transfer of radionuclides fromsoil to plants and fungal fruit bodies depends on the depth
profile of the radionuclides and the vertical distribution of fineroots and fungal mycelia in soil. At least in the case of fungi,
the use of transfer factors referring explicitly to the soil layer
exploited by fungal mycelia seems to be the best approach forquantifying the uptake to radionuclides, balancing overall
simplicity with mechanistic considerations of the dynamic
processes [S37]. However, the concentrations of radionuclides
in understorey vegetation, trees and fungal fruit bodies can be
estimated roughly in a simplified manner using aggregatedtransfer factors. The ranges of aggregated transfer factors
given in table 5 summarize the available observations.

Table 5. Typical ranges of aggregated transfer factors for 137Cs from soil to vegetation and fungal fruit bodies in forest
ecosystems [A8, B27, G7, I16, I17, K15, L7, Z1]
Data are given on a dry weight basis unless otherwise noted
Species or genus

TFagg (Bq/kg organism (d.m.) per Bq/m2 soil)
Fungal fruit bodies

Agaricus
Amanita
Armillaria
BoletusCantharellus
Clitocybe
Collybia
Coprinus
Cortinarius
HydnumHygrophorus
Laccaria
Lactarius
Leccinum
Lepista
Lycoperdon
Macrolepiota
Paxillus
Ramaria
Rozites
RussulaSarcodonSuillus
Tuber
Xerocomus

0.002–0.007
0.008–5
0.001–0.2
0.001–10
0.01–20.01–2
0.03–0.3
0.004a
0.02–103a0.2–7
0.4–100.006–5
0.005–0.9
0.002a0.009–0.5
0.000 7–0.1
0.01–50.05–0.6
0.08–10
0.04–5
0.3–0.4
0.02–20.000 3–0.008b
0.002–7

236

UNSCEAR 2008 REPORT: VOLUME IISpecies or genus

TFagg (Bq/kg organism (d.m.) per Bq/m2 soil)
Understorey vegetation

Rubus chamaemorus (cloudberry), fruit
Vaccinium vitis-idaea (lingonberry), fruit
Vaccinium myrtillus (bilberry), fruit
Rubus idaeus (raspberry), fruit
Fragaria vesca (strawberry), fruit
Rubus fruticosus (blackberry), fruit
Green parts of understorey vegetation, including
the stems of berry plants

0.002–0.2
0.03–0.07
0.02–0.1
0.001–0.004
0.004–0.01
0.006–0.05
0.001–1
Trees

Fagus sp. (beech)
Bole wood
Leaves0.001–0.002
0.002–0.003

Picea sp. (spruce)
Bole wood
Needles

0.000 3–0.002
0.000 6–0.02

Pinus sp. (pine)
Bole wood
Needles

0.000 2–0.003
0.001–0.04

Quercus sp. (oak)Bole wood
Leaves

0.002–0.004
0.008–0.01

Betula sp. (birch)
Bole wood
Leaves0.000 03–0.001
0.000 3–0.04

Populus sp. (aspen)
Bole wood
Leaves0.000 5–0.002
0.008aAlnus sp. (alder)
Bole wood
Leaves0.001a0.008aa Only a single value available.
b Data are given on a fresh weight basis and refer to the top 10 cm of soil.

76. Fungi are able to accumulate radiocaesium in theirfruit bodies [G14, H8]. Some species exhibit activity levels
that exceed those of green plants by more than one order ofmagnitude. On average, the radiocaesium levels in symbiotic fungi are higher than those in saprophytic species [R7,Y4, Y5].
77. Radionuclides in growing wood originate from twosources: the initial atmospheric deposits that enter the plantby foliar absorption, and root uptake from the soil. Theirrelative contributions depend on the type of tree (coniferous
versus deciduous) and the age [B20, E7, G5, H9], the season
at the time of deposition and the time elapsed after deposition, with root uptake being the dominant pathway for growing wood in the long term. Transfer factors or concentration
ratios that are calculated on the basis of the total content ofradionuclides in wood inevitably include both uptake pro­
cesses and therefore are likely to overestimate root uptake(table 5) [G5].

6.

Migration in soil

78. Vertical migration of radionuclides in the soil column
is driven by various transport mechanisms, such as convection, dispersion, diffusion and bioturbation. The long-term
consequences of downward migration differ considerably,
however, depending on the dominant mechanism. For­convective-driven migration, for example, the radionuclide
input due to the Chernobyl accident moves down the soil asa marked peak and shows broadening with time as a result ofdispersive mixing. Convective transport of radionuclides
usually dominates in soils showing high hydraulic conductivities, e.g. sandy soils. For further discussion of the importance of downward migration of radionuclides in soil andforest litters, see section III and the references cited.
79. For diffusive transport, the concentration is always at a
maximum at the surface with a close to exponential decrease
with depth. For this type of transport, which is typical inANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

soils of low hydraulic conductivity, the bulk of the radio­
nuclides deposited from the atmosphere thus remains within
the rooting zone of plants.
80. Agricultural practices have a major impact on radio­
nuclide behaviour. Depending on the intensity and type ofsoil cultivation, mechanical redistribution of radionuclides
may occur. This causes, in arable soils, a rather uniform distribution of radionuclides in the tilled horizon. Fertilization
shifts the ratio of radionuclide to nutrient concentrations insoil and soil solution and thus may influence plant root
uptake of the radionuclides [E6].
81. Some investigations indicate [B21, S16] that elementindependent transport mechanisms, such as the transport ofradionuclides attached to clay particles or soil colloids, may
play a relevant role in determining the migration rate of radio­
nuclides in soil. Furthermore, the activity of soil animals thatcause a turnover of soil, e.g. earthworms, cannot be neglected.
The authors of references [B21, S16] suggest that a value of
100 years for the default residence half-time for the upper
25 cm layer is adequate for all elements with low mobility,
such as radium, lead, uranium, plutonium and americium.
Iodine under aerobic conditions is strongly bound to organic
matter and therefore a residence half-time of 100 years canalso be assumed [K7]. On the other hand, iodine can bereleased from soil to soil solution under anaerobic conditions,such as in a flooded paddy field [M25].
82. The situation with forest soil is more complex owing to
the more pronounced soil horizons. Radionuclides deposited
directly onto forest soil or washed from the canopy andunderstorey vegetation initially infiltrate the soil rather rapidly. They are therefore initially assigned to a labile pool. In
the long term, they will become immobilized through fungal
or microbial activity or by mineral constituents of the soil.
The radionuclides in the non-labile pool may be available forroot uptake, e.g. via symbiotic fungi, but are assumed not tobe leached to deeper soil layers. The rate of downward migration is correspondingly reduced considerably over time, and,in the organic horizons, is determined mainly by the rates ofdecomposition of the organic material, and litter accumulation. Subsequently, downward migration of radionuclides israther slow and partially offset by upward translocation byfungal mycelia and roots [R4]. Fungal and microbiologicalactivity is likely to contribute substantially to the long-term
retention of radionuclides, notably radiocaesium, in organic
layers of forest soil. In this phase, radiocaesium is well mixed
and almost equilibrated with stable caesium within the biologically connected compartments [Y6]. When radionuclides
reach the mineral horizons of forest soil, essentially the sameprocesses may occur as in arable soils, e.g. radiocaesium canbe fixed by micaceous clay minerals.
7.

Resuspension

83. Resuspension refers to the removal of deposited material from the ground to atmosphere as a result of wind, traffic,

237

soil cultivation and other activities. Potentially, resuspension
is a persistent source of radionuclides in air subsequent totheir deposition on the ground. Furthermore, it may lead toredistribution of radionuclides and their deposition onto cleansurfaces. Resuspension is influenced by a variety of factors,
such as the time since deposition, meteorological conditions,surface characteristics and human activities. For biota, resuspension is of low importance. For animals living in the soil, it
is not relevant. The contribution of resuspension to the activity concentration of radionuclides in plants in humid eco­systems usually is negligible compared to that of dry­deposition and interception [G6, H10].
8.

Transfer to animals

84. The transfer of radionuclides to animals is usuallyestimated using element-dependent concentration ratios ortransfer factors. The transfer factor is defined either as theratio of the activity concentration in an organism or tissue
and the intake rate under equilibrium conditions, or as theratio of the activity concentration in an organism or tissue
and the deposition density (activity per unit area). It isonly applicable to an intake of a radionuclide by adult animals that is constant over long periods. To account for
time-dependent (dynamic) intakes, one or more biologicalhalf-lives are considered [M4].
85. In recent decades, many data have been accumulatedon the transfer factors for domestic animals. They depend on
animal mass, performance level, feeding regimes and feed
components. However, these data are not generally applicable to estimating activity concentrations in biota, since they
were determined in order to estimate activity concentrationsin animal products for human food (such as meat, milk andeggs) while this annex is concerned with the estimation ofactivity concentrations in whole animals. Furthermore, theapplication of transfer factors presumes knowledge of thefeed intake as well as the activity concentrations of the feed
components. It has been demonstrated that highly contaminated feed components may determine the activity levels ofgame, even if consumed in low quantities. The seasonal peak
activity concentration of 137Cs in roe deer, for example, hasbeen attributed to the ingestion of mushrooms [Z1]. Fungal
fruit bodies can show radiocaesium levels exceeding thoseof green plants by one order of magnitude or more. Wildboar ingest deer truffle (Elaphomyces granulatus), a preferred “delicacy”, which dominates the radiocaesium uptake,despite being only a few per cent of the boar’s total diet [F14,P12]. However, the relevant data are not available for wild
animals in general.
86. In most cases, the activity concentrations of radio­
nuclides in game are calculated in a simplified manner using
aggregated transfer factors. This transfer factor neither takes
into account the time-dependent intake rates nor can reproduce the time-dependent activity concentrations in game.
Values for aggregated transfer factors for different species
are compiled in table 6.

238

UNSCEAR 2008 REPORT: VOLUME IITable 6. Aggregated transfer factors (soil-to-game) for 137Cs [A9, I16, J3, K8, S19, Z1]
Data are given on a fresh mass basis unless otherwise noted
Species

TFagg (Bq/kg organism (dry mass) per Bq/m2 soil (dry mass))
Default value

Range of literature data

0.02
0.05
0.03
0.03
0.004
0.3
0.02

0.006–0.03
0.001–0.2
0.02–0.04
0.009–0.1
0.002–0.05
0.01–10a

Alces alces (moose)
Capreolus capreolus (roe deer)
Cervus elaphus (red deer)
Lepus arcticus (arctic hare)
Lepus capensis (brown hare)
Lynx lynx (lynx)
Game except roe deera Data are given on a dry weight basis.

87. Table 7 summarizes the equilibrium concentration
ratios for the reference organisms considered. The values are“order-of-magnitude” estimates based on the compilation inreference [F4]. Some of the original values were given as
aggregated transfer factors and have been converted to concentration ratios. At least in temperate environments, concentration ratios are higher in forest and semi-natural
ecosystems than in agricultural systems, because of theiroften lower nutrient supply and pH values. Furthermore, thehigh content of organic matter in forests is accompanied byhigh concentrations of fulvic and humic acids, which act as

Table 7.

complexing agents and increase the mobility of cationicradionuclides in soil.
88. The nominal values of transfer factors provided in table
7 have been suggested for use [E10, F4], in the absence ofsite-specific information, to estimate the exposure rates forbiota after the release of radionuclides to atmosphere andtheir subsequent transfer to soil. As such, these transfer­factors were intended to be applied for screening purposes toobtain an order of magnitude estimate, but they may not beappropriate for application to specific sites.

Nominal values of transfer factors for reference organisms (adapted from [E10, F4])

Element

Transfer factors (Bq/kg (fresh weight) per Bq/kg soil)
Earthworm

Rat

Deer

Duck

Frog

Bee

Grass

Pine tree

H

150

150

150

150

150

150

150

150

Cl

0.2

7

7

7

7

0.3

20

1

Sr

0.01

2

2

0.6

1

0.06

0.2

0.5

Tc

0.4

0.4

0.4

0.4

0.4

0.4

20

0.3

I

0.2

0.4

0.4

0.4

0.4

0.3

0.1

0.1

Cs

0.09

3

3

0.8

0.6

0.06

0.7

0.2

Np

0.1

0.04

0.04

0.04

0.04

0.1

0.02

0.3

Pu

0.03

0.02

0.02

0.02

0.02

0.06

0.01

0.03

Am

0.1

0.04

0.04

0.04

0.04

0.1

0.005

0.000 1

Pb

0.03

0.04

0.04

0.06

0.1

0.06

0.07

0.08

Ra

0.09

0.03

0.03

0.04

0.04

0.04

0.04

0.000 7Th

0.009

0.000 10.000 10.000 40.000 4

0.009

0.04

0.001

U

0.009

0.000 10.000 10.000 50.000 5

0.009

0.02

0.007

C.

Transfer to freshwater organisms

89. Radionuclides can enter water bodies as a result of discharges to the aquatic environment (e.g. directly from anuclear facility), by deposition of airborne radioactive material onto the water surface and by run-off of material

deposited onto soil. For a point source of emission into aswiftly flowing stream, the flow rate of the stream can bedivided by the flow rate of the effluent discharge to obtain
the dilution factor. A certain mixing distance must be
assumed, which could vary from a few tens of metres for asmall stream to a few kilometres for a large river. Beyond theANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

mixing distance, a uniform concentration of the radionuclidein water can be assumed. Suspended material may be deposited as sediment. The deposited material may become lockedin the sediments and, over time, migrate to deeper sediments
or be redissolved by physical and biological processes andre-enter the water column. Dissolved or finely suspended
material may be transported over large distances, being progressively diluted by water from other streams and rivers,
eventually reaching the oceans.
90. The movement of radionuclides in rivers is often model­
led using the diffusion–transport equation and the behaviourof radionuclides in the “water column–river bed sediment”
system is often assessed using compartment ­models [M23].
At present, although the structures of the models have notbeen subjected to significant revisions, the scope of the transfers modelled (physical, chemical and biological) and of theassociated radionuclide specific parameters has been considerably enlarged. For instance, the previous state-of-the-art
publication of the IAEA, “Handbook of parameter values forthe prediction of radionuclide transfer in temperate environments” [I16], listed solely values of water–­sediment partition
coefficients and concentration factors for edible portions offish. The most recent version also incorporated equations andparameters for representing transfer by wash-off from watersheds of deposited radionuclides, interaction between liquidand solid phases, migration to and from sediments, and­transfers to freshwater biota [I14].
91. The mixing of radionuclides discharged into a lake orpond is much slower than is the case for rivers. As a first239

approximation, a uniform radionuclide concentration throughout the pond could be assumed, with a dilution factor equal tothe pond outflow rate divided by the effluent input rate. In alarge lake or coastal environment, a uniform concentration
would never be reached. Plume models have been developed
for lake-shore environments analogous to atmospheric transport models. The lake-shore environment is often complicated by thermal layering within the water column, which
impedes vertical mixing. Moreover, removal of material fromthe water column via sedimentation is an important longterm process which results in an approximately exponential
decline with time of the radionuclide concentrations present
in the water column.
92. Sedimentation and attachment to suspended particulates
are the main processes influencing the residence times ofradionuclides in freshwater. Fractions of dissolved and ofparticle-bound radionuclides are usually determined by the
distribution coefficient, Kd, which is defined as the ratio of theradionuclide concentration in water and the concentration of
the radionuclide attached to particulate matter, under equilibrium conditions. Values of Kd are element-dependent. Low Kdvalues and concentrations of suspended matter indicate highdissolved fractions, whereas high Kd values and suspended
load values indicate a considerable sorption of radionuclides
by particles and favour sedimentation. Once deposited, radionuclides may migrate down within the sediment or may
become involved in resuspension processes. These processes
may create additional sources or sinks with potential impact
on the long-term behaviour. The distribution coefficients forvarious elements in freshwater are given in table 8.

Table 8. Distribution coefficients Kd in freshwater ecosystems [I14]
Element

Kd (m3/kg)
Geometric mean

Geometric standard deviation

Be

42

3.6

Mn

130

12

Co

43

9.5

Sr

0.18

4.6

Ru

32

1.9

Ag

85

2.3

Sb

5

3.8

I

4.4

14

Cs

8.5

6.7

Ba

2

3.6

Ce

220

2.8

Th

180

21

Ra

7.4

3.1

Pu

240

6.6

Am

850

3.7

240

UNSCEAR 2008 REPORT: VOLUME II

93. Aquatic organisms may be directly irradiated byradio­nuclides present in their habitats (e.g. water, sediment). They may also take up radionuclides from water
and/or the food chain and incorporate them into their­tissues. External irradiation of most aquatic organisms,with the exception of burrowing invertebrates and benthic
organisms, is limited by the shielding provided by the­surrounding water or sediment.

that in water expressed in units of Bq/L, under equilibrium
conditions) for 137Cs ranging from 500 to 9,500 L/kg for
freshwater fish, compared to values of 3 to 25 L/kg formarine fish. The lower values for marine fish were thought tobe as a result of the competition for uptake from potassium
and other cations. Freshwater amphibians can also showhigh values of CR (1,000 to 8,000 L/kg) in the aqueous
environment.

94. Considerable attention has been focused on fish because
they are at a higher trophic level in aquatic food chains andserve as food for humans and predators. ­Polikarpov [P2] hasgiven concentration ratios, CR, (CR here is the ratio of theactivity concentration in fish expressed in units of Bq/kg and

95. Table 9 gives values of CR for 137Cs in fish in Canadianlakes in the Northwest Territories [L5] and for the upper
Great Lakes [T15]. High trophic level fish such as trout,pike and cisco show an especially high accumulation ofradiocaesium.

Table 9.

Concentration ratios for 137Cs in freshwater fish
Species

Concentration ratio (L/kg)
NWT Lakes [L5]

BurbotGreat Lakes [T15]800

Lake whitefish

400–1 000Round whitefish

1 000–1 800

Sucker700

1 500–2 500

Chub

1 900

Alewife

1 800–2 300

Bullhead

2 300

Cisco

1 600–5 000

Pike

2 500–5 500

Lake trout

3 000–6 000

6 100

96. Swanson [S20] has summarized concentration ratios for water to fish tissues for the naturally occurring radionuclides ofuranium, 226Ra, 210Pb, and 228Th (table 10).
Table 10.

Concentration ratios for natural radionuclides in freshwater fish [S20]

Element/
radionuclide

Concentration ratio (L/kg)
Bone

Flesh

Liver

Kidney

Gonad

Gut

U

20–8000.1–25<0.04–0.5

0.1–0.5

0.01–0.35

0.05–0.5Ra

35–1 800

1–60

1–45

3–30

5–115

7–45

Pb

100–2 500

4–100

3–420

6–780

10–150

11–206Th

15–160

4–32

4–36

5–46

13–50

23–50

226

210

228

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

D.

Transfer of radionuclides to marine organisms

where A is the activity of the radionuclide discharged perunit time to a specific part of the sea (Bq/a), V is the­volume of this part (m³), τ is the mean residence time (a),lr is the radioactive decay constant (a-1), Kd is the distribution coefficient (m³/kg), and S is the concentration ofsuspended particles (kg/m). The steady-state activity
concentration of the ­radionuclide in ­suspended particles,
Cs (Bq/kg), is then:

97. The main processes that modify the activity concentrations of radionuclides in marine water are (a) dilution due toconvective and dispersive mixing during transport, driven by
local, regional and global currents, (b) sedimentation after
attachment to suspended particles and (c) radioactive decay.
98. For a given continuous discharge rate into a specific section of the marine system, the steady-state concentration of adissolved radionuclide in water, Cw (Bq/m3), can be calculated
according to:

Cw =



A
V ⋅ (τ

−1

1+ λr ) 1 + K d ⋅ S
⋅

241



Cs =

A
V ⋅ (τ

−1

Kd+ λr ) 1 + K d ⋅ S⋅(3)The distribution coefficients for a number of elements inmarine waters are summarized in table 11.

(2)

Table 11. Distribution coefficients Kd for open ocean and ocean margins [I20]
Element

Kd (m3/kg)
Open ocean

Ocean margins

H

0.001

0.001

Cl

0.001

0.000 3

Sr

0.2

0.008

Tc

0.1

0.1

I

0.2

0.07

Cs

2

4

Pb

1 × 104

1 × 102

Ra

4

2

Th

5 × 103

3 × 103
1

U

0.2

Np

1 × 102

1Pu

2 × 103

1 × 102Am

2 × 103

2 × 103

99. A value of 3 years was given in reference [U3] for themean residence time, t, in a specified part of the marine system,
for all radionuclides in coastal waters with the exception of
239
Pu, for which a value of 3.5 years was assumed. These values
took account of radionuclide losses from water to sediment.

Table 12.

From simulations of the transport of radionuclides discharged
from the reprocessing plants at Sellafield and La Hague throughthe North Atlantic and its marginal seas, the mean residence
times given in table 12 were estimated using the North ­Atlantic–
Arctic Ocean Sea Ice Model (NAOSIM) [I21].

Residence times in different parts of the North Atlantic according to the NAOSIM modelPart of ocean

Volume (km³)

Mean residence time (a)North Sea

41 0002.5 ± 0.36

Norwegian Sea

59 0000.37 ± 0.11

Barents Sea

220 000

2.4 ± 0.24

Kara Sea

38 0004.5 ± 1.2

Central Nordic Seas

44 0000.52 ± 0.18

242

UNSCEAR 2008 REPORT: VOLUME II

100. As for freshwater aquatic biota, activity concentrations of radionuclides in marine biota can be estimated using
a concentration ratio approach. Concentration ratios for various elements in marine biota are compiled in table 13. For
Table 13.

Concentration ratios for marine biota [I20]
Element

Concentration factors (L/kg fresh weight)
Fish

Macroalgae

Crustaceans

H

1

1

1

Cl

0.06

0.05

0.06

Sr

3

10

10

Tc

80

30 000

1 000

I

9

10 000

100

Cs

100

50

30

Np

1

50

100

Pu

100

4 000

200

Am

100

8 000

400

Pb

200

1 000

9 000

Ra

100

100

100

Th

600

200

1 000

U

1

100

10

E.
1.

most elements, these data are based on concentrations inmuscle (fish) and soft tissue (crustaceans). For the boneseeking elements such as strontium, however, the entries intable 13 are based on whole body concentrations.

Evaluating doses to biota

Fraction of radiation absorbed by organism

101. Radionuclides distributed in the environment lead toexternal exposure of an organism living in or close to a
medium that contains radionuclides. The external exposureof biota is the result of complex and non-linear interactionsof various factors:– The geometrical relation between the source of theradiation and the target;– The activity levels of the radionuclides in theenvironment;– The materials in the environment and their shielding
properties;– The radionuclide-specific decay properties characterized by the radiation type, the energies emitted
and their emission probabilities; and– The habitat and size of the organism.
102. The geometric relationship between the radiation source
and the exposed organism is an important factor in relation to
the absorbed dose rate incurred. The intensity of the radiation
field around a source decreases with distance and is influenced
by the material between the radiation source and the target.
The number of possible source target configurations is infinite;
therefore, a number of limited and representative situations
need to be selected for detailed consideration.

103. The exposure due to radionuclides incorporated into
the organism is determined by the activity concentrations in
the organism, the size of the organism, and the type and theenergy of the emitted radiation. A key quantity for estimating internal doses is the absorbed fraction of energy, f(E),which is defined as the fraction of energy emitted by a radiation source that is absorbed within the target tissue, organ ororganism. In the simplest case, the organism is assumed to
be in an infinite homogeneous medium and to have a uniform activity concentration throughout its body. The densities of the medium and the organism’s body are assumed tobe identical. Under these conditions, both internal (Dint) andexternal (Dext) dose conversion coefficients (DCCs; the DCC
is defined as either the absorbed dose or the absorbed doserate, according to the circumstances, per unit activity concentration of the relevant radionuclide in the organism or
medium) for monoenergetic radiation can be expressed as afunction of the absorbed fraction [N1, V2]:

Dint = E ⋅φ ( E )and  Dext = E ⋅(1 − φ( E ))(4)104. Absorbed fractions for photon and electron sources
uniformly distributed in soft-tissue spherical bodies
immersed in an infinite water medium have been systematically calculated by Monte Carlo simulation [U17]. The calculations covered a particle energy range of 10 keV to
5 MeV, a range for the mass of the body from 10−6 to 103 kg,
and shapes from spheres to ellipsoids with varying degrees
of non-sphericity. Figures III and IV show, respectively, theresults for electrons and photons.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

Figure III. Absorbed fraction, φ(E), for electrons of different
energy uniformly distributed in spheres of different mass ina water medium

10-1

105. For electron energies below 100 keV, the absorbed
fraction is close to unity, even for very small organisms. The
mean free path of electrons in living tissue increases from
160 µm for 100 keV electrons to 5 mm for 1 MeV electrons.
Thus, even above 100 keV, the absorbed fraction is close tounity if the diameter of the target is much greater than therange of the electron. Only for very small targets and highenergies does the absorbed fraction become considerably
smaller than 0.5.
106. The mean free path of photons is considerably longer
than that of electrons. The absorbed fractions cover a range
from nearly unity for low photon energies and large organisms to less than 0.0001 for small organisms and high photon
energies. Absorption is a non-linear function of target sizeand energy. The main processes causing absorption of photon energy are the Compton effect, the photoelectric effectand pair production; their contributions to absorption dependon the energy of the emitted photons. As a result, theabsorbed fraction of photons in the energy range from 20 to
100 keV decreases by a factor of 10–15 for small organisms,
but is relatively constant for photons with energies between
100 keV and 1 MeV. Beyond energies of 1 MeV, the absorbed
fraction decreases steeply with energy.

(g)

106
105
104
103
102
101
100

SS

10-2
10-1
E (Me

100

V)

10-1
10-2

MA

Φ(E)

100

243

10-3

Figure IV. Absorbed fraction, φ(E), for photons of different
energy uniformly distributed in spheres of different mass ina water medium

100

107. The range of alpha particles in living tissue is very
short, increasing from 16–130 µm within the energy range of
3–10 MeV. Therefore, with the exception of bacteria, it isassumed for all organisms that all the energy emitted isabsorbed. Since the dimensions of bacteria are well below
the range of alpha particles, the absorbed fraction is assumed
to be zero.
108. Re-scaling factors have been derived from the computed absorbed fractions for spheres to determine the dosecoefficients for ellipsoidal shaped organisms, using the massand proportions of the organism. The relationship between there-scaling factors and the non-sphericity parameter of theorganism’s body are described analytically in reference [U17].
Owing to the short range of alpha particles, the internal exposure due to incorporated alpha emitters is independent of the
shape of the organism.

10-1

109. The approach was also applied to the calculation of
the absorbed fractions for non-aquatic animals and theirinternal exposures. With the use of the absorbed fractions forspheres and the suggested re-scaling and interpolation techniques, a set of internal DCCs has been calculated for allreference animals and plants [U17].

Φ(E)

10-2

10-3

10
105
4
10
103
2
10
101
100
10-1
10-2
10-3

6

10

g)

-4

MA
SS
(

10-2
10-1

E (Me

V)

100

110. The estimation of external exposures of terrestrial reference animals and plants is more complex than that of biota
in the aquatic environment. The intrinsically different density and composition of soil, air and organic matter cannot,
in general, be adequately taken into account by the application of analytical solutions. Dosimetric models for estimating external doses to biota in the terrestrial environment
were developed within the FASSET project [F4, T10]. A key
factor for determining external exposure is the geometric

244

UNSCEAR 2008 REPORT: VOLUME II

relationship between the radiation source and the exposedorganism. A number of limited and representative exposure
situations were selected for detailed consideration.
111. Simple three-dimensional phantoms, i.e. ellipsoids
and cylinders, were defined as model geometric equivalentsof reference organisms based on their average mass and size
characteristics. The dimensions ranged from a millimetre toa metre and the respective masses range from 0.2 g to
550 kg. The ellipsoids represented organisms such as woodlouse, earthworm, mouse, mole, snake, fox, deer and cattle.
Details of the assumed exposure conditions are given in reference [T10]. The fur and the outer layers of skin consist of
non-active tissue, and therefore shield the living organism.
112. Herbaceous vegetation, shrubs and trees were considered as reference plants. Exposure of the meristem and buds
was calculated because these organs are characterized byvery intensive cell division, which may make them highly
radiosensitive.
113. In order to take account of the distribution of radio­
nuclides in the canopy, a distinction was made between
alpha, beta and gamma radiation because of their different
ranges. For gamma radiation, the whole canopy was considered to have a homogeneous activity concentration. For
high-energy beta radiation, the irradiation of the target wasalso assumed to result from a canopy with a homogeneous
activity concentration. However, owing to the much shorter
range of alpha and low-energy beta radiation, the irradiation
resulting from external deposits on, or internal activity of,
the target organ had to be considered explicitly. Because of
the very short range of alpha particles in air, only the exposure due to the external deposits on, or internal exposure of,the target needed to be taken into account [T10].

114. The elemental composition and density of the materials involved have an important impact on the radiation transport calculation. All organisms were assumed to be composedof skeletal muscle alone with the characteristics/parameters
given in reference [I15]. The DCCs were derived using
Monte-Carlo techniques; all relevant processes of radiationtransport and interaction with matter were included. For
electrons, a thick-target bremsstrahlung model was usedinstead of an electron-transport simulation. For the calculation of DCCs for a species in the soil, a volume source withuniform activity concentration was assumed. For the calculation of DCCs for a species on the ground, a planar radiation source on top of the soil with a surface roughness of
3 mm and a volume source with a depth of 10 cm wereassumed. Calculations were made for monoenergetic gamma
energies of 50 keV, 300 keV, 662 keV, 1 MeV and 3 MeV.
Data for other energies were obtained by interpolation.

2.

