SOURCES AND EFFECTS
OF IONIZING RADIATION
United Nations Scientific Committee on the Effectsof Atomic Radiation
UNSCEAR 1996 Report to the General Assembly,
with Scientific Amex

UNITED NATIONSNew York, 1996

NOTE
The repon of the Committee without its scientific annex appears as Official Records of theGeneral Assembly, Fifty-first Session, Supplement No. 46 (A151146).
The designation employed and the presentation of material in this publication do not imply
the expression of any opinion whatsoever on lhc parr of thc Secretariat of the United Nations
concerning the legal slarus 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 rhis document are, in most cases, those that were in use at thetime the data 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
Sales No. E.96.1X.3
ISBN 91-1-142219-1

ANNEX
Effects of radiation on the environment

CONTENTSPage

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
I.

DOSIMETKY FOR ENVIRONMENTAL. EXPOSURES . . . . . . . . . . . . . . . . 9
A . METHODS O F DOSE ESTlh/lATION . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
B . DOSE CALCULATIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1
I . Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 1
2 . Anirnals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I5
C. COMPARISONS O F ENVIRONMENTAL EXPOSURES . . . . . . . . . . 18
D . SUMMARY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

I1 . EFFECTS O F RADIATION ON PLANTS AND ANIMALS . . . . . . . . . . . . 20
.4. TERRESTRIAL PLANTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
I . Cultivated and pasture crops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
7 . Forest trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3-3
3 . Shrubspccies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
1. Herb communities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
5 . Lichens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
6 . Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
7. Indirect effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
8. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
B . TERRESTRIAL ANIMALS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
1 . Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
2 . Birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
3 . Reptiles and amphibians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
4. Invertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3s
5 . S u m m a y . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
C . AQUATICORGANISMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
D . CLASSIFICATION O F RADIOSENSITIVITIES . . . . . . . . . . . . . . . . . 43
111. EFFECTS OF RADIATION ON POPULATIONSO F PLANTS A N D ANIMALS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
A . STUDY LIMITATIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44

USSCEAR 1996 REPORT

8

B.
C.

D.

EFFECTS ON PLANT POPULATIONS AND COMMUNITIES . . . . . 46
EFFECTS ON ANIMAL POPULATIONS AND COMMUNITIES.. .. 47
1. Terrestrial environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
2. Aquatic environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
3. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50
EFFECTS OF ACCl DENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 1
1. The accident in the southeastern lJrals . . . . . . . . . . . . . . . . . . . . . . . 52
2. The Chernobyl accident . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
3. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57

CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
Tables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77

INTRODUCTIONI.
The effects of radiation on plant and animalcommunities have not so far been specifically addressedby the Committce. Living organisms have primarily
been considered as part of the environment in whichradionuclides become dispersed and as resources which.
\vhen contaminated, may contribute to humanesposures. For example, some plants and animals are
elenicnts of food-chains and represent path\vays for thetransfer of radionuclides to man and an eventual sourceof internal exposure. Like man. ho\vever. otherorsanisms are themselves exposed to internal irradiationfrom accumulated radionuclides and to esternal
exposure from contamination of both the living andinanimate components of their environment.
In the absence of reports of obvious deleterious
2.
effects in other organisms from environmental
radiation, either natural or frorri controlled releases ofman-made radionuclides, it has generally been acceptedthat priority should be given to evaluating the potential
consequences for man. \+ho is among the mostradiosensitive mnrnmalian specics, and to providing asound basis for protecting hu~nanhealth. This positionhas. however. been questioned recently [D-l. TI 1. and it
has been shown that there is at least one situation.
namely in deep-sea sediments, an en\ironnient very
remote from man, \vilere the above accepted priority
could be incorrect 1131. It should also be noted thatdetrimental effects on the environment have been

observed in localized areas as a consequencu of plants andanimals having received short-tenn, bier)' high radiation
doses follo\ving major accidental releases of ndionuclides,
c.g. in areas alfccted by the southeastern Urals accident of1057 and the Cliernobyl accident of 1986.
3.
In response to such concerns. and to demonstrateesplicitly that li~llaccount can be, and is being, taken oftlie potential cfl'ects of radiation on the environment.
reports have been prepared that consider a number of
specific situations, e.g. fresh-\\rater and terrestrial
environments [14. M5. NI], the deep ocean [I31 andcoastal kvaters IW9]. In view of these many activities, itu.ould seem lo be an appropriate time for theCommittee to make an independent revie\v of thesituation and summarize the present state of knowledgeof the impact of ionizing radiation on plant and animal~~opulationsin natural and contaminated environments.
Such a summary \vould, of necessity, draw upon theprevious. niorc li~nited revieus and studies. but itshould adopt the widest possible scope and, inparticular. should utilize the results of the Con~mittee's
own earlier summaries of the radiobiological \+ark
carried out over the last 50 years. I t is not, ho\vever, theintention of the Committee to make any jud,Oement on
particular environmental situations.
The presence of cosmic radiation and natural andartificial radionuclides in the onvironrnent implies a4.

ANNEX: EFFEC'I'S OF RADIATION ON THE ENVIRONMENT

consequential radiation exposure of the indi,(venous
populations of organisms and, as is the case for man, it
is to be expected that the probability of adverse effects\vould be greater where exposures are higher than therange of the natural background radiation close rate.
There is. however, a fundamental differe~~cc
in theviewpoint adopted for the evaluation of the risk. For
man. ethical considerations make the individual theprincipal object of protection, and in practice this meansthat the incremental risk to the individual arising fromincreased radiation exposure must be constrained below
some level which society judges to be acceptable; thislevel of risk. although small. is not zero [IS]. Although
Inan displays an enormous range of attitudes towards
the other species that share this planet (consider, forexample, a population of mosquitoes at one estretne andan individual giant panda at the other). for the vast
majority of organisms it is the population that is
considered to be important. and protection of each
population from increased risk fiom radiation might be
the appropriate ob.jective: exceptions might bepopulations of small size (rare specics) or those
reproducing slowly (long generation times and/or low
fecundity). for which it might be more appropriate totarget protective measures at the level of the individualorganism. Thus, depending on whether it is theindividual or the population that is of interest. there arelikely to be differences in the responses that are
significant for the assessment of potential or actual
impact. Nevertheless, it is self-evident that there cannot
be any effect at the population level (or at the higher
levels of community and ecosystem) if there are noeffects in the individual organisms constituting thedifferent populations. I t is not the case. however, that
detectable radiation-induced effects in some membersof a population \vould necessarily have any significant
consequences for the population as a whole.

95. In considering impact assessment. it is also
necessary to note that natural populations of organisms
exist in a state of dynamic equilibrium within theircommunities and environments and that ionizing
radiation is but one of the stresses that may influence
this equilibrium. The incremental radiation exposure
from human activities cannot, therefore, be considered
in isolation from other sources of stress, both natural(e.g. climate, altitude, volcanic activity) and of humanorigin (e.g. synthetic chemical toxins, oil discharges,
exploitation for food or sport, habitat destruction).
When, as is not uncommon, ionizing radiation andchen~icals, both from human activities, are acting
together on a population. there arises the difficult
problem of correctly attributing any observed response
to a specific cause.
6 . The objective of this Annex is to summarize andrevie\\? information on:(a) the radiation exposures (actual or potential)
received by organisms in their natural habitats
from the natural radiation background. fiom
radionuclides released to the environment in acontrolled manner from industrial activities andfrom radionuclides released as a consequence ofaccidents: and(b) the responses to acute and chronic irradiation ofplants ant1 animals, both as individuals and as
populations;
It is not the purpose of this Annes to predict the impactof specitic incremental radiation esposures arising fromhuman activities on populations of wild organisms. butwith the information base provided, national andinternational bodies may be able to select appropriate
criteria for [lie radiological protection of natural
populations, communities and ecosystems.

I. DOSIMETRY FOR ENVIRONMENTAL EXPOSURES
A. METHODS O F DOSE ESTIMATION
Accurate estimation or determination of the dose
rate and the integrated dose to organisms is essential forassessing the potential or actual impact of contaminantradionuclides in the environment. This simple statement
conceals a multitude of difficulties that prevent the easyachievement of that estimation. In certain very restrictedcircumstances it has been possible to use thcr~noluminescent dosimeters to obtain direct rstimntcs of theradiation esposure, but such techniques are of limited
general applicability.
Direct measurements areespecially difficult if the dose rate is low, if theorganism is small, if the dose rate to a specific or,"an or
tissue is required or if alpha or beta particles are a major
source of esposure. For mobile species of wild organ7.

isms there is rhe additional difficulty of recapturing
sufficient dosi~neter-markedanimals to determine therange of dose rates and doses experienced by the
population.
Although there is usually little need for highprecision in the quantification of the radiation exposureof organisms in the environment, it is neverthelessnecessaq to distinguish behveen the various dosimetricquantities and to indicate their interrelationships. In thecase of a photon field in air, that is, for laboratory
studies employing either x rays or gamma rays fromsealed sources and for field studies with large gammaray sources, it has been common practice to determine
the esposure in free air. The conversion of these data toestimates of the absorbed dose in the relevant targets is
8.

10

UNSCEAR 1996 REPORT

complex because of the assumptions that are necessary
concerning the ~miforniity of the photon field, thepresence of h l l secondary electron equilibrium and theabsence of photon scattering.
9.
When the now obsolete units roentgen and radwere employed to quantify the irradiation of organisms
by photons, it was usual to equate the numerical valueof the esposure in f?ee air to the absorbed dose in theorganisms (see, for esample. [SI]). This approsirnation
may be adequate, provided that the organism is
sufficiently small for absorption and multiple scattering
to be neglected but large compared with the range of
secondary electrons.

10. A more accurate and Inore general numerical
relation can be based on the air kerma. K,, which is
given bytvhere X is the exposure in C kg-' and a is theconversion factor applicable for most photon energies
behveen 0.1 and 4 MeV. 33.85 Gy per C kg'. It may be
noted that the form of this relation (and those given
below) applies equally to the time derivatives.
11. In the case of radiation equilibriuni. D,.
theabsorbed dose in an organism, is numerically equal toK,,,, the tissue kerma at tlic same point. Then.

where s is the ratio of the Inass energy absorption
coefficients of the tissue of the organism and the air(taken to be 1.10 for photon energies in the range
0.1-4 MeV). Thus.