Principal relationships for internal and external exposure(a)External exposure

115. Although the simulations cover only a limited numberof possible exposure conditions, they allow the relationships
between organism size, radiation energy and habitat to be
deduced. The DCC (Gy per photon per kg) increases in proportion to the photon energy as illustrated in figure V for a
volumetric source with a thickness of 0.5 m and target organisms that live at a depth of 0.25 m. Whereas the DCCs varyby a factor of 200 between photon energies of 50 keV to
3 MeV, the variation between the organisms does not exceeda factor of 2, even for low-energy photons (for high-energy
photons, the difference is a factor of only 1.5).

Figure V. Dose conversion coefficients for various soil organisms at a soil depth of 25 cm, for monoenergetic photons from a
uniformly distributed source in the upper 50 cm of soil (soil density: 1,600 kg/m³) [F4]DCC (Gy per photon/kg)

10-12

10-13

Woodlouse
Earthworm
Mouse
Mole
Snake
Rabbit
Fox

10-14

10-15
0.01

0.1

1

PHOTON SOURCE ENERGY (MeV)10

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

116. The DCC (Gy per photon per kg) for an earthworm as
a function of soil depth for monoenergetic photons is shownin figure VI. The upper 50 cm of the soil was assumed tohave a homogeneous activity concentration. The maximum

245

DCC was found to be at a depth of 25 cm and the lowest, at
depths of 0 cm and 50 cm. The maximum DCC is a factor of
2 higher than the lowest.

Figure VI. Dose conversion coefficients for an earthworm at various depths in soil, for monoenergetic photons from a
uniformly distributed source in the upper 50 cm of the soil (soil density: 1,600 kg/m3) [F4]DCC (Gy per photon/kg)

10 -12

10 -13Depth = 0.00 m
Depth = 0.05 m
Depth = 0.25 m
Depth = 0.50 m

10 -1410 -15
0.01

10

1

0.1

PHOTON SOURCE ENERGY (MeV)

117. The DCC at a depth of 5 cm is only about 20% lower
than the maximum. This is because of the relatively shortmean free path of photons in soil, which is about 0.2, 2 and10 cm for photon energies of 20 keV, 100 keV and 3 MeV,
respectively. Thus, an organism in soil would be irradiatedby photons originating within a surrounding shell of, at
most, 10 cm radius.
118. The DCCs (Gy per photon per m2) for different reference organisms for a planar source on the soil surface are

given in figure VII. The DCCs decrease as the photon energy
increases from 10 to 100 keV by a factor of about 5 for small
animals and 2 for large animals. Above 100 keV, the DCCs
gradually increase by approximately two orders of magnitude; the DCCs for small animals are greater than those forlarge animals owing to the more effective self-shielding inlarge organisms. Such differences are more pronounced at
low energies; for example, the difference between the mouseand the cow is a factor of about 6 for 50 keV photons,
whereas it is a factor of 3 for 3 MeV photons.

Figure VII. Dose conversion coefficients as a function of the source energy for various reference organisms for a planarsource on top of the soil [F4]-142DCC (Gy per photon/m )

10

10

-15

10

-16

10

-17

Cow
Roe deer
Wolf
Rabbit
Mole
Mouse

0.01

0.1

1

PHOTON SOURCE ENERGY (MeV)1010-14(a) Mouse
10-15

UNSCEAR 2008 REPORT: VOLUME II

119. The DCCs for different animals as a function of thedepth of a planar source in the soil are summarized in figure VIII. The results show that the DCCs for low-energy

DCC (Gy per photon/m2)

246

10-16

photons
for animals living on soil are low. Relatively shal10-17
low depths of soil over the planar source suffice to attenuate
the photons
completely.
10-18
Source depth:
0 g/cm2
1 g/cm2

10-19

10 g/cm2and depth of a planar source in the soil for (a) the
Figure VIII. Dose conversion coefficients as a function of the source energy
10-20
0.01
0.1
10
1
mouse and (b) the cow living on the soil
PHOTONfor soil densities of
The source depth quantifies the amount of soil by which the photon source is covered (e.g. the source
depthSOURCEof 10ENERGY
g/cm2 (MeV)
1.0 and 1.6 g/cm2 are equivalent to a depth of the source in the soil of 10 and 6.25 cm, respectively) [F4]
10-14

10-14

(a) Mouse(b) Cow
10-15
DCC (Gy per photon/m2)

DCC (Gy per photon/m2)

10-15
10-16
10-17
10-18

Source depth:
0 g/cm2

1 g/cm2

10-19

10-16
10-17
10-18

Source depth:

10-19

1 g/cm2

0 g/cm2

10 g/cm2
10-20

0.01

0.1

1

10 g/cm2
10-20

10

0.01

PHOTON SOURCE ENERGY (MeV)

10-14

DCC (Gy per photon/m2)

120. The(b)data
indicate that the relationship between the
Cow
DCCs,
-15 the size and habitat of the organism and the energy
10and type of the radiation is complex. Nevertheless, these
data10provide
an appropriate basis for deriving data, either by-16
interpolation or by extrapolation, for other exposure conditions
10-17that were not explicitly considered. They were used toderive radionuclide-specific DCCs (µGy/h per Bq/kg) forinternal
and external exposure of a numberSourceof reference
10-18
depth:
organisms, taking into account the type of radiation
as well
0 g/cm2
as theenergyandintensityoftheemission,asspecifiedby
1 g/cm2
10-19
the ICRP [I13]. Table 14 summarizes the DCCs10(µGy/h
g/cm2 perBq/kg)
for external exposure. The data are provided accord10-20
ing to the 0.01
habitat of organisms
considered.
0.1
1 Animals living
10
in soil were assumed to PHOTON
be at a SOURCE
depth ENERGY
of 25 cm
in
a
soil
layer
(MeV)
that is homogeneously contaminated by radionuclides to adepth of 50 cm. Above ground organisms were assumed tobe irradiated by a source homogeneously distributed in thesoil layer to a depth of 10 cm. For the terrestrial organisms,
only the contribution of photons was included, whereas foraquatic organisms, exposure due to electrons (including
bremsstrahlung) was also implicitly taken into account.
This has the effect of causing the DCCs for 3H, 90Sr and

0.1

1

10

PHOTON SOURCE ENERGY (MeV)

Cs to appear to be inconsistent: the DCCs for 3H and 135Cs
for terrestrial organisms are zero, whereas the values foraquatic organisms are very small. Aquatic organisms are in
direct contact with the contaminated medium, whereas electrons emitted from soil are attenuated by the surface roughness of the soil, the air and the fur of terrestrial organisms.
So, this apparent inconsistency is of no significant practicalconsequence.
135

(b)

Internal exposure121. The DCCs (µGy/h per Bq/kg) for internal exposure
are provided in table 15 [U17]. The values are given interms of weighted absorbed dose rate per unit activity concentration in the organism, assuming homogeneous distribution of the radionuclides. The DCCs have been weighted
to take account of the different RBEs of the different qualities of radiation; a factor of 10 to reflect the RBE has beenused for alpha radiation and a factor 1 to reflect that for
gamma and beta radiation including that from tritium (seethe next subsection).

1.5 × 10‑100

3.5 × 10‑6

1.9 × 10‑4

8.3 × 10‑40

3.0 × 10‑4

6.0 × 10‑7

9.0 × 10‑4

1.4 × 10‑7

1.2 × 10‑7

7.6 × 10‑6

8.5 × 10‑8

1.6 × 10‑7

6.1 × 10‑6

Sr

Tc

I

I

Cs

Cs

Cs

Pb

Ra

Th

U

Np

Pu

Pu

Am

In soil a

5.5 × 10‑6

1.3 × 10‑7

7.2 × 10‑8

7.0 × 10‑6

1.0 × 10‑7

1.2 × 10‑7

8.5 × 10‑4

5.2 × 10‑7

2.8 × 10‑40

7.8 × 10‑4

1.8 × 10‑4

3.0 × 10‑60

1.2 × 10‑100Rat

9.2 × 10‑7

1.4 × 10‑8

9.5 × 10‑9

1.4 × 10‑6

1.0 × 10‑8

1.3 × 10‑8

1.8 × 10‑4

7.7 × 10‑8

5.6 × 10‑50

1.6 × 10‑4

3.7 × 10‑5

4.0 × 10‑70

4.6 × 10‑12

0

Deer

2.4 × 10‑6

5.4 × 10‑8

3.0 × 10‑8

3.3 × 10‑6

4.3 × 10‑8

3.9 × 10‑8

3.2 × 10‑4

2.6 × 10‑7

1.1 × 10‑40

2.9 × 10‑4

7.1 × 10‑5

1.1 × 10‑60

1.5 × 10‑11

0

Duck

2.6 × 10‑6

6.0 × 10‑8

3.3 × 10‑8

3.6 × 10‑6

4.8 × 10‑8

4.3 × 10‑8

3.4 × 10‑4

2.8 × 10‑7

1.1 × 10‑40

3.2 × 10‑4

7.7 × 10‑5

1.1 × 10‑60

1.6 × 10‑11

0

Frog
0

Bee

2.6 × 10‑6

6.2 × 10‑8

3.3 × 10‑8

3.6 × 10‑6

5.0 × 10‑8

4.4 × 10‑8

3.5 × 10‑4

2.9 × 10‑7

1.2 × 10‑40

3.2 × 10‑4

7.8 × 10‑5

1.1 × 10‑60

1.6 × 10‑11

On soil b

2.6 × 10‑6

6.1 × 10‑8

3.3 × 10‑8

3.6 × 10‑6

4.9 × 10‑8

4.3 × 10‑8

3.4 × 10‑4

2.9 × 10‑7

1.1 × 10‑40

3.2 × 10‑4

7.8 × 10‑5

1.1 × 10‑60

1.6 × 10‑11

0

Grass

2.6 × 10‑6

6.1 × 10‑8

3.3 × 10‑8

3.6 × 10‑6

4.9 × 10‑8

4.3 × 10‑8

3.4 × 10‑4

2.9 × 10‑7

1.1 × 10‑40

3.2 × 10‑4

7.8 × 10‑5

1.1 × 10‑60

1.6 × 10‑11

0

Pine
tree

Absorbed dose rates per activity concentration (µGy/h per Bq/kg)

a Organisms are assumed to live at 25 cm depth of a soil with radionuclides distributed homogeneously to a depth of 50 cm.
b Organisms are assumed to live on a soil layer with radionuclides distributed homogenously to a depth of 10 cm.
c Organisms are assumed to be immersed in water.

241

240

239

237

238

232

226

210

137

135

134

131

129

99

90

3

0

Earthworm

H

Radionuclide

Table 14. Dose conversion coefficients for external exposure of reference organisms [E10, T10, U17]

1.1 × 10‑5

1.4 × 10‑7

8.2 × 10‑8

1.2 × 10‑5

1.0 × 10‑7

1.5 × 10‑7

9.1 × 10‑4

2.7 × 10‑6

2.7 × 10‑4

4.5 × 10‑8

7.6 × 10‑4

1.9 × 10‑4

7.7 × 10‑6

1.2 × 10‑7

2.2 × 10‑5

7.9 × 10‑12Pelagic
fish

1.2 × 10‑5

1.9 × 10‑7

1.0 × 10‑7

1.3 × 10‑5

1.3 × 10‑7

1.8 × 10‑7

9.6 × 10‑4

4.7 × 10‑6

2.9 × 10‑4

4.5 × 10‑8

8.0 × 10‑4

2.0 × 10‑4

9.2 × 10‑6

1.2 × 10‑7

4.9 × 10‑5

7.8 × 10‑12

Benthic
fish

Brown
seaweed

1.7 × 10‑5

6.8 × 10‑7

3.0 × 10‑7

1.8 × 10‑5

5.1 × 10‑7

5.0 × 10‑7

1.1 × 10‑3

4.7 × 10‑5

3.4 × 10‑4

4.3 × 10‑7

8.9 × 10‑4

2.3 × 10‑4

1.3 × 10‑5

1.5 × 10‑6

2.0 × 10‑4

8.2 × 10‑11

In water c

1.1 × 10‑5

1.6 × 10‑7

8.7 × 10‑8

1.3 × 10‑5

1.1 × 10‑7

1.6 × 10‑7

9.1 × 10‑4

3.0 × 10‑6

2.8 × 10‑4

5.2 × 10‑8

7.6 × 10‑4

1.9 × 10‑4

7.9 × 10‑6

1.4 × 10‑7

2.2 × 10‑5

1.0 × 10‑11

Crab

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA
247

1.6 × 10‑4

6.2 × 10‑4

5.8 × 10‑5

4.2 × 10‑4

1.4 × 10‑4

1.9 × 10‑4

3.9 × 10‑5

1.8 × 10‑4

2.4 × 10‑4

1.3 × 10‑1

5.3 × 10‑4

5.8 × 10‑5

3.8 × 10‑5

1.1 × 10‑4

1.1 × 10‑4

3.9 × 10‑5

1.5 × 10‑4

2.3 × 10‑4

1.3 × 10‑1

Sr

Tc

I

I

Cs

Cs

Cs

Pb

Ra

Rat

1.5 × 10‑4

Earthworm

3.0 × 10‑2
3.0 × 10‑2
3.2 × 10‑2

Pu

Pu

Am

a Assumes a homogeneous activity distribution in the organism.
b Assumes an RBE of 10 for alpha and 1 for beta.

241

240

239

237

238

232

2.7 × 10‑2

1.3 × 10‑1

2.3 × 10‑4

1.4 × 10‑4

3.9 × 10‑5

1.1 × 10‑4

1.1 × 10‑4

3.8 × 10‑5

5.8 × 10‑5

5.1 × 10‑4Np

1.4 × 10‑1

2.2 × 10‑4

1.4 × 10‑4

3.8 × 10‑5

9.9 × 10‑5

1.1 × 10‑4

3.7 × 10‑5

5.7 × 10‑5

4.4 × 10‑4

2.4 × 10‑2

1.3 × 10‑1

2.4 × 10‑4

1.6 × 10‑4

3.9 × 10‑5

1.4 × 10‑4

1.2 × 10‑4

3.9 × 10‑5

5.8 × 10‑5

5.9 × 10‑4Grass

1.5 × 10‑4

3.3 × 10‑6

1.5 × 10‑4BeeU

1.4 × 10‑1

2.5 × 10‑4

2.0 × 10‑4

3.9 × 10‑5

2.5 × 10‑4

1.5 × 10‑4

4.4 × 10‑5

5.8 × 10‑5

6.3 × 10‑4

1.6 × 10‑4

Frog

2.3 × 10‑2

1.4 × 10‑1

2.5 × 10‑4

3.7 × 10‑4

3.9 × 10‑5

7.1 × 10‑4

2.6 × 10‑4

5.0 × 10‑5

5.8 × 10‑5

6.5 × 10‑4

1.6 × 10‑4

Duck

Th

226

210

137

135

134

131

129

99

90

1.6 × 10‑4Deer

1.4 × 10‑1

2.5 × 10‑4

3.5 × 10‑4

3.9 × 10‑5

6.5 × 10‑4

2.5 × 10‑4

5.0 × 10‑5

5.8 × 10‑5

6.5 × 10‑4

1.6 × 10‑4

Pine tree

Weighted absorbed dose rates per activity concentration (µGy/h per Bq/kg)a,b

Weighted dose conversion coefficients for internal exposure of reference organisms [T10, U20]

Cl

36

3

H

Radionuclide

Table 15.

1.4 × 10‑1

2.5 × 10‑4

1.9 × 10‑4

3.9 × 10‑5

2.3 × 10‑4

1.4 × 10‑4

4.3 × 10‑5

5.8 × 10‑5

6.3 × 10‑4

1.6 × 10‑4Pelagic
fish

1.3 × 10‑1

2.4 × 10‑4

1.8 × 10‑4

3.9 × 10‑5

1.9 × 10‑4

1.3 × 10‑4

4.2 × 10‑5

5.8 × 10‑5

6.0 × 10‑4

1.6 × 10‑4

Benthic
fish

1.4 × 10‑1

2.0 × 10‑4

1.3 × 10‑4

3.8 × 10‑5

9.7 × 10‑5

1.0 × 10‑4

3.8 × 10‑5

5.7 × 10‑5

4.5 × 10‑4

1.4 × 10‑4

Brown
seaweed

1.4 × 10‑1

2.5 × 10‑4

1.9 × 10‑4

3.9 × 10‑5

2.3 × 10‑4

1.4 × 10‑4

4.3 × 10‑5

5.8 × 10‑5

6.3 × 10‑4

1.6 × 10‑4

Crab

248
UNSCEAR 2008 REPORT: VOLUME IIANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

(c)Relative biological effectiveness122. The effects of radiation exposure on biota depend not
only on the absorbed dose, but also on the type or quality of
the radiation. For example, alpha particles and neutrons can
produce observable damage at much lower absorbed doses
than beta or gamma radiation. Thus, the absorbed dose (ingray) is often multiplied by a factor in order to account for
the RBE of the quality of the radiation.
123. A number of authors have evaluated the data on the
RBE of different types of radiation [A1, C1, E2, F4, T7,
U4, U26]. Nominal values for the factor to reflect theRBE of alpha particles derived from these reviews are249

summarized in table 16. The experimental values of RBE
are specific to the endpoint studied, the biological, environmental and exposure conditions (e.g. reference radiation,dose rate, and dose) amongst other factors. Thus, as noted
in a FASSET report [F4], it is difficult to develop a generally valid factor to reflect the RBE for different radiation
qualities for use in an environmental risk assessment. The
ACRP [A1] and FASSET [F4] have therefore proposed
ranges of values for general application. Both selected afactor of 10 to reflect the RBE for alpha particles, the
ACRP, citing references [K2, T7, U4], referring to it as a
notional central value, and FASSET as a value “to illustrate” the impact of the RBE for an internally depositedalpha emitter.

Table 16. Modifying factors to reflect the RBE of alpha radiation for deterministic effects on non-human biota (relative to
low-LET radiation)
SourceNominal value

Comment[N1]

1

Built-in conservatism in dose model

[I4]

20

Numerically the same as the radiation weighting factor used in the protection of humans

[B22]

2–10

Non-stochastic effect of neutrons and heavy ions

[U4]

5

Average for deterministic effects

[T7]

10

Deterministic population-relevant endpoints

[C1]

20

Likely to be conservative for deterministic effects

[E3]

40

Includes studies with high RBE values

[E12]

<35

Based on concentrations in the whole body

[A1]

5–20 (10)

5–10 deterministic effects (cell-killing, reproductive)
10–20 cancer, chromosome abnormalities
10 nominal central value[F4]

5–50 (10)10 to illustrate the effect of the alpha RBE[K19]<7 to <35

Upper bound of estimate of RBE

124. Chambers et al. [C5] reported a review of the literature on experimentally determined RBEs for internallydeposited alpha-emitting radionuclides. The relevance ofeach experimental result in selecting a factor to reflect theRBE for alpha particles was judged on the basis of pre-­established criteria. They recommended a nominal factor of
5 to reflect the RBE for alpha particles for population-­
relevant deterministic and stochastic endpoints but, to reflect
the limitations in the experimental data, they also suggested
uncertainty ranges of 1–10 and 1–20 for population-relevant
deterministic and stochastic endpoints, respectively. The

data developed by Chambers et al. [C5] after application of
their evaluation criteria are summarized in figure IX. Threeevaluation criteria were used in reference [C5]. Criterion 1
required the dosimetric conditions to be sufficiently welldefined and not peculiar to the source of radiation. Criterion 2 required the dose–effect relationships to be sufficiently well known so that the results from the dose rates
used experimentally can be applied to effects that may occur
with environmental dose rates. Criterion 3 required theexperimental uncertainties to be discussed by the authors of
the original studies.

250

UNSCEAR 2008 REPORT: VOLUME II

Figure IX. Application of the criteria to the distribution of RBEs (all endpoints) [C5]80
RBEs eliminated by criterion #3 only

70

NUMBER OF RBE VALUESRBEs eliminated by criterion #2 only
60

RBEs eliminated by criterion #1 only
RBEs remaining after all criteria applied

50
40
30
20
10
0

<5

5-10

11–20

21–40

41–80

81–160>160

RBE RANGE

125. Knowles [K19] reported on experimental studies ongroups of zebra fish that were exposed from an early age todifferent dose rates of gamma and alpha radiation (the latter
was from 210Po). Among the gamma-irradiated fish, only
those in the highest dose-rate group (7,400 mGy/h) showedradiation-related damage. No groups of alpha-irradiated fish
showed evidence of radiation-induced reduction in egg production even though autoradiographs showed concentrationsof 210Po in the testes and ovaries. Since the highest alphadose rate (214 mGy/h) showed no effect, comparison withthe gamma dose rate of 7,400 mGy/h, which caused egg production to cease, resulted in only upper limits to the RBE.
These were calculated to be in the range of <7 to <20 basedon ovary concentrations and <35 based on whole body concentrations. The authors suggested that the RBEs derived
from their work provide the best available (upper bound)estimates for a population-relevant effect for fish.
126. The ACRP [A1] considered tritium beta radiation
because the low velocity of the beta particles (maximum
energy = 18.6 keV) results in a relatively high LET over ashort path length. It has an LET very similar to that of 70 keV
photons, which are representative of the X‑rays used inradio­biological research and in diagnostic medicine [M6]. In
their review of the effects of tritiated water (HTO) in mammals and fish, Environment Canada in their Priority Substances List (PSL2) [E3] listed tritium RBE values ranging
from 1.7 to 3.8, with gamma rays from 60Co or 137Cs being
used as the reference radiation. Based on this, they recommended a factor of 3 to reflect the RBE of beta radiationfrom tritium. Research conducted at Atomic Energy of Canada Ltd. on breast cancers in female rats [G1] and on myeloid leukaemia in male mice indicated an RBE value of 1.2
for tritium, with X‑rays being used as the reference

radiation. The difference between these values is largely the
result of the choice of reference radiation. Sinclair [S8] has
shown that, at low doses, X‑rays are about twice as effective
as gamma rays in producing damage. Hence, the radiationfrom tritium has an effectiveness for biological damage inthe higher part of the range expected for the gamma and
X‑ray photon energies likely to be experienced in the environment. Citing Straume and Carsten [S9] amongst others,
the ACRP concluded that for the dosimetry of non-humanspecies, where the endpoints are usually deterministic innature, a reasonable average factor to reflect the RBE of beta
particles may be 2 with a range of 1–3, depending on theendpoint being assessed [A1].
127. A number of studies suggested that beta radiation
with energies below 10 keV has a higher RBE than electrons
with energies above 10 keV [M10, S9]. Straume and Carsten[S9] reviewed 33 studies of the RBE of tritium beta particles
and found arithmetic means of 1.8 based on X‑rays as thereference radiation, and 2.3 with 137Cs or 60Co gamma rays as
the reference radiation. Most of these studies related todeterministic effects. Moiseenko et al. [M10] considered an
appropriate factor to reflect the RBE of beta particles fromtritium (mean beta energy <10 keV) to be between 2 and 3.
The UK Health Protection Agency (HPA) [H21] reviewed
the RBE studies on tritium beta particles along with a wide
variety of experimental studies using X‑rays and gamma
rays as reference radiations and noted that the RBEs generally ranged from 1 to 2 when compared to orthovoltage
X‑rays and from 2 to 3 when compared to gamma rays
[H21]. Little and Lambert [L9] also reviewed the experimental studies of cancer induction, chromosomal aberration, cell
death and various other endpoints and arrived at similar­conclusions for the RBE of tritium in water.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

128. In order to illustrate the effect of the radiation quality ofemissions from internally deposited radionuclides, the ­FASSET
programme recommended the use of a factor of 10 to reflect
the RBE of alpha radiation, 3 for low-energy beta radia­tion(E < 10 keV), and 1 for both beta radiation with energies
greater than 10 keV and for gamma radiation [F4, L4].

results are particularly sensitive to the choice of factor,
especially for radiation from the actinides and tritium. The
contributions of weighted internal doses to the total normalized doses are close to or above 90%, which indicates thatinternal exposure is the dominant pathway.
131. These annual doses took account of external exposure
as well as internal exposure via inhalation and ingestion.
They are compared with the weighted absorbed doses to biota
in table 19. The ranges given in the table for biota reflect thevariations between the different reference organisms considered. This comparison has however some inherent limitations. The values for humans are expressed in terms of annual
effective dose, whereas the values for biota are in terms ofweighted absorbed dose and were estimated assuming ahomogeneous distribution of the radionuclide in the organism. Furthermore, the annual effective doses per unit deposition to humans were based on a radiation weighting factor of
20 for alpha particles, whereas the weighted absorbed doses
to biota were based on a factor of 10 to reflect the RBE foralpha particles. Further still, the values for humans reflectlargely the transfer of radionuclides through agricultural ecosystems, whereas the values for biota are more typical of thetransfer in forests and semi-natural ecosystems.

129. The Committee, in its UNSCEAR 1996 Report [U4],recommended a nominal factor of 5 to reflect the RBE forinternally deposited alpha emitters. The Committee now­recommends a nominal (generic) factor of 10 to reflect theRBE for internally deposited alpha radiation. For beta andgamma radiation, the Committee recommends a nominal(generic) factor of 1 to reflect the RBE. However, it should beunderstood that the most appropriate factor to reflect the RBE
for low-energy (<10 keV) beta radiation remains an open
question and ought to be the subject of future research. These­recommended values to reflect the RBE are intended to apply
on a generic basis across all organisms and endpoints. Where
appropriate scientific information specific to a particularorganism and endpoint exists, such information is preferred.
(d)

251

Dose rates for internal exposure132. Despite these differences, the estimated normalized
effective doses to humans and the weighted absorbed doses tobiota are about the same order of magnitude, except in thecases of 129I and 131I. These exceptions are probably due to thespecial importance of radiation exposure of the human thyroid in evaluating effective dose, which has no counterpart in
the dosimetry for biota. Thus, apart from these exceptions,the comparison indicates that for similar levels of radio­
nuclides in the environment, the effective doses to humans
and the weighted absorbed doses to biota are comparable.

130. The dose from unit exposure of the selected reference
organisms is estimated from the weighted absorbed dose
rate due to external exposure arising from deposits in the
ground and that due to internal exposure. Weighted absorbed
dose rates to the reference organisms normalized for continuous exposure to 1 Bq/m3 in air for each radionuclide are
given in table 17. These weighted absorbed dose rates were
calculated assuming the factors to reflect the RBE recommended by the Committee. Table 18 summarizes the ratiosof weighted to non-weighted normalized total doses. The

Table 17. Normalized weighted absorbed dose rates per unit activity concentration to various biota from internal exposureRadionuclide

Weighted dose rate per unit activity concentration (µGy/h per Bq/m3)
Earthworm

Rat

H

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19

1.7 × 10‑19Cl

5.6 × 10

3.3 × 10

3.3 × 10

3.3 × 10

3.3 × 10

9.3 × 10

5.4 × 10

5.5 × 10‑14

Sr

‑15

6.1 × 10

1.2 × 10

1.3 × 10

7.3 × 10

7.5 × 10

5.1 × 10

1.8 × 10

4.3 × 10‑13

Tc

4.4 × 10‑15

4.4 × 10

4.4 × 10

4.4 × 10

4.4 × 10

4.4 × 10‑13

2.4 × 10

4.8 × 10‑15

129I

2.3 × 10‑14

4.8 × 10‑14

4.9 × 10‑14

4.5 × 10‑14

4.0 × 10‑14

2.9 × 10‑14

1.7 × 10‑14

2.1 × 10‑14I

4.6 × 10‑16

1.3 × 10‑15

1.8 × 10‑15

4.2 × 10‑16

3.4 × 10‑16

1.9 × 10‑16

1.6 × 10‑15

2.8 × 10‑15Cs

1.7 × 10

2.7 × 10

4.5 × 10

9.7 × 10

8.1 × 10

6.6 × 10

8.7 × 10

1.2 × 10‑13

Cs

8.3 × 10

2.7 × 10

2.7 × 10

7.1 × 10

5.4 × 10

5.0 × 10

6.7 × 10

1.7 × 10‑14Cs

4.7 × 10

4.4 × 10

1.1 × 10

1.9 × 102.0 × 102.0 × 10‑13

1.9 × 10

2.3 × 10‑13

3

36
90

99

131
134
135
137

‑13
‑15
‑13

‑13
‑12
‑15

‑13
‑13
‑13

Duck

‑13
‑12
‑15

‑13
‑13
‑13

Frog

‑13
‑13
‑15

‑14
‑14
‑13

Bee

‑13
‑13
‑15

‑14
‑14
‑13

Grass

‑15
‑14
‑15

‑14
‑15
‑13

Pine tree

‑13
‑13

‑14
‑14

Pb

2.9 × 10‑14

9.4 × 10‑15

9.2 × 10‑15

1.2 × 10‑14

1.2 × 10‑14

1.1 × 10‑14

1.3 × 10‑14

8.7 × 10‑16Ra

5.0 × 10‑12

2.1 × 10‑12

4.7 × 10‑13

8.9 × 10‑13

9.3 × 10‑13

3.7 × 10‑12

1.5 × 10‑11

1.3 × 10‑12Th

4.9 × 10

6.4 × 10

5.6 × 10

2.8 × 10

2.8 × 10

4.9 × 10

8.4 × 10

4.0 × 10‑13U

5.8 × 10

2.4 × 10

2.4 × 10

2.4 × 10

2.4 × 10

7.5 × 10

9.9 × 10

1.8 × 10‑11

210
226

‑15

Deer

232

238

‑13
‑12

‑15
‑12

‑15
‑12

‑14
‑12

‑14
‑12

‑13
‑12

‑13
‑13

Np

1.9 × 10

1.5 × 10

1.5 × 10

1.5 × 10

1.5 × 10

4.0 × 10

4.1 × 10

4.9 × 10‑12

239

Pu

2.1 × 10

1.7 × 10

1.7 × 10

1.7 × 10

1.7 × 10

4.4 × 10‑12

4.5 × 10

5.4 × 10‑12

240

Pu

7.2 × 10‑12

2.9 × 10‑12

2.9 × 10‑12

2.9 × 10‑12

2.9 × 10‑12

9.3 × 10‑12

3.9 × 10‑12

3.1 × 10‑12Am

8.8 × 10‑14

8.6 × 10‑14

7.6 × 10‑14

7.9 × 10‑14

8.0 × 10‑14

8.0 × 10‑14

3.7 × 10‑12

3.3 × 10‑12

237

241

‑12
‑12

‑12
‑12

‑12
‑12

‑12
‑12

‑12
‑12

‑12
‑12

‑12

252

UNSCEAR 2008 REPORT: VOLUME IITable 18.

Ratio of weighted and unweighted doses
Ratio of weighted dose/unweighted dosea

Radionuclide
Earthworm

Rat

Deer

Duck

Frog

Bee

Grass

Pine tree

H

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

3

Cl

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

Sr

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

36
90

Tc

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

129

I

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

99

I

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

Cs

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

Cs

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

Cs

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

131
134
135
137

Pb

1.0

1.0

1.0

1.0

1.0

1.0

1.0

1.0

Ra

2.0

1.0

1.1

1.2

1.1

3.3

7

2

Th

9.9

7.1

9.5

9.7

9.7

10

10

10

U

10

10

10

10

10

10

10

10

Np

9.1

8.9

9.6

9.4

9.3

9.6

9.6

9.7

Pu

10

10

10

10

10

10

10

10

210
226

232

238
237

239

Pu

10

10

10

10

10

10

10

10

Am

4.1

4.3

7.9

6.1

5.9

5.9

10

10

240
241

a Factors to reflect the RBE: alpha radiation, 10; beta and gamma radiation, 1.

Table 19.

Comparison of doses to biota and humans, normalized for unit deposition to terrestrial ecosystems
Radionuclide

Biota (range)a
Normalized weighted absorbed dose rate
(Gy a‑1 per Bq m‑2 a‑1)

Humansb
Normalized effective dose rate
(Sv a‑1 per Bq m‑2 a‑1)

Minimum

MaximumSr

6.2 × 10‑9

1.3 × 10‑6

4.7 × 10‑7Tc

4.4 × 10‑9

2.5 × 10‑7

1.8 × 10‑8129I

1.7 × 10‑8

5.0 × 10‑8

6.3 × 10‑7I

2.0 × 10‑10

2.8 × 10‑9

1.0 × 10‑7

134

Cs

6.7 × 10‑8

4.6 × 10‑7

1.3 × 10‑7

135

Cs

5.1 × 10‑9

2.8 × 10‑7

1.2 × 10‑8

137

Cs

1.1 × 10‑7

4.8 × 10‑7

1.3 × 10‑7Pb

8.9 × 10‑10

2.9 × 10‑8

2.5 × 10‑6Ra

4.8 × 10‑7

1.5 × 10‑5

1.6 × 10‑6Th

5.6 × 10‑9

8.5 × 10‑7

1.2 × 10‑6U

1.0 × 10‑6

1.8 × 10‑5

6.0 × 10‑7Np

1.5 × 10‑6

5.0 × 10‑6

4.9 × 10‑7Pu

1.7 × 10‑6

5.5 × 10‑6

6.8 × 10‑7Pu

3.0 × 10‑6

9.5 × 10‑6

6.8 × 10‑7Am

7.7 × 10‑8

3.8 × 10‑6

5.8 × 10‑7

90

99

131

210
226

232

238
237

239
240
241

a Range represents the minimum and maximum among the organisms considered.
b Calculated according to [I11].

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

3. Doses to non-human biota(a)

TFflora,r is the transfer factor from soil to flora (Bq/kg flora per
Bq/kg soil).

Calculation of doses to biota

133. In terrestrial environments, the most important sourceof radiation exposure as a consequence of discharges ofradio­nuclides to the environment is due to deposition on soil.
Radionuclides present in soil are generally a persistent radiation source for all terrestrial biota. Aquatic organisms areirradiated externally by the activity in water and, in the casesof bottom dwellers and benthic organisms, the activity insediments, and internally by incorporated radionuclides. The
dose rate, D, can be calculated according to:

D = ∑  DCCext ,r ⋅ Csoil ,water ,r + DCCint,r ⋅ Cbiota ,r 
r(5)where DCCext,r is the DCC for external exposure to radio­
nuclide r (µGy/h per Bq/kg); Csoil,water,r is the activity concentration of radionuclide r in soil or water (Bq/kg); DCCint,r isthe DCC for internal exposure to radionuclide r (µGy/h per
Bq/kg); and Cbiota,r is the internal activity concentration ofradionuclide r in biota (flora or fauna) (Bq/kg).
(b)

Activities in environmental media

134. In the absence of measurements, in order to evaluate
equation (5), the activity concentrations, Csoil,water,r , and Cbiota,r ,have to be estimated. Assuming a constant discharge of radionuclides over a period of 50 years, the activity in soil for thelast year of that period is calculated as indicated in reference[I11]:
C s ,r =Dtot ,r(lr + lm ) ⋅ ms

253

⋅ [1 − exp(−(lr + lm ) ⋅ te )] (6)where Cs,r is the activity concentration in soil (Bq/kg); Dtot,ris the total (wet plus dry) deposition rate to soil (Bq m‑2 a‑1);
ms is the mass of the upper soil layer (kg/m2); lr is the radioactive decay constant (a‑1); lm is the loss rate from the upper
soil layer (a‑1); and te is the discharge period (50 a).
135. The total deposition is calculated as the sum of dry(Ddry,r) and wet deposition (Dwet,r). The activity concentrationin flora, Cflora,r, is estimated by taking into account direct
deposition on the foliage and uptake from soil according toreference [I11]:

136. The activity concentration in reference fauna is estimated from the soil concentration and the soil–fauna transfer
factor as follows:C fauna ,r = Cs,r ⋅ TFfauna ,r(8)

where TFfauna,r is the soil–fauna transfer factor (Bq/kg fauna
per Bq/kg soil).
137. The habitats of the reference fauna are differentiatedaccording to whether the organisms live in or above soil.
DCCs for species living in soil are expressed in units ofµGy/h per Bq/kg and are based on the assumption that theorganism lives in the centre of a slab containing radio­
nuclides uniformly distributed to a depth of 50 cm. For
organisms living on soil, it is assumed that radionuclides arehomogeneously distributed to a depth of 10 cm; the DCCs inthis case have units of µGy/h per Bq/m2.
138. The estimation of the activity concentration of a radio­
nuclide in aquatic biota (Caqua biota) is usually obtained fromthe activity concentration in water (Cwater) and the concentration factor (CFwater–biota) according to:Caqua biota = Cwater ,r ⋅ CFwater −biota ,r(9)139. As outlined above, the exposure due to incorporated
radionuclides is determined by the size and geometry of theorganism, the radionuclide distribution, and the type andenergy of the emitted radiation. Currently, DCCs are notavailable for specific target organs in the reference organisms; the DCCs for internal exposure are therefore based on
the assumption that the radionuclides are homogeneously
distributed throughout the organism [T10].
(c) oses to marine organisms and to humans due toDc­ onsumption of marine food

140. As an example of the calculations of exposures ofaquatic organisms, the exposures to marine organisms arecalculated assuming a radionuclide concentration in water of
1 Bq/m3 and applying the appropriate concentration factor
for water–biota in table 13 and the appropriate DCCs given
in tables 14 and 15. The weighted absorbed dose rates toDdry ,r + fw ⋅ Dwet ,rflatfish, crab and brown seaweed are summarized in table 20.
C flora ,r =⋅ [1 − exp(−(lw,r + lr ) ⋅ t w )] + Cs,r ⋅ TFflora ,rFor all radionuclides considered, the dose rates to biota are(lw,r + lr ) ⋅ balmost completely a result of internal exposure. For comparison, the effective dose rates to an adult human are given− exp(−(lw,r + lr ) ⋅ t w )] + Cs,r ⋅ TFflora ,r(7)
assuming an annual fish intake of 20 kg. In general, thewhere fw is the interception fraction (dimensionless); b is theeffective dose rates to humans are much less than thestanding biomass (kg/m2); lw is the activity loss rate fromweighted absorbed dose rates to biota for a unit activity
plants due to weathering (a-1); tw is the exposure time (a); and­concentration of a radionuclide in marine water.

254

UNSCEAR 2008 REPORT: VOLUME IITable 20.
1 Bq/m3Comparison of doses to non-human biota and humans, normalized to an activity concentration in marine water ofRadionuclide

Non-human biota

Humansa

Weighted absorbed dose rate (µGy/h per Bq/m3)

Normalized effective dose rate(µSv/h per Bq/m3)

FlatfishCrabMacroalgaeH

3.3 × 10‑9

3.3 × 10‑9

3.3 × 10‑9

4.1 × 10‑11Cl

9.6 × 10

9.6 × 10‑9

7.0 × 10

1.3 × 10‑10Sr

1.8 × 10‑6

6.3 × 10‑6

4.5 × 10‑6

1.9 × 10‑7Tc

4.6 × 10

5.8 × 10‑4

1.7 × 10

1.2 × 10‑7I

3.8 × 10‑7

4.3 × 10‑6

3.8 × 10‑4

2.3 × 10‑6I

1.2 × 10

1.4 × 10‑3

1.0 × 10

4.5 × 10‑7

134

Cs

1.9 × 10‑5

6.9 × 10‑6

4.9 × 10‑6

4.3 × 10‑6

135

Cs

3.9 × 10‑6

1.2 × 10‑6

1.9 × 10‑6

4.6 × 10‑7

137

Cs

1.8 × 10

5.7 × 10

‑6

6.5 × 10

3.0 × 10‑6Pb

4.8 × 10‑5

2.3 × 10‑3

8.0 × 10‑4

3.2 × 10‑4Ra

1.3 × 10

1.4 × 10‑2

1.4 × 10

6.4 × 10‑5Th

1.4 × 10‑2

2.3 × 10‑2

4.6 × 10‑3

3.2 × 10‑4U

2.4 × 10

2.4 × 10‑3

2.4 × 10

1.0 × 10‑7Np

2.7 × 10‑3

2.7 × 10‑3

1.4 × 10‑3

2.5 × 10‑5Pu

3.0 × 10

6.0 × 10‑1

1.2 × 10

5.7 × 10‑5Pu

3.0 × 10‑3

6.0 × 10‑3

1.2 × 10‑1

5.7 × 10‑5Am

3.2 × 10

1.3 × 10

2.5 × 10

4.6 × 10‑5

3

36
90

99

129
131

210

‑5

‑2

238

‑5

237

239

‑3

240
241

‑6

‑6

226

232

‑9

‑3

‑9

‑5

‑5

‑6

‑2

‑4

‑3

‑2

‑1

a For an intake of marine fish of 20 kg/a.

4.

Conclusions

141. In this section, approaches have been described for theassessment of exposures of flora and fauna to radiation fromnatural background levels of radionuclides or regulated discharges of radionuclides to the environment. The models cover
two major fields. One is concerned with the transport processesof radionuclides from the source to plants and animals, to whichapproaches may be applied that are similar to those used toassess the exposures of humans. In the terrestrial environment,these are mainly atmospheric dispersion, deposition, interception, weathering and uptake from soil. For discharges to aquatic
systems, models can be used that describe dispersion, dilution,
sedimentation and uptake by freshwater or marine organisms.
142. There are major differences in the dosimetry involved in
the assessment of the exposures of humans and non-humanbiota. The current approaches for biota rely on the mean activity
concentrations in the whole organism rather than on those in distinct organs or tissues. Thus, the calculated absorbed doses are to
the whole organism. There is an ongoing discussion about theappropriate factors to be applied in order to account for the different RBEs of the different kinds of radiation involved. Example calculations in this annex show that the estimated weighted
absorbed doses from exposure to alpha radiation are sensitive tothe value of the factor used. This is relevant to the assessmentof doses to biota both as a result of radioactive discharges froma nuclear site and as a result of exposure to radiation fromradio­nuclides that are naturally present in the environment.
143. The estimated doses to biota are compared in thisannex with those to humans in accordance with the approachgiven in reference [U3]. The comparison shows that theweighted absorbed doses to terrestrial non-human biota andthe effective doses to humans are generally of a similar orderof magnitude, for a given level of environmental contamination by radionuclides. The weighted absorbed doses to marine
biota are, in general, considerably higher than the effective
doses to humans (for whom an annual consumption of marine
fish of 20 kg is assumed for illustrative purposes).
144. The results of the dosimetric calculations presented inthis annex are based on stylized models of ecosystems using
average values for most of the model parameters. Thus, they do
not accurately reflect the variability of ecosystems and the pro­
cesses present in nature that control the environmental mobilityof radionuclides. In addition, the exposures due to the various
sources of natural background radiation and their variabilities
would have to be included if the results presented in this annex
were to be used in a site-specific assessment. As indicated earlier, there are substantial uncertainties associated with the estimation of dose rates to non-human biota, including those
associated with the environmental pathways (such as in the values of the transfer factors) and those related to dosimetric issues.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

II.

255

Summary of dose–effects data from the UNSCEAR 1996 Report145. In the absence of reports of obvious deleterious
effects on other organisms from exposure to environmental
radiation, whether of natural origin or due to the controlled
discharges of radionuclides to the environment, it had generally been accepted that priority should be given to evaluating the potential consequences for humans (which areamong the most radiosensitive mammalian species) and toproviding a sound basis for protecting human health. By
1996, this position had, however, been questioned [D1, T1],
and at least one situation (namely deep-sea sediments, anenvironment very remote from man) had been identified
where the above accepted priority could be incorrect [I3]. In
response to such concerns, the Committee noted that the
impact of radiation exposure of non-human biota had beenstudied in a number of situations [I2, I3, I4, M1, N1, W1,
W2] and considered that it was appropriate to conduct an
independent review of the matter and to summarize the stateof knowledge existing at that time. The UNSCEAR 1996
Report [U4] took account of the earlier reviews and studies
and the Committee’s summaries of the radiobiological work
carried out over the previous 50 years.
146. In its 1996 report, the Committee noted that there wasa fundamental difference in the approaches to the protectionof humans and non-human biota from the effects of exposure
to ionizing radiation. For humans, ethical considerations had
made the individual the principal object of protection. This
meant, in practice, that any incremental risk to the individual
arising from increased radiation exposure was to be constrained below some level that society judged to be acceptable; this level of risk, although small, was not zero [I5]. For
non-human biota, the populations of the biota were considered to be important and protection from a significantly
increased risk to each population arising from radiation
exposure might be the appropriate objective. Exceptions
might be populations of small size (rare species) or those
reproducing slowly (i.e. with long generation times and/or
low fecundity) for which protective measures might be more
appropriately targeted at the level of the individual organism. The Committee noted that there could not be any effectat the population level (or at the higher levels of communityand ecosystem) if there were no effects on the individualorganisms constituting the different populations. It went on
to suggest that radiation-induced effects on some membersof a population would not necessarily have any significant
consequences for the population as a whole.
147. The Committee noted that natural populations oforganisms existed in a state of dynamic equilibrium within
their communities and environments and that exposure toionizing radiation was but one of the stresses that may affectthis equilibrium. The incremental radiation exposure fromhuman activities could not, therefore, be considered in isolation from other sources of stress, whether natural (e.g. climate, altitude, or volcanic activity) or of human origin (e.g.
synthetic chemical toxins, oil discharges, exploitation forfood or sport, or habitat destruction). When (as is not uncommon) ionizing radiation and chemicals, both resulting fromhuman activities, acted together on a population, the difficult
problem arose of correctly attributing any observed response
to a specific cause.
148. The objective of the UNSCEAR 1996 Report on the“Effects of radiation on the environment” [U4] was tosummarize and review information on:– The exposures (actual or potential) of organisms in their natural habitats to the natural background radiation, to radionuclides discharged
into the environment in a controlled mannerfrom industrial activities, and to radionuclides
released as a consequence of accidents; and– The responses of plants and animals, both as individuals and as populations, to acute and chronic
irradiation.
149. The Committee hoped that its review would assist
national and international bodies to select appropriate ­criteria
for the radiological protection of natural populations, communities and ecosystems. The following paragraphs recapitulate
the information available to the Committee in 1996.

A. Dosimetry for environmental exposures150. As discussed in the annex to the UNSCEAR 1996
Report [U4], reliable determination of the dose rate to organisms is essential for assessing the potential or actual impacts
of contaminant radionuclides in the environment. The Committee noted that “this simple statement conceals a multitudeof difficulties that prevent the easy achievement of that estimation”. In practice, it is necessary to make simplifying
assumptions, with the degree of simplification depending on
the purpose of the assessment. For example, for the purposeof screening, the concept of a single generic biota that represented all plants and animals had been used [A2]. Moresophisticated models attempted to account for the dose distributions within reference organisms of assumed shapes andsizes and the fraction of radiation being absorbed within theorganism [W2]. The Committee’s views on dosimetry for
estimating the exposure of biota based on what was known
in the UNSCEAR 1996 Report [U4] are summarized below.
151. A dosimetric model is essentially a mathematical construction that allows the energy deposition in a defined target
to be estimated from a given radionuclide (source) distribution. The model was often derived using theoretical or
empirical functions that described the distribution of doseabout a point source [B2, B3, L1, W2]. The dose at a point in
the target was then obtained by integrating the point source
dose distribution function over the defined radionuclide
source, either internal or external to the organism. This

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procedure was frequently simplified by using ideal
geometries (spheres, ellipsoids, etc.) of appropriate size torepresent the target and by assuming that the radionuclide
distribution was uniform (over a surface or through a volume) or varied in a way that could be described by a simple
mathematical expression (e.g. an exponential decline in radionuclide concentration with depth in soil or sediment).
Alternatively, Monte-Carlo calculations had been used todetermine the absorbed fractions of energy for a variety ofsource and target geometries [B4, E2]. These data could be
used, either directly or with interpolation (or, to a lesser
extent, with extrapolation) for geometries that could represent targets of environmental concern. In principle, these procedures could be adapted for use in estimating doses toterrestrial and aquatic organisms, from both the plant and animal kingdoms, for both internal and external sources ofradiation.
152. Dosimetric models had been developed to takeaccount of the radiation type; the specific geometry of thetarget (e.g. the whole body, the gonads, the developing
embryo or the plant meristem); and the source of exposure(e.g. radionuclides accumulated in body tissues, adsorbed
onto the body surface or distributed in the underlying soil).
Clearly, it was not possible to consider all organisms, andthere were limitations in the basic data that were available as
input to the models (e.g. the spatial and temporal distributions of radionuclides both within the organism and in theexternal environment). Additional sources of complexity
arose from the behaviour of mobile organisms, particularly
some aquatic organisms and many insects, which inhabit different environmental niches at different stages of their life
cycles. Thus, the models had to be simplified and generalized without undue loss of the realism that is essential for avalid estimation of dose.
153. The presence of an alpha particle component in the
total absorbed dose rate to a tissue in a plant or animal raised
the question of how to take account of the probably greater
effectiveness of this type (quality) of radiation in producing
biological damage. The RBEs of different qualities of radiation had been very critically examined for the purposes ofhuman radiation protection. Each component of the absorbed
dose to a tissue or organ was weighted by a factor which
took account of the RBE of the radiation involved [I5]. It
seemed reasonable to apply a similar approach to the radiation dosimetry for organisms other than man. In practice,
however, there were circumstances that altered the detailed
application of this approach. In the human case, the major
concern had been with the induction of stochastic effects(principally cancer) at low doses and dose rates. For alpharadiation, experimental determinations of the RBE had led toa recommended radiation weighting factor of 20 for the purpose of human radiation protection. In the case of wild animals, however, the Committee assumed that it was likely that
deterministic effects were of greater significance. For alpharadiation, the experimental data for animals indicated that alower factor to reflect the RBE would be more appropriate;
the factor to reflect the RBE of beta and gamma radiations

would however be numerically the same as the radiation
weighting factor used in human radiation protection. On theassumption that mammals are the most sensitive species,
these values could be applied to other taxonomic groups.
154. In its 1996 UNSCEAR Report [U4], the Committee
assumed that these factors would also apply to effects onplants, although there were no definitive experimental data
to support this. In the absence of protection quantities(equivalent and effective dose) for non-human organisms,
the absorbed doses from low-LET radiation (beta particles,
X‑rays and gamma rays) and from high-LET radiation (alphaparticles) were assessed and specified separately in the
UNSCEAR 1996 Report [U4]. The absorbed doses retained
the unit, joule per kilogram (J/kg), with the special namegray (Gy).
155. An IAEA technical report [I4] provided estimates ofthe dose rates to terrestrial plants due to radionuclides deposited following discharges to the atmosphere. The model,
PATHWAY [W3], developed to estimate doses to humans,
had been used to derive the equilibrium concentrations ofradionuclides in plants and animals for the limiting case inwhich humans, while living on the land, breathing the air
over it and eating the food produced from it, would receive
an annual effective dose of 1 mSv. To estimate the dose toplants from internal sources, it was assumed that the energyof alpha and beta particles would be totally absorbed (except
for emissions from 32P, which would be 50% absorbed) andthat 10% of the gamma-ray energy would be absorbed. An
additional degree of conservatism was provided by using
estimates of the radionuclide concentrations in plant tissue
on a dry weight basis (which are 5–10 times higher than ona wet weight basis) to calculate the absorbed dose rates toliving (i.e. “wet”) plant tissue. The results are given intable 21. As these estimates had been made using a radio­
ecological model and a scenario designed for calculating
exposures to humans, the calculated exposures of nonhuman species should be interpreted cautiously.
156. The annex of the UNSCEAR 1996 Report [U4] notedthat there have been fewer estimates of the potential exposures of fully terrestrial animals than of animals occupying
semi or fully aquatic niches. This was thought to be a reflection of the greater use that had been made of aquatic systems
for the discharge of radioactive waste.
157. The annex of the UNSCEAR 1996 Report [U4] suggested that naturally occurring alpha-emitting radionuclides
appeared to be the most significant sources of backgroundradiation exposure for the majority of wild organisms.
158. In its 1996 report, the Committee considered that thedata on the radiation exposures of non-human biota due toboth natural background radiation and contaminant radio­
nuclides were incomplete, more in some areas than in others.
The Committee also noted that the aquatic environment wasprobably the most thoroughly studied environment up to thattime [I2, I3, I7, N1, N2, W1], even with the substantial

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

generalizations that had had to be made, particularly withrespect to the range of organisms that could reasonably beconsidered [I3]. As had been emphasized elsewhere [I3, I6],
the limiting factor was not the development of an appropriate dosimetric model for a particular organism but rather theacquisition of essential input data on the temporal and spatial distributions of the radionuclides both external to andwithin the organism. Although dynamic models had been
employed to describe the dispersion and dilution of radio­
nuclides in a water body, related phenomena (e.g. transfers
to sediments and biological tissues) were almost always

257

modelled as equilibrium processes, i.e. using simple distribution coefficients and (whole-body) concentration factors.
This simplification largely neglected the temporal variations
in dose rate due, for example, to short-term fluctuations indischarge rate, differing stages in the life cycle, and behavioural and short-term environmental processes (e.g. seasonality). As a consequence, while the estimated absorbed dose
rate might be a reasonable indication of the general magnitude of the actual environmental value, the Committee considered that it did not provide a very secure basis forevaluating total doses over time.

Table 21. Estimated dose rates to organisms from controlled discharges of radionuclides that would each result in an annual
dose of 1 mSv to humans residing in the same environment
Table 6 of UNSCEAR 1996 Report [U4]; based on [I4, N1]
Radionuclide

H
C
32
P
60
Co
90
Sr
95
Zr
99
Tc
131
I
137
Cs
226
Rad
235 d
U
238 d
U
239 d
Pu
241
Amd
3

14

Dose rate (µGy/h)Plantsa

Animalsa,b

Fishc

5.8
18
32

5.8
11
28

0.59

2.0
38

0.042
2.0

1.2
5.4

0.058
3.1

0.023

0.000 55

4.8
0.53
67
3.8
0.72
3.6
2.6
4.7
0.49
0.71

a Discharges to atmosphere.
b Domestic sheep.
c Discharges to water (lakes).
d High-LET radiation.

159. The Committee also noted that accident situations
were by nature quite different from routine situations, particularly in their potential to produce high dose rates anddoses to the environment. It concluded that generalization isdifficult because the actual exposure regime depends on thetypes and quantities of radionuclides released, their initialdispersal and deposition patterns, and their redistribution
over time in the environment. Following the accident at the
Chernobyl nuclear power plant, large quantities of shortlived radionuclides were released, leading to high dose rates
in the local area. Total doses up to 100 Gy were delivered totrees (and, by inference, to most other organisms in the locality) over a period of a few days [K1]. This radiation regime
might have been characterized as “acute” in that the doses
were delivered in periods that were shorter than or comparable to the time taken for severe damage to become apparent.
During this initial (acute) phase, the dose rates declined rapidly as the very short-lived radionuclides decayed. The
release following the accident in 1957 in the south-eastern
Urals was dominated by 144Ce–144Pr (approximately 66%;t½ = 285 d) and 95Zr–95Nb (approximately 25%; t½ = 65 d). In
that case, the dose rates locally were also relatively high during the initial phase (more than 4 mGy/h) but declined more
slowly, such that high total doses (causing severe effects,
including mortality) could still be accumulated from essentially chronic exposure. Close to the release point, total doses
up to 2,000 Gy were experienced [T4]. In the longer term,
the exposure regime for the Chernobyl release was dominated by 137Cs (t½ = 30 a) and 90Sr (t½ = 28.6 a), and that forthe south-eastern Urals accident area by 90Sr. In both cases,
the exposures were chronic and moderately high, withresponses other than mortality becoming significant.
160. Radioactive waste discharges to atmosphere, landfills
or aquatic systems from man-made practices entail increased
radiation exposure of wild organisms. The incremental
radia­tion exposures are chronic (i.e. continuing) at absorbed
dose rates of generally no more than 100 μGy/h, but, very
exceptionally, they may reach several thousand microgray
per hour. The Committee [U4] noted that these additional

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radiation exposures may be greater than the normal range ofnatural background exposures but generally are within theextreme range of background exposures, if the exceptional
cases of areas of uranium and thorium mineralization are
included. Given that radioactive waste discharged to theenvironment will normally be dispersed and diluted, dose
rates higher than those due to normal natural backgroundexposure are likely to apply to only a small proportion of
the individual organisms in any population and the average
dose rate to the population would probably be much lower[W8, W9].
B.

direct or indirect interactions among its members are more
important than those between its members and members ofother populations” [B6]. Notwithstanding this definition, it
has to be understood that a population of a particular species
is always linked to its environment. Such a population would(or could) be a self-sustaining unit, independent of other,geographically separate populations of the same species.
However, protection of this population would require that
increased radiation exposure did not significantly affect the
attributes mentioned in the definition on which the population depended for its maintenance within the normal dynamic
range of variation dictated by the interactions of natural
physical, chemical and biological factors.

Effects of radiation exposure on plants and animals

161. Studies of the effects of ionizing radiation exposure
on plants and animals were started immediately following
the discovery of X‑rays and radioactivity (see, for example,
reference [A4]). Since 1945, when the first nuclear detonations were conducted, there was widespread concern about
the impact of environmental radiation exposures and interestin the environmental behaviour of radioactive materials. As
a result, studies using a wide variety of plant and animal­species were performed [A4, B5, C3, P1].
162. The Committee, in its 1996 report [U4], noted that the
responses of organisms to radiation exposure were varied
and may become manifest at all levels of organization, fromindividual biomolecules to ecosystems. The significance of agiven response depended on the criterion of damage adopted,
and it was not to be concluded that a response at one level oforganization would necessarily produce a consequential,
detectable response at a higher level of organization.
163. The Committee also noted that a population might bedefined as all members of a population species [U4]. Alternatively, a population might be considered as an aggregate ofinter-breeding individuals of a species occupying a specificlocation in space and time [S5]. The latter definition is perhaps more useful given the Committee’s observation thatradiation fields, such as those arising from radioactive waste
discharges, generally show large spatial variability, not least
because of the often discrete nature of the source, and therefore many members of a population might not receive any
significant exposure from a particular source. The natural distributions of most species are inhomogeneous because of thevariations in physical, chemical and biological conditions
under which the individuals of the species are able to survive,
i.e. species are geographically restricted. Thus, it is probablethat a more limited, and relevant, definition of a population
could be developed for the purposes of environmental impact
assessment.
164. The following definition (developed for use in population ecology) has been suggested as a useful basis for discussion and progress [I4]: “A population is a biological unit forstudy, with a number of varying statistics (e.g. number, density, birth rate, death rate, sex ratio, age distribution), andwhich derives a biological meaning from the fact that some165. These attributes, which could be defined only for
popu­lations of organisms and might be taken to be indicatorsof their health, are nevertheless amalgamations of properties
that relate to individuals (in no sense was this meant to imply
simple addition). The Committee concluded, in effect, thatfor a response to radiation exposure at the population level(or, indeed, at any higher level of organization) some clearly
detectable effect in individual organisms (i.e. at lower levelsof organization) would be expected. This clearly implied thatthe protection of the population (as the ultimate objective)
might be achieved by restricting the exposure of individualorganisms to the extent that there are no significant radiation
effects on those processes necessary for the maintenance ofthe population. It is therefore necessary to consider the available information on the effects of radiation exposure (mainly
at chronic low dose rates) on the relevant processes in individual organisms, to consider how these responses mighttranslate to an impact on the population, and to examine theresults of studies of population responses to deliberate
experimental irradiation or to exposure in the environment
due to controlled or accidental releases of radionuclides.
166. Examination of the population attributes indicatedthat the individual responses to radiation exposure likely to
be significant at the population level are mortality (affecting
age distribution, death rate and density), fertility (birth rate),
fecundity (birth rate, age distribution, number and density)and the induction of mutations (birth rate and death rate).
These individual responses can be traced to events at thecellular level in specific tissues or organs. An extended summary discussing the processes involved was provided inannex J, “Non-stochastic effects of irradiation”, of the
UNSCEAR 1982 Report [U9]. There was a substantial bodyof evidence indicating that the most radiosensitive sites areassociated with the cell nucleus, specifically the chromosomes, and that, to a lesser extent, damage to intracellular
membranes is additionally involved. The end result is thatthe cells lose their reproductive potential. For most cell
types, at moderate doses, death occurs when the cellattempts to divide; death does not, however, always occur at
the first post-exposure division: at doses of a few gray, seve­ral division cycles might be successfully completed before
death eventually occurs. It was also well known that radiosensitivity varies within the cell cycle, with the greatest sensitivities being apparent at mitosis and the commencement

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

1.

of DNA synthesis [U9]. It followed that the greatest radiosensitivity is likely to be found in cell systems undergoing
rapid cell division for either renewal (e.g. spermatogonia) or
growth (e.g. plant meristems and the developing embryo);these examples clearly underlie the processes in individualorganisms that are important for the maintenance of the
population.