The product of s and a, which ICRU designates as thefactor f [Ill. relates the absorbed dose at a specified
point in the nlediunl to the esposure at that point. It has
the value 37.0 Gy per C kg-' for muscle tissue and37.5 Gy per C kg-' for water [I I].
12. For organs and tissues at some depth in larger
organisnis. tlie effect of geometry is taken into accountby introducing tlie factor g:where K, is the air ke~.nl:iin PIee air. For example, anaverage value of 0.7 has been assumed for sg toestimate the absorbed dose in the gonads of liunlan
beings: this is a11 average value for males and females tobe applied in both outdoor and indoor esposure
conditions [(El. Because the value of s is taken to be
1.10. it may be inferred that g has a value of 0.64.
Values of sg have also been given for srnall mammals[Zl]. Again. assuming s = 1.lo, the values of g are 0.89
for the mouse. 0.87 for the rat. 0.81 for the monkey and0.70 for the dog in cotiditions of bilateral exposure with
'OCo gamma rays. These values give a qualitative
indication of the effect of'animal size on the nlidline
absorbed dose in tlie organism for a constant air kernia
but are applicable only for the specific situation
described.
13. Even in the relatively straightfonvard situations
considered above, simplifications have been made. e.g.
by averaging over photon energy for the parameters a.
f and s. In a natural environment. where the assumptions of photon field uniformity, secondary electron
equilibrium and no photon scattering are unlikely to bevalid and the radionuclide distribution is certain to be
inhornogeneous, simple derivation of the absorbed dosefrom an estimation of the esposure is not possible.

14. In these circumstances it is necessary to employ
dosinietric models to estimate the radiation exposure.
These can be developed to take account of the radiation
type: the specific geometry of the target. e.g. the wholebody. the gonads. the developing embryo or the plantnieristem: ruid the source of esposure, e.g. radionuclidesaccu~nulatedin body tissues, adsorbed onto the bodysurface or distributed in the underlying soil. Clearly. it
is not possible to considcr all org'misms, and h e r e arelimitations on the basic data that can be made available
as input for thc models. e.g. the spatial and temporal
distributions of the radionuclides both \\ithim theorganism and in the external environme~it.Additionalsources of complexity arise from the behaviour of
nob bile organisms in moditjling the esposure fromexternal sources and. particularly for some aquaticorganisms and ~ilanyinsects. frolti the occupation ofdifferent environmental niches at different stages of thelife cycle. 11ius the models must be simplified andgeneralized without losing the realism essential for thevalid estin~ationof dose.
15. A dosimetric model is essentially a mathenlaticalconstructioli that allows the energy deposition in adefined target to be estimated from a given radionuclide(source) distribution. The model is often derived using
theoretical or empirical functions that describe the
distribution of dose about a point source 11. B12. LS.
W7]. The dose at a point in the target is then obtainedby inlegrating tlie point source dose distribution
fi~nctionover the defined radioril~clidesource, either
internal or csternal. This procedure is frequently
sitilplified by using silnple geo~netries (spheres.
ellipsoids etc.) of appropriate size to represent the target
and by assuming that the radionuclide distribution is
unifonn (over a surface or through a volume) or that it
varies in a way that can be described by a simple mathematical expression (e.g. an exponential decline in radionuclide concentration with depth in soil or sediment).

An'NEX: EFFECTS OF RADIATION ON THE ENVIIIONMENT

16. Another approach that has been employed for
gamma radiation is to use tlie known cross-sections forphoton absorption and scattering in Monte Carlo calculations to determine the absorbed fraction, defined as@=

Photon energy absorbed in targct
Photon energy emitted b y the source(5)

for a variety of source and target geometries [B 13. E3].
These data can be used, either directly or withinterpolation (or, to a lesser extent. estrapolation), forgeometries that can represent targets of environiliental
concern [N 1.041.
17. In principle, these procedures can be adapted foruse wid1 terrestrial and aquatic organisms from both theplant and animal kingdoms and for both internal andexternal sources of radiation. In practice, the use has
been more limited.
18. The presence of an alpha-particle component in
the total absorbed dose rate to a tissue in a plant or
animal raises the question of how to take account of theprobably greater effectiveness of this radiation type
(quality of radiation) in producing biological damage.
Such considerations have been very critically esaniinedfor the purposes of human radiological protection,
where each component of the absorbed dose lo a tissueor organ is \veightcd according to tlie radiation qllalih[IS]. It seems reasonable to apply a similar approach toradiation dosimetry for organisms other than man. In
practice. ho\vever, there are circumstances that alter thedetailed application of the approach, in particular, thechoice of the radiation weighting factors and thedescriptive terms employed. In the hunian case. themajor concern has been with the induction of stochastic
effects (priicipally cancer) at low doses and dose rates.
For alpha radiation, experimental determinations ofrelative biological effectiveness (RBE) lead to a
recommended radiation weighting factor of 20 for the
purpose of human radiation protection. In the case ofwild organisms. however, it is likely to be deter~ninistic
effects that are of greatest significance, and for alpharadiation the experimental data for animals indicate thata lower weighting factor. perhaps 5, tvould be Illore
appropriate; the weighting factors for beta and gamma
radiation tvould remain unity. It has been assunied thatthese weighting factors ivould also apply for effects inplants, although there are no definitive experimental
data. It should be pointed out that the various equivalentdose quantities. and the name of the unit, sievert (SV).
are specific to human radiation protection. In theabsence of corresponding dosimetric concepts andquantities developed for application to non-humanorganisms, in this report tlie absorbed doses tiom lowlinear energy transfer (LET) radiations (beta particles.
x ravs and gamma rays) and from high-LET radiation(alpha particles) are 'assessed and specified separately.

11

The absorbed doses retain the unit joule per kilogramme(J kg-') and the unit nanie gray (Gy).

6. DOSE CALCULATIONS

1. Plants

19. In the case of plants, the absorbed dose fromphotons is generally not equal to air kerma (seeparagraph 8), and there is a complex relation between
the radiation field and the absorbed dose that depends
not only on the relative mass e n e r g absorption
coefficients of air and the plant material but also on therelative stopping powers for electrons. For beta
particles, electron scattering. as well relative stopping
power, is involved. In approximate calculations it may
be adequate to assume that the ratios of the coefficientsand stopping powers are unity and to neglect scattering.
It may also be assunied that there is radiation
equilibrium in air, i.e. that the absorbed dose. D, isequal to the kerma. K.
30. With these simplifications Jacobi and Paretzke[JI] considered methods of calc~~lating
doses to plants.
specifically for leaves of trees and pine needles. fromesposure to natural and artificial sources of radiation.
The dose rate to the plant material. Dp, has external
and internal components. For the external component,
the relationship between the absorbed dose rate to theplant and the air kerma rate is

The factors is taken to be unity. The geometry factor gequals one for gamma rays and higher energy beta
particles but drops to zero for low energy beta particles
unable to penetrate the leaf cuticle to the cell growthlayer, at a depth of around 0.1 mm. If the radiation
exposure results from radionuclides in air. the dose rate
may be expressed in terms of the radionuclide
concentration in air:where \v is the disintegration Fraction, E is the energy
per disintegration (1 MeV = 1.602 lo-'' J). C, is theconcentration ot'the radionuclide in air (Bq 111") and p,
is the density of air (may be taken to be 1.3 kg ma). The
cumulative doses to plant components may be estimatedfrom assumed niean lifetimes for leaves of 0.5 years andneedles of 7 years [Jl].
21. For estimating internal dose rates in plants, therelevant equation is

UNSCEAR 1996 REPORT

12

where 4 is tlie absorbed fraction of the energy released
through disintegrations, C, is the concentration of theradionuclide in the plant material (Bq 1n") and p, is thedensity of tlie plant material (taken to be 800 kg m").
Because of tlie small diniensions of leaves and needles,
the factor 4 is small for gamma radiation and higher
energy beta particles and increases to unity as the beta
energy declines and for alpha particles.
22. There are nvo points to be noted about thisapproach: first, the calculation of the dose rate from theexternal source takes no account of the possibility ofself-shielding and is thus likely to be an overestimate:and secondly. the expression for the dose rate from th:internal source does not include the contribution fromcontaniination in other parts of the same plant and willthus tend to underestimate the dose rate.