259

Terrestrial plants

168. Radiation injury in plants expresses itself as abnormal
shape or appearance, reduced growth or yield, loss of reproductive capacity, wilting and (at high exposures) death [S1].
Acute lethal doses to higher plants ranged from 10 to about
1,000 Gy (approximate mean absorbed doses averaged over
the whole plant). The Committee concluded that plants suchas mosses, lichens and unicellular species are at one extremeof radiosensitivity being highly resistant to radiation exposure; woody species are at the other extreme being the mostsensitive. In 12 species of woody plants assessed 10–14 months
after exposure, the lethal doses were found to be in the range
of 8–96 Gy [S2]. The pine tree was the most sensitive, experiencing mortality following short-term absorbed doses ofabout 10 Gy [W5]; growth was severely inhibited at 50–60%
of the lethal dose. Floral inhibition was observed at 40–50%
of the lethal dose, and failure to set seed at 25–35%. Thus, thecapacity of the plant population to maintain itself could bedamaged at acute doses lower than those required to cause
mortality. Below 10% of the lethal dose, effects were not soapparent and the plants maintained a normal appearance.
These general observations for several herbaceous plant species are illustrated in figure X [S3]. Another general relationship was that the dose that reduced survival by 10% (LD10)
was roughly equivalent to the dose that reduced the yield by
50% (YD50) [S1].

167. Fractionation or protraction of exposure to low-LET
radiation increases the total dose required to produce a given
degree of damage since at low dose rates, the factors responsible for mitigating the response come into play. These
include the repair of sublethal damage, the repair of potentially lethal damage, the replacement of killed cells throughproliferation of survivors, and other slow repair processes
not related to cell repopulation [U9]. Although it was clear to
the Committee that repair, in the general sense, is possible,
the existence and extent of residual injury was less clear.
While such an outcome might be demonstrated for moderate, acute doses, it was not possible to extrapolate theseresults in order to predict the likely response to low-level
exposures extending over a significant fraction of the lifetime of an organism. However, given that genetic mutations
might be passed from generation to generation, it was reasonable to suppose that somatic mutations individually consistent with cell survival could occur and accumulate overtime until the combined impact might reduce cell viability.

Figure X. General ranges of response to radiation exposure by herbaceous plants as a percentage of the lethal dose (LD100) [S3]Mortality in 50% of plants
Severe growth inhibition
Floral inhibition
Pollen sterility
Mortality in 10% of plants
Yield reduced by 50%
Failure to set
Yield reduced by 10%
Normal appearance
0

10

20

30

40

50

60

70

80

PERCENTAGE OF LETHAL DOSE

169. The Committee, in the UNSCEAR 1996 Report [U4],noted that protraction of radiation exposures increased thetotal doses required to kill plants [S4].
170. A range of sensitivities to radiation exposure was
exhibited by the components of plants, ranging from dryseed (least sensitive) to apical meristems (most sensitive).
Various crop plants showed different reductions in yieldfollowing radiation exposures, with further modifications
being caused by external factors (e.g. temperature andhumidity).

171. Plant species also varied in their tolerance to chronic
radiation exposures. For the more sensitive pine species, dose
rates of more than 3 mGy/h over 3–4 years reduced needle
growth; in one‑year-old saplings, needle length was substantially reduced when subjected to a dose rate of 7 mGy/h over a
single growing season. Trunk growth was reduced in maturepine trees by dose rates in the range 0.4–2 mGy/h over a 9‑year
period. Delayed bud burst and an extended period of leafing
out was demonstrated in white oaks chronically exposed to
gamma radiation. At dose rates greater than 4 mGy/h, the trees
were more susceptible to aphid infestation.

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172. In view of the effects on the most sensitive plants evident with chronic exposure at dose rates of 1–3 mGy/h andof some specific changes noted at dose rates of 0.4–2 mGy/h,the Committee [U4] suggested that chronic dose rates at or
below 400 μGy/h (10 mGy/d) should have only slight effects
on sensitive plants but would be unlikely to produce any significant deleterious effects on the wider range of plants
present in natural plant communities.
2.

176. While acknowledging that the numbers of mammalian species that had been (or indeed were likely to be)­studied were extremely limited and probably atypical, theCommittee noted [U4] that, even taking account of substantial interspecific variability, the available data provided very
little evidence that chronic dose rates below 400 μGy/h(approximately 10 mGy/d) to the most exposed members of
the population would seriously affect their mortality (and,thus, the death rate in populations of these species) fromeither deterministic or stochastic responses.

Terrestrial animals

173. The effects of radiation exposure on mammals had been
extensively studied in radiobiological experiments using laboratory animals (mice, rats, dogs and monkeys) and domestic
livestock (pigs, sheep, goats, burros and cattle) [B7, B8].
Except in the case of exposure involving unusually high doses,
radiation damage or lethality in mammals results from disturbances in the haematopoietic system and the gastro­intestinal
mucosa. These cell self-renewal systems contain stem cells,
differentiating cells and functional end cells, with the stem
cells being the most radiosensitive and thus having the predominant influence on the radiation response. Symptoms
become apparent when end cells are not replaced.
174. Protraction of a given total exposure generally reduces
the extent of injury, as it allowed two distinct processes tointervene. First, sublethal damage is reparable at the cellularlevel, which is particularly important for exposures to lowLET radiation. Secondly, cell proliferation could replacelethally damaged cells and maintain the cell population at a
new level, which is determined by the dynamic interaction
between the dose rate and the rate of cell death, and by the
total reserve proliferative capacity.
175. The Committee noted that at reduced dose rates (protraction of a given total dose) of low-LET radiation, all species
showed a gradual increase in LD50, i.e. higher total doses were
tolerated. This changing response was attributed to the increasingly effective influence of cellular repair of sublethal damage
at the lower dose rates. As the dose rate was further reduced, asharply increasing trend in the values for the median lethal
dose was apparent for mice, pigs, dogs, goats and sheep; theapproximate threshold dose rates for this change in response
corresponded to the accumulation of an LD50 dose within periods ranging from 0.2 days (mouse) to 9 days (goat). This rapidchange in LD50 with dose rate was interpreted as being theconsequence of a shifting balance in the dynamic interaction
between the dose-rate-dependent cell loss and the cell proliferation and maturation kinetics in the haematopoietic system;
the latter processes are under homeostatic control, i.e. theirrate constants can alter in response to radiation-induced cellloss. The data for the burro (donkey) and primates did notshow any sharp increase in the median lethal dose at dose rates
down to 8.3 mGy/h (LD50 in 18 days) and 5.4 mGy/h (LD50 in
60 days), respectively. There did not appear to be any data for
LD50 values at dose rates of less than 4 mGy/h or for exposure
periods exceeding 60 days, although studies had been madeoutside these levels for other purposes.

177. The effects of radiation exposure on reproduction had
also been much studied, with most of the results suggestingthat natality is a more radiosensitive parameter than mortality in species other than man and therefore of more relevancein an environmental context. The Committee considered thatthe minimum dose required to depress reproduction rates
might be less than 10% of the dose required to produce directmortality [W6].
178. The Committee suggested that damage to the developing mammalian embryo appeared to be a potentially significant criterion for assessing the impact of contaminantradionuclides in the natural environment. Dose rates of
420 μGy/h throughout gestation produced readily detectablereductions in the populations of germ cells in the developing
gonads of a number of mammalian species, and the lowest
dose rate at which damage had been seen was 10 μGy/h fromtritium (as HTO in drinking water) incorporated in female
mouse embryos. In addition, dose rates of the order of
420 μGy/h induced reductions in neonatal brain weight,
although the significance of this deficit was unknown infunctional or behavioural terms. The wider significance of
these responses at the population level had not been investigated. Even recognizing that only very limited data wereavailable, the Committee concluded that maximum dose
rates of 100 μGy/h (2.4 mGy/d) to pregnant members of a
mammalian population were unlikely to have any consequences for the population as a whole from the induction ofdamage in the developing embryos.
179. The Committee noted that the data on the radiosensitivity of terrestrial animals were dominated by data on mammals, the most sensitive class of organisms. Acute lethal
doses (LD50/30) were 6–10 Gy for small mammals and 1.5–
2.5 Gy for larger animals and domestic livestock. When atotal dose of magnitude similar to the LD50/30 was delivered
over a lifetime—for example, 7 Gy to the mouse (420 μGy/h,or 10 mGy/d)—the average loss of lifespan had been estimated to be about 5% and resulted from the induction ofneoplastic disease [U9]. There was substantial inter-species
variability, but, in general, little indication that dose rates
below about 400 μGy/h to the most exposed individual
would seriously affect mortality in the population.
180. The Committee noted that reproductive capacity was
more sensitive to the effects of radiation exposure than life
expectancy (mortality) and felt that the reproductive rates ofmammals might be depressed at doses that were 10% ofANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

those leading to mortality. It also felt that some loss ofoocytes might occur at 1% of the lethal dose, but because ofexcess oocyte production, fecundity should be affected to alesser extent. Mice, exposed from conception to a dose rateof 800 μGy/h, could be made sterile at 25 weeks. In the mostsensitive mammal studied, the beagle dog, a dose rate of
180 μGy/h caused progressive cell depletion and sterility
within a few months, but a dose rate of 36 μGy/h over thewhole life produced no damaging response. The Committee
concluded that a radiation dose rate of less than 40 μGy/h tothe most exposed individual in a population (and most probably, therefore a lower mean dose rate to individuals in the
population as a whole) would be unlikely to have an impact
on the overall reproductive capacity of a mammalian population as a consequence of the effects of radiation exposure on
fertility, fecundity or the production of viable offspring.
181. The effects of radiation exposure on birds had beenshown to be similar to those on small mammals. Reptiles
and invertebrates were less radiosensitive, although physio­
logical differences began to make direct comparisons withother species less appropriate. The chronic exposure of one
short-lived species of lizard in enclosures had shown noevident effects when exposed over 5 years at a dose rate of830 μGy/h. In two longer-lived species of lizard, some individuals had been made sterile after 3.5 years at a dose rateof 630 μGy/h in one species and after 5.5 years at a dose
rate of 210 μGy/h in another species. Adult invertebrates
were seemingly quite insensitive to the effects of radiation
exposure in terms of induced mortality, but the process ofgametogenesis, developing eggs and juvenile stages weremore sensitive.
3.

Aquatic organisms

182. A number of reviews of the studies of the effects of
exposure to ionizing radiation on aquatic organisms wereavailable to the Committee [A3, B9, C3, E2, I2, I3, N1, N2,
P2, T5, W9] during the preparation of the annex of the
UNSCEAR 1996 Report [U4]. Some of these had been prepared specifically to provide a basis for assessing the potential effects of discharges of liquid radioactive effluents onaquatic organisms in their natural environment [I2, I3, N1,
N2, W1].
183. Among aquatic organisms, fish were the most sensitive to the effects of radiation exposure; the developing fishembryos were particularly sensitive. The LD50 for acute irradiation of marine fish was in the range 10–25 Gy for assessment periods of up to 60 days following exposure. The upper
end of the range of LD50 for marine invertebrates had beenfound to be several hundred grays. Embryos, on the other
hand, were affected at much lower doses, for example, theLD50/90 for salmon embryos was 0.16 Gy [B10].
184. Chronic exposures at dose rates of 10–30 mGy/h had
no effect on the mortality of snails, marine scallops, clams
and blue crabs. Dose rates somewhat above this range had

261

some effects on food-limited populations of Daphnia pulex.
Short-term (40 days) exposure of mosquito fish at dose rates
in the range 14–54 mGy/h showed no radiation-induced
mortality, but, for the closely related guppy, there was someindication that long-term exposure (>470 days) at dose rates
above 1.7 mGy/h reduced the normal lifespan, particularly
for males.
185. Reproductive effects are a more sensitive indicator ofradiation response for aquatic organisms. Chronic dose rates
in the range 3.2–17 mGy/h reduced the reproductive capa­
city in the freshwater snail, Physa heterostropha, and in themarine polychaete worms, Ophriotrocha diadema and Neanthes arenaceodentata. Exposure at a dose rate of 7.3 mGy/hrendered male freshwater fish (Ameca splendens) effectively
sterile after 50 days, and exposure at a dose rate of 1.7 mGy/hover the lifespan of pairs of guppies (the freshwater fish,
Poecilia reticulata) significantly reduced the lifetime production of offspring [W7]. It had been concluded that significant effects on fish gonads from chronic radiation
exposure would be unlikely at dose rates less than 1 mGy/h[I3, W1]. Overall consideration of the data available led tothe conclusion that chronic irradiation at dose rates up to400 μGy/h to a small proportion of the individuals in an
aquatic population (and, therefore, with correspondingly
lower average dose rates to the whole population) would nothave any detrimental effects at the population level [I4, N1].
C. Effects of radiation exposure on populationsof plants and animals
186. The Committee noted in the annex of the UNSCEAR
1996 Report [U4] that one of the difficulties in evaluating theeffects of radiation exposure on populations and ecosystems
was the determination of the parameters to measure. Typically measured attributes at the population level included
numbers of individuals, mortality rate, reproduction rate andmean growth rate. The Committee also noted that measurable changes in populations and communities required rather
severe effects to be induced at the cellular and individualorganism levels [e.g. W8]. The Committee also noted thatgenetic or somatic mutations that could be produced by relatively low levels of exposure might have little or no impact
on population or community performance because of natural
selection [B10, C4, M2, P3, T5] and the convergence ofgenetic information among adjacent populations [R1, T5].
187. The Committee also noted that the effects of radiation
exposure at the population and community levels were manifest as a combination of direct changes due to radiation damage and indirect responses to the direct changes. This
seriously complicated the interpretation of the effects ofradiation exposure on organisms in the natural environment.
The wide range of radiosensitivities of the organisms thatmake up most natural communities creates a situation where,
if doses are such that the sensitive species, but not the moreresistant ones, are affected, the latter might gain a significant
competitive advantage and increase in abundance or vigour.

262

UNSCEAR 2008 REPORT: VOLUME IIThis could erroneously be interpreted as a hormetic response;such a response might not however be produced if the resistant species alone were irradiated. This is but one of many
examples of indirect response to the direct effects of ­radiation
exposure.
188. Because of the compensation and adjustment possible
in animal species, the Committee considered that it isunlikely that radiation exposures causing only minor effects
on the most exposed individual would have significant
effects on the population. Reproductive changes are a moresensitive indicator of the effects of radiation exposure thanmortality, and mammals are the most sensitive animal organisms. On this basis, chronic dose rates of less than 100 μGy/h
to the most highly exposed individuals would be unlikely tohave significant effects on most terrestrial animal communities. The Committee also concluded that maximum dose
rates of 400 μGy/h to a small proportion of the individuals inaquatic populations of organisms would not have any detrimental effect at the population level. These conclusions
referred to the effects of low-LET radiation exposure. Wherea significant part of the incremental radiation exposure
comes from high-LET radiation (alpha particles), the Committee considered that it is necessary to take account of thedifferent RBEs.
D.

Effects of major accidents

189. The UNSCEAR 1996 Report [U4] discusses theeffects of two accidents in the former Soviet Union (at­Chernobyl and at Mayak in the south-eastern Urals) leading
to major releases of radioactive material into the environment [A28, G19, I23, I24, K1, K22, K23, N9, S29, S34, S40,
T4, T27]. These accidents provided opportunities to observe
radiation-related changes in plant and animal communities.
The Committee noted however that any major accident islikely to be unique in terms of the quantity and compositionof the radioactive material released, the time course of therelease, the dispersal and deposition patterns, which are governed by local and regional meteorological or hydrologicalconditions, and the biochemical and geochemical characterof the areas subject to contamination. Where long-lived
radio­nuclides are released, biochemical and geochemical
processes would determine the long-term behaviour andredistribution of the radionuclides in the environment. Given
this multiplicity of factors, any major nuclear accident would
be expected to yield new radioecological information. However, the primary concern following an accidental release ofradionuclides is to ensure that the radiation risks to humanpopulations are controlled and minimized. Consequently,
the only environmental information likely to be collected isthat which is immediately necessary to meet this objective.
Such information is unlikely to be sufficient for the purposesof developing a complete radioecological description of thesituation. The larger the incident and the greater its potential
human impact, the more limited would be the resources
available to collect radioecological information, particularlyin the early phase following the accident.

190. In particular, the data required to develop estimatesof the radiation exposure of wild organisms (i.e. the space
and time-dependent variations of the radionuclide concentrations, especially of the short-lived radionuclides bothwithin the organisms and in their external environment
immediately following an accident) would not be known.
These variations would result in substantial intra-species
and inter-­species inhomogeneities in exposure and would
pose considerable difficulties for establishing a clear andreliable relationship between cause (the accumulated radiation dose) and any observed effect. In practice, it is likelythat estimates of the dose rates in the early period following
the release would be calculated subsequently from theobserved distribution of deposition densities of the longerlived radionuclides, from a knowledge of the relative quantities of the radionuclides released, and using models ofradionuclide behaviour in the environment. Such dose-rate
estimates are inevitably imprecise and could be subject tosignificant systematic error.
191. The highly variable habits and target geometries of
the wild organisms are additional complicating factors.
These range, for example, from soil bacteria to single-celledalgae and protozoa, and include a wide variety of terrestrial
and aquatic invertebrates, mammals (ranging from shrews todeer) and large deciduous or evergreen trees. Plants provide
a very high surface area to mass ratio (compared with animals) for deposition/adsorption of a radioactive aerosol.
Because the leaves, flowers and terminal buds of plants are
responsible for energy absorption, growth and reproduction,a coincidence arises between radionuclide accumulation(and hence radiation dose) and potential radiosensitivity.
Other examples of coincidence are the surface litter layer
and its populations of invertebrate decomposers in terrestrial
environments, and surface sediments and benthic organisms
in aquatic systems.
192. Depending on the quantities of specific radio­
nuclides released following an accident, the radiation
exposures might range from low (a few multiples of thenatural background) to high (absorbed doses greater than
1 Gy). Different phases of biological response to thehigher total doses might be distinguished. Initially, and, inparticular if short-lived radionuclides made up a significant proportion of the release, there might be an acutephase in which total doses sufficient to produce immediate
or relatively early detectable biological responses areaccumulated. In the intermediate phase, dose rates would
decrease owing to the decay of the short-lived radio­
nuclides and possibly, but not necessarily, owing to theredistribution of the longer-lived radionuclides by naturalprocesses. Even in this phase, the slower accumulation ofradiation dose might still result in total integrated doses
sufficient to prevent recovery of organisms damaged in theinitial phase or lead to the appearance of medium-term
damage. In the long-term phase, post-irradiation recovery(and adaptation) becomes apparent, provided that the initial and medium-term damage had not been large enoughto radically alter the population or community structure.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

III.

263

Summary of dose–effects data from the Chernobyl accident

193. A great deal of scientific information concerning theeffects of exposure to ionizing radiation has been developed
from studies of non-human biota in the area surrounding thesite of the Chernobyl accident. The follow-up studies provided the main source of new information on the effects ofradiation exposure on non-human biota since the UNSCEAR
1996 Report [U4]. This area has a temperate climate andflourishing flora and fauna. Much of the new information,
originally reported in Russian, has been summarized in areport prepared for the Committee [A5] and by the work of theChernobyl Forum [E8]. The following discussion of radia­tionlevels and effects on biota observed in the region around theChernobyl nuclear power plant is based on information­presented in reference [E8] and in other recent reviews [G26].
A.

Radiation exposure

194. The Chernobyl Forum Expert Group on Environment(EGE) [E8] noted that the effects of the Chernobyl accident
should be studied within specific time periods. Three distinct
phases of radiation exposure have been identified in the area
local to the accident [U4]. In the first 20 days, radiation
exposures were essentially acute because of the large quantities of short-lived radionuclides present in the passing cloud(99Mo, 132Te/I, 133Xe, 131I and 140Ba/La). Most of these shortlived, highly radioactive nuclides deposited onto plant andground surfaces, resulting in gamma radiation dose rates of
up to about 20 Gy/d. However, for surface tissues and small
biological targets (e.g. mature needles and the growing budsof pine trees) there was a considerable additional dose rate
due to the beta radiation from the deposited radionuclides.
High doses to the thyroids of vertebrate animals also
occurred during the first days/weeks following the accident
owing to the inhalation and ingestion of radioactive isotopesof iodine and their radioactive precursors.
195. The second phase of radiation exposure extended
through the summer and autumn of 1986, during which time
the short-lived radionuclides decayed and the longer-lived
radionuclides were transported to different components ofthe environment by physical, chemical and biological pro­
cesses. Dominant transportation processes included raininduced transfer of radionuclides from plant surfaces onto
soil, and bioaccumulation through plant tissues. Dose rates
at the soil surface declined to much less than 10% of theinitial values owing to radioactive decay of the short-lived
radionuclides, but damaging total doses were still accumulated. Approximately 80% of the total radiation dose accumulated by plants and animals was received within 3 monthsof the accident, and over 95% of this was due to beta radiation exposure [E8]. Measurements made with thermoluminescent dosimeters on the soil surface at sites within the
30‑km exclusion zone indicated that the ratio of beta to
gamma dose was about 26:1, (i.e. 96% of the total dose wasdue to beta radiation exposure) [P18].

196. The EGE [E8] also defined a third (and continuing)phase of radiation exposure with chronic dose rates less than
1% of the initial values and derived mainly from 137Cs. With
time, the decay of the short-lived radionuclides and themigration of much of the remaining 137Cs into the soil meantthat the contributions to the total radiation exposure from thebeta and gamma radiations tended to become more comparable. Reference [E8] noted that the balance depended on the
degree of bioaccumulation of 137Cs in organisms and the
behaviour of the organism in relation to the main source of
external exposure resulting from the 137Cs in the soil.
B. Effects of radiation exposure on plants
197. The report of the EGE was a great advance on previous publications describing the follow-up work on theeffects of the Chernobyl accident. In particular, the reportgave considerable attention to evaluating the dosimetry of,and consolidating the information on the effects on nonhuman biota. Thus, given both the greatly improved qualityof the data and the comprehensive nature of the evaluation
provided by the EGE, much of the following discussion isadapted from reference [E8].
198. Doses received by plants arising from the depositedradionuclides resulting from the Chernobyl accident were
influenced by the physical properties of the various radio­
nuclides (i.e. their half-lives, radiation emissions, etc.), thephysiological stage of the plant species at the time of theaccident, and the different species-dependent propensities totake up radionuclides into critical plant tissues [E8]. The
occurrence of the accident in late April 1986 was thought tohave enhanced the damaging effects of the deposition
because it coincided with the period of accelerated growth
and reproduction of plants.
199. The deposition of beta-emitting radionuclides onto
critical plant tissues resulted in their having received a significantly larger dose than animals living in the same environment [P18, P19]. According to reference [G9], large
apparent inconsistencies in the dose–response observations
occurred when the beta‑irradiation component was not
appropriately taken into account.
200. Within the 30‑km zone around the Chernobyl plant,
the doses to plants associated with the deposition of total beta
activity (0.7–3.9 GBq/m2) were sufficient to cause short-term
sterility and reduction in productivity of some species [P19].
By August 1986, crops that had been sown prior to the accident began to emerge. Growth and development problems
were observed in plants in fields with deposition densities of
0.1–2.6 GBq/m2 of total beta activity, and with estimateddose rates initially received by the plants having reached
300 mGy/d. Spot necroses on leaves, withered tips of leaves,
inhibition of photosynthesis, transpiration and metabolite

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UNSCEAR 2008 REPORT: VOLUME II

synthesis were detected, as well as an increased incidence ofchromosome aberrations in meristem cells [S22]. The frequency of various anomalies in winter wheat exceeded 40%
in 1986–1987, with some abnormalities apparent for several
years afterwards [G12].
201. Coniferous trees were already known to be among themore radiosensitive plants, and the pine forests, 1.5–2 km
west of the Chernobyl nuclear power plant, received sufficient doses, more than 80 Gy, at dose rates that exceeded
20 Gy/d, to cause mortality [T18]. The first signs of radiation
injury were yellowing and needle death in pine trees in close
proximity to the nuclear power plant and appeared during
the summer of 1986. The colour of the dead pine stands
resulted in the forest being referred to as the “red forest”.
202. Tikhomirov and Shcheglov [T18] and Arkhipov et al.
[A11] found that mortality rate, reproduction anomalies, standviability, and re-establishment of pine-tree canopies weredependent on absorbed dose. Acute irradiation of Pinus silvestris at doses of 0.5 Gy caused detectable cytogenetic damage;at doses of more than 1 Gy, growth rates were reduced andmorphological damage occurred; and, at more than 2 Gy, thereproductive abilities of trees were altered. Doses of less than
0.1 Gy did not cause any visible damage to the trees. Table 23
shows the variation in activity concentration and dose amongpine trees within the 30‑km zone. The radiosensitivity of
spruce trees was observed to be greater than that of pines. At
absorbed doses as low as 0.7–1 Gy, spruce trees had ­malformed
needles, buds and shoot growth [K1].
203. About 90% of the absorbed dose to critical parts of thetrees was due to beta irradiation from the deposited radio­
nuclides with the remaining 10% from gamma irradiation.
Table 22 summarizes the external gamma dose rates and theinternal radionuclide concentrations in the conifers around theChernobyl plant. By 1987, recovery processes were evident in
the surviving tree canopies and the forests were re-­establishingthemselves where the trees had perished [A11]. In the decimated pine stands, a sudden invasion of pests occurred thatlater spread to adjoining areas. Grassland, with a slow invasion of self-seeding deciduous trees, has now replaced thedeceased pine stands. Four distinct zones of radiation-induced
damage to conifers were discernable (table 23).

Table 22. Activity concentration in needles of coniferous trees and estimated external gamma dose rates in October 1987 as
a function of distance from the Chernobyl nuclear power plant
For azimuth 205 to 260 degrees (adapted from reference [K12])
Distance from NPP(km)

External exposure rate
(μGy/h)a

Accumulated external dose(mGy)a

2

2 500

4
16

Activity concentration in needles (kBq/kg)
144

Ce

106

Ru

95

Zr

95

Nb

134

Cs

137

Cs

126 000

13 400

4 100

800

1 500

1 500

4 100

120

5 000

150

60

8

15

17

72

0.4

14

1.5

0.6

0.1

0.17

0.18

0.55

a Based on gamma radiation levels at 1 m height above the soil surface. The values given in the original reference were in mR/h and have been converted assuming 1 mR/h isequivalent to 10 μGy/h.

Table 23. Zones and corresponding damage to coniferous forest in the area around the Chernobyl nuclear power plant (fromreference [K1])
Zone and classification

External gamma dose
(Gy)

Exposure rate
(μGy/h)aInternal dose to needles(Gy)over 80–100

over 5 000

over 100Sublethal (38 km2)
Death of most growth points
Partial death of coniferous trees
Morphological changes to deciduous trees

10–20

2 000–5 000

50–100Medium damage (120 km2)
Suppressed reproductive ability
Dried needles, morphological changes

4–5

500–2 000

20–50

Minor damage
Disturbances in growth, reproduction and morphology
of coniferous trees

0.5–1.2<200<10Conifer death (4 km2)
Complete death of pines
Partial damage to deciduous trees

a The values given in the original reference were in mR/h and have been converted assuming 1 mR/h is equivalent to 10 μGy/h.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

C.

Effects of radiation exposure on soil invertebrates

265205. A fourfold reduction in earthworm numbers wasfound in arable soils, but no catastrophic mortality in anygroup of soil invertebrates was observed. The dose to invertebrates in forest litter was 3–10 fold higher than that tothose residing in unploughed surface soil since the radio­
nuclides deposited on the surface had not migrated downwards. The result was no reduction in the numbers of soil
invertebrates below a depth of 5 cm in the soil as they wereshielded by the overlying soil [K11].

204. Between 60% and 90% of the initial fallout of radionuclides was captured by the forest canopy and other plants[E8]; however, within weeks to a few months, the processesof wash-off by rain and leaf fall removed most of the initialdeposition to the litter and soil layers, where soil and litter
invertebrates were exposed to high radiation levels for protracted time periods. The timing of the accident coincidedwith the most radiosensitive life stages of the soil invertebrates: reproduction and moulting following their winterdormancy [T18]. Within two months after the accident, thenumbers of invertebrates in the litter layer of forests 3–7 kmfrom the nuclear power plant were reduced by a factor of
30 [K11], and reproduction was strongly impacted (larvaeand nymphs were absent). These effects corresponded todoses of approximately 30 Gy (estimated from TLDs
placed in the soil) resulting in mortality of eggs and earlylife stages, as well as reproductive failure in adults.
­However, within a year of the accident, reproduction of
invertebrates in the forest litter resumed, due, in part, to themigration of invertebrates from less contaminated sites.
After 2–3 years, the ratio of young to adult invertebrates in
the litter layer, as well as the total mass of invertebrates perunit area, were no different from those in control sites;
however, species diversity remained markedly lower [K11].
As noted in the report of the EGE [E8], this is importantsince the diversity of invertebrate species within the soil
facilitates an analysis of the community-level effects ofradiation exposure (i.e. changes in species composition andabundance). For example, only five species of invertebrates
were found in 10 soil cores taken from pine stands in July
1986, 3 km from the Chernobyl nuclear power plant, compared to 23 species at a control site 70 km away. The meandensity of litter fauna was reduced from 104 individuals
per 225 cm2 core at the control location to 2.2 at the 3‑km
site. Six species were found in all 10 cores taken from thecontrol site, whereas no one species was found in all
10 cores from the 3‑km location [K13]. The number of
invertebrate species found in the heavily contaminated sites
was only half that of controls in 1993, and complete species diversity did not recover until 1995, almost 10 years
after the accident [K11].

206. Although, the researchers were unclear if sterility of
invertebrates occurred in the heavily contaminated sites aroundthe Chernobyl nuclear power plant [K11], the 30 Gy cumulative dose reported in the field studies was within the range ofexperimental doses used to control pest insects by external irradiation. A recent review indicated that most insect, mite andtick families require a sterilization dose of less than 200 Gy[B40], although the sterilization dose for some insects andrelated arthropods is much lower than this and varies widely.
As was found for plants [S2], the radiosensitivity of insects is
related to the average interphase nuclear volume [B40].
D. Effects of radiation exposure on farm animals
207. Ruminants, both domestic (cattle, goats and sheep)
and wild (elk and deer), generally receive relatively highdoses in radioactively contaminated environments, because
they consume large amounts of vegetation, and many radionuclides accumulate in their bodies. For example, a single
cow consumes about 75 kg of fresh grass each day.
208. In the period shortly after the accident, domestic livestock within the 30‑km zone were exposed to high levels ofradioactive iodine (131I and 133I with half-lives of 8 days and21 hours, respectively). This resulted in significant internaland external doses due to beta and gamma radiation exposure (table 24). A dose of about 76 Gy is sufficient to cause
harm to the thyroid gland [B23]. Soils of Ukraine and­Belarus are naturally low in stable iodine, cobalt and manganese. In conditions of endemic deficiency of stable iodine,
the transfer of radioactive iodine from blood to the thyroid
gland may be 2–3 times greater than normal [P19]. These
conditions accentuated the consequences of the accident.

Table 24. Doses to cattle that stayed in the 30‑km zone around the Chernobyl plant from 26 April to 3 May 1986 [K12]Distance from nuclear
power plant (km)Surface activity(108 Bq/m2)

3

Absorbed dose (Gy)Thyroid

GI tract

Whole body internal

8.4

300

2.5

1.4

10

6.1

230

1.8

1.0

14

3.5

260

1.0

0.6

12

2.4

180

0.7

0.4

35

1.2

90

0.4

0.2

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209. Depressed thyroid function in cattle was related to thedose received (69% and 82% reductions in function withthyroid doses of 50 Gy and 280 Gy, respectively). The concentration of thyroid hormones in the blood of animals was
lower than the physiological norm during the whole lactation
period. Radiation damage to the thyroid gland was confirmed by histological studies (i.e. hyperplasia of connective
tissue and sometimes adipose tissue, vascular hyperaemia
and necrosis of epithelium). Animals with practically no thyroid tissue were observed in Ukraine. Disruptions of the hormonal status in calves born to cows with irradiated thyroid
glands were especially pronounced [A12]. Similar effects
were observed in cattle evacuated from the Belarusian­portion of the 30‑km zone [I18].
210. Although most livestock were evacuated from thearea after the accident, several hundred cattle were maintained in the more contaminated areas for a 2–4 month
period. By autumn 1986, some of these animals had died;others showed impaired immune responses, lowered bodytemperatures and cardiovascular disorders. Hypothyroidism
lasted until 1989, and may have been responsible for reproductive failures in animals that received thyroid doses ofmore than 180 Gy [I18]. Offspring of highly exposed cows
had reduced weight, reduced daily weight gains, and signsof dwarfism. Reproduction returned to normal in the springof 1989. Haematological parameters were normal for animals kept in areas with 137Cs deposition densities of 0.2–
1.4 MBq/m2 (5–40 Ci/km2) [A12].
211. No increase in the rates of birth defects were detected
above background levels at annual doses below about
0.05 Gy [P17].
E. Effects of radiation exposure onother terrestrial animals
212. Surveys and autopsies of wildlife and of abandoned
domestic animals that remained within 10 km of the­Chernobyl nuclear power plant were conducted four months
after the accident. [K11]. Fifty species of birds were identified, including some rare ones; all appeared normal inappearance and behaviour. No dead birds were found. Swallows and house sparrows were found to be producing progeny that also appeared normal. Forty-five species ofmammals from six orders were observed and no unusual
appearances or ­behaviours were noted.
213. In a review of thirty-three studies of the biologicalconsequences of the Chernobyl accident, Møller and­Mousseau [M19] commented on various increases in mutations and cytogenetic abnormalities attributed to elevatedradiation levels. They noted that the fitness consequencesof such increases were largely unknown and cited a studyof differences in phenotypes in barn swallows from near
Chernobyl and those from relatively uncontaminated control areas [M18]. The authors suggested that mutations
with slightly negative fitness effects could have been
exported from the contaminated zones and potentiallyaffected unexposed populations. In an exchange of views,
Møller et al. [M17, M20] challenged the hypothesis ofSmith [S26] that the impacts on barn swallows arose fromfactors other than radiation exposure, namely the change inhabitat and wildlife community arising from changes inagricultural practices resulting from efforts to reduce thespread of radioactively contaminated food. Smith however
noted that the most contaminated sites were located within
abandoned lands, which had large differences in both land
use and ecology from the control sites.
214. Some wildlife and domestic animals were shot andautopsied in August and September 1986. Dogs and­chickens showed signs of chronic radiation syndrome(reduced body mass; reduced fat reserves; increased massof lymph nodes, liver and spleen; haematomas present inliver and spleen; and thickening of the lining of the lower
intestine). No eggs were found in the nests of chickens,nor in their ovaries.
215. During the autumn of 1986, the number of smallrodents on highly contaminated research plots decreased bya factor of 2–10. Estimates of absorbed doses during the first
five months after the accident ranged from 12–110 Gy for
gamma and 580–4,500 Gy for beta irradiation. By the springof 1987, the numbers of animals were recovering, mainly
due to immigration from less affected areas. In 1986 and1987, the percentage of pre-implantation deaths in rodents in
the highly contaminated areas was 2–3 fold greater than thatin the controls. Resorption of embryos also increased markedly in rodents from the impacted areas; however, thenumber of progeny per female did not differ from that of thecontrols [T16].
F. Effects of radiation exposure on aquatic organisms
216. Cooling water for the Chernobyl nuclear power plant
was obtained from a 21.7 km2 man-made reservoir located tothe south-east of the plant site. The cooling reservoir becameheavily contaminated following the accident with a total
activity of over 6.5 ± 2.7 PBq of a mixture of radionuclides(alpha and beta emitters) in the water and sediments [K14].
Aquatic organisms were exposed to external radiation fromthe radionuclides in the water, contaminated bottom sediments, and aquatic plants. Internal irradiation occurred asorganisms took up radionuclides in their food and water or
inadvertently consumed contaminated sediments. The resultant doses to aquatic biota over the first 60 days following theaccident are depicted in figure XI.

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267

Figure XI. The dynamics of absorbed dose rate to organisms within the Chernobyl nuclear power plant cooling pond during
the first 60 days following the accident
Data are model results based on concentrations of radionuclides in the water column and lake sediments (adapted from reference [K12])
1 000

Benthicorganisms

Macroalgae

mGy/d

100

Fish

10

Zooplankton

Phytoplankton
1
0

10

20

30

40

50

60

DAYS POST ACCIDENT

217. The maximum dose rates to aquatic organisms(excluding fish) were reported in the first two weeks after
the accident, when short-lived radionuclides (primarily
131I) contributed 60–80% of the dose. During the second
week, the contribution of short-lived radionuclides to thedoses of aquatic organisms decreased by a factor of two.
Maximum dose rates to fish were delayed (see figure XI)
owing to the time required for their food webs to becomecontaminated with longer-lived radionuclides (largely
134,137
Cs, 144Ce/Pr, 106Ru/Rh and 90Sr/Y). The dose rates tofish depended on their trophic positions. Non-predatory
fish (carp, goldfish and bleak) incurred estimated peakdose rates of 3 mGy/d due to internal exposure in 1986,
followed by significant reductions in 1987. Dose rates topredatory fish (perch), however, increased in 1987 anddid not start to decline until 1988 [K12]. Accumulated
doses were greatest for the first generation of fish born in1986 and 1987. Bottom-dwelling fish (goldfish, silver
bream, bream and carp) that were significantly irradiatedby the bottom sediments accumulated total doses ofapproximately 10 Gy.

218. The reproductive capacity of young silver carp was
analysed in 1990 [R10]. The fish were in live boxes within
the cooling pond at the time of the accident. By 1988, the fish
had reached sexual maturity. Over the entire post-­accident
period, they received a dose of 7–8 Gy. Biochemical analysesof muscles, liver and gonads indicated no difference from thecontrols. The amount of fertilized spawn was 94%; 11% of
the developing spawn was abnormal. Female fertility was
40% higher than that of the controls, but 8% of the irradiatedsires were sterile. The level of fluctuating asymmetry in offspring did not differ from that of the controls, although thelevel of cytogenetic damage (22.7%) significantly exceededthat of controls (5–7%). In contrast, Pechkurenkov [P20]reported that the number of cells with chromosome aberrations in 1986–1987 in carp, bream flat and silver carp waswithin the norm. It is worth noting that the cooling pond was
subjected not only to radioactive contamination, but also tochemical pollution. Table 25 provides a summary of therecent reviews of the chronic effects of ionizing radiation
exposure on the reproduction in fish. The Chernobyl accident
data are included.

Table 25. Chronic effects of exposure to ionizing radiation on reproduction in fish
Derived from the FASSET database [C11]
Dose rate(μGy/h)Dose rate(mGy/d)Reproductive effects

0–99

0–2.4

Background dose group, normal cell types, normal damage and normal mortality observed

100–199

2.4–4.8

No data available

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UNSCEAR 2008 REPORT: VOLUME II

Dose rate(μGy/h)Dose rate(mGy/d)Reproductive effects

200–499

4.8–12

Reduced spermatogonia and sperm in tissues

500–999

12–24

Delayed spawning, reduction in testis mass

1 000–1 999

24–48

Mean lifetime fecundity decreased, early onset of infertility
Reduced number of viable offspring
Increased number of embryos with abnormalities

2 000–4 999

48–120

Increased number of smolts in which sex was undifferentiated
Increased brood size reported
Increased mortality of embryos

5 000–9 999

120–240

Reduction in number of young fish surviving to 1 month of age
Increased vertebral abnormalities
Inter-brood time tends to decrease with increasing dose rateSignificant reduction in neonatal survival
Sterility in adult fish

>10 000>240

Destruction of germ cells within 50 days in medaka fish
High mortality of fry, germ cells not evident
Significant decrease in number of male salmon returning to spawn; after 4 years, female salmon had
significantly reduced fecundity

G. Genetic effects in animals and plants
219. High quality data on the incidence of radiogenic
mutations in plants and animals as a result of the accident are
relatively sparse. An increased mutation level was apparent
in 1987 in the form of various morphological abnormalities
in Canada fleabane, common yarrow and mouse millet.
Examples of abnormalities included: unusual branching ofstems; doubling the number of racemes; abnormal colour
and size of leaves and flowers; and development of “witch’s
broom” in pine trees. Similar effects within 5 km of thenuclear power plant also appeared in deciduous trees (leafgigantism, and changes in leaf shapes). Morphologicalchanges were observed at an initial gamma dose rate of 4.2–
6.3 mGy/d. At a dose rate of 15.8–31.5 mGy/d, enhancementof vegetative reproduction (in heather) and gigantism ofsome plant species were observed [A11, K10, T17, T18].
220. Cytogenetic analysis of cells from the root meristem
of winter rye and wheat germ of the 1986 harvest demonstrated a dose dependency in the number of aberrant cells. A
significant excess over the control level of aberrations wasobserved at an absorbed dose of 3.1 Gy. Inhibition of mitotic
activity occurred at a dose of 1.3 Gy, and germination was
reduced at a dose of 12 Gy [G10]. The analysis of three successive generations of winter rye and wheat on the most contaminated plots revealed that the rates of aberrant cells in theintercalary meristem in the second and third generations
were higher than in the first.
221. From 1986–1992, mutation dynamics were studied in
populations of Arabidopsis thaliana Heynh. (L.) within the

30‑km zone [A10]. On all study plots during the first
2–3 years after the accident, Arabidopsis populations exhibited an increased mutation burden. In later years, the level oflethal mutations declined; nevertheless the mutation rate in1992 was still 4–8 times higher than the spontaneous level.
The dose dependence of the mutation rate was best approximated by a power function with an exponent value of lessthan one.
222. Zainullin et al. [Z2] observed elevated levels of sexlinked recessive lethal mutations in natural Drosophila melanogaster populations living under conditions of increased
chronic exposure to radiation resulting from the Chernobyl
accident. The mutation levels were increased during 1986–
1987 in flies inhabiting the more contaminated areas withinitial exposure rates of 2 mGy/h (expressed as 200 mR/h in
the original text) and more. During the subsequent two years,
mutation frequencies gradually returned to normal.
223. Shevchenko et al. [S21] and Pomerantseva et al. [P16]reported studies of adverse genetic effects in wild mice.
These involved mice caught during 1986–1991 within a
30‑km radius of the Chernobyl nuclear power plant with different levels of gamma radiation exposure and, during 1992–
1993, on a site in the Bryansk Oblast, Russia. The estimatedtotal doses of gamma and beta radiation varied widely; thedose rates reached 3–4 Gy per month in 1986–1987. One
endpoint was dominant lethality, measured by embryo mortality in the offspring of wild male mice mated with unexposed female laboratory mice. The dominant lethality rate
was elevated for a period of a few weeks following capturein mice sampled at the most contaminated site. At dose rates

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

of about 2 mGy/h, 2 of 122 captured males produced no offspring and were assumed to be sterile. The remainder showeda period of temporary infertility and reduced testis mass.
Fertility and testis mass, however, recovered with time after
capture.
224. The frequencies of reciprocal translocations in mouse
spermatocytes were consistent with previous studies. A
dose-rate-dependent incidence of increased reciprocal translocations (scored in spermatocytes at meiotic metaphase I)
was observed in all collected mice. The frequency of miceharbouring recessive lethal mutations decreased with timeafter the accident [P16]. Radiation-related gene mutation isunlikely to have any adverse effect on populations, at thedose rates that prevail now.
225. Increasing sophistication in the technologies for thedetection of molecular and chromosomal damage haveallowed researchers on the genetic consequences of theChernobyl accident to examine endpoints not previously
considered [E8]. Most prominent, and controversial, is thetechnique involving the measurement of mutation frequencies in repeat DNA sequences termed “minisatellite loci” or“expanded simple tandem repeats” (ESTR). These are repeat
DNA sequences that are distributed throughout the germline
and have a high background (spontaneous) mutation rate.
Presently, ESTRs are considered to have no function,although this is a matter of much interest and discussion[B33, C10, I9]. Minisatellite mutations have only rarely
been associated with recognizable genetic disease.
226. Although laboratory examination of mutations inmouse ESTR loci show clear evidence of a mutational dose
response [D4, F16], the EGE was not aware of any convin­cing data on elevated levels of minisatellite mutations inplants or animals residing in the contaminated areas having
been published in peer-reviewed scientific literature [E8]. In
general, quantitative interpretation of the ESTR data is difficult because of conflicting findings, their weak association
with genetic disease, dosimetric uncertainties and methodological problems [C10]. This is an area of science that
requires additional research.

269

occurred within this zone. As a result of the elevated radiation
doses associated with the contamination, human activities
such as agriculture, forestry, hunting and fishing within the
exclusion zone were stopped [E8]. After the accident, thefields continued to yield agricultural produce for a number ofyears and, in the absence of active management in the areasthat had been evacuated, many animal species, especiallyrodents and wild boars, consumed the abandoned cereal
crops, potatoes and grasses as an additional source of forage[E8]. This was advantageous to these animal species and,along with the special reserve regulations established in the
exclusion zone (e.g. a ban on hunting), tended to compensate
for the adverse biological effects of radiation exposure andpromoted an increase in the populations of wild animals,
including game mammals (wild boars, roe deer, red deer, elk,
wolves, foxes, hares, beaver, etc.) and bird species (black
grouse, ducks, etc.) [G8, S23]. In addition, the ­Chernobyl
exclusion zone has become a breeding area of white-tailed
eagles, spotted eagles, eagle owls, cranes and black storks[G9].
229. The high dose rates from ionizing radiation during thefirst few weeks following the Chernobyl accident affected
the balanced community by killing sensitive individuals,
altering reproduction rates, destroying some resources (e.g.
pine stands), making other resources more available (e.g.
soil water), and opening niches for immigration of new andsometimes negative organisms (e.g. negative entofauna).
These components and more, were interwoven in a complex
web of action and reaction that altered populations and­communities of organisms [E8].
230. Overall, the EGE [E8, H25] arrived at a number ofgeneral observations from their evaluation of the Chernobyl
data, namely that:– Radiation from radionuclides released as a resultof the Chernobyl accident caused numerous acute
adverse effects on the biota located in the areas ofhighest exposure (i.e. up to a distance of a few tensof kilometres from the release point). Beyond theexclusion zone, no acute radiation-induced effects
on biota have been reported;

227. According to the EGE [E8], prior to the accident,much of the area around the Chernobyl nuclear power plant
was covered by 30–40 year old pine stands that, from a successional standpoint, represented mature, stable ecosystems.
The high dose rates due to ionizing radiation exposure during the first few weeks following the accident altered the balance in the community and opened niches for immigrationof new individuals.

– The environmental response to the increased radiation exposure incurred as a result of the Chernobyl
accident was a complex interaction among radiation dose, dose rate and its temporal and spatial
variations, as well as the radiosensitivities of thedifferent taxons. Both individual and population
effects caused by radiation-induced cell death
were observed in plants and animals and included
increased mortality of coniferous plants, soil invertebrates and mammals; reproductive losses inplants and animals; and chronic radiation sickness
in animals (mammals, birds, etc.);

228. The ecological conditions within the 30‑km ­Chernobyl
exclusion zone arose from the complex interaction of anumber of factors. The highest level of contamination– No adverse radiation-induced effects were reported
in plants and animals exposed to a cumulative doseof less than 0.3 Gy during the first month after theaccident (i.e. <10 mGy/d, on average); andH.

Overall observations on the effectsof the Chernobyl accident

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UNSCEAR 2008 REPORT: VOLUME II– Following the natural reduction of exposure levels
due to radionuclide decay and migration, populations have been recovering from acute radiation
effects. By the next growing season following theaccident, the population viability of plants andanimals substantially recovered as a result of the
combined effects of reproduction and immigration.
A few years were needed for recovery from the
major radiation-induced adverse effects on plants
and animals.

and indicated that the minimum dose rate at which morphological changes have been seen in the Chernobyl zone wasabout 1.2 mGy/d. The authors also indicated that this dose
rate is about nine times lower than the reference dose rate
provided in reference [U4] but suggested that such discrepancies can be explained by the use of generic reference dose
rates for all terrestrial plants rather than for specific plants.
For herbaceous plants, they suggested a reference dose rate ofabout 8.2 mGy/d [F17] which is comparable to the value suggested in reference [U4]. For cattle, they suggested a reference dose rate of about 1.6 mGy/d based on data given inreferences [C16, S36] but go on to indicate that radiation
harm to farm animals in the Chernobyl zone was more related
to damage to the thyroid from internally deposited radio­
nuclides. Based on the assumption that impairment of reproduction usually occurs at doses about one order of magnitude
below the LD50 of about 0.8 Gy and on observed reductionsin the numbers of invertebrates, the authors [F17] suggested
a reference dose rate of about 2.5 mGy/d. Finally, for aquatic
systems, the authors [F17] suggested that fish are generally
more radiosensitive than plankton and zoobenthos and­proposed a reference dose rate of about 1.6 mGy/d.

231. Fesenko et al. have compared the relative radiologicalimpact on people and non-human biota arising from the
Chernobyl accident [F17]. They reviewed the data on reference dose rates for non-human biota (which they refer to as
critical exposure doses or CDVb below which an effect would
not be expected). The authors adopted the commonly used
endpoints of early mortality, morbidity, reduced reproductive
success and deleterious genetic effects. Their values of CDVb
for non-human biota near Chernobyl are summarized intable 26. They noted that coniferous trees were known to beamong the most radiosensitive components of the biosphere

Table 26. Review of CDVb for non-human species inhabiting the study area
(adapted from reference [F17])
Non-human species

CDVb (mGy/d)cited in [F17]

Literature data

Terrestrial ecosystems
Coniferous trees (pine)

1.1

1.1 [S35], 2.4 [C16], 10 [U4]Herbaceous plants (meadow grasses)

8.2

1.1 [S35, S36], 2.4 [C16], 10 [U4]Herbaceous plants (cereals)

8.2

1.1 [S35, S36], 2.4 [C16], 10 [U4]Cattle1.6 (137a)

1.1 [S36], 2.5 [C16]

Mouse-like rodents

1.1

0.1 [S35], 0.2 [S36], 1 [C16], 1 [U4], 2.7 [B31]

Soil invertebrates

2.5

1.1 [S35, S36], 2.4 [C16], 5.5 [B31]

Aquatic ecosystems
Phytoplankton

8.2

2.4 [C16], 2.7 [B31]

Zooplankton

6.8

2.4 [C16], 2.7 [B31]

Zoobenthos

2.5

1.6 [C16], 5.5 [B31]

Fish

1.6

0.3 [S35], 0.5 [C16], 0.5 [B31], 10 [U26]a Dose to the thyroid.

232. Another report provided a comprehensive evaluationof the effects of radiation exposure resulting from the Chernobyl accident on non-human biota along with corresponding dosimetry information [G26]. In total, 250 referenceswere evaluated. Of these, some 79 papers were considered tohave adequate information on environmental contaminationand doses to biota. The review focussed on the assessment of

the effects of radiation exposure on plants and animal populations inhabiting the contaminated areas around Chernobyl
at the time of, and following, the accident [G26]. As
described earlier, the radiation doses associated with the firstphase following the Chernobyl accident was a period ofshort-term quite high radiation dose rates followed by aperiod with a gradual decline in dose rate. The most severeANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

environmental effects were associated with the high dose
rates. Effects of radiation exposure were seen in both naturaland agricultural systems. The authors noted that the effects
depended on the radiosensitivity of the dominant species andobserved that coniferous trees were one of the most sensitiveplant species and mammals were the most radiosensitive animal species [G26]. To date, reference [G26] provides themost comprehensive evaluation of observations of the effectsof the Chernobyl accident on non-human biota. The key
observations from the review are summarized in table 27,
which shows various effects on non-human biota around
Chernobyl and the corresponding doses below which such
effects were not observed.

Forum [E8]. Table 27 provides a summary of the informationon the effects and associated doses and dose rates from studies of non-human biota around the Chernobyl nuclear power
plant. However, given the importance of this topic, a few
additional comments are appropriate. The available information indicates that the forest close to the Chernobyl power
plant captured much of the radioactive dust following theaccident, reducing the spread of radioactive material outside
the 10‑km zone [A11]. The dose rate within the 10‑km zone
showed an exponential decay, with the majority of the total
dose absorbed by the environment within the first month[A11, K20, S30]. Thus, the Committee has assumed, in table
27, that most (80% or so) of the dose would have been delivered in (about) the first month following the accident. Where
appropriate for comparison purposes, a notional daily dose
rate was derived by dividing the reported doses by 30.

233. The reliability of the estimated doses arising from the
Chernobyl accident has been examined by the Chernobyl

Table 27.

271

Effects on populations of non-human biota around the Chernobyl power plant [G26]
Species effect

Estimated minimum doses (or dose rates)
at which effect was observed

Estimated maximum doses (or dose rates)
at which effect was not observed

Scots pine
Death of weakened trees

8–12 Gy [A11, K20]

5 Gy

Mass death of young cones and anthers

10–12 Gy [S29]5 Gy

35–40 years old, mass yellowing of needles

8–12 Gy [K20]5 Gy

Inhibition of reproductive capacity (reduced number of seeds per cone andincreased fraction of hollow seeds)

1–5 Gy [F10]0.5 GyMorphological disturbances one year after accident

0.1–1.0 Gy [A11]0.05 Gy

Significant increase in cytogenetic effects in seedlings and needles

0.5 Gy [F10]0.05 Gy

Frequency of mutations of enzyme loci in seed endosperm

0.07 Gy [F10]0.01 Gy

Spruce10–15 years old. Death of trees

4–5 Gy [K20]

1 Gy

25 years old. Dying-off of young sprouts. Mortality of much of the trees within
2–3 years

8–10 Gy [K21]5 Gy

40 years old. Noticeable reduction in sprout mass

2.5–3 Gy [K21]

1 Gy

Mass yellowing of needles

3.5–5 Gy [K21]2 Gy

Herbaceous plants
Reduced density of plants and species diversity in following year

17 mGy/d [S30]

10 mGy/dMorphological changes

4.2–6.3 mGy/d [S30]

2 mGy/dEnhanced vegetative reproduction and gigantism of some herbaceous species

16–30 mGy/d [S30]

10 mGy/d

Sterility of seeds

40 Gy – vetch; 10 Gy – dandelion andarabidopsis [S30]

Decrease in the number of peas in pods of wild vetch, increase in bothf­raction of sterile pods and fraction of embryonic lethalities

0.4 mGy/d [S31]5 Gy
0.1 mGy/dSoil fauna
Drastic decrease in the population density and species composition of forest
litter mesofauna

Dose absorbed on the soil surface 9 Gy
[K13]

1 Gy

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UNSCEAR 2008 REPORT: VOLUME IISpecies effect

Estimated minimum doses (or dose rates)
at which effect was observed

Estimated maximum doses (or dose rates)
at which effect was not observed

Amphibians (brown frogs)
Dose rate, mGy/d: 0.01 from 90Sr tobone tissue, 0.038 from other sources
to the whole body, 0.013 from external
g-radiation exposure [E18, E19]

Increased yield of chromosome aberrations and damage severity in aberrant
cells

0.01 mGy/dHydrobionts
9–11 Gy for 5 years [B19, M21]

Silver carp. Higher occurrence of reproduction system alterations, reduced
viability of progeny

1 Gy/aSmall mammals
Inhibition of reproductive capacity (the significantly reduced testis mass aswell as irreversible or temporary sterility in some males)

Absorbed gonad doses of 3 Gy per month[P16]

1 Gy/aPathological changes in haemopoietic system, liver, adrenals and thyroid

Absorbed dose from external g‑radiation
exposure from the moment of accident
till animal catching in autumn 1986 was
1 Gy. Contribution of b‑radiation was
2–5 times higher than g and incorporated
radionuclides by 1–2 orders lower thanfrom external [E20, M22]

0.5 GyA dose-dependent increase in the frequencies of chromosome aberrations
in bone marrow cells and embryonic losses in bank voles, high frequency ofpolyploid cells and genome mutations

Whole-body absorbed dose rate in 1986:
approximately 6–600 µGy/d [R17]5 µGy/dCattleDestruction of thyroid, chronic radiation disease

Doses absorbed by thyroid >200 Gy, withdose to the whole body being no morethan 0.2 Gy [A24, B16]

20 Gy to thyroidaa Effect in the early days after the accident was mainly determined by 13II action and depended greatly on content of stable iodine in animal ration.

IV.

Effects of radiation EXPOSURE on NON-HUMAN BIOTA

234. This chapter provides an overview of the independent
evaluations of the published literature on the effects of radiation
exposure on non-human biota, briefly considers the relevant
observations from case studies where dose rates to non-humanbiota have been estimated and compared to reference dose rates(from, for example, reference [U4]), and extracts additional key
observations from the post-1996 literature.
A.

Overall conclusions of the UNSCEAR 1996 Report235. The main observations from the Committee’s 1996
evaluation [U4] are described in chapter III of this annex.

The Committee, while emphasizing that only limited data
were available for consideration, concluded that the production of viable offspring through gametogenesis and reproduction is a more radiosensitive population attribute than the
induction of individual mortality.
236. The Committee also noted that there was a wide dose
range over which organisms were sensitive to the lethal
effects of radiation exposure. A schematic representation of
the Committee’s qualitative assessment of the overall sensitivities of various taxa to an acute dose of radiation is shownin figure XII [U4].

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273

Figure XII. Approximate acute lethal dose ranges for various taxonomic groups [S12, W6]
Reproduction of figure VII of reference [U4]
Viruses
Molluscs
Protozoa
Bacteria
Moss, lichen, algae
Insects
Crustaceans
ReptilesAmphibians
Fish
Higher plants
Birds
Mammals
100

101

102

103

104

ACUTE LETHAL DOSE (Gy)237. Overall, the Committee judged that for the most sensitive plant species, the effects of chronic radiation exposure
were noteworthy at dose rates of 1–3 mGy/h. It suggested thatchronic dose rates of less than 400 μGy/h (10 mGy/d) would
have effects, although slight, on sensitive plants but would be
unlikely to have significant deleterious effects on the wider
range of plants present in natural plant communities.
238. The Committee concluded that “for the most sensitive
animal species, mammals, there is little indication that dose
rates of 400 μGy/h to the most exposed individual would seriously affect mortality in the population. For dose rates of up to
an order of magnitude less (40–100 μGy/h), the same statement could be made with respect to reproductive effects. For
aquatic organisms, the general conclusion was that maximum
dose rates of 400 μGy/h to a small proportion of the individuals and therefore, a lower average dose rate to the remaining
organisms, would not have any detrimental effects at the population level. The radiation doses necessary to produce a significant deleterious effect are very difficult to estimate becauseof long-term recovery (including natural regeneration and themigration of individuals from surrounding less affected areas),
compensatory behaviour and the many confounding factors
present in natural plant and animal communities in both­terrestrial and aquatic environments”.

B.