(a)Natural sources

23. For natural tritiuni and '"C produced in theatmosphere through the interactions of cosmic rays, thedoses to terrestrial plants are, owing to the very shortranges of the beta particles, almost entirely frominternal sources. The concentrations of theradionuclides in plant tissue may be estimated fromenvironmental data. Tlie natural concentration of tritiumin surface \tfaters is about 0.3 Bq kg' [Uj]. For average
conceritrations of water in leaves and pine needles of
70% and 50%. respectively [J I]. and assuming the dry
matter is cellulose equivalent (6% hydrogen by weight).
the estimated tritium contents are 0.35 Bq kg-' (leaves)and 0.3 1 Bq kg" (pine needles). The activity of '"C interrestrial biological material is 230 Bq kg-' carbon.
Again assuming that the plant dry matter is cellulose
equivalent (44% carbon by weight). the I4C
concentrations are 3 I Rq kg" (leaves) and 5 1 Bq kg-'(pine needles). These concentrations of cosmogenic
radionuclides correspond to absorbed dose rates ofabout
pGy 11-I to both leilves and pine needles fromtriti~~niand 0.0009 uG> h-' and 0.0016 uGy 11.' to leaves
and pine needles, respectively, from "C. It is fairly
straightfonvard to estimate tlie dose rates for thesenatural, global and artnospheric sources of tritium and"C, because the resultant distributions are. more or less.
in dynamic equilibrium throughout the biosphere.
24. There are. however, niany data on tlie concentrations of tritium and "C in environ~nentalmaterials
that demonstrate, through the presence of different
specific concentrations (activity amount per unit massof the element) in different compartments, titnedependent transport processes. Some of them have been
demonstrated. for csample, in monitoring andmodelling the time-dependence of tritium in air. soil
and vegetation at the Savannah River fuel reprocessing
plant in the United States [M20]. General features oftritium in plants have been considered in a review byRelot II3 161. The formation and behaviour oforganically bound tritiuni in plants has been determined
and compared with that of tritiated water in plantsystems, e.g. [D 19, 161. These aspects. which give riseto an overall variation by a factor of up to 10 in specificconcentration, conlplicate the more simplified view oftritium in the environment, which considers that it
occurs only in the form of tritiated water and thatequilibrium specific concentrations prevail. Sirnilar
considerations. although of lesser degree (overallvariation in specific concentration by a factor of up to
4 IB3 I]) arise from riiore detailed analyses of "C
beliaviour. Thus, assessments of the impact ofadditional sources of these two radionuclides in theenvironment. often very localized in nature and often
involving releases to compartnients other than theatmosphere. e.g. surface waters and landfdl. need totake account of tlie time-dependent pathways forradionuclide redistribution, the chemical forms andtransfoniiations and the potential influence of sourcedependent factors on nuclide accumulations in plants.
25. Potassium-40 is both an internal and an externalsource of radiation exposure to plants. The external
component may he considered using the generalapproach discussed in paragraphs 8-12. The internal
dose depends on the potassium content of the plant.
wliich is 0.1%-0.5% of the fresh weight in leaves andneedles. The atom ratio of the potassium isotopes.
4"I</'"K, is 1.2 10". giving a speci tic concentratio11 of'
32 Bq g-' potassium and a SuK concentration in fresh
plant tissues in the range 32-160 Bq kg-'. Because of therelatively high beta energy ofaK, the absorbed fraction,
4, may be no more than 0.1-0. I5 [J I]. In roots, trunks
and branches of trees, the value of 4 would be morenearly equal to one. With these assumptions, the "I( inplant tissue could deliver a dose rate in the range 0.00 1 0.006 1tGy h-'.
The coriceritrations of radon, "'Rn. in surface air
variable. 'I'imc-averaged concentrations innormal areas may be in the range 2-30 Bq n1". With lessvertical air exchange in forests, the radon concentrations
may be expected to be higher there than over open land
for the same rate of radon exhalation from the ground.
f o r the noble gases, the radionuclide concentration inplant material is given by
2

i1r.e quite

where L is the dimensionless solubility coefficient. The
value of 1, depends on temperature and isapproximately 0.5 for radon in leaves and needles at
15°C [Jl]. In soil in the root zone, the radon
concentrations limy be higher by a factor of about 1.000
than in open air [JI].
Tlie average concentration of '"Rn in groundtvater
varies ~lidely.depending on the composition of the soil

27.

ANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT

13

and the bedrock. For soil with an average '%a content(c) the absorbed dose rates for the long-lived U8U and"?Th series radionuclides are as given in [J I];
of 40 Bq kg" [U2] the average radon concentration intheaverage content of *"Rn in forest air issoil water would be about 60 Bq kg-' [U3]. Much higher
(d)
10
Bq
m", with concentrations ranging up tovalues have been measured in deep groundivater in
50
Bq
m".
The dose factor (0.00066 pGy k'per
cenain areas, for example, 8,000 Bq kg-' in granitic
Bq
m"
for
the betalgamma component) is taken
areas of Maine in tlie United States [l-141 and
from
[Jl].
For '22Rn in air, only the external
50.000 Bq kg" in Finland [J2]. Lewis and McDonell
betalgamma dose from short-lived decay products[L6] found that the main route of accumulation of "Rn
is of significance. The remainder of the dose
into plants was through niass flow with water uptake byfroni "'Rn comes From the "'Rn dissolved in
the roots, although the s~~bsequentloss was not related
groundwater and taken up by the roots into theto transpiration. 'The data indicate that the "'Rn is lost
plant.
faster than the water, resulting in a lower -'Rnconcentration in water in the aerial tissues of plants than
30. I t is apparent from Table 3 that the greatest part ofin groundwater. This is consistent \\rith the data ofthe dose rate. and its potential variation. arises from theKirclunann and Bcrino [K8], who showed that less than:"Rn dissolved in the groundwater and taken up by the
10% of the "'Rn produced From the u1 sit11 decay ofroots. Other sources of variability. such as the range of""Ra was retained by pea plants. Thus there is likely toO' K contents in the plant material and the increase in
be a significant "'Rn concentration gradient in the plant\+later. fiom a high value (close to the gr~und\\~ater cosmic radiation exposure with altitude WZ]. are ofminor consequence. Small herbaceous plants experience
concentration) in the roots to a value lower by a factor
a1 additional exposure from the beta radiation from MK,of as much as 10 in the leaves. Assuming that the radon"%I
series and '"Th series radionuclides in the soil. For
content in plant water in the leaves is one tenth that in
the range of concentrations given in [UZ] and assuming
groundwater (i.e. 6 Bq kg'' on average). that theequilibrium in the two decay chains, the maximum
fractional water content of the plant is 0.8 and that theadditional exposure froni these sources could be 0.1.0.1
short-lived decay radionuclides are at equilibrium, thenand 0.05 pGy h-I, respectively; the actual exposure is,the absorbed dose rate from this source is approximately
however, likely to be much less. owing to geometrical
0.06 pGy h-I, of which 95% is from high-LET alphafactors.
radiation. This is within the range 0.005-0.54 pGy h-'suggested by Jacobi and Paretzke [J I]. It is clear that the
3 I. Point source dose distribution functions have beenabsorbed dose rate to the root meristem tissue could be
used to estimate the absorbed dose rate to
substantially greater. Because the data cited above relate
phytoplankton
in both fresh and marine waters fromto small plants [Kg. L6]. it is possible that the dose ratenaturalradionuclides[12. W9]. The results areto trees. for a givcn concentration of '"Rn in
sunimarized
in
Table
3.
For both fresh-water andgroundwater, could bc greater. owing to the longer
marinephytoplankton,
thegreatest part of the naturalresidence time of the "'Kn in the plant.
background dose rate is delivered by alpha particles: inthe fomier case by "Rn and its decay products in the
28. The radon decay products "OPb and 'loPo alsosurrounding water and in the latter case by "'U and DJU
contribute to tlie dose to plant components. While "OPbandby '?'Th plus its decay products accumulated in the
may be taken up by the plant through roots and leaves,organisn~s.
As has been noted in another context [Hj].
it occurs predominantly as deposited surface contarninalow
valuesforthe estimated absorbed dose rate to smalltion [JI]. Average concentrations of 'IoPb in leaves andorganisms
must
be interpreted with care. For example,
needles are I0 and 5 Bq kg'l, respectively [J 11. and a
tlie
low
total
radionuclide
content in any individual""PoP'OPb activity ratio of 0.8 may be applied to derive
phytoplankton
cell
and
the
discrete nature of the"'Po conccnh-ations.
radiation enlission process mean that many cells willpass through a number of divisions without experienc29. The factors for estimating doses to leaves anding any dose; conversely, a cell in which a radionuclide
needles of trees from natural radionuclides in the plant
decay
does occur will experience a relatively higher
material, as derived by Jacobi and Paretzkc [JI]. arc
dose.
Inthese circumstances. macroscopic dosimetry
presented in Table I. They provide a basis forprinciples,
tvhich average the absorbed radiation energy
estimating the radiation dose rate received by trees fiomarelatively
large mass ( I g or greater), arc veryovernatural background sources. The results are summarized
unlikely to be appropriate.
in Table 2. Four additional assumptions are made inderiving these values:(b) Artificial sources(a) the absorbed dose rate from the ionizing
component of cosmic radiation is 0.032 pGy h" at
32. The factors for estimating doses to the leaves andsea level [U3];needlesof trees from artificial radionuclides of noble
theabsorbed
dose
rate
from
the
neutroncom(b)
gases in air, as derived by Jacobi and Paretzke [J I]. areponent of cosmic radiation is 0.0004 pGy h-' [U?];14

U3'SCEAR 1996 REPORT

summarized in Table 4. They can be used to indicate
absorbed doses to the leaves and needles of trees using
the nomialized discharges to the atmosphere from
nuclear reactors given in e.g. ([U2]). It is assumed thatthe average integrated iictivity concentrations at 1 lcm
from the source for dispersion in all directions can be
estinlated by a simple approximation [U5], the value
being 3 10.' Bq s nr' per Bq. No allowance has been
made for radioactive dccay during the transit time fromenlission to target. The results are given in Table 5. Ttie
values of normalized dose may be multiplied b> theannual electrical energy generated (e.g. 0.5 or 1 GWa) toobtain estimates of the annual dose for a typical reactor.