Evaluations since 1996

239. Since the UNSCEAR 1996 Report [U4], several
national and international authorities have reviewed theavailable literature on the effects of ionizing radiation exposure on non-human biota [C1, E1, F5, W11, W17]. This section provides a short discussion of the recent work relevantto this annex.
1.

United States Department of Energy

240. The United States DOE has conducted a considerable
amount of work in developing a graded approach to radioecological risk assessments [H1, H2, J1, U26]. In developing their approach, the DOE considered a number of issues
relevant to the re-evaluation, including assessment endpoints, effort levels and dosimetry. The DOE noted thatradioecological risk assessments focused on population
rele­vant endpoints, such as reproduction, and cited guidance from national and international organizations [I4, N1,
U4]. The DOE went on to adopt screening dose rates corresponding to expected safe levels of exposure of populations of biota based on reviews of the data on the acute andchronic radiation effects of exposure to a dose rate of

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UNSCEAR 2008 REPORT: VOLUME II

10 mGy/d to populations of aquatic animals, 10 mGy/d topopulations of terrestrial plants and 1 mGy/d to populationsof terrestrial animals [I4, N1, R2, U4]. The DOE indicatedthat, if the dose rate to the most exposed individual in the
population does not exceed the expected safe dose rate, thepopulation should also be protected [B18].
2.

Canada241. In response to requirements under the Canadian Environmental Protection Act (CEPA), 1999 [C6], Environment
Canada and Health Canada carried out an assessment of the
impact of the discharge of radionuclides from nuclear facilities on non-human biota for all aspects of the uranium fuelchain, from mining and milling to power generation andwaste management [E5].
242. The approach used in reference [E5] for ecological risk
assessment required identifying “chronic toxicity values”(CTVs) from which “estimated no-effects values” (ENEVs)
were derived using appropriate application factors [E2].
The application factor was intended to address the uncertainties related to differences between observed effects on
endpoints and the success of organisms in the field. An
application factor (safety factor) of 1 was used to estimate
ENEVs for radiation exposure. The CTVs for the various
taxonomic groups reported in reference [E5] were based on
measures of effect applicable to the survival of populationsof sensitive species and on chronic exposures. In assessing
radiological risks, Environment Canada and Health Canada[E5] used factors of 1 for gamma and beta radiation and 40
for alpha radiation to account for the differences in the
RBEs of the different types of radiation. The ENEVs usedby Environment Canada and Health Canada are summarized in table 28 and were based on detailed evaluations of
the published literature [I4, R2, U4] as well as on evaluations specifically carried out in support of the assessment[E4, H3, M3].

Table 28. Summary of “estimated no-effects values” (ENEVs) used to assess the potential toxicity of exposure of non-humanbiota to radiation near Canadian nuclear facilities [E2]Taxa

ENEV (Gy/a)a

Fishb

0.2

Benthic invertebrates

2

Algae

1

Macrophytes1

Mammals

1

Terrestrial plants

1

Terrestrial invertebrates

2

a In all cases, the application factor used to convert the CTV to an ENEV was 1.
b The assessment given in reference [E2], citing the lack of data for Canadian fish, referred to effects on carp (species different from those found in Canada) in the Chernobyl
cooling pond, and acknowledged that the ENEV for fish may be conservative.

243. The (former) Advisory Committee on RadiologicalProtection (ACRP) to the Canadian Nuclear Safety Commission also reviewed the available information relevant to theprotection of non-human biota [A1]. The ACRP consideredthat the ultimate goal of “ecological protection” is to ensurethat communities and populations of organisms can thrive
and that all the component parts will be self-sustaining.
Simi­lar to the DOE [H1], the ACRP [A1] reported thegeneric dose-rate criteria summarized in table 29 for theeffects of ionizing radiation exposure on biota, which werebased on reviews by national and international authorities,
including UNSCEAR [U4], the NCRP [N1] and the IAEA
[I4]. The ACRP also suggested that overall, dose-rate criteria
in the range of 1–10 mGy/d were generally protective of
populations of non-human biota and, given current know­
ledge (and the associated uncertainties), that perhaps a single
nominal dose-rate criterion of about 3 mGy/d might be suitable on a broad basis for assessing risks to non-human biota.

Table 29. Generic dose-rate criteria for biota [A1]
Biota

IAEA [I4]

NCRP [N1]

UNSCEAR 1996 Report [U4]Terrestrial plants

10 mGy/d (4 Gy/a)—

10 mGy/d (4 Gy/a)Terrestrial animals

1 mGy/d (0.4 Gy/a)——   mortality—

10 mGy/d (4 Gy/a)   reproduction—

1 mGy/d (0.4 Gy/a)Aquatic organisms

10 mGy/d (4 Gy/a)

10 mGy/d (4 Gy/a)ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

244. The ACRP [A1] noted that radionuclides incorporated
in biota are not uniformly distributed and that some radio­
nuclides tend to concentrate in certain tissues or organs butthat for dosimetric calculations, radionuclides were often
assumed to be distributed uniformly throughout the organism. This assumption can result in underestimation of thedoses to specific tissues for those radionuclides that concentrate in these tissues (for example, bone-seeking radio­
nuclides in fish). The ACRP emphasized that, in practice,simplifying assumptions have to be made especially fordemonstrating compliance with regulatory standards or criteria and that the degree of simplification will depend on the
purpose of the application [A1]. For screening purposes, theconcept of a single “generic” biota, which represents allplants and animals irrespective of size, shape and composition, has been used [A2] while somewhat more sophisticatedmodels took account of the dose distributions within reference organisms of assumed shapes and sizes and the fractions of radiation energies absorbed in the organisms [W2].
The ACRP also recognized that it is impractical to addressorganisms individually and recommended the use of reference biota, typically developed in terms of simple physicalshapes and dimensions for the purpose of dosimetry [B14,
I2, N1, P7].
3.

275

– Morbidity (including growth rate, effects on the
immune system, and the behavioural consequences ofdamage to the central nervous system from radiation
exposure of the developing embryo);– Mortality (including the stochastic effect ofsomatic mutation and its possible consequence forcancer induction, as well as deterministic effects inparticular tissues or organs that would change theage-dependent death rate);– Reduced reproductive success (including fertility
and fecundity); and– Mutation (induced in germ and somatic cells).
246. Table 30 gives an overview of the quality and quantityof the available data within the FRED, based on a simplified
categorization (ecosystem type, exposure duration and irradiation pathway). The data on effects are strongly weighted
in favour of terrestrial ecosystems (73% of all data) and, foreach ecosystem, the available data appear to be biased
roughly 2:1 in favour of data of acute effects and an external
gamma radiation exposure situation. As a consequence, thedata on chronic effects are limited and largely dominated byexternal gamma radiation exposure conditions experimentally obtained using gamma sources (frequently either 137Cs
or 60Co); thus, mathematical modelling such as that describedin section I is needed to estimate doses for comparison withreference dose rates [G3, G15].

FASSET

245. The group working on the Framework for Assessmentof Environmental Impact (FASSET) [F1, F4, F6, L4]
reported on a wide range of issues relevant to the protectionof non-human biota from ionizing radiation, including dosimetric information and data on the effects of radiation on
non-human biota. The FASSET project developed a database (FASSET Radiation Effects Database—FRED) on theeffects of radiation exposure on non-human biota under four
broad effects categories, referred to by FASSET as “umbrella
effects”. These included:

247. Real et al. [R9] summarized the available informationfrom the FRED on the effects of continuous low dose-rateirradiation of plants, fish and mammals. The effects observedon plants, fish and mammals are shown in tables 31, 32 and33, respectively. Each of these tables provides a brief description of the effect, the corresponding endpoint and the dose
rate resulting in the effect. Table 34 provides an overall summary of the data on chronic effects of radiation exposure asprovided by reference [R9].

Table 30. Allocation of the data on effects within the FRED database to freshwater, terrestrial and marine ecosystems, andto the radiation exposure regimes (duration and irradiation pathways) [G3]
Ecosystem(number of references)

Terrestrial(579)

Freshwater(195)

Total number ofdata (%)

19 983(72.6)

6 067(22.0)

Number of data for each exposure duration

Number of data for each exposure irradiation pathway

Total number%

External

Internal

OtheraAcute

12 273

61.4

11 564288

421

Chronic

6 795

34.0

3 449

344

3 002

Transitoryb

913

4.57

670

40

203

Not stated

2

0.03

0

0

2

Acute

4 526

74.6

4 058

97

371

Chronic

1 484

24.5

970

20

494

Transitory

54

0.89

12

2

40

Not stated

3

0.01

0

0

3

Type

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UNSCEAR 2008 REPORT: VOLUME II

Ecosystem(number of references)

Marine(45)

Total number ofdata (%)

1 470
(5.4)

Number of data for each exposure duration

Number of data for each exposure irradiation pathway

Total number%

External

Internal

Othera

Acute

1 116

75.9

995

58

63

Chronic

353

24.1

286

0

67

Transitory

0

0

0

0

0

Not stated

1

0

0

0

1

Type

a “Other” means that the experiment reported in the literature was devoted to the study of the effects involved by mixed irradiation pathways, and/or not well characterized to
be used for the present analysis.
b “Transitory” means in between “acute” and “chronic” in terms of exposure duration.

Table 31.

Effects of chronic irradiation on plants [R9]Dose rate(µGy/h)SpeciesRadiation

100–1 000

Pine

Gamma

(1–5) × 103(5–10) × 10

3(1–2) × 104

Pine

Pine

Pine

Gamma

Gamma

Gamma

Effects described

Endpoint

Reference

Reduced trunk growth of mature trees

Morbidity[W4]

Death of some conifers; little changes in populations

Morbidity[A6]

Reduced canopy cover of individual conifers; whole canopy remains constantMorbidity[A6]

Decreased stem growth of saplings

Morbidity[A23]

Reduced photosynthetic capacity of pines and thus growth

Morbidity[B11]

Death of all conifers within 2–3 years

Mortality[A6]

Reduced seed production and germination

Reproduction[W11]

Morphological changes in leaves of some plants

Morbidity[W11]

Withered crowns

Morbidity

[W11]

Birch

Gamma

Underdeveloped leaves

Morbidity[W11]

Herbaceous

Gamma

Reduced reproductive potential

Reproduction

[U4]

Birch

Gamma

Death of trees

Mortality[A6, W11]

Grasses

Gamma

Death of grasses and forbs

Mortality[W11]>1 × 105

PlantsGamma

Death of all higher plants

Mortality[A6, W11]>1 × 106

LichenGamma

Reduced diversity of lichen communities after one year exposure

Mortality[B13, W18]

Endpoint

Reference>2 × 104

Table 32.

Effects of chronic irradiation on fish [R9]Dose rate(µGy/h)SpeciesRadiation(1–10) × 102

Plaice,Medaka,
Roach

Gamma

Reduction in testis mass and sperm production. Lower fecundity. Delayed
spawning

Reproduction[H11, K16,
N1](1–5) × 103

Plaice,Eelpout,
Medaka,Guppy,
Rainbow
trout

Gamma orbeta

Reduction in testis mass and sperm content. Severe depletion of s­ permatogonia.
Reduced fertility or complete infertility. Reduced fecundity. Reduced male­courtship activity. Reduced immune response

Reproduction
Morbidity[E10, G20,
H11, H16,
K16, K17, P5,
W7](5–10) × 103

MedakaGamma

Depletion of spermatogonia

Reproduction[H11](1–5) × 10

Medaka,
Guppy

Gamma

Sterility. Reduction in larval survival. Increase in vertebral anomalies

Reproduction[H17, W7]

>5 × 104

Guppy

Gamma

No impact on offspring survival following parental irradiation

Mortality[W7]

4

Effects describedANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

Table 33.

277

Effects of chronic irradiation on mammals [R9]Dose rate(µGy/h)SpeciesRadiation

<102

Mouse
Rat

Gamma

No detrimental effects have been described

Dog

Gamma

Mouse

(1–10) × 102

Endpoint

Reference

Morbidity
Mortality
Reproduction[C17, P8]
[C17, U21]
[L2, Y2]

Life shortening

Mortality

[C18]

Gamma

Life shortening

Mortality

[M13]

Mouse

Neutrons

Life shortening

Mortality

[M13]

Pig

Gamma

Prenatal irradiation decreased the number of primitive stem germ cells andthe ovary and testis weight

Reproduction[E14, E15]

Rat

Gamma

Reduction in number of A1 spermatogonia

Reproduction

[E16]

Mouse

Beta

Irradiation from conception to 14 days of age decreased the number ofprimary oocytes

Reproduction[D2]

Reduction of mean number of litters per female; higher mortality between
birth and weaning; reduction in number of primary oocytes

Reproduction[S6]

Irradiation during three consecutive generations increased the % of sterile
mice and the % of early deaths and decreased the mean litter size

Reproduction[M14, M15]

Field study. Increased % of sterile pairs; reduced mean offspring sired andweanedReproduction

[L3]

Mouse

Gamma

Effects described

Reindeer

Gamma

Natural forest. Increased number of chromosomal aberrations

Mutation

[R3]

Goat

Gamma

Life shortening

Mortality

[H18]

Mouse

Gamma

Increased mortality ratio (the effect was dependent on the mice strain used);decreased mean after survival

Mortality[G25, T2]

Mouse

Neutrons

Life shortening

Mortality

[U21]

Goat

Gamma

Reduced number of liveborn per female in the third generation and reduced
total sperm production

Reproduction[H19]

Irradiation during the 2nd week after birth reduced the fertility and the litter
size

Reproduction[R5]

Irradiation during 4–90 days reduced the fertility span, the germ cells per
ovary and the testis weight

Reproduction[M16, R12,
R13]

Prenatal irradiation reduced the litter size and increased the % of resorptions

Reproduction[L2, L6]

Reduced number of spermatogonia and testis weight

Reproduction[P15, P21]

Prenatal irradiation reduced the number of germ cells in females and males

Reproduction[E14](1–5) × 103
Mouse

Gamma

Rat

Beta

Rat

Gamma

Mouse

Gamma

Increased mutation frequency at seven specific loci in mouse spermatogonia

Mutation

[R14]

Sheep

Beta

Reduction in the number of leukocytes in peripheral blood

Morbidity

[B15]

Rat

Gamma

Reduced brain weight and cingulum volume

Morbidity[R15]Life shortening after exposures of 68 days or longer

Mortality[S7, S24]

Mouse

Gamma

Increased paternal expanded simple tandem repeat (ESTR) mutation rate andpaternal mutation per offspring band at loci MMS10 plus Ms6-hm plus Hm-2

Mutation[D3, D5]

Dog

Beta

Reduced survival

Mortality

[R16]

Mouse

Gamma

Increased mortality ratio (dependent on the strain used)

Mortality

[G25]
[C19]

Gamma

Prenatal irradiation reduced the length and weight of embryos and increased
the % mortality

Reproduction

Rat

Reduction in ovary and testis weight

Reproduction[E17](5–10) × 10

3

>10

4

278

UNSCEAR 2008 REPORT: VOLUME IITable 34. Overall summary of data on the effects of chronic irradiation for plants, fish and mammals, based on the FASSET
Radiation Effects Database (FRED) [R9]Wildlife groupMorbidity

Mortality

Reproductive capacity

Mutation

Plant

Plant growth begins to be affected
at more than 100 µGy/h.
Continued exposure at 21 µGy/h
for 8 years increases thesensitivity in pines

50% mortality at 8 years at~1 000 µGy/h in pines

A field study indicated a decrease
in seed weight of a herb at
5.5 µGy/h

The mutation rate in microsatellite
DNA increased at ~40 µGy/hFish

One experiment, but not another,indicates effects on the immune
system at 8.3 µGy/h

Too few data to draw conclusions

One study showing effects on
gametogenesis at 230 µGy/h.
Otherwise effects at more than
1 000 µGy/h

Radiation exposure increases themutation rate

Mammals

Rat growth not affected at
16 µGy/h but affected at morethan 3 000 µGy/h.
Some blood parameters affected
at 180–850 µGy/h. No effect on
thyroid function at 8 000 µGy/h

No effect on mouse lifespanat 460 µGy/h, but significant
reductions above ~1 000 µGy/hin the mouse, goat and dog

Threshold for effects at~100 µGy/h, with clear effects at
more than 1 000 µGy/h

Too few data to draw conclusions.
One of nine references gives an
LOEDR of 420 µGy/h for mice

248. Real et al. [R9] noted that plant morphology (size,
shape and density of plant stands) can alter the exposure andthe resulting radiation dose. They also noted that plants with
exposed meristems or buds can receive higher doses to thecritical tissues than those plants that grow and reproduce
underground or are protected by thick scales.
249. Real et al. [R9] concluded that chronic exposures up
to 4 × 103 µGy/h to developing fish embryos will not resultin significant effects on growth. Furthermore, they considered that the available data suggest that dose rates of lessthan 4 × 103 µGy/h at any life stage would not be expected toaffect survival. However, they felt that the limited amount ofdata further suggests that genetic damage caused by chronic
irradiation is likely to occur at all dose rates and that theradiosensitivity for this damage is similar to that of othervertebrates.
250. There are a large number of data on mammals available
within the FRED; therefore, Real et al. [R9] had to be selective in summarizing the information. Altogether, the authors
considered 183 references for mammals, which provided
more than 3,000 data points on effects. The authors concluded
that chronic radiation dose rates lower than 103 µGy/h do not
result in irreversible effects on mortality, morbidity and reproduction. A dose rate of 100 µGy/h (i.e. 2.4 mGy/d) had been
described for reproductive capacity impairment; however, thedetrimental effects observed were reversible [R9]. The authors
indicated that the majority of the work had been conductedusing mice and rats and that it would be beneficial to haveadditional information on the effects of chronic radiation
exposure on other species.
251. An overall summary of the effects due to chronic
exposure of plants, fish and mammals identified by FASSET
was reported in reference [R9] for the different endpointclassifications (morbidity, mortality, reproductive capacityand mutation) provided in table 34. The authors concluded
that the amount of available information on the effects of low
dose rates (less than about 100 µGy/h) for continuous­radiation exposure is reasonable for both plants and animals
and that for chronic exposure conditions “the reviewed
effects data give few indications for readily observableeffects at chronic dose rates below 100 µGy/h”. However,they advised that “using this information for establishingenvironmentally ‘safe levels’ of radiation should be donewith caution, considering that the database contains large
information gaps for environmentally relevant dose rates andecologically important wildlife groups” [F5, R9].

4.

ERICA

252. The project on Environmental Risks from Ionizing
Contaminants: Assessment and Management (ERICA) carried out under the European Commission’s 6th Framework
Programme was the successor of the FASSET project.
Extensive quality assurance of the data was carried out andthis led to the development of an expanded effects database(referred to as FREDERICA). A database on the effects ofchronic radiation exposure of fish, which was developed in
the project on Environmental Protection from Ionising Contaminants in the Arctic (EPIC) [S25] was subsequently
incorporated into the FREDERICA effects database [C12].
253. The ERICA integrated approach adopted an Ecological
Risk Assessment tiered methodology that required values of
the risk assessment screening dose rates for risk characterization within Tiers 1 and 2. The screening values used within
Tiers 1 and 2 were derived on the basis of data taken from the
FRED and compared from some key data from the EPIC
project (making thus the best use of the FREDERICA database) [C12]. The method applied follows recommendations of
the European Commission for the estimation of Predicted

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

No-Effect Concentration (PNEC) for chemicals [E11]. A
three-step methodology was used. First, a coherent data subset
was extracted from each experiment, covering endpoints
related to mortality, morbidity and reproduction. Next, a systematic mathematical treatment was applied to reconstructdose-rate–effect relationships and to estimate critical toxicity
endpoints. For chronic exposure, the critical toxicity endpoint
was the estimated Effect Dose Rate (EDR10, expressed in
μGy/h), the dose rate that gives rise to a 10% change in
observed effect. The final step of the method consisted inusing these estimated critical toxicity data to derive a Predicted No-Effect Dose Rate (PNEDR) by means of the species
sensitivity distribution method (SSD) [E11, G15, G27].

279

separate analyses of the data available for different ecosystems, the authors [G15] concluded there was no statisticaljustification for attempting to derive ecosystem-specificscreening dose rates and all data were therefore analysed
together as a generic ecosystem. The resultant HDR5 was
82 µGy/h (with 95th percentile confidence intervals of 23.8
and 336 µGy/h). To derive the final dose rate for screening(i.e. PNEDR), a safety factor (SF) of 5 was used to allow for
any remaining extrapolation and the resultant number
rounded down to the nearest one significant figure. Basedon this approach, the authors suggested a reference dose
rate for incremental exposure of 10 μGy/h for “screening forpotential radiological effects”. The methodology and pro­
cess used to derive this screening value are documented
within references [G3, G11, G15] where the value is shown
to be similar to that derived using alternative methods to
SSD (figure XIII).

254. The SSD method was used to estimate the Hazardous
Dose Rate (HDR5), the dose rate at which 95% of the species in the aquatic/terrestrial ecosystem are protected. After

CUMULATIVE WEIGHTED PROBABILITY(%)

Figure XIII. Species sensitivity distributions for generic ecosystems and chronic external gamma irradiation conditions
The log-normal distribution with its associated 95% confidence interval is fitted to geometric means per effect category for each species
calculated on critical ecotoxicity data (EDR10) [G3]
100
80
60
Number of data = 24
Number of species = 18
HDR5 = 81.8 Gy
CI95% = [23.8–336] µGy/h

40
20
0
1

10

103

102

104

105

106

107

DOSE RATE (µGy/h)Plants255. At the ecosystem level, the value of the ERICA
integrated approach screening dose rate lies in the range
giving rise to minor effects [F5, G3, G15, G27]. The
authors suggested that such effects are not expected to be
directly relevant at higher organizational levels, such as
the structure and functioning of ecosystems.
256. The same method was also applied to acute exposure conditions to guide interpretation of accidental situations; however, in this case, the authors [G11, G15] did
find a difference between marine ecosystems compared toterrestrial and freshwater ecosystems. The values derived

Invertebrates

Vertebrates

from an SSD analysis on the set of Effect Doses giving a
50% change in observed effect (ED50) for limiting thepotentially affected fraction to 5% of the species underacute external gamma irradiation conditions varied fromabout 1 to 5.5 Gy, according to the ecosystems type, withassociated 95% confidence intervals covering less than
one order of magnitude (see figure XIV). To derive screening values, an SF of 5 was applied and the results rounded
down to the nearest one significant figure. This resulted in
Predicted No-Effect Doses (PNED) of 900 mGy for marine
ecosystems and 300 mGy for terrestrial and freshwater
ecosystems [G3, G15, G27].

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UNSCEAR 2008 REPORT: VOLUME II

Figure XIV. Species sensitivity distributions for generic ecosystems and acute external gamma irradiation conditions
The log-normal distribution with its associated 95% confidence interval is fitted to geometric means per effect category for each species
calculated on critical ecotoxicity data (ED50) [G3]Generic continental ecosystem (freshwater and terrestrial)
100

CUMULATIVE WEIGHTEDPROBABILITY
(%)

90
80
70
60

Number of data = 60

50

Number of species = 50
HD5 = 1.86 Gy

40
30

CI95% = [1.16–2.98] Gy

20
10
0
0.1

1

10

102

103

104

DOSE (Gy)Marine ecosystem

CUMULATIVE WEIGHTEDPROBABILITY
(%)

100
80
60

Number of data = 13
Number of species = 8
HD5 = 4.84 Gy
CI95% = [0.64–12.7] Gy

40
20
0
0.1

1

10

102

103

104

105

DOSE (Gy)

Plants257. Dose rates below which no significant effects are
expected at various levels of organization (population, wildlife group or ecosystem) were compared by different organizations/authors [G3, G15], and are summarized in table 35.
The selection was mainly based on observations of effects

Invertebrates

Vertebrates

and expert judgement. The approach using SSD provides analternative methodology for assessing radiation risks byderiving, for the first time for radioactive substances, protection thresholds using a rational and transparent process basedon the approach adopted for chemicals in Europe [G15].

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

281

Table 35. Dose-rate values proposed by various organizations/programmes to support effect analysis for chronic exposure
to radiation [G3, G11]
Targeted protected level as describedin the source

Method/justification of the value

Dose rate(µGy/h)Sourcereference

Terrestrial ecosystems
Generic ecosystems

SSD-95% species protected plus SF of 5
SSD giving an HDR5 of 81.8 mGy/h divided by an SF of 5 and rounded down

10

[G3]

Generic ecosystems

SF method: SF of 10 applied to the lowest critical radiotoxicity value EDR10

0.6

[G3]

PlantsBackground

0.02–0.7[U4]

Plants

Review, SF on the lowest critical radiotoxicity value

110[B31, E5]

Plants

Review based on NCRP 1991; IAEA 1992; UNSCEAR 1996

400

[O1, U26]

Plants

Critical review for screening purpose from IAEA 1992

400

[E12]

Organisms

Background – external irradiation and non-weighted

0.01–0.1[G21]

Animals

Background0.01–0.44[U4]

Animals

Review based on NCRP 1991; IAEA 1992; UNSCEAR 1996

40

[O1, U26]

Animals

Critical review for screening purpose from IAEA 1992

40

[E13]

Small mammals

Review, SF on the lowest critical radiotoxicity value

110[B31, E5]

Invertebrates

Review, SF on the lowest critical radiotoxicity value

220[B31, E5]

Vertebrates and cytogenetic effects

Review contaminated environments

4–20

[S28]

Vertebrates and effects on morbidity

Review contaminated environments

20–80

[S28]

Vertebrates and effects on reproduction

Review contaminated environments

80–200[S28]

Aquatic ecosystems
Generic freshwater ecosystems

SSD-95% species protected plus SF of 5
SSD giving an HDR5 of 81.8 mGy/h divided by an SF of 5 and rounded down

10This annex

Generic freshwater ecosystems

SF method: SF of 50 applied to the lowest critical radiotoxicity value EDR10

10This annex

Generic marine ecosystems

SSD-95% species protected plus SF of 5
SSD giving an HDR5 of 81.8 mGy/h divided by an SF of 5 and rounded down

10

[G3]

Generic marine ecosystems

SF method: SF of 50 applied to the lowest critical radiotoxicity value EDR10

3.7

[G3]

Freshwater organisms

Background0.022–0.18[U4]

Freshwater organisms

Background–external irradiation and non-weighted

0.02–6[B32]

Aquatic algae/macrophytes

Review, SF on the lowest critical radiotoxicity value

110[B31, E5]

Aquatic animals

Review based on NCRP 1991; IAEA 1992; UNSCEAR 1996

400

[O1, U26]

Freshwater and coastal marine organisms

Critical review for screening purpose from IAEA 1992

400

[E12]

Amphibians/reptiles

Review, SF on the lowest critical radiotoxicity value

110[B31, E5]

Benthic invertebrates

Review, SF on the lowest critical radiotoxicity value

220[B31, E5]

Fish

Review, SF on the lowest critical radiotoxicity value

20[B31, E5]

Marine organisms

Background–external irradiation and non-weighted

0.03–1[B32]

Marine mammals

Critical review for screening purpose from IAEA 1992

40

[E13]

Deep ocean organisms

Critical review for screening purpose from IAEA 1992

1 000

[E13]

Aquatic and terrestrial flora and fauna

Review concluded that few indications of readily observable effects at chronic dose
rates below

<100

[F5]

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UNSCEAR 2008 REPORT: VOLUME II

258. As indicated elsewhere in this annex, few new data on
the effects of ionizing radiation exposure on non-human biota
have been developed since 1996. In all the recent literature
reviews [C1, F5, G16, R9, W11]), the specificities of the environmental situations of interest (chronic low-level exposure
regimes) consistently emphasized the importance of all reproductive parameters to the population within a given ecosystem
to the structure and functioning of that ecosystem. These
reviews clearly argued for the need of a research programme
to acquire specific data related to chronic low-level exposureand the effects on reproductive capacity in such a way as to beable to shift from observations on individual organisms toobservations on populations. A brief summary of the data on

Table 36.

effects from the FRED is given in table 36 along with assigned
weight ratios based on the numbers of data sets available
related to acute versus chronic exposure and, for chronic
exposure data, to external versus internal exposure and reproductive endpoints. The extrapolation on the basis of the existing knowledge will become increasingly critical as the relative
weights increase. In reviewing these data, ­Garnier-Laplace etal. [G16] concluded that operationally for any site-specificrisk assessment, the present state-of-the-art on extrapolation
issues allows the relative magnitudes of the various sources of
uncertainty to be ordered as follows: one species to another >acute to chronic = external to internal = mixture of stressors >individual to population > ecosystem structure to function.

Brief overview of the data on effects from FRED (adapted from reference [G16])

Wildlife group

Number of data

Weight data ratio
All data: acute/chronic

Chronic data: (external)/(internal+mixed)
All endpoints

Reproduction

Aquatic plants

616

2.7

4.1

0/0a

Aquatic invertebrates

542

1.2

4.1

8.3

Amphibians

749

1.3

0.02

0/0

Bacteria

171

0.5

2.4

0/0

Birds

1 732

3.4

3.4

5.5

Crustaceans

850

3.7

180

20/0

Fish

2 802

2.8

1.0

0.8

Fungi

120

0/120

120

0/0

Insects

1 237

5.2

5.4

0.8

Mammals

4 112

2.5

4.7

3.3

Molluscs

484

2.4

1.7

0.4

Moss/lichen

44

0/44

0.5

0/0

Plants11 984

1.6

0.7

0.5

Reptiles

271

6.7

0/35

0/0

Soil fauna

398

1.6

0.15

0/0

Zooplankton

111

4.3

21/0

9/0

a (number of data devoted to reproduction endpoints and chronic external irradiation) / (number of data devoted to reproduction endpoints and chronic internal or mixed irradiation): for example, 0/0 means that no data exist.

5. Observations from recent literature
259. The European Commission (EC) has been supporting
research on the effects of ionizing radiation exposure on
non-human biota for the past several years. This included thedevelopment of the FRED. More recently, the ERICA project
conducted a review of the quality of the data in the FRED
and merged the FRED with the Russian EPIC database toform a new database, FREDERICA, with several hundredadditional references [C12]. This database includes references to over 1,200 papers that focus on the effects of radiation exposure on non-human biota and is a valuable sourceof information. General information on the new data on
effects or new interpretations of the data on effects isprovided in the previous section. Additional observations
from the literature identified in the ERICA database as wellas the open literature are provided in the following section in
an attempt to supplement the previous information in several
areas of current interest.
(a)Terrestrial biota

260. Hingston et al. have described the effects of low dosesof ionizing radiation on terrestrial invertebrates and reported
experiments on earthworms (Eisena fetida) and woodlice(Porcellioscaber) [H23]. Both species were continuously
exposed to gamma radiation from a 137Cs source over a rangeof dose rates with total exposures for each experimental group

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

of 0.5–20 Gy delivered over a total of 14 and 16 weeks,
respectively. The investigators considered a number of endpoints relevant to reproduction, growth and mortality. They
reported on the results for woodlice [H23]. They found nodele­terious effects for the endpoints studied up to a maximum
dose rate of approximately 8 mGy/h (192 mGy/d); the woodlice were unaffected by the doses given. However, they notedthat the results may, in part, have reflected the laboratory conditions, i.e. an environment protected from predation. HertelAas et al. reported the results from a study of the reproductive
capacity (numbers of cocoons, hatchability, etc.) of earthworms exposed chronically to gamma radiation [H22]. In thisstudy, earthworms (Eisena fetida) were exposed over two generations to gamma radiation from a 60Co source at five dose
rates, from 0.18–43 mGy/h. The lowest dose rates at whichan effect was observed was 4 mGy/h and 11 mGy/h in F0 andF1 worms, respectively. The experiments also suggested a
possible acclimatization in F1 worms.

283

neonates showed significantly reduced resistance to starvation
at every dose rate compared to the control.
264. Gilbin et al. [G22] reported effects on Daphnia magna of
external gamma radiation exposure at dose rates ranging from
0.4–31 mGy/h over a 23‑day period (i.e. 5 broods). Gamma
radiation exposure caused no significant change in somatic
growth. The mass-specific respiration rate was significantly
lower at dose rates of 31 mGy/h than for the control. Broods
were deposited earlier and fecundity was 20% lower at the highest dose rate than for the control. The combination of decreased
fecundity and unchanged individual offspring mass resulted in asmaller total mass of eggs produced per daphnid at dose rates of
4.2 and 31 mGy/h than for the control. A decreased resistance of
neonates to starvation was observed at every dose rate.

262. The great majority of the data on aquatic invertebrates
in the FRED concern the effects of chronic irradiation on
crustaceans. The data indicate that observable impacts atdose rates up to 103 mGy/h are unlikely and that a dose rateof ~104 mGy/h is probably the lower limit for the onset ofsignificant effects. However, effects were apparent in theembryonic development of the goose barnacle (Pollicipes
polymerus) following a 32‑day exposure to tritiated water atdose rates of 0.7, 6.5 and 64 mGy/h [F5].

265. Alonzo et al. [A27] tested the chronic effects of internalalpha irradiation on Daphnia magna respiration, somatic
growth and reproduction over three successive generations.
They showed that the toxicological effects of internal alphairradiation on life-history traits of Daphnia magna increased
across generations. A 70‑day experiment was performed with
Daphnia magna exposed to waterborne 241Am corresponding
to average dose rates of 0.3, 1.5 and 15 mGy/h. In the first
generation (F0), a reduction in body length (5%) and the dry
mass of females (16%) and eggs (8%) was observed after
23 days of exposure, while mortality and fecundity remained
unaffected. New cohorts were started with neonates of broods
1 and 5, to examine the potential consequences of the reduced
mass of the offspring for subsequently exposed generations.
At the highest dose rate, an early mortality of 38–90% affectedjuveniles while survivors showed delayed reproduction andreduced fecundity in F1 and F2. At dose rates of 0.3 and1.5 mGy/h, the mortality of daphnids in generation F1 ranged
from 31–38%. Reproduction was affected through a reductionin the proportion of breeding females occurring in the first
offspring generation at a dose rate of 1.5 mGy/h (to 62% of
total daphnids) and in the second generation at 0.3 mGy/h (to69% of total daphnids). Oxygen consumption remained significantly higher at dose rates ≥0.3 mGy/h than for the control
in almost every generation. Body size and mass continued
decreasing in relation to dose rate, with a significant reduction
in mass ranging from 15% at a dose rate of 0.3 mGy/h to 27%
at 15 mGy/h in the ­second offspring generation.

263. Concerning the effects of internal radiation exposure on
crustaceans, recent data exist on daphnids which were chronically exposed internally to alpha radiation from 241Am underexperimental conditions at dose rates up to 990 µGy/h [A19].
These authors reported that exposure to dose rates of 110 µGy/hor higher resulted in a significant (15%) reduction in bodymass. Daphnids also showed increased respiratory demand
after 23 days at the highest dose rate, suggesting increased
metabolic cost of maintenance resulting from the need to copewith the stress from alpha irradiation. Fecundity remained
unchanged over the 23‑day period, but individual masses of
eggs and neonates were significantly smaller compared to thecontrol. This suggested that increased metabolic expenditure inchronically alpha-­irradiated daphnids came at the expense of
their energy investment per offspring. As a consequence,

266. Dose rates above 0.1 mGy/h to developing mollusc
embryos affected the incidence of developmental abnormalities but not the subsequent overall survival of the resulting larvae. Significant detrimental effects are to be expected at dose
rates greater than 1 mGy/h [F5]. Recently, Jha et al. [J4]exposed mussels (Mytilus edulis) to a series of concentrationsof HTO equivalent to a dose rate ranging from 12–485 µGy/h
for 96 hours. The study revealed a dose-dependent increase in
the response for both the micronuclei test and the comet assay.
Dose rates below 500 µGy/h induced genetic damage in the
haemocytes. For the same species but another life stage (i.e.
one-hour-old embryos exposed during 12 to 24 hours to arange of HTO doses between 0.02 and 21.41 mGy), ­Hagger et
al. [H13] found that the embryo–­larvae showed dose or­concentration-dependent effects for mortality, developmental

261. Tanaka et al. [T3, T25] discussed the effects of chronic
exposure of mice (SPF B6C3F1) to gamma rays at low dose
rates. Mice of both sexes were divided into 4 groups, one ofwhich was not irradiated and the other three which were irradiated. The exposed mice were irradiated at dose rates of
0.05, 1.1 and 21 mGy/d for about 400 days using a 137Cs
source. All mice were maintained until natural death, after
which pathology was performed to identify the cause ofdeath. Females exposed to 1.1 mGy/d and both sexes exposed
to 21 mGy/d had significantly shortened lifespans compared
to non-exposed mice. The mean survival times of mice ofboth sexes exposed to 0.05 and 1.1 mGy/d were shorter thanfor non-exposed mice but not significantly so.
(b)Aquatic and marine biota

284

UNSCEAR 2008 REPORT: VOLUME II

abnormalities and induction of sister chromatid exchanges.
However, they reported that there was a lack of a clear dose
response for chromosomal aberrations and proliferative-rateindex.
267. For annelids, Knowles and Greenwood [K3] exposed
Ophryotrocha diadema to beta radiation at a dose rate of
7.3 mGy/h and observed that the number of eggs surviving
to the larval stage was reduced, but did not affect egg production. This is in contrast to previous studies related to
gamma irradiation where egg production is reduced but not
the number becoming larvae.
268. Kryshev and Sazykina [K18] reported an evaluation of
the radioecological effects on aquatic organisms exposed tohigh levels of radioactive contamination in lakes affected by
the Mayak reprocessing facility, in lakes affected by the
Kyshtym accident, in the cooling pond of the Chernobyl

nuclear power plant (NPP) and in the littoral area downstreamof the Leningrad NPP. The authors reported doses based on
the concentrations of radionuclides in water, sediments andfish and indicated that the highest dose rates, up to 300–
800 mGy/d, were to organisms in the lakes affected by the
Mayak complex. They also noted that the biota in the Mayaklakes were exposed to chemical contamination in addition toradiation but commented that the fish population had retained
its viability for the period of observation of 30 years. The
lowest dose rates were for the Leningrad NPP, where theauthors noted that, typically, aquatic organisms were exposed
to background levels of radiation. However, the dose rates toaquatic organisms in the liquid radioactive-waste canal of theLeningrad NPP were elevated. Here, the authors noted anincreased asymmetry of the soft rays of the pectoral fins ofroach and suggested that this was due to the combined effects
of exposure to radiation and elevated temperature. The overall observations from this study are summarized in table 37.

Table 37. Radioecological effects in water bodies exposed to radioactive contamination(adapted from reference [K18])
Water body (period of assessment) species under study

Dose rate assessment(µGy/d)Brief description of the effects

300 000–800 000
30–2 000

Total death of lake ecosystem
Mass death of fish in the upper reaches of the riverSouthern Urals [K24, K25, K26]
Lake Karachai (1951–1952)
Techa River (1951–1951)
Cooling pond of the Chernobyl NPP[B19, K12, K28] (1986–1992):
Silver carp Hypophthalmichthys molitrix

0.2–3

Increased anomalies of the reproductive system; disturbances in the stateof sexual cells to 47–90%; sterility of gonads

Waste channel of the Leningrad NPP[K27, R18] (1980–1983)
Roach Rutilus rutilus

0.007–2

Increase by a factor of 2.3 in the variance of fluctuating asymmetry of thenumber of soft rays of pectoral fins at different sides of the body of roach

269. Real et al. [R9] in their review of the information in the
FRED observed that the developing embryos of fish that were
subjected to chronic exposures at dose rates up to 4 mGy/hwill not result in significant effects on subsequent growth.
They also noted conflicting results for the effects of radiation
exposure of the immune system: for rainbow trout irradiatedas embryos, there was a threshold at dose rates between 8.3–
83 µGy/h from exposure to beta radiation from tritium, while
there was no effect at a dose rate of 9 mGy/h from exposure
to radiation from 137Cs. According to the authors [R9], thelimited data available on mortality effects of chronic irradiation indicated that dose rates less than 4 mGy/h at any life
stage were unlikely to affect survival and that there was little
consistent, significant evidence for any effects on reproductive capacity at dose rates of less than 0.2 mGy/h. Finally, theauthors [R9] suggested, based on a very limited amount of
data, that chronic irradiation-induced genetic damage probably occurs at all dose rates and that radiosensitivity for thisdamage is similar to that of other vertebrates.
270. An interesting recent study has been performed withzebrafish larvae by Jarvis and Knowles [J5]. Gamma radiation
was delivered externally from sealed sources (137Cs) at a dose
rate ranging from 0.3–7.4 mGy/h. The alkaline comet assay
was used to assess DNA damage on larvae (5–6 days post

laying, 2 days post hatching), exposed for 24 hours to dose rates
of 0.4, 1.2 or 7.2 mGy/h and for 1 hour to 0.4 or 1.2 mGy/h.
Entire larvae were macerated and their cells embedded in agarose gel. Larvae exposed at dose rates of 7.2 or 1.2 mGy/h for
24 hours (total dose of 173 and 29 mGy, respectively) showed asignificant increase in the percentage of DNA in the comet tail.
The same observation was made for larvae exposed at the samerates for 1 hour (total dose of 7.2 and 1.2 mGy, respectively).
The increase in tail movement was not correlated to the exposure time, indicating that DNA damage was repaired with time.
No information was available on DNA repair in long-term irradiated or contaminated fish. It must be noted that for a similardose rate (1 mGy/h), no effect on reproduction in adults after
exposure of more than 12 months could be observed [E12].
(c)

Genotoxicity

271. Data on genotoxicity are summarized in table 38.
Knowles [K16] irradiated plaice under laboratory-controlled
conditions using sealed 137Cs sources to investigate potential
genotoxic effects. No effect on the coefficient of variation(CV) of the DNA content, aneuploidy or polyploidy, measured
by flow cytometry (FC), was observed even for the maximum
exposure period (197 days) and maximum dose rate (1 mGy/h).

n.d.
n.d.

125 µGy/hb
80 µGy/hc
400–25 000 Gy/h
260 µGy/h

3 000 µGy/h (24 d)
6 000 µGy/h (48 d)

1 000 µGy/h to >100 Gy/h
Background
5 × 10‑3 to 0.5 µGy/hd
240–1 000 µGy/h

In situ, Chernobyl, cooling pond, 137Cs

In situ, Savannah River site, 134,137Cs +89, 90
Sr + Hg

Lab in vivo, external, 60Co

In situ, Savannah River site, 134,137Cs +89,90
Sr + Hg

Lab in vivo, external, 60Co

Lab, external, 137Cs

Various conditions (literature review)

Lab, in vivo, external, 137Cs

In situ, Swedish lake, Chernobyl fallout
1988, external + internal, 137Cs

In situ, Swedish lake, Chernobyl fallout
1988, external + internal, 137Cs

In situ, Siberian (Tomsk‑7) nuclear site

Channel catfish (I. Punctatus), adults

Largemouth bass (M. salmoides),adultsMarine polychaete worm (N. arenaceodentata), larvae

Midge (C. tentans), larvae

Marine polychaete worm
(N. arenaceodentata), larvae

Slider turtle (T. scripta), fibroblasts andlymphocytes

18 different fish species

Plaice, (P. platessa), adult

Pike (E. lucius), perch (P. fluviatis),roach (R. rutilus) and bream (A. brama)

Pike (E. lucius), perch (P. fluviatis),roach (R. rutilus) and bream (A. brama)

Pike (E. lucius), adults

n.d.
n.d.
n.d.

10 000 Bq/kg d.w. 137Cs
10 µGy/hd
18 000 Bq/kg d.w. 137Cs
Ext. dose rate : 10 µGy/hd
57 000 µGy/hd
1 200 Bq/kg
w.w.

MN per 1 000 erythrocytes

MN per 1 000 erythrocytes

MN per 1 000 erythrocytes

MN per 1 000 erythrocytes

MN per 1 000 erythrocytesn.d.

197 days

CA (symmetrical translocations)

CA (metaphase)

24 days
48 days

n.d.

CA

SCE

Alkaline unwinding (hepatocytes,
gill cells, erythrocytes)

Alkaline unwinding (hepatocytes,
gill cells, erythrocytes)

Agarose gel electrophoresis(hepatocytes, erythrocytes)

Alkaline and neutral unwinding(hepatocytes)

Alkaline comet (tail moment)

Assay(parameter)

Lifetime

12 hours
24 hours

49 years

External dose rate:
50 µGy/hIn situ, (Oak Ridge) external + internal,
235
U, 239,240Pu, 137Cs, 60Co, 90Sr, Hg, HAP, PCB

Mosquitofish (G. affinis), adults

1 hour;24 hours

Exposure
durationn.d.

In situ, (White Oak Lake) external +internal, 235U, 239,240Pu, 137Cs, 60Co, 90Sr, Hg,
HAP, PCB

Pond slider (T. scripta)
Snapping turtle (C. serpentina), adults

400, 1 200,
7 200 µGy/h

Dose rate, dose orinternal concentration

External dose rate:
50 µGy/ha

Lab in vivo, external, 137Cs

Type of exposure

Zebrafish (D. rerio),
larvae (2 d)Species(life stage)

Table 38. Genotoxicity in aquatic species exposed to radionuclides in the laboratory or in situ [A13]++57 000 µGy/h

=

=

=

+
Mean [min; max] : 3 [0; 13]
5 × 10‑3 to 0.5 µGy/h

230 000 µGy/h (LNOEDR)+
3 000 µGy/h+
6 000 µGy/h+++ : inversion+ : deletion
260 µGy/h+
400 µGy/h==+
50 µGy/h+
50 µGy/h+
1 200 µGy/h

EffectLOEDR (µGy/h)(LNOEDR or LOED)

[I22]

[A21]

[A20]

[K16]

[G23]

[H14, U18]

[P4]

[B34]

[H15]

[S17]

[S18]

[T21]

[M5]

[J5]

Reference

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA
285

n.d.

n.d.

n.d.

n.d.

9 months

125 µGy/hb

125 µGy/hb

80 µGy/hc

80 µGy/hc

80 µGy/hc

In situ, Chernobyl, cooling pond, 137Cs

In situ, Chernobyl, cooling pond, 137Cs

In situ, Savannah River site, 134,137Cs +Sr + Hg

In situ, Savannah River site, 134,137Cs +89,90
Sr + Hg

In situ, Savannah River site, 134,137Cs +89,90
Sr + Hg

Crucian carp (Carassius carassius),
adults

Crucian carp (Carassius carassius), carp
(Cyprinus carpio), tench (Tinca tinca),channel catfish (I. punctatus), adults

Slider turtles (P. scripta), adults

Slider turtles (P. scripta), adults

Mallard (A. platyrhynchos), ducklings

FC erythrocytes(DNA CV, aneuploidy and cellproliferation)

FC erythrocytes(DNA CV and aneuploidy)

FC erythrocytes(DNA CV and aneuploidy)

FC whole blood, erythrocytes,
leukocytes (DNA CV, aneuploidy,
cell proliferation)

FC (DNA CV, aneuploidy)

FC erythrocytes (DNA CV, aneuploidy
and CV distribution)

FC (DNA CV, aneuploidy, polyploidy)

MN per 1 000 erythrocytes

Assay(parameter)= : aneuploidy= : cell proliferation+ : CV
80 µGy/h= : aneuploidy+ : CV
80 µGy/h= : aneuploidy+ : CV
80 µGy/h= : aneuploidy+ : CV blood & erythrocytes++ : CV leukocytes+ : cell proliferation
125 µGy/h= : aneuploidy+ : CV125 µGy/h= : aneuploidy+ : CV+ : CV distribution
80 µGy/h=-EffectLOEDR (µGy/h)(LNOEDR or LOED)

[G24]

[L11]

[B35]

[D8]

[L10]

[L8]

[K16]

[S18]

Reference

Symbols and abbreviations: Dose rates are either those indicated in the article or those taken from other studies (a from reference [T21]; b from reference [K9]; c from reference [H14]; d from reference [T6]). SCE : sister chromatid exchange;
CA : chromosomal aberration; MN : micronuclei; FC : flow cytometry. Effect description: + : increase; ++ : strong increase (>3 fold the value of the control group); +++ : very strong increase; = : no significant response; - : decrease; -- : strong
decrease (>3 fold the value of the control group). LOEDR (µGy/h) : Lowest Observed Effect Dose Rate; LNOEDR (µGy/h) : Lowest No Observed Effect Dose Rate; LOED (µGy) : Lowest Observed Effect Dose. By default, the endpoint is LOEDR. If notavailable, LNOEDR or LOED are given.

89,90

n.d.

80 µGy/hc

In situ, Savannah River site, 134,137Cs +89,90
Sr + Hg

Largemouth bass (M. salmoides),adults197 days

240–1 000 µGy/hLab, in vivo, external, 137Cs

Plaice, (P. platessa), adultn.d.

Exposure
duration

125 µGy/hb

Dose rate, dose orinternal concentration

In situ, Chernobyl, cooling pond, 137Cs

Type of exposure

Channel catfish (I. Punctatus), adults

Species(life stage)

286
UNSCEAR 2008 REPORT: VOLUME IIANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

272. To date, experiments have failed to demonstrate aclear correlation between micronucleus (MN) induction andthe 137Cs concentration in fish muscle. Al‑Sabti [A20] collected blood samples from pike, perch, roach and bream in
Swedish lakes contaminated by Chernobyl fallout. Even if
the 137Cs concentrations in the muscle were high, up to
18 kBq kg–1 (dry weight), and MN induction significant, they
were not correlated and the highest MN frequency (42 per
1,000 erythrocytes) was observed in the control lake. A similar observation was made in another study on Swedish lakes[A21]. In another in-situ study conducted by Sugg et al.
[S18] on catfish from the Chernobyl area, the highest MN
frequency (6 per 1,000 erythrocytes) was found in fish fromthe control site, although alkaline unwinding assay showed
an increase (non-significant) of single-strand breaks (SBs) inthe cooling pond. The authors hypothesized that other pollutants might have been present in the control lake or that thefish might have displayed an adaptive behaviour andincreased defence mechanisms against ionizing radiation
exposure. On the other hand, Ilyinskikh et al. [I22] found apositive correlation between the 137Cs concentration in pikemuscle (up to 1.2 kBq/kg wet weight) and the frequency of
micronucleated erythrocytes, for fish caught in Siberian
nuclear facilities. A positive correlation was also foundbetween micronuclei frequency and age.
273. Gustavino et al. [G23] exposed carp to acute doses of
X‑rays (250 kV, 6 mA, 0.75 Gy/min). They found a dose andtime-dependent response of MN to irradiation, the peak
being 21 days after treatment. The lowest dose tested, forwhich there was a significant MN induction, was 0.1 Gy. It isinteresting to remark that the baseline of micronuclei induction ranges over 2–3 orders of magnitude between different
fish species. In the medaka (Oryzias latipes), an X‑ray doseof 4 Gy (0.5 Gy/min) increased the frequency of MN toapproximately 7 per 1,000 gill cells. Knowles [K16] irradiated plaice using 137Cs sealed sources. He did not observe
any MN induction, even for the highest dose tested (1 mGy/hover 197 days, total dose of 4.6 Gy). The lack of sensitivityof this assay for fish could be linked to its application to nondividing cell populations or to dividing cell populations inwhich the kinetics of cell division are not well understood orcontrolled.
274. Ulsh et al. [U18, U19] used the fluorescence in situ
hydridization (FISH) technique in a study involving slider
turtles. They showed for Trachemys scripta fibroblasts andlymphocytes, that the dose rate below which no reduction in
effect per unit dose was observed with further dose protraction was about 230 mGy/h. Interestingly, they also showedthat this species had a much lower spontaneous backgroundof symmetrical translocations in lymphocytes than humans(30‑fold less), which makes it a sensitive species for the
study of low doses and dose rates.
275. Theodorakis and Shugart [T21, T22] found different
allele frequencies for mosquitofish populations exposed toradionuclides within the Oak Ridge nuclear site compared tofish in reference lakes. They showed that heterozygotes for287

the allozyme locus nucleoside phosphorylase (NP), an
enzyme involved in nucleoside synthesis, were more prevalent in fish in the radionuclide-contaminated sites and, moreover, that they had fewer DNA strand breaks than thehomozygotes. Finally, they showed that NP heterozygotes
had a greater fecundity than homozygotes.
276. Genetic adaptation, i.e. the genetic basis for resis­
tance, can be evaluated in populations exposed to a contaminant. The individuals that are not resistant are naturally
eliminated, while tolerant individuals can be bred. Subsequently, F1 and F2 generations can be tested for resistance.
If tolerance persists or increases in F1 and F2 generations,then the response can be said to be genetic. Further analyses can be conducted using molecular techniques to­investigate thoroughly the mechanisms involved. Suchexperiments have been scarcely performed, probably
because they are costly and time consuming. In a series of
papers, ­Theodorakis et al. used such an integrated approach,and demonstrated the effects of contaminants (mostly
radio­nuclide) on genetic patterns [T20, T21, T22, T23].
The bacterium Escherichia coli population became radio­
resistant after daily X‑­irradiation over many generations[E21], and it was shown that the most radioresistant strain
isolated from this population has the mutation(s) in genes
involved in ­inducible DNA repair [E9].
(d)Effects of acute exposure277. For primary producers, the information is still rather
limited (only 10 papers in the FRED), mainly describing
morphological changes and growth inhibition for green
microalgae at high doses (approximately 100–1,000 Gy).
Chromosome aberration at doses from 1–5 Gy was evident
in the macroalgae Nitella flagelliformis (as discussed in­reference [F5]).
278. From the information in the FRED, acute doses up to
1 Gy have no significant effects on species representative ofannelid, mollusc and crustaceans. Acute doses as low as
0.5 Gy can significantly decrease the percentage of live
embryos in broods of the particularly radiosensitive polychaete worm, Neanthes arenaceodentata. This radiosensitivity is confirmed by the finding of an increased incidence ofradiation-induced sister chromosome exchanges in juvenile
worms exposed at total doses greater than 0.17 Gy. The
explanation was that the response was due to the inductionof dominant lethal mutations in gametes of irradiated adultworms [F5].
279. For fish, the existing knowledge mainly relates toacute exposures greater than 5 Gy. Acute doses below 1 Gy
are unlikely to have any significant influence on their general
health (morbidity). Fish embryos are much more radiosensitive than free swimming larvae, juveniles and adults. Dosesless than 2 Gy are likely to have little effect on mortality. The
lowest dose reported in the FRED with significant effect, is
as low as 0.16 Gy delivered in the early 1‑cell stage of288

UNSCEAR 2008 REPORT: VOLUME II

development and the consequent mortality is scored overlong periods—150 days post fertilization. The developing
fish embryo is very sensitive to the effects of acute irradiation, particularly at the very early stages just prior to, or
immediately after the actual fertilization and during theprocess of division of the single cell. Irradiation of silver
salmon embryos at this stage gave an estimated LD50 of
0.16 Gy when assessed at 150 days post-irradiation. Apartfrom this critical period in embryonic development, ­FASSET[F5] concluded that it appears unlikely that significant effects
will follow doses below 0.5 Gy. An acute dose of this magnitude at any later stage of development will be unlikely tohave any significant influence on adult male and female fertility. Mutagenic damages (specific locus mutations, dominant and recessive lethal mutations, polygenic characters,
and chromosome aberrations) have been observed at allradia­tion doses used in the relevant studies. Where comparisons of relative radiosensitivity have been made, it has beenconcluded that fish show a sensitivity similar to, and mostoften less than, that of the mouse. There is a single example
of apparently greater sensitivity—for specific locus mutations induced in medaka sperm [R9]. Although there are nodata relating to radiation-induced mutagenesis in marine
fish, there is no reasonable basis for expecting them torespond differently from freshwater fish.
6.

Effects on populations and ecosystems

280. Ecosystems consist of various organisms that have awide range of radiosensitivities and interact with one anotherin a complex fashion. As a result, indirect responses to thedirect effects of radiation exposure are observed in the­natural environment. Since these indirect responses cannot
neces­sarily be deduced from the effects on individuals andpopulations, effects at the community level are evaluated bymathematical modelling, model ecosystem experiments andfield irradiation experiments.
281. In mathematical modelling, physical, chemical andbiological components of natural ecosystems and interactions among them are mathematically defined, and ecosystems are simulated in computers. Effects on the entire
ecosystems are evaluated by applying single-species effectdata to the mathematically constructed ecosystems. For
example, Bartell et al. developed a comprehensive aquaticsystems model (CASM) [D6]. The CASM model is a bio­energetic ecosystem model that simulates the daily production
dynamics of populations (including predator–prey interactions) with time, in relation to daily changes in light intensity,
water temperature, and nutrient availability. This model has
been adopted for estimating the ecological risks of chemicals
for aquatic ecosystems in Quebec [B24], central Florida[B25] and Japan [N7]. In time, this type of model will also be
useful for the evaluation of the effects of radiation exposure.
282. Model ecosystem experiments provide biotic or ­abiotic
simplicity, controllability and replicability, which cannot be
expected in field experiments. At the same time, they

simulate the inter-species interactions of natural ecosystems.
It is therefore expected that model ecosystem experiments
can investigate the indirect effects of radiation exposure,which cannot be evaluated by conventional single-species
experiments. Model ecosystem experiments can therefore be
regarded as a bridge between single-species experiments andfield experiments. Some model ecosystem experiments havebeen performed to investigate the effects of radiation exposure. For example, Williams and Murdoch [W14] made studies using two different types of marine model ecosystems.
However, no effects for 23 possible effect endpoints wereobserved at dose rates of up to 0.79 Gy/d.
283. Ferens and Beyers [F18] acutely irradiated aquaticmodel ecosystems derived from a sewage oxidation pondconsisting of various kinds of microorganisms. Effects onbiomass, chlorophyll content and gross-community meta­bolism were more severe at doses of 1,000 Gy than at
10,000 Gy. This unexpected phenomenon might arise fromthe disappearance of inhibitory inter-species interactions
after elimination of certain species at doses of 10,000 Gy.
284. Fuma et al. [F19] studied effects of acute gamma irradiation on the aquatic model ecosystem consisting of theflagellate alga, Euglena gracilis, as a producer, the ciliate
protozoan, Tetrahymena thermophila, as a consumer and thebacterium, Escherichia coli, as a decomposer. After a doseof 1,000 Gy, the cell density of T. thermophila was increased
temporarily, and then decreased compared with controls.
This complicated change in T. thermophila might be an indirect response to direct effects on the other species, i.e. extinction of E. coli and decrease in Eu. gracilis. Doi et al. [D7]mathematically simulated a dose–effect relationship for thisexperimental model ecosystem with a particle-based model,
in which inter-species interactions were taken into consideration. This suggests that experimental model ecosystems
are useful for validation of mathematical models.
285. Hinton et al. [H12] constructed a Low Dose-Rate Irradiation Facility (LoDIF) in the Savannah River Ecology
Laboratory (Aiken, South Carolina, USA). This facility consists of outdoor open-air tanks and is designed to house avariety of aquatic organisms. Gamma irradiation is conducted with an irradiator placed over each tank. Each irradiator contains a 0.74, 7.4 or 74.0 MBq sealed 137Cs source. The
7.4 MBq source delivers a mean dose rate of approximately
10 mGy/d. The LoDIF is now used only for studies of theeffects of chronic irradiation on the reproduction of small
fish (Japanese medaka; Oryzias latipes), but can be used as
an experimental model ecosystem.
286. Some field irradiation experiments have been performed, though these have already been terminated. The
Brookhaven Irradiated Forest Experiment is a typical example. This experiment was designed to study the effects ofradia­tion exposure on plant and animal communities [W15].
In 1961, a 350 TBq 137Cs source was placed in an oak–pine
forest at the Brookhaven National Laboratory (Upton, New
York, USA). The dose rate within a few metres from theANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

source was in the order of 10 Gy/d; it decreased to backgroundlevels beyond 300 m. After commencement of irradiation,
biomass, species composition, densities and other ecologicalpara­meters were measured for plants, insects, fungi, lichensand soil algae. Many examples of the indirect effects describedin the UNSCEAR 1996 Report [U4] were observed in a seriesof experiments conducted with this source.