33. The potential impacts of releases of tritium and"C can be assessed in a similar manner, with theadditional assumptions [CS] that at I kni from a nuclear
power plant these radionuclides have become uniformly
incorporated into the background atmospheric water
vapour (3 g rn") and carbon dioxide (0.016% byweight), respectively, and that the corresponding
specific concentrations are also appropriate for tree
leaves and needles. Using the assumptions of hydrogenand carbon contents of leaves and needles given inparagraph 23, the normalized absorbed dose rates may
be estimated. 11e resulting values are, however, likely to
be overestimates, because tlie specific concentrations inwill probably be less than
the terrestrial conipar~~iients
those in tlie atniospliere. 'rile extent of the overestimatiori
will depend on the rcliitive sizes of the hydrogen andcarbon pools in the different compartments, the net rates
of exchange between them arid the histories of thedischarges; it will, therefore, be site-specific.
34. The absorbed dosc rates to fresh-water and marine
phytoplankton from contaminant artificial radionuclides
have been assessed using point source dose distribution
hnctions [I?, W9]; the results are sunimarized inTable 3. The caveat in paragraph 3 l concerning theinterpretation of low absorbed dose rates to small organisms is equally applicable here.
35. Absorbed dose rates to aquatic macrophytes havebeen esrinlated by a nu~nberof authors [K4. h l j , N3]
using a generally conservative model based on radiation
absorbed fractions in a 30 cm diameter sphere. Using
derived values for tlie environmental concentrations
arising from discharges in liquid effluents at 16 nuclear
power station sites, Kaye [K4] estimated the dose rates
lion1 internal sources ill the range 0.009-70 pGy h",mainly from iso~opesol'caesium. Myers [blj] estimatedtlie dose rates fi.om n variety of radionuclides forindividual conccntratio~ls in water used either as
drinking water (intakc 3 1 d") or as a source of fish forhunian consumption (0. I kg d-'). with either pathway
leading to an effective dose equivalent of I mSv a-'. In
both cases the estim;~tedabsorbed dose rates to aquaticplants were as high as 1,000 pGy 11-', \\ ith the highest

values being due to the alpha-emitting radionuclides.
These figures are theoretical and reflect the limited useof resources (water and fish) by humans rather thanpotentially realistic doses to aquatic organisms.
36. Neither ol'thc above authors [K4. M5] considered
exposure from cx~ernalsources, and it is likely that theoverestin~ationof the dose rate from gamma radiation
within rhc plants (inlplicit in the model) \vould bepartially compensated by this absence of an estimate fortlie contribution froni gamma-ray sources in the waterand sediment. Although the model probably does notoverestinlate the absorbed dose rate froni alpha radiation from internal sources, for \vhich complete absorption is a reasonable assumption. a number of considerations suggest that the dose-rate estimates should nonetheless be treated with caution:
the large surface area per unit weight of aquatic
macrophytcs almost certainly means that theobserved concentration factors represent adsorbed
as well as metabolically incorporated radionuclides;
the dose factors for certain of the radionuclides[N3] include contributions from both short- andlong-lived dccay products where appropriate, but
for the latter tlie derived concentrations in water
are based on an extremely conservative model. inthat there are no loss processes operating in thewater column over a 30-year period: andon the basis of the information given concerning
tlie model and its parameters [N3], the dose-rate
factors for the alpha-emitting radionuclides appear
to be too Iiigh by a factor of up to 10.
These considerations lead to the conclusion that thedose rates are likely to be overestimates.

37. A technical report published by IAEA [I41 also
provides estimates of the dose rates to terrestrial plantsfrom deposited radionuclides following discharges tothe atmosphere. The model PATHWAY [WIO],
developed to estimate doses to man. was used to derive
the cquilibri~imconcentrations of radionuclides in plants(and animals. see below) for the limiting case that man,
while living on the land, breathing the air over it andeating food produced frorn it, would receive an annual
effective dose of I mSv. To estimate the dose to theplant fro111 internal sources, it was assumed that theenergy of alpha ant1 beta particles tvould be totallyabsorbed (except 32P,which ~vouldbe 50% absorbed)
and that 10% of tlie emitted gamma-ray energy would
contribute to the dose. An itdditional degree ofconsel-vatism was provided by using estimates of theradionuclide concentrutio~is in plant tissue on a dry
weight basis, \vhicli are 5-10 times higher than on a wetweight basis, to calculate tlie absorbed dose rates toliving (\vet) plant tissue. The results are given in
Table 6.

ANNEX: EFFECTS O F RADlA,TION O N THE ENVIRONMENT

38. Spirin [S?3] developed a dosimetric iliodel toestimate radiation doses to agricultural crops fromradionuclides in the soil. The air plus the plant material
is represented as a hon~ogeneousmedium of uniform
density (intermediate behveen the densities of air and ofplant material) that attenuates the radiation field,
developed by integrating a point source isotropic dose
function over the (plane) source in the soil. This
provides a dose distribution through the dcpth of theplant layer. Redistribution of the radionuclides from thesurface of the soil into a 20 cm deep layer reduces theestimated beta dose by a factor of 30 and the gamma
dose by a factor of 3. It was concluded that tlie dosefrom external alpha e~llittercontamination would be
negligible compared with that from radionuclides taken
up by the plants. In the latter case. the alpha radiation isassumed to be conipletely absorbed in the critical tissue(the apical meristenl or leading shoot). in wluch theradionuclide concentration \+.as related to that in the soil
by a simple uptake factor. For equal degrees of soil
contamination (1 Bq in'* mised to 20 cm depth) the
calculations showed that alpha radiation, e.g. fiom"'Np, could be a much more significant source of
exposure than beta and gamma radiation fiom '%r-%Yor 'jiCs [S23].
2. Animals

39. There appear to have been fewer estimates of thepotential exposure of truly terrestrial animals than of
animals occupying semi- and fully aquatic niches. Thisis probably a reflection of the greater use that has been
made of aquatic systems for waste discharge.
(a)

Natural sources

40. Estiination of the natural esposure of terrestrial
animals appears to have attracted little attention,
probably because it is implicitly assumed that themagnitude (and range) of the esposure will be little
different from those of the exposure of man. This is
likely to be a reasonable assumption, given that man
coexists with animals throughout the terrestrial environment and that even situations leading to enhanced
esposure. e.g. arctic food-chains [H3] or the occupationof burrows (enhanced radon esposure) seem to haveparallels in the case of man. There can also. however,be significant differences. Animals living above groundin the open are likely to receive a lower alpha radiationdose to the lungs. because the concentration of radonand short-lived progeny will. 0x1 average. be lower by afactor of 5 than the concentration esperienced by the
local hurnan population indoors. Animals living belour
ground receive, in addition to the increased lung dosefrom radon and its short-lived progeny. an increased
dose from terrestrial gamma radiation: for small
animals. the beta component from the external sources\\fould also need to be taken into account.

15

41. In areas of human habitation with nomial soil
concentrations of "K, =%U and ='Th. the mean external
gamma-ray dose rate in air has been estimated to be
0.057 pGy h" [U?]. For animals living most oftheir life
underground in those areas. it may be assumed that theincident gamma radiation field has 3n geometry(approximately), yielding a mean gamma dose rate in
air of about 0.09 pGy h-': if a mean burrow occupancy
factor of 0.9 is assumed, the annual dose to small
znimals is about 0.7 mGy.
42. The alpha dose to rodent species inhabiting
burrows from "'Rn and its short-lived progeny arises
from hvo sources: the radon and decay products in theinhaled air and the uptake of radon into soft tissue. For
both sources, estimates are required of the radionuclide
concentrations in burrow air. The equilibrium radon
concentration in soil air. C,,(Rn.z), at a depth of z
metres is given by:where f is the radon(equation 14. Annex D v5]).
emanation fraction. taken to be 0.2: C,(Ra) is the massconcentration of '26Rain the soil. taken to be equal to
the representative "'U concentration, 40 Bq kg': p isthe bulk density of soil, taken to be 1,600 kg m": c isthe soil porosity, taken to be 0.25: A, is the decay
constant of -%I. 2.1 lo4 s"; and D, is the effective
diffusion constant for radon in bulk soil. taken to be 5
lo-' ni2 s-'. All parameter values have been taken £ram
tlie UNSCEAR 1993 Report (paragraph 83. Annes A)[U2]. The derived estimate for the "Rn concentrationin burrow air at a depth of 0.2 ni is 1.7 lo4 Bq m-3. This
will be a maxinluin value because equation (10) does
not take account of the influence of adveetive flows.
Owing to adsorption of the short-lived progeny to soil
particles. their concentrations in burrow air will belower than that of the parent radon by a factor in therange 10-100 [J3].
43. The dose rate from 2"Rn taken up into soft tissue
can be estimated on the assumption that the meansolubility coefficient for radon is about 0.4 10" Bq kg-'
tissue per Bq m" in air and that the short-lived decay
products are in equilibrium with the "R' n in tissue. Thisapproach yields a dose factor of about 5 lo4 pGy h-'per
Bq m') of '"Rn in air. For the estimated '"Rn concentration in burrow air of 1.7 lo4 Bq m-), the absorbed
dose rate to lung tissue (and probably other soft tksues,i~~cluding
the gonads, in small animals) is about 0.085
pGy h-I. The dose rate to the alveoli of the rodent lungfiom =Rn (1.7 10' Bq m-I) and its decay products (1701.700 Bq 111-') in inhaled air can be estimated to be 0.25
pCiy h-' using the model developed by Drew andEisenbud [Dl 11.

16

UNSCEAR

44. Rodents inhabiting an area of enhanced natural
background. the Morro do Ferro, Minas Gerais, Brazil.
were marked with fluoroglass dosimeters and retrapped
after about five weeks. The absorbed dose rates fromexternal sources over this period were in the range 1.57.6 pGy h i . The concentrations ofUgTh."'Ra and 2'6Ra
were determined in bone, leading to an estimate of
0.16 pGy h-I for the average absorbed dose rate [Dl 01.
Vie concentrations of '-"f<n and "'Rn in the burrows of
the animals were high and very variable. An extensive
laboratory study of tlie deposition of the daughter
products in the lungs after inhalation allo\ved thedevelopnlent of a dosimetric model giving estimates of
180 and 29 pGy h-I for the absorbed dose rates at thesurfaces of the trachea and alveoli. respectively: themaximum values could be greater by a factor of 4
[Dl I]. Studies have been carried out in areas of Russia
where the gamma dose rate from esternal sources
reaches SO pGy h-I [MI]. If the internal dose to soft
tissues from "Rn absorbed through the lungs and fromits short-lived decay products varies with the external
dose rate in the same way as indicated by thecalculations in the preceding paragraph. it niay beconcluded that the absorbed dose rates to the soft
tissues of rodents inhabiting burrows in these highnatural background areas of Russia could reach as muchas 100 pGy h-I.

45. The transfer of the natural radionuclides "'Pb arid
'lUPoalong a lichen-caribou-wolf food-chain has beenstudied in northern Canada and estimates made of theabsorbed dose rates in ti variety of tissues. In caribou,
there appeared to be no discrimination in uptake
benveen 'I0Pb and "'Po, and for concentration ratios
less than unity, there was no biomagnification fromlichen to caribou. The '"'Po:~''P~ activity ratio was lessthan unity in bone and greater than unity in all othertissues measured (except the foetus). and with aweighted average value of about 0.9 for the whole body,it was concluded that the greater part of the 21'lJo bodyburden \\as derived tiom "OPb decay in bone andtranslocation of the "'10'
to soft tissue. The highest
absorbed dose rates, 0.7- 1.1 pGy h-', were estimated forthe liver; hut perhaps of greater significance in thecontest of this review, tlie absorbed dose rate in thetestes was estimared to be 0.05 pGy h-I. The tvolf
appeared to discriminate against "'Pb relative to "'Po
and to gain the greater part of its "'Po body burden
directly from food intake, although with concentration
ratios less than unity, there was no biomagnificationfrom caribou to wolf. Again, the highest absorbed dose
rates. 0.4- 1.2 pGy k l , were estimated for the liver. withvalues in the range 0.02-0.04 pGy h" in the testes [ E 5 ,T26]. The greater part of all the radiation dose wasdelivered by high-LEI' alpha particles from "'Po.
The methods for estimating the doscs to aquaticorganisms are more completely developed than those46.

for estiniating doses to terrestrial orgarlisms [12, 13.
W7]. This is clue morc to the growing need in recent
years to specifically consider the impact of radioactive
waste disposal on natural populations in aquatic
environments [13. N I . Pj] than to any intrinsic digerelices in the problems posed. The models are based on
point source dose distribution functions or absorbed
fractions, as appropriate, and simplifications are madeto the extent dictated by the data available for input tothe model. Estimates of radiation doses from natural
background are summarized in Table 3 for fish andmolluscs. More detailed data for these and other aquaticorganis~iisare given i l l [I2, 13, P5, W8, W91. but the
infomiation in Table 3 is quite rcpresentative.
47. T\vo points may be made about the data presented
in 'I'able 3. First. the radiation exposure of the molluscs
is generally greater than that of the fish, because thebenthic (bottom-living) mollusc is exposed to radiationfrom the sediments and tlie pelagic (surface water) fish
is not. More itnportaritly. the dose rate from internalsources is greater for the molluscs because most of theavailable data on radionuclide accumulation(concentration factors) are for filter-feeding detritivores.
The fine particles making up the food scavenge
radionuclides efficiently from the water, thus leading tohigher body burdens of the radionuclides. Secondly. theabsorbed dose rates from internal exposures to naturalradiation sources are relatively high due to the liighLET contribution from Y". Indeed, for certain pelagic
oceanic organisms. tlie absorbed dose rates in particular
tissues from this source can be very high, c.g. up to
150 pGy 11-' in the hepatopancreas and 4 pGy h-I in thetestes of a small mid-water shrimp [C7. H6] and30 pGy h-' in the intestine and I pGy h-' in the gonads
o f a sardinc [Cg].
(b)

Artificial sources

48. Coughtrey [Cj] estimated dose rates lo the soil
fauna. as exemplified by the earthworm, from thedeposition into woodland of iodine, strontium andcaesiunl radionuclidcs released to the atmosphere froma pressurized water reactor at a distance of 300 ni. The
radionuclide concentrations in the surface soil were
estimated from a dispersion calculation and an assumed
deposition rate. The consequent accumulations of theradionuclidcs by the earthworm were estimated using
concent~ationfactors. The dose rates were calculated on
the following assunlptions: for the external sources, thatthe dose ratc lrom both beta and gamma radiation wasthat to the soil, ~vhichwas effectively infinite in extent:
and for the internal source that only the beta component
was significant and that it was totally absorbed. A
difTerent approach was adopted for 'I I and I4C releases,
which were assumed to equilibrate with the atmospheric\\later vapour and carbon dioside. respectively. The
resulting concentrations of 'H per gram hydrogen andANNEX: EFFECTS O F RADIA.TION ON THE E N V I R O h J E N T

I4C per gram carbon in the plume were assu~iiedto
apply to the earthworm. This is likely to be aconservative assumption. since it neglects the input of
uncontaminated water (as rain froni outside the plume)and die diluting effect of the large organic carbon poolin living plants and the soil hu~iius;an estimate of thedegree of conservatism would require detailed
modelling of the particular situation (see also the next
paragraph). The total dose rate to tlie earthworm for thepredicted operating conditions of tlie power plant was
0.0 1 pGy h-I, and since the greatest part of this was due
to I4C. it is certain to be an overestimate; if the station
was operated such that the effective dose rate to manreached 1 mSv a-', then the estimated dose rate to theearthworm ~vouldbe 5.7 uGy h-I.
49. As was the case for plants (paragraph 24), thedose from tritium should consider tritium in body waterand organically bound tritium in tissues. The relative
amount of the two components depends on the source ofthe tritium, i.e. either tritiated drinking water ororganically bound tritium in food (with food type also
having an influence [K21]) [L 12, I,] 3, P16, P17. Rl I,
T271. Although the assumption of a constantconcentration of tritium (as Bq kg" hydrogen) in thebiosphere could be questioned, it is difficult to see howrnore specific data could be translated to theenvironmental context to generate iniproved estimatesof radiation doses from contaminanr tritium. A rnore
detailed model of the behaviour of tritium in the vicinityof the input, including the dynamic processes along
food-chains, would be required. Similar considerations
probably also apply to "C.
50. Soil fauna arc also potentially at risk froni therelease of waste radionuclides from shallow landfill
repositories. Coughtrey [Cj] considered the case inwhich radionuclides \ifere accuniulated by bank soil
from stream water draining a trench disposal site. The
total dose rates to the soil organisms ivere estimated to
be 18 pGy h-' from low-LET radiation and 14 pGy h-'from alpha radiation.
5 1. The PATHWAY model [W IO] has been used toestimate radionuclide concentrations in surface-living
animals from aerial deposition [14]. 'fhe domestic sheep
was used as a model terrestrial animal, and it was
assumed that the predicted radionuclide concentrations.
except for '"Cs. would be typical of wild animals. For"'Cs, the estimated tissue concentrations generated by
the model were increased by a factor of 10 to takeaccount of the known influences of either carnivorous
behaviour or the consumption of certain plants on theaccumulation of this radionuclide by different wild
animals. The predicted concentrations in sheep riiuscle
were assumed to apply to the gonads for all radionuclides except '%, for which thc muscle value wasincreased fourfold to give the concentration in the17

gonads. The dosimetry model assumed total absorptionof the alpha and beta radiation in the gonads and a 30%
absorption of the gamma energy. The results for theabsorbed dose rates from these internal sources. given
in Table 6, correspond to the limiting case of humans
receiving 1 mSv a-' from occupation of the sameenvironment.
52. Kozmin et al. w9] developed models to estimate
the radiation exposure of farm animals following
accidental releases of radionuclides to the atmosphere.
The radiation exposure pathways considered were
external expos~lrefrom the plume. inhalation from thecontaminated ground-level air. contaminated pasture(external and internal source). contaminated soil (external and internal source) and contaminated livestockbarns (ester~ial).In practice, it is the internal exposure
following ingestion that is of particular significance.
Compartment models were developed to predict theradionuclide distributions within the animals and theconsequent radiation exposures. Cumulative dose
estimates for sheep, pigs and cattle are presented inTable 7 for acute and chronic exposures to "'I (thyroid).
"Sr-90Y (bone) and '"Cs (muscle).
53. Models based on point source dose distributionfunctions or absorbed fractions. as appropriate, havebeen used to estimate the absorbed dose rates to pelagic
fish and benthic molluscs from contaminant radionuclides. The results are summarized in Table 3, whereir can be seen that, as was the case for the natural
sources and for the same reasons. the exposure ofbenthic niolluscs is greater than that of pelagic fish (seeparagraph 47).
54. The dose rates to fresh-water fish have also been
estimated for the situation in which humans receive thelimiting effective dose rate of 1 mSv a-' froni the combined exposure pathways of drinking water (2 I dl). fishconsumption (0.1 kg d-I) and external esposure f r o ~ ncontaminated sediments (occupancy 2.000 h a") wl].
The results for a selection of radionuclides in the liquid
effluents are given in Table 6. These data are consistent\\lit11 those from the controlled waste discharge from the
Magnox nuclear power station into Lake Trawsfynydd
in northern Wales, where the total absorbed dose rate to
fresh-water fish from all sources was estimated to be
0.08-0.3 pGy 11" (0.7-2.6 mGy s')[W8] when theeffective dose rate to the human critical group was
estimated to be no greater than 0.25 mSv a" [M7].
5 5 . For a benthic fish (the plaice. Pleuro~lectes
plaressa) in the northeastern lrish S e a the estimateddose rates from contaminant radionuclides accuniulated
in the seabed from the waste discharges from theWindscale (now Sellafield) nuclear fuel reprocessing
plant were sufficiently large (up to 50 1iGy 11-') toattempt direct riieasurements. S~nallthermoluniinescent

18

UNSCEAR 19% REPORT

dosimeters \\!ere developed that could be attached to thefish, and 3,580 fish were niarked with a combined
tas'dosimeter and released in the vicinit). of the waste
outfall. In a period of 2.5 years. 1.053 fish were recaptured, and the dosi~neterson 969 of them yielded
useful results. After allo\ving for the mobility of the
fish. the data essentially confimied (within a factor of 2)
tlie estimates of radiation esposure calculated on thebasis of a simple model using the measured distributions of the radionuclides in the sediments [W8, W9].
Small thennoluminescent dosimeters have also beenused to obtain an estiniate of 4 11Gy h i for the absorbed
dose rate to periphyton 24 km downstream from thepoint of discharge. the Hariford plant. into the ColumbiaRiver [L7].

C. COMPARISONS OF ENVIRONMENTALEXPOSURES
56. At present. data on radiation exposures of wildorganisms from both natural background and contaminant radionuclides are incomplete. the more so insome areas than others. The aquatic environment isprobably the most thoroughly studied environment todate [I2, 13. 19. NI, N3, W9], but even for it, substantial
generalizations have had to be made, particularly inrespect of the range of organisms that can reasonably beconsidered (131. As has been emphasized [13, 191. thelimiting factor is not the development of an appropriate
dosirnetric model for a particular organism but theacquisition of essential input data on the tmiporal andspatial distributions of the radionuclides both estemal
to arid within the organistii. Although dynamic models
have been employed to describe the dispersion anddilution of radionuclides in a water body. the accornpanying reconcentration transfers to sediments andbiological tissues are almost always modelled as equilibrium processes, i.e. simple distribution coetficientsand (whole-body) concentration factors are used. Thislargely neglects the temporal variation in dose rate due
to short-term fluctuations in the discharge rate. todiffering stages in the life cycle. to behaviour and to
short-tenii environmental processes (e.g. seasonality)
etc. As a consequence, while the estiniated absorbed
dose rate might be a reasonable indication of the generalmagnitude of the environmental value. it does not provide a veQ secure basis for evaluating total doses overtime. Such reservations apply with equal validity to themore limited data that have been developed for releases
to the atmosphere [C5, 141, for shallow landfill sites [CS,141 and tor a deep repository [MS]. It is, nevertheless,possible to draw some general conclusions.

57. As is the case for man [U2], naturally occurringalpha-emitting radionuclides appear to be the mostsignificant sources of' background radiation esposurefor the ma.jority of wild organisms. In the terrestrial

environment tlie main source is radon and its short-lived
decay products. The estimated range of absorbed dose
rate to the leaves and needles of trees from this sourceis 0.005-0.5 pGy h". Given the apparent significance of
this source of exposure, it would be useful if the radon
content of plant tissues could be determined by direct
measurement rather than by inference from concentrations in groundwater. Studies of the uptake ofmK intoplants from potassit~ni-richsoils would also be worthwhile, because plants do riot have the same regulatory
mechanisms for potassium content as animals. For
terrestrial animals in areas where the soil has the nomialconcentrations of uranium and thorium, the highest
radiation exposures will be experienced by burrow
dwellers. In this case, the absorbed dose rate fromextcrnal sources is about 0.09 pGy h-I, that from radon(and from its short-lived decay products) accumulated
in soft tissue is about 0.085 pGy h-' and that to the lungs
from radon and its decay products in the burrow air isabout 0.25 pGy h'l. Exceptionally, in areas of uraniumor thorium mineralization. th2 natural backgroundabsorbed dose rates could be higher by a factor of asmuch as 1.000. In aquatic environnients, 'loPo is theniajor contributor, with absorbed dose rates of up to
several microgray per hour to the gonads of marine
animals. The recognition that alpha particles (sliortrange. high-LET radiation) are the principal source of
background radiation esposure underlines the need for(a) detailed knowledge of the distribution of theradionuclides in relation to potential targets as well as
realistic models for the estimation of absorbed dose
rates and (b) the selection of a radiation weighting
factor appropriate to the biological effect of concern.
58. Discharges of tritium, I4C and noble gas radionuclides to the atmosphere during normal operation ofa reactor do not appear to be an important additionalsource of exposure to plants. because the increment islikely to be much less than the variability (andunccrlninty) in the estiniate of the natural esposure.
Discharges to the atmosphere of other radionuclides
could be more significant. and in the limiting situation
for humans (1 1nSv a"), it appears that some plants andanimals in the vicinity of the reactor might experienceclose rates up to a f w tens of microgray per hour; inpractice. the actual discharges during normal operation(and, hence. the dose rates) are likely to be much lower.
59. For discharges to aquatic environnients both theestimates of dose rates based on measurements of*coricentrations of radionuclides in contaminatedenvironments and the estimates inferred for the limiting
situation of 1 niSv a-' to man are much greater than theestimates of the natural background esposure (seeTable 3). The organisms might receive dose rates up to
60 11Gy h-I (500 niGy a-I), and in one case an absorbed
close rate of 5,700 pGy h" (50 Gy a-l) was estimated l'or
aquatic niacrophytes [Mj].

ANh'EX: EFFECTS OF RADIATION ON THE ENVIRONMENT

60. Accident situations are by nature quite different.
particularly in their potential to produce high dose rates
and doses in the environment. As the actual exposure
regime obviously depends on the quantities of specificradionuclides released, the initial dispersal anddeposition patterns and their redistribution over time intlie environment, it is difficult to generalize. Following
the accident at the Chernobyl nuclear reactor, large
quantities of short-lived radionuclides were released,leading to high dose ratcs in the local area. Total doses
up to 100 Gy were delivered to trees (and, by inference,
to most other organisms in the locality) over a period ofa few days [Dl. This radiation regime may becharacterized as "acute". in that the doses weredelivered in times that were shorter than, or comparable
to, the times taken for severe damage to become
apparent. During this initial, acute phase the dose rate
declined rapidly as the very short-lived radionuclides
decayed. The release following the accident in 1957 in
the southeastern Urals was dominated by lJ"Ce-lJJPr(approximately 66%: T,: = 285 d) and ''Zr-''Nb(approximately 25%: T,; = 65 d). In that case. the dose
rates in the local area were also relatively high(24,000 pGy 1 1 - I ) but declined more slotvly, such thathigh total doses causing severe effects (including
mortality) could still be nccumulated from essentiallychronic esposure. Close to the release point, total doses
up to 2.000 Gy were experienced [TI 71. In tlie longer
term. the esposure regime for the Chernobyl release has
been dominated by I3'Cs (Tk = 30 a) and 90Sr (T,, =28.6 a) and that for the southeastern Urals accident area
by ?Sr: in both cases, the exposures are chronic andmoderately high. with responses other than mortality
becoming significant. Further experience derived fromthe study of exposures and effects from these accidents
is presented in Section I I I.D.

D. SUMMARY
61. Dose rates to plants and anirnals in theenvironment from naturally occurring or contaminantradionuclides may be estimated from basic dosimetric
relationships. The accuracies of tlie estimates are
generally limited by uncertainties in knowing theconcentrations of radionuclides that prevail in the media
surrounding the organism and that accumulate within
the organism. Based on reasonable assumptions. dose
factors have been derived for a number of radionuclides, and these have been applied to estimate dose
rates in various environments. 11 is recognized that thesimplifications often implied in these assumptions leadto overestimated dose rates.

19

62. In areas of normal background. the absorbed dose
rates to terrestrial plants are 0.07-0.8 pGy h-' (0.6-7
mGy a-I). mainly from 222Rn
taken up from the groundwater. Absorbed dose rates to aquatic plants would
nomially be at the lower end of this range. Absorbed
dose rates to terrestrial animals are highest for those
inhabiting underground burrows; in this case the roughestimates are 0.25 pGy h-' in the lungs from "Rn andits decay products arid about 0.09 j~Gyh" each fromabsorbed radon in tissue and external exposwe. In areasof uranium or thorium mineralization. the absorbed
dose rates could be higher by a factor of as much as
1,000. In aquatic environments. "'Po is a major
contributor to dose. with absorbed dose rates to the
gonads of some marine animals reaching several microgray per hour.

63. Radioactive waste discharges to the atmosphere.
to landfills or to aquatic systems from man-madepractices entail increased radiation exposures of wildorganisms. The incremental radiation exposures arechronic (i.e. continuing) at absorbed dose rates ofgenerally no more than 100 pGy h'' but very
exceptionally several thousand microgray per hour.
These additional radiation exposures are greater than
the normal range of natural radiation background but
are generally within the extreme range of backgroundwhen tlie exceptional cases of areas of uranium andthorium mineralization are included. Given that waste
discharges are point sources and that releases normally
become dispersed and diluted (account is taken ofreconcentration processes in developing the database of
distributions and concentrations of radionuclides used
as input to the dosimetric models), these dose rates arelikely to apply to only a small proportion of theindividuals in any population; the average dose rate to
the population v,fill probably be much lower (see, forexample. [W8, W91).

64. Detailed information on the responses oforganisms to radiation exposures at absorbed dose
rates up to 1.000 pGy h-' is required to make anassessment of potential environmental impact. Responses to acute irradiation or to short-term exposures
ai higher dose rates can also provide useful inforniation, particularly about the relative sensitivities ofdifferent species and classes of organism and of thedifferent life stages of a species. Information on thesensitivity of individual plants and animals to radiation exposure and the possible effects on populations
and communities of organisms is presented in Chapters
I1 and 111.

20

UNSCEAR 1996 REPORT

II. EFFECTS OF RADIATION ON PLANTS AND ANIMALS
65. The effects of ionizing radiation on plants andanimals began to be studied immediately follo~vingthe
discovery of x rays and radioactivity (see, for example.
[A 13, T241). Since 1945. when the first nuclear detonations were conducted. there has been widespread concern about the impact of environmental radiation
exposures and interest in the environmental behaviourof radioactive materials, as of result of which manystudies, usins a wide variety of plant and animal
species, have been performed [A 1, B 1. C3. 15, P3].
66. The responses of organisnis to radiation esposure
are many and varied and may become manifest at alllevels of organization, ftom the individual biomoleculeto the ecosystem. The significance of a +en response
depends on the criterion of damage adopted. and it
should riot be concluded that a response at one level oforganization will necessarily produce a consequential,
detectable response at a higher level. It has been noted(paragraph 4) rhat for humans it is the risk of harm to
the individual that must be minimized but that for thegreat majority of all other species it is the populationthat is valued and for whose protection appropriate
radiation exposure controls could be implemented.
67. In tlie widest sense. a population may be definedas all n~enibersof a particular species. Ho\vever, radiation fields arising from radioactive waste discharges
generally show large spatial variability. not least because of the discrete nature of the input, and manymembers of a population may not receive any significant exposure liom a particular source. The natural
distributions of most species are inhomogeneous("patchy") in response to the variable occurrence of theranges of physical, chemical and biological conditions\vithin which. in combination, the individuals of thespecies are able to survive, i.e. species are geographically restricted. Thus, it is probable that a more limited,
and relevant, definition of a population could be
developed for tlie purposes of environmental impact
assessment.
68. In a similar contest [I-l] the following definition,
developed for use in population ecology, has beensuggested as a useful basis for discussion and pro,oress:"A population is a biological unit for study, with anumber of varying statistics (e.g. number. density, birthrate, death rate, sex ratio. age distribution). and which
derives a biological meaning from the fact that somedirect or indirect interactions among its niembers are
more important than those between its ~nenibersand
members of other populations [Bl4]." Such a population would be (or could be) a self-sustaining unit,
independent of other. geographically separate populations of the same species. Protection of this population~vouldrequire that increased radiation esposure did not

significantly affect those attributes (i-e. those mentioned
in the definition) on which the population depends formaintenance within the normal dynamic range ofvariation dictated by the interactions of natural physical,
chemical and biological factors.
69. These attributes, which can be defined only forl~opulationsof organisms and which may be taken to be
indicators of their health, are, nevertheless. integrationsof properties that relate to individuals (in no sense isthis meant to imply simple addition) (see. for esarnple,
IM81). It may be concluded, therefore. that there can be
no response to radiation at the population level (or.
indeed, at any higher level of organization) without
there being some clearly detectable effect in individualorganisms (or at lower levels of organization). This
clearly implies that the protection of tlie population (astlie ultimate ob-jective) may be achieved by restricting
tlie exposure of individual organisms to the extent that
there are no significant radiation effects on those processes that arc necessary for the maintenance of the
population. I t is therefore necessary to consider theavailable information on the elTects of radiation (mainly
at chronic low dose rates) on the relevant processes inindividual organisms, to consider how these responses
might translate to an impact on the population, and to
examine the results of studies of population responses
to deliberate experimental irradiation or in environments contaminated by controlled or accidental releases.
70. Examination of tile population attributes(paragraph 68) indicates that the individual responses toradiation exposure that are likely to be significant at the
population level are mortality (affecting age
clistribution, death rate and density), fertility (birth rate).
fecundity (birth rate. age distribution. number, density)and the induction of mutations (birth rate, death rate).
The response of these individual hnctions to radiation
exposure can be traced to events at the cellular level in
specific tissues or organs. An extended summary
discussion of the processes involved was given in the
UNSCEAR 1982 Report ([Uj]. Annes J, 'Wonstochastic effects of irradiation"). There is a substantial
body of evidence indicating that the most radiosensitivesites are associated with the cell nucleus, specifically on
the chromosonies, and, to a lesser extent, implying theadditional involvement of damage to intracellular
membranes. 'I'he end result is that the cells lose theirreproductive 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 postexposure division: at doses of a few gray, several
division cycles may be s~~ccesshlly
completed before it
eventually occurs. I t is also well known thatradiosensitivity varies within the cell cycle. with thegreatest sensitib ities being apparent at mitosis and theANNEX: EFFECTS OF RADlATION ON THE ENVIROhWENT

conlmencement of DNA synthesis [U5]. It follows thatthe greatest radiosensitivity is likely to be found in cellsystems undergoing rapid cell division for either
renewal (e.g. sperniatogonia) or growth (e.g. plant
meristems and the developing embryo); these examples
clearly underlie tlie processes in individual organismsthat are important for maintenance of the population.

7 1. Fractionation, or protraction, of exposure to lowLET radiation increases the total dose required to
produce a given degree of damage. At low dose rates,e.g. those that arise from the controlled discharge ofradioactive effluents into the environment, the factors
responsible for mitigating the response are the repair ofsublethal 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 [Uj]. Although it
is clear that repair, in the general sense, is possible, theesistence and extent of residual injury is less clear.
While such an outcome may be demonstrated formoderate, acute doscs. it is not possible to extrapolatethese results to predict the likely response to lo\\.,-level
exposures extending over a significant fraction of the
lifetime of an organism. However, given that genetic
nuta at ions may be passed from generation to generation,
it is reasonable to suppose that sonlatic mutationsindividually consistent with cell survival can occur andaccun~ulate over time until tlie combined impact
reduces cell viability.
72. In addition to the intrinsic factors already mentioned as affecting radiosensitivity, account should also
bc taken of the extrinsic factors in a contaminatedenvironment. such as season (rapid growth of plants inspring. lotver metabolic activity in hibernating animals)
and temperature (metabolism in poikilotherms). The
response of an organism to increased radiation exposureis also likely to bc modified if it is undcr stress fromother sources, e.g. if there are non-radioactive contaminants in the environment or if it is at tlie limit of thenormal biogeographical range for the species. It has
been s h o ~ n ,for esample, that exposure to DDT
increases the retention of '"Cs in rals; thus, in addition
to the potential stress from pesticide exposure and its
possible interaction with radiation. there is also a DDTdependent increase in the radiation dose rate frominternal sources [U 131.

A. TERRESTRIAL PLANTS

73. Radiation i~i.iury in plants expresses itself as
abnormal shape or appearance. reduced growth or yield,
loss of reproductive capacity. wilting and, at highexposures, death [S7]. Acute lethal doses to higher
plants range from 10 to about 1.000 Gy (approximate
mean absorbed doses averaged over the whole plant).

21

At the extremes of radiation sensitivity are plants suchas mosses, lichens and unicellular species. which arehighly resistant. and woody species. which are the mostsensitive. In 12 species of woody plants assessed 10- 14
months after exposure, the lethal doses were 8-96 Gy[S12]. The pine tree is tlie most sensitive, experiencing
severe niortality following short-term absorbed doses ofabout 10 Gy [Wl I]. Growth is severely inhibited at
50%-60% of the lethal dose. Floral inhibition isobserved at 40%-50% of the lethal dose and failure to
set seed at 25%-35%. Thus, the capacity of the plant
population to maintain itself can be damaged at acutedoses lower tlian those required to cause mortality.
Below 10% of the lethal dose. effects are not soapparent, and the plant maintains a normal appearance.
These general observations from several herbaceous
plant species are illustrated in Figure I [S8]. Anothergeneral relationship is that the dose that reduces
survival by 10% (LD,,) is roughly equivalent to thedose that reduces the yield by 50% (YD,) [S7].
74. Because there is interest in the mo~pliologicalchanges produced by tissue damage and repair (rather
than by mutation) that may be observed at contaminatedsites. it is worthwhile mentioning the changes of thiskind that have been observed in the laboratory. Leavesof plants fonned during irradiation may show abnormalities such as dwarfing, asyn~n~etricaldevelopment anddistorted venation as well as changes in texture andthickening, which occurs at dose rates above 2.4 Gy d-'in Atltirrhirlzrnl sp., an annual flowering plant (the total
dose was not given. but for a late spring-early summer
growing season of 150 days. it could be up to 360 Gy)[S9]. Older leaves formed prior to irradiation are littlechanged by exposures. except in respect of texture: they
commonly become dry. stiff. coarse and thickened [S9].
Effects in flowers include additional and abnormal buds
and inflorescences at dose rates of 0.20-0.24 Gy d-' for
56 days (total dose 1 1- 13 Gy). At a higher dose rate of
0.34 Gy d" (19 Gy). vegetative rather than floral
production was hvoured and modified leaves occurredin floral positions [S9]. The needle length of pine trees
becomes progressively shorter as acute exposures are
increased above 0.5 Gy. Needle length is 10% of thecontrol at 3 Gy in growing plants and at 4.5 Gy indormant plants [S 101.
75. The sensitivity of plants to external x radiation or
g m m a radiation varies over a wide range and depends
on both the stage of individual development and the
pnylogcnctic category of the particular specics. A comparative analysis [S45] of the radiosensitivity of higher
plants in ternis of the median lclhal dose has shown thatthe range of variation exceeds two orders of magnitude
in both the dormant seed phase (from 5 Gy in Picea
abics to 2.000 Gy in Raphurtus sativzrs, of 99 species
studied) and the vegetative phase (from 4 Gy in
Pse~rdot~~rgu
do~rgIu.s.sito 580 Gy in Cupsella btrrsa-

7?
--

UNSCUR 1996 REPORT

pastoris, of 64 species studied). Within a species, theradiation sensitivity (in terms of LD,,) may vary by afactor of more than 20 behveen different stages ofdevelopment: the dry seed is most resistant and thegametogenic cells at meiotic prophase (the stage prior
to the reduction division, when the duplicated chromosomes become visible in cell preparations) are mostsensitive. Overall, the data suggest a close relationshipbetween radioresistance and phylogenetic position [S45].
The more primitive species in the Gyn~nospermneare
the most radiosensitivc and show a relatively narrow
range of LD,, (5-63 Gy for dormant seeds and1.6-16 Gy for the vegetative phase). The more advanced
groups sho\v generally greater radioresistance but also
greater variability, viz. the Monocotyledon class (10350 Gy for dormant seeds and 9.6-52 Gy for thevegetative phase) and the evolutionary advanced
Dicotyledon class (50-2,000 Gy and 4.8-580 Gy.
respectively). It may be noted that a similar trend isapparent \vithin individual families; thus the radiosensitivity of the more primitive YiciuJirha (50 Gy and
9.8 Gy, respectively) is about 25 times greater than thatof the more advanced and specialized Trfoliimi repeiis(1.250 Gy and 243 Gy, I-espectively) [S45].
76. Because phylogenetic development in higher
plants is accompanied by the elimination of redundant
hereditary information and a reduction in genome size
[S45], it can be suggested that there should be somerelationship bet\veen radiosensitivity and cell nucleus
parameters. Sparrow and Miksche [S46] investigatedthe dependence of the tolerance of higher plants tochronic irradiation on cell nuclear volume and DNA
content. Lincar relationships were developed [S47] that
could be used to predict radiosensitivity; Figure I1
sho\vs the dependence of acute lethal dose on interphase
chromosonic volume for woody and herbaceous speciesof angiosperms [S 121. Experimental studies with 28
species demonstrated good agreement between thepredicted radiosensitivity and that nieasured in the field.
although it was accepted that significant variability
could be introduced by tlie specific conditions of irradiation and uncontrolled environmental factors [S48].
1. Cultivated and pasture crops

77. hlost studies of the effects of radiation on
agricultural plants utilize the dose required to reduce theyield by 50% or 100% (YD,, or YD,,) as the measureof radiation response [S7]. The major cereal crops show
the highest radiosensitivity ~vhenthe ears (seed heads)
are developing (YD,, = 4- 16 Gy); rice is an esception(YD,, = 75 Gy). At other stages of development theYD, is 20-60 Gy, with rice again being an exception at
160 Gy [Fb]. A specitic feature of the response of
cereals at early stages of development is an increased
production of shoots caused by damage to apicalmeristems and a loss orapical dominance; by producing

an increased numbers of ears, this may somewhat
compensate for thc loss of grain per ear [F6]. Legumes
have YD,,s in the range 3-60 Gy for the vegetative
stage and 1-4 Gy for flowering stages. Root crops areless sensitive. wit11 YD,,s ranging from 14 Gy foronions to 90 Gy for radishes. Miscellaneous crops, inorder of increasing resistance, are lettuce, pineapple,
strawbeny. squash, spinach, cabbage and tomato, whichhave YD,,s of 45-120 Gy [S7]. Oil seed crops aremoderately insensitive, with YD,$ of 120-160 Gy [F6].
Pasture and forage crops, where the yield is related tovegetative mass rather than seed production. show thelowest sensitivities (YD!, = 150-230 Gy) [S7].

78. A number of factors have been shown to modify
tlie radiation responses of crop plants. Adverse weather
conditions (an increase in temperature and a reduction
in relative hu~nidity)after acute irradiatio~iof spring
wheat reduced the YD, by a factor of 4; this effect wasdependent on the cultivar studied. Substantial differcnces have becn found behveen cultivars of spring\vlieat (172 varieties) in their growth after seedirradiation. Depending on the age of the plants at
irradiation, tlie YD,, can vary ninefold. with the lo\+est
radiosensitivity observed at the time when the multiple
apical meristems are produced [FG].
79. The irradiation of seeds with acute doses up to
10 Gy stimulated early emergence in flax and early
growth in spring wheat and barley under laboratory
conditions. Field trials with irradiated wheat seed
showed, however, that any hormetic effect was notcorisistently translated to an increase in grain yieldIS2.11. Substantiill vnriations in hormetic responses were
Ibund both within and behveen cultivars and species.
and an early stimulation of growth in response toirradiation did not necessarily yield benefits at harvest,
mainly because other environmental variables had a~iiuchgreater intluence [S25, S261.
80. As a consequence of the observed relationships
between radiosensitivity and nuclear and chromosomal
parameters (paragraph 76 [S12, S46, S37. S48]),
cultivars of tlie salne species having similar nuclear
volumes at interphase would be expected to display
similar radioscnsitivities. Hotvever. a cornparative
analysis of 172 cultivars of hesaploid wheat [S45] hasrevealed a 2-5-fold variation in thc radiosensitivity of
tlie seeds as indicated by changes in morphometriccharacters in tllc seedlings. It was shown that increased
r:ldioscnsitivity correlated with the degree ofbiocheniical polymorphism. i.e. the differentiation of
the genome. in the cultivars [S45].
An investigation of the combined effects ofirradiation and exposure to lead or cadmium salts on tile
induction of cymgenetic damage in tlie leaf meristern of'spring barley has demonstrated statistically significant
81.

ANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT

interactive responses, primarily at low doses of theagents [Gl I]. Taken together with other data [Uj],these results. ~vhich indicate non-linear biologicalresponses to combined exposures to contaminants,emphasize the importance of taking account of multiple
filctors when assessing the potential impact of radiationon the environment.
2. Forest trees

82. Studies have been made of the effects of shortterm ( 16-1 8 days) acute exposures of pine trees (in amixed birch-pine forest) in the spring and the autumn.
After the autumn exposure the LDw declined from50 Gy after hvo years to 30 Gy after five years. whenthe expression of the acute radiation damage was
essentially complete. After the spring exposure the trees
showed greater radiosensitivity, with the LD,, after two}.ears being 30 Gy (greater by a factor of 1.7) [K5]. It
was noted that suppression of normal growth at themain and all lateral shoots was a more sensitive
indicator of darriage than tree mortality [Kj]. and anabsorbed dose of 15 Gy in the spring has been Pound to
be 100% lethal within one year for cell proliferation in
the apical meristcm and for the processes of needle
formation [Sl4]. The developing radiation response ofpine trees following radiation esposure in the autumn
has been covered in more detail by Karaban et al. [Kb](they also give dala for birch trees. which show lower
radiosensitivity). Although pine trces appear to be moreresistant ro acute radiation exposure in the autumn,
when the period over which radiation mortality isexpressed is extended to six years after irradiation, theL,D,, declines. approaching thi~t sho\vn by trees
irradiated in the spring [MIO].
83. In the first year follo\ving acute irradiation of pinetrees in the spring, photosynthetic activity was reduced
at all doses greatcr than 5 Gy in a dose-dependent
fashion. Together with [lie loss of needles and growth
points (apical and lateral meristems), this reduction
decreased primary productivity. Although the photosynthetic rate recovered to above control values in thesecond year for doses below 25 Gy and in the third year
for doses below 50 Gy. this was insufficient tocounterbalance thc continuing loss of needles. and theoverall productivily of the pine stands continued to
decline. An acute esposure of 12.5 Gy depresses the net
rate of photosynthesis in Pitlus taeda and Pititcs eNiottii
saplings in the period 1-20 days after irradiation andalso depresses the rate of CO, evolution by stems [ I 181.
Birch trees show greater radioresistance [S27]. Using
common end-points as indicators of damage, it has beenshown that the responses of birch trecs to a combinationof acute irradiation (0-30 Gy) and sulphur dioxide esposure (7 mg n1") exceeded by a factor of 1.5 the sumof the responses to each of the factors separately, i.e.
there was a synergistic interaction. It was concluded that23

a complex mechanism underlay the combined response,
because the final outcome depended on the order inwhich the hvo factors were applied and was not simply
proportional to radiation dose [S 161.
84. The maintenance of reproductive viability isnecessary for the continued survival of the populationand is certainly required for recovery if some radiationmortality occurs. The esposure of pine trees to doses in
the range 0.3-22 Gy over 16 days in the autumn, whenthe early stages of pollen (the male gamete) formation
takes place, has been shown to produce damage [TI 11.
In the spring following exposure, vegetative growth andthe production of male cones occurred in trees that hadreceived less than 12 Gy; in the following year all theexperimental trees (in ~vhichdoses had been up to
22 Gy) wcre productive. At doses greater than 3 Gy
there was a substantial reduction in the fertility andviability of the pollen produced; viability recovered in
the second year, and in the third year neither pollen
fertility nor viability differed from control values at any
dose studied ( e 2 Gy). At doses exceeding 0.7 Gy.
morphological changes in the male cones, particularly
in terms of size and pollen production rate, persisted
into the second year, but by the third year recovery tocontrol values \vas apparent at doses up to 12 Gy [TI 1 1.
Rom these data it cannot be determined whether radiation-induced changes in either male fertility or mortality
would be limiting for a pine tree population.
85. In seeds of the ash tree (Frarinzrs at?~ericana,adeciduous tree) water content was shown to significantly affect sensitivity to acute gamma irradiation.
Seeds with a 3.4% water content showed a dosedependent reduction in germination at doses greaterthan 100 Gy; storage of the irradiated seed for three
years. or irradiation of three-year-old seed, further
reduced germination rates but did not materially affectthe pattern of dose dependence. The survival of thegerminated seed to the production of seedlings was very
low at 100 Gy and zero at higher doses. Raising thewater content of the seeds to 40% increased the germination rate at all doses up to 400 Gy and substantially
increased survival at doses up to 200 Gy. The reason
given for this lower radiosensitivity was that the lifetime of the radiation-induced free radicals in ~iioistened
seeds is shorter than in dry seeds [H7]. More than 50%
of one-year-old ash seedlings survived all doses up to
114 Gy when irradiated in the dormant state (lateautumn), but esposure in the spring (at bud break)produced over 70% mortality at doses grcater than
56 Gy. Over the next few years, the seedlings irradiatedin the dormant state grew faster than those irradiated in
the spring at all doses greater than 24 Gy, a dose atwhich the survival was also unaffected [H7].
86. Within a forest, the development and vigour oftrees of a given species and age will vary owing to. for

24

UNSCEAR 1996 REPORT

example, light interception (crowding andfor shading bydominant individuals), exposure to wind and soil
quality. For disadvantaged pine trees. these factors
cause reduced heisht and poorly developed crowns. The
less vigorous trees show greater radiosensitivity overthree years follo\ving short-term (eight days) acuteexposures up to 25 Gy; at 50 Gy there is no differencein the overall cumulative response [Slj]. It has also
been noted that acute radiation exposure renders pinetrees more susceptible to attack by xylophagous (woodeating) insects [S 171. These results have been confirmed
by observations made arter the Chernobyl accident,
tvhich found that poorly developed and less vigorouspine trees experienced the highest mortality [K22]. Suchfindings eniphasize the importance of regarding
radiation esposure as only one of the stresses likely to
be experienced by plants.
87. Of course. a pine-birch forest does riot consist
only of pine and birch trees. In addition to other tree
species, there is a herbaceous understorey component of
the plant community adapted to the conditions of lightintensity. moisture, exposure to wind etc. that prevail
under the upper canopy formed by the leafy cro\tfnsof
the pines and birches. Short-term acute exposure of thiscommunity in the autumn did not, in the following year,
lead to tlie loss of any of the 188 herbaceous species
present, nor was there ariy substantial change in species
content [S 181. There were. however, delays (in eightspecies) and advances (in three) in the normal, seasonal
developmental progression of some of the plants at
absorbed doses in the range 30-50 Gv. In the same dose
range, morphological variation from normal was noted
in 16 species. These cl'l'ccts had disappeared by thc
second season after exposure. At doses greater than
100 Gy, and particularly in the second season after
exposure. there were increases in the relative biomass
and the relative number of species in the experimental
plots. This response was ascribed to the increased
illurnination of the forest floor following tlie radiationinduced loss of the sensitive upper canopy (tlie pinetrees) and is thus indirect rather than direct [SI 81. In thefirst two years following acute exposure. tlie light andprecipitation penetrating to the forest floor \!ere