289

radiation had not shown any individual or population effectfrom chronic exposure to low-LET external radiation in therange of 10–100 mGy/d and that the current guidelines in therange of 1–10 mGy/d appeared suitable as benchmarks forgeneral environmental protection purposes [M11].
288. Simulation can be used to illustrate population-level
effects arising from individual effects with different endpoints.
By modelling the delay in population growth on the basis of
the observed effects on individual traits (figure XV), simulation of the effects of chronic exposure to radionuclides at the
population level appeared to be mediated through individualeffect endpoints as follows: (a) effects on the hatchability of
cocoons and the number of hatchlings per hatched cocoon forearthworms; and (b) effects on larval resistance to starvation
for daphnids. Ultimately, effects increase the early mortalityof larvae in both species (offspring are produced but they
never reach reproduction age) which are, with regard to population dynamics, equivalent to not producing those offspring.
Observed effects can be assimilated to a reduction in fecundity in every case: 10% reduction in fecundity in earthworms
at a dose rate of 4 mGy/h (point A on figure XV), 55% reduction in fecundity in earthworms at a dose rate of 11 mGy/h(point B on ­figure XV), 70% reduction in starved control
daphnids and up to 100% reduction (i.e. extinction) in starved
contaminated daphnids independent of the dose rate (point C
on figure XV). The last result indicates that this species
becomes more vulnerable to food depletion for the radio­
nuclide-contaminated environment than for non-contaminatedhabitats [G3].

287. Two field-irradiation experiments were conducted at
the Whiteshell Laboratories in Manitoba, Canada. One is the
Field-Irradiated Gamma (FIG) experiment in which a boreal
forest was chronically irradiated from 1973–1986 to study
the effects on plant communities [G13]. The radiation source
was 370 TBq 137Cs, and the dose rates ranged from 0.12–
1,560 mGy/d. The effects of radiation exposure were investigated for tree canopy, naturally growing shrubs, groundcover species, germination of seeds, morphological change
and tree-ring growth. One experimental observation was thatthe seed germination of Jack Pine showed deleterious effects
at a dose rate of 1.1 mGy/h [S38]. In contrast, reference[S38] reported hormetic effects (increased germination) at
dose rates up to 0.6 mGy/h. The other experiment was the
Zoological Environment Under Stress (ZEUS) that was performed from 1981–1985 to study the effects on the individual or population characteristics of meadow voles [M11].
Vole populations were irradiated at nominal dose rates of200, 9,000 and 40,000 times that from natural backgroundradiation. No effects on individual or population-level characteristics were observed at a dose rate up to 81 mGy/d, thehighest dose rate used. Mihok noted that experiments with

Figure XV. Relationship between effects at the individual level and their relative consequence at the population level (fromreference [G3])Earthworms chronically exposed to external gamma radiation: A: 10% reduction in fecundity at 3.3–3.6 mGy/h; B: 55% reduction in fecundity
at the dose rate of 9–9.5 mGy/h. Daphnids chronically exposed to internal alpha radiation (241Am); C: 70% reduction in starved control and up
to 100% reduction (i.e. extinction) independent of the dose rate
Delay in population growth(up to 50,000 daphnids)

Delay in population growth(up to 50,000 worms)
1

RELATIVE CHANGE IN
INDIVIDUAL ENDPOINT

RELATIVE CHANGE IN
INDIVIDUAL ENDPOINT

1
0.8
0.6
0.4

C

0.2
0
0.0

A

0.8
0.6

Survival
Fecundity
Age of reproduction

B

0.4
0.2
0

0.2

0.4

0.6

0.8

RELATIVE DELAY
IN POPULATION GROWTH

1.0

0.0

0.2

0.4

0.6

0.8

RELATIVE DELAY
IN POPULATION GROWTH

1.0

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289. The consequences of radiation exposure at the population level depend on the particular stage in the life historyof the organism. Small effects on individual endpoints critical for population dynamics may impair population growthrate to a greater extent than large effects on neutral individual endpoints. The impact of chronic exposure to radio­
nuclides at the population level depends on which stage inthe life history is impaired. Individual endpoints do not show
the same importance at the population level, population
growth being by far more sensitive to changes in age ofreproduction than changes in fecundity or survival [A26,G3] (figure XV).

radiation damage to individuals to an acceptable degree will
also provide a sufficient degree of protection for populations. However, in situations where the most sensitive life
stage has not been positively identified, or where there is alack of data on the most sensitive life stage, there may be aneed to introduce a margin of safety when using the available dose–effect information on individual life stages todevelop measures to protect field populations. Furthermore,
population-level consequences of hereditary mutations
might in some cases need to be allowed for in these extrapolations. If and how this might be done requires additional
research and scientific review [G16].

290. Specific studies have provided evidence linking
geno­toxic syndrome to population-level changes [T20, T21,
T22, T23]. Trabalka and Allen [T19] raised 2 generations ofmosquitofish collected from a radionuclide-contaminatedsite. They showed that fish from the F2 generation were lesstolerant to thermal stress than fish from the control site.

294. Most studies of the effects of exposure to ionizing
radiation have been performed under non-limiting growth
conditions (i.e. sufficient food and space were available).
In contrast, wild organisms are often regulated by various
types of density-dependent factors such as competition forresources. Based on current knowledge, it is hard to draw
general conclusions on how density-dependent factors
may influence the propagation of effects on individuals to
populations [G16].

291. Mutations occur at the molecular level, but heritable
mutations in germ cells are capable of affecting the genetic
diversity of populations, and can lead to increased or
decreased genetic diversity, as well as to changes in phenotype that can affect Darwinian fitness. Increases in mutation
rate can increase genetic diversity of the population by producing new alleles or genotypes, but they can also result in
decreased genetic diversity, since the mutations could reducethe viability or fertility of the individuals [T14]. Consequently, increases in mutation rate can affect the genetic
structure of the population, and thereby have ecologically
relevant effects.
292. Exposure to contaminants can lead to alterations in
the genetic makeup of populations, a process termed evolutionary toxicology. It is generally hypothesized that there isan alteration of genotype frequencies and a reduction in
genetic variation in genotoxicant-contaminated environments. These changes may occur as a result of selection on
specific alleles, selection for multi-locus genotypes, mortality in specific life stages, and changes in breeding period.
They may induce reduction in population size, alterations in
the degree of inbreeding, alteration of the level of gene flow
and changes in age or class structure. Potentially, these shifts
may alter population viability and fitness. Theodorakis andShugart [T21] observed a higher percentage of polymorphism and heterozygosity in mosquitofish from the radio­
nuclide-contaminated site, correlated with a higher fitness
and lower level of DNA strand breaks. These findings suggest that there is a selective advantage in radionuclide-­contaminated areas. More surprisingly, they found a higher
genetic diversity in the radionuclide-contaminated populations, for which no definite explanation was given. The
authors hypothesized that the higher diversity was linked togenomic rearrangements or different life-history processes.
293. Even though several factors complicate extrapolationsof individual-level effects to populations, current knowledge
supports the conclusion that measures intended to limit

295. In its 2008 report, the ICRP [I10] suggested that, in
considering the potential effect of exposure to ionizing radia­tion, context should be provided by comparing the estimateddose rates to multiples of the dose rates experienced by thevarious biota in their natural environment. In this regard, the
ICRP proposed the use of the concept of “Derived Consideration Levels” (DCLs) which were intended to serve as
points of reference for assessing the potential effects of
exposure to ionizing radiation on non-human biota. In doing
this, the ICRP compiled available information for their various biota categories and summarized the data into bands ofdose rate from less than 0.1 to more than 100 mGy/d. In
commenting on the available data, the ICRP emphasized thatthe data are both incomplete and of varied quality and that
their summary tables represent “an extreme oversimplification of existing data”. The range of DCLs (dose rates) for
various biota categories (e.g. mammals, birds, and trees)summarized by ICRP were:– With regard to the mammals (“higher vertebrates”),
deer and rat, the ICRP suggested that at dose rates
in the region of 0.1–1 mGy/d, there was only avery low probability of certain effects occurringthat could result in reduced reproductive success or
morbidity. At dose rates in the band of 1–10 mGy/d,there was some potential for reduced reproductive
success;– For birds (the reference bird was the duck), the
ICRP suggested that based on metabolism, longevity, and reproductive behaviour, it was reasonable
to assume similar results to those for mammals;– With regard to the “lower” poikilothermic vertebrates (frog, trout and flatfish), data are generally
lacking below about 1 mGy/d. However, considering the general lack of physiological data on

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

amphibians, the ICRP suggested a lower DCL(dose-rate) band of 0.01–0.1 mGy/d for frogs
compared to the two types of fish. For dose rates
in the range of 1–10 mGy/d, the ICRP suggested
that some reduction in reproductive capacity mightoccur in frogs and possibly also in fish species;– The ICRP indicated that there are essentially nodata for the invertebrates, bee, crab and earthworm,

V.

291

but suggested that invertebrates are less sensitiveand recommended a DCL of 10–100 mGy/d; and– The data for trees, plants and seaweeds are highlyvariable across species, the best data being for pinetrees. The ICRP suggested DCLs of 1–10 mGy/dfor grasses and seaweeds but a 10‑times lower
value for pine trees, which they attribute in part totheir potential for very long periods of exposure.

Summary and conclusions

296. All living organisms have existed and developed inenvironments where they are exposed to ionizing radiationfrom the natural background and, recently, to radiation
resulting from global fallout of radioactive material following the atmospheric nuclear weapons tests. In addition, biota
are exposed, generally in areas of limited spatial extent, toradiation from man’s activities, such as the controlled discharge of radionuclides to the air, ground or aquatic systems,
or from accidental releases of radionuclides.
297. Prior to the development of the annex, “Effects ofradiation on the environment” of the UNSCEAR 1996
Report [U4], the Committee had not specifically addressed
the effects of radiation exposure on plant and animal communities. Living organisms had been considered primarily
as part of the environment in which radionuclides might bedispersed and as resources that, if they took up radio­
nuclides, might contribute to human exposures via thehuman food chains. Like humans, however, organisms arethemselves exposed internally from radionuclides that they
may have taken up from the environment, and externally
due to radiation from radionuclides in the environment.
298. In the past decades, scientific and regulatory activities
related to radiation protection focused on the radiation exposure of humans arising from both artificial and natural
sources. The prevailing view was that, if humans were adequately protected, then “other living things are also likely tobe sufficiently protected” [I8] or “other species are not put atrisk” [I5]. Over time, the general validity of this view has
been challenged on occasion and more attention has therefore been given to the potential effects of exposure to ionizing radiation on non-human biota. In part, this has occurred
as a result of the increased worldwide concern over sustainability of the environment, including the need to maintainbiodiversity and protect habitats or endangered species (e.g.
[U22, U23]), and, in part, as a result of various efforts toassess the effects of exposure to ionizing radiation on plants
and animals [D1, I1, I2, I3, I4, I9, N6, T1].
299. Since the Committee issued its first report in 1996
[U4] on the doses and dose rates of ionizing radiation below
which effects on populations of non-human biota areunlikely, the approaches to evaluating radiation doses havebeen reviewed and progress has been made (e.g. by the DOE[U26], the Environment Agency [C1], FASSET [F1], ERICA[E1]). In addition, the continuing follow-up of the consequences of the Chernobyl accident has provided a great dealof new information on the radiobiological effects of ionizing
radiation exposure on non-human biota (e.g. [E8, G26]).
Similarly, information not previously available to the Committee on the levels of radiation exposure below whichradio­biological effects on non-human biota are unlikely has
been further compiled and evaluated, in part, through thework carried out in support of the development of the­FASSET effects database, FRED, and the subsequent­FREDERICA effects database [B26, E1, F1]. The Committee undertook a review of the new scientific information that
had become available since its previous report and assessed
whether it needed to modify its previous recommendations
concerning the dose rates below which effects on non-humanbiota are considered unlikely.

A. Estimating dose to non-human biota
300. The radiation dose received by an organism (or someorgan or tissue of the organism) is the sum of both the external and internal exposure. Absorbed doses are calculated as
the dosimetric endpoint; however, for radionuclides taken
into the organism, an appropriate factor may be applied inorder to account for the different RBEs of the different kindsof radiation.
301. External exposures of biota are the result of complex
and non-linear interactions of various factors, such as thelevels of radionuclides in the habitat, the geometrical relationship between the radiation source and the target, theshielding properties of materials in the environment, the sizeof the organism and the radionuclide-specific decay properties (characterized by the radiation type, the energies emitted
and their emission probabilities).
302. Internal exposures of plants and animals are determined by the activity concentration in the organism, the sizeof the organism, the radionuclide distribution and the specificdecay properties of the radionuclide.
303. In considering the potential effects of ionizing radiation exposure on non-human biota, the Committee assumed

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that natural populations of non-human biota are in a state ofdynamic equilibrium within their environment. Equilibrium
models assume that radionuclide concentrations reach equilibrium within various environmental compartments and thattransfer between compartments is reasonably characterizedby time-invariant ratios of concentration between the compartments. One of the advantages of the equilibrium model is
its simplicity. Such models are widely used by national regulators for assessment purposes. However, when it is necessary to assess a time-dependent response—for example,
when considering an accidental release of radio­nuclides—
dynamic radioecological models are needed. Within the context of this annex, equilibrium ­models have been assumed in
the exposure assessments, unless otherwise indicated. Readers interested in dynamic radioecological models are referredto the published ­literature [M4, M7, S1, W3].
B. Summary of dose–effects datafrom the UNSCEAR 1996 Report304. Notwithstanding the limitations of the data available
in 1996, the Committee considered it unlikely that radiation
exposures causing only minor effects on the most exposed
individual would have significant effects on the population.
It also suggested that the effects of radiation exposure at the
population and community levels are manifest as somecombination of direct changes due to radiation damage andindirect responses to the direct changes [U4].
305. The Committee considered that the individual
responses to radiation exposure likely to be significant at
the population level are mortality (affecting age distribution, death rate and density), fertility and fecundity (bothaffecting birth rate, age distribution, number and density)and the induction of mutations (birth rate and death rate).
The response of these individual functions to radiation
exposure could be traced to events at the cellular level in
specific ­tissues or organs. An extended summary discussing the pro­cesses involved had been provided in annex J,“Non-­stochastic effects of irradiation”, of the UNSCEAR
1982 Report [U9]. The Committee also considered there
was a substantial body of evidence indicating that the mostradiosensitive sites are associated with the cell nucleus,
specifically the chromosomes, and that, to a lesser extent,
damage to intracellular membranes was additionallyinvolved. The end result is that the cells lose their reproductive potential. For most cell types, at moderate doses,
death occurs when the cell attempts to divide; death does
not, however, always occur at the first post-exposure division: at doses of a few gray, several division cycles might
be successfully completed before death eventuallyoccurred. It was also well known that radiosensitivity varies within the cell cycle, with the greatest sensitivities
being apparent at mitosis and the commencement of DNA
synthesis [U9]. It followed that the greatest radiosensitivity is likely to be found in cell systems undergoing rapid
cell division for either renewal (e.g. sperma­togonia) or
growth (e.g. plant meristems and the developing embryo);these examples clearly underlie the processes in individualorganisms that are important for the maintenance of the
population. Effects of radiation exposure on populations
occur as the result of exposure of individual organisms.
The propagation of effects from individual organisms topopulations is complex and depends on a number of factors; however, the Committee considered that of the various effects on populations of non-human biota, the key
effects are those that affected reproductive success.
306. The Committee noted that the responses of organisms
to radiation exposure are varied and might become manifest
at all levels of organization, from individual biomolecules toecosystems. The significance of a given response depends onthe criterion of damage adopted, and it was not to be concluded that a response at one level of organization would
necessarily produce a consequential, detectable response at ahigher level of organization.
307. In its 1996 assessment, the Committee considered that
reproductive changes are a more sensitive indicator of theeffects of radiation exposure than mortality, and mammals
are the most sensitive animal organisms. On this basis, theCommittee concluded that chronic dose rates of less than
100 μGy/h to the most highly exposed individuals would be
unlikely to have significant effects on most terrestrial animal
populations. The Committee also concluded that maximum
dose rates of 400 μGy/h to a small proportion of the individuals in aquatic populations of organisms would not haveany detrimental effect at the population level. These conclusions refer to the effects of low-LET radiation. Where a significant part of the incremental radiation exposure comesfrom high-LET radiation (especially alpha particles) that isinternal to the organism, it is necessary to apply an appropriate factor to adjust for the different RBEs of the different
radiations.
308. Acute lethal radiation doses to plants had been noted
to range from 10–1,000 Gy. In general, larger plants are
more radiosensitive than smaller plants, with radiosensitivity
decreasing in the order coniferous trees, deciduous trees,
shrubs, herbaceous plants, lichens [U4]. The data on radiosensitivity of terrestrial animals were dominated by data on
mammals, the most sensitive class of organisms. Acute lethal
doses (LD50/30) were 6–10 Gy for small mammals and 1.5–
2.5 Gy for larger animals and domestic livestock [U4]. The
Committee concluded [U4] that the effects of radiation
exposure on birds are similar to those in small mammals.
Separately, it [U4] found that reptiles and invertebrates areless radiosensitive than birds, with studies of acute radiation
exposures of adult amphibians indicating LD50 values ofbetween 2–22 Gy. With respect to aquatic organisms, fish are
the most sensitive to the effects of radiation exposure; thedeveloping fish embryos are particularly so. The LD50 for
acute irradiation of marine fish is in the range of 10–25 Gy
for assessment periods of up to 60 days following exposure[U4]. Overall, a notional range of dose of 1–10 Gy fromacute radiation exposure is unlikely to result in effects on
populations of non-human biota.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTAC.

The current evaluation

309. Many of the new data subsequent to the Committee’s
1996 report [U4] arose from follow-up studies of the consequences of the Chernobyl accident. Prior to the accident,much of the area around the Chernobyl nuclear power plant
was covered in 30–40-year old pine stands that, from a successional standpoint, represented mature, stable ecosystems[E8]. The high dose rates during the first few weeks following the accident altered the balance in the community andopened niches for immigration of new individuals. All thesecomponents and many more, were interwoven in a complex
web of action and reaction that altered populations and communities of organisms. In addition to the effects from theradiation exposure, activities such as agriculture, forestry,hunting and fishing within the 30‑km zone were stopped[E8]. Moreover, after the accident, the agricultural fields
remained productive for a number of years and, in theabsence of active management of areas that had been evacuated, many animal species, especially rodents and wild boar,
consumed the abandoned cereal crops, potatoes and grasses
as an additional source of forage [E8]. This advantage, alongwith the special reserve regulations established in the exclusion zone (i.e. a ban on hunting) tended to mask potential
adverse biological effects of radiation exposure and led to anincrease in the populations of wild animals, including gamemammals (wild boar, roe deer, red deer, elk, wolves, foxes,
hares, beaver, etc.) and bird species (black grouse, ducks,etc.) [G8, S23]. The exclusion zone has become a breedingarea of the white-tailed eagle, spotted eagle, eagle owl, craneand black stork [G9].
310. Overall, based on an evaluation of the available dataarising from studies of plants and animals in the zone
around the Chernobyl nuclear power plant, the Chernobyl
Forum [E8] arrived at a number of general observations,
including:– Radiation from radionuclides released as a resultof the Chernobyl accident caused numerous acute
adverse effects on the biota located in the areas ofhighest exposure (i.e. up to a distance of a few tensof kilometres from the release point);– The environmental response to the increased radiation exposure incurred as a result of the Chernobyl
accident was a complex interaction among radiation dose, dose rate and its temporal and spatial
variations, as well as the radiosensitivities of thedifferent taxons. Both individual and population
effects caused by radiation-induced cell death
were observed in plants and animals and included
increased mortality of coniferous plants, soil invertebrates and mammals; reproductive losses inplants and animals; and chronic radiation sickness
in animals (mammals, birds, etc.);– No adverse radiation-induced effects were reported
in plants and animals exposed to a cumulative doseof less than 0.3 Gy during the first month after theaccident (i.e. <10 mGy/d, on average); and293– Following the natural reduction of exposure levels
due to radionuclide decay and migration, populations have been recovering from acute radiation
effects. By the next growing season following theaccident, the population viability of plants andanimals substantially recovered as a result of the
combined effects of reproduction and immigration. A few years were needed for recovery frommajor radiation-induced adverse effects in plants
and animals.
311. Another, and even more recent comprehensive
review of the effects of radiation exposure arising from the
Chernobyl accident on non-human biota compiled andexamined the data on effects along with the associateddosimetric information [G26]. The authors evaluated
250 references in total, of which, some 79 papers wereconsidered to have adequate information on environmental
contamination and doses to biota as well as information on
the associated effects. The effects of radiation exposure
were seen in both natural and agricultural systems. Consistent with the Committee’s 1996 report [U4], the authors
noted that the effects depended on the radiosensitivity ofthe dominant species and observed that coniferous trees
are one of the most sensitive plant species and mammals
are the most radiosensitive animal species. Table 27 summarizes the various effects seen in non-human biota
around the Chernobyl nuclear power plant and the corresponding doses or dose rates below which such effects
were not observed.
312. Alexakhin et al. [A29] reported on the environmental and agricultural impact of the Chernobyl accident.
These authors described the effects of countermeasureson the doses to ecosystems and the public. High radiation
doses within the 30‑km exclusion zone led to numerous
effects on biota ranging from subtle effects at the molecular and subcellular levels, to significant degradation of
ecosystems, pine stands for example. On the other hand,evacuation of people from the 30‑km zone reduced
stresses arising from human use of the environment.
Exclusion of people, along with the special reserve regulations established in the exclusion zone (i.e. a ban on
hunting) overcame potential adverse biological effects ofradiation exposure and led to an increase in the populations of wild animals and birds. Based on an evaluation of
the FRED database, FASSET concluded that the information available on the effects of radiation exposure on nonhuman biota from low dose rates (less than about
100 µGy/h or 2.4 mGy/d) for continuous irradiation isreasonable for both plants and animals and that, forchronic exposure conditions, “the reviewed effects data
give few indications for readily observable effects at
chronic dose rates below 100 µGy/h”. However, it advisedthat “using this information for establishing environmentally ‘safe levels’ of radiation should be done with caution, considering that the database contains large
information gaps for environmentally relevant dose rates
and ecologically important ­wildlife groups” [F5, R9].

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313. For chronic exposures, the ERICA project used statistical methods to estimate the dose rates below which 95% of
species in the aquatic/terrestrial ecosystems should be protected. Their analysis of the data on effects from external
gamma irradiation of species of different ecosystems concluded that there was no statistical justification to attempt toderive ecosystem specific screening dose rates and hence alldata were analysed together as a “generic” ecosystem. The
resultant dose rate that would protect 95% of the species in
the generic ecosystem was estimated at 82 µGy/h (with 95th
percentile confidence intervals of 23.8 and 336 µGy/h). Thisis generally consistent with the Committee’s 1996 assessment [E11, G27]. It should be noted that these authors
implicitly adopted a further safety factor of 5 in an attempt toaccount for data limitations.

and shoot growth at absorbed doses as low as 0.7–1 Gy[K1]. Information has been reported [G3] that shows adecrease in population density and species composition offorest litter mesofauna at doses in the range of 1–9 Gy.
Based on a review of the FRED, FASSET concluded that
acute doses of up to 1 Gy have no significant effect onannelids, molluscs and crustaceans, that acute doses below
about 1 Gy are unlikely to have a significant effect on general health (morbidity), and that doses below about 0.5 Gy
are unlikely to have any significant effect on adult maleand female fertility [F5]. When the SSD method wasapplied to data on the effects of acute exposures, HDR5
values in the range of about 1–5.5 Gy were estimated.
Thus, on the basis of the available data, the Committee
continues to recommend a nominal reference dose of about
1 Gy, within a factor of 2 or so, as a reference value below
which population-­level effects on non-human biota areunlikely in the event of an acute exposure.

314. ERICA also applied the same statistical methods tothe data on effects for acute exposure conditions but in thiscase, a statistically significant difference was seen between
marine ecosystems compared to terrestrial and freshwater
ecosystems. The values derived from a statistical analysisof the set of doses giving a 50% change in the observed
effect for limiting the potentially affected fraction to 5% of
the species under acute external gamma irradiation varied
from about 1–5.5 Gy, according to the ecosystems type,with the associated 95% confidence intervals covering lessthan one order of magnitude. For screening purposes,
ERICA applied a further SF of 5 and reported Predicted
No-Effect Doses (PNED) of 900 mGy for marine ecosystems and 300 mGy for terrestrial and freshwater ecosystems [G3, G15, G27]. The application of such additionalsafety factors is of great interest in developing regulatory
approaches for the protection of non-human biota; however, such judgements are beyond those of the Committee
and properly lie in the domain of the ICRP and national
authorities.

D. Conclusions
316. As discussed in the UNSCEAR 1996 Report, theCommittee considered it unlikely that radiation exposurescausing only minor effects on the most exposed individual
would have significant effects on the population. It also
considered that reproductive changes are a more sensitive
indicator of the effects of radiation exposure than mortality,
and that mammals are the most sensitive animal organisms.
Since 1996, new data on the effects of exposure to ionizing
radiation have been developed from follow-up observationsof non-human biota in the zone around the Chernobyl
nuclear power plant (section III) and various organizations
have carried out comprehensive reviews of the scientific
literature on the data on effects and, in some cases, developed new approaches to the assessment of the potential
risks to non-human biota (section IV). There is a considerable range of endpoints and corresponding effects levels(dose or dose rate) presented in the literature and also considerable variation in how different researchers have evaluated these data. Table 39 provides a summary of the data on
the effects of radiation exposure for aggregated categories
of biota. Details of endpoint effects are described in thecorresponding references.

315. Information on the effects of acute doses of radiation has also been reviewed. For example, soil fauna areunlikely to be affected at doses below about 1 Gy [G3].
The same authors reported data that suggested that the
reproductive capacity of Scots pine is inhibited at doses in
the range of 0.5–5 Gy. The radiosensitivity of spruce isgreater than that of pines with malformed needles, buds,

Table 39.

Overall summary of data on chronic effects of radiation exposure for plants, fish and mammals

Category

Dose rate(μGy/h)Plant

100–1 000Fish

Effects

Endpoint

Reference

Reduced trunk growth of pine trees

Morbidity[W4]

400–700

Reduced numbers of herbaceous plants

Morbidity[G26]

100–1 000

Reduction in testis mass and sperm production, lower fecundity,
delayed spawning

Reproduction[H11, K16, N1]

200–499

Reduced spermatogonia and sperm in tissues

Reproduction[C11]

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

Category

Dose rate(μGy/h)Mammals<100

Generic ecosystems(terrestrial and aquatic)

about 80

Effects295

Endpoint

Reference

No detrimental endpoints have been described

Morbidity,
mortality,
reproduction[C17, L2, P8,
R9, U21, Y2]

A new statistical approach (species sensitivity distribution, SSD) wasapplied to the data on radiation effects to estimate HDR5 , the dose
rate at which 95% of the species in the ecosystem are protected

Morbidity,
mortality,
reproduction[G3, G11, G15]

317. Overall, the Committee concluded that chronic dose
rates of less than 100 μGy/h to the most highly exposed
individuals would be unlikely to have significant effects onmost terrestrial communities and that maximum dose rates
of 400 μGy/h to any individual in aquatic populations oforganisms would be unlikely to have any detrimental effectat the population level. For acute exposures, significant
effects on populations of non-human biota are unlikely atdoses below (about) 1 Gy. These conclusions refer to theeffects of exposure to low-LET radiation. Where a significant part of the incremental radiation exposure comes fromhigh-LET radiation (alpha particles), the Committee concluded that it is necessary to take account of the different
RBEs of the radiations.
318. In addition to new data on the levels at which theeffects of radiation exposure have been observed, notably
from follow-up studies of the consequences of the ­Chernobyl
accident, various authors have investigated new analyticalmethods, notably that of species sensitivity distribution[G3, G11], which involves meta-analysis of the variations inradiosensitivity among species. However, at this time, insufficient data are available for the application of such methods. It is anticipated that as new information is developed in
the future, the application of these new methods of analysis
will facilitate future re-evaluations of the effects of ionizing­radiation exposure on non-human biota.

319. A great deal of work has been done since 1996 to
improve the data and methods for evaluating pathways throughwhich biota are exposed to radiation from radioactive material
in the host environment and many improvements in biota
dosimetry have been made. However, many opportunities still
remain to improve our understanding of the relation between
the levels of radioactive material in the environment and thepotential effects on biota residing in that environment.
320. Based on the new information described in this annex,
and considering the overall limitations of the available data,
the Committee considered that there is no need to change its
previous conclusions of the values of nominal chronic dose
rates below which direct effects on non-human species areunlikely at the population level. Nonetheless, where data ofsuitable scientific quality are available for a specific species
endpoint and/or other level of biological organization, theCommittee would encourage their use in assessments of thepotential effects of radiation exposure. However, there arevery limited data for many taxa and therefore many assumptions are needed to extrapolate between species. There is aneed to better understand the chronic effects at a multigenerational time scale, chronic effects for multiple stressors, andthe propagation of effects at the molecular and cellular levels
to higher levels of ecological organization. In this respect, theapplication of so-called “-omic” techniques (transcriptomic,
proteomic and so on) will help in future assessments.

ACKNOWLEDGEMENTS
321. The Committee gratefully acknowledges the considerable help received by the principal consultants, D. Chambers

and G. Kirchner, from M. Doi, J. Garnier-Laplace, J‑J. Leguay,
G. Pröhl, K. Sakai and D. Woodhead.

ANNEX E: EFFECTS OF IONIZING RADIATION ON NON-HUMAN BIOTA

297

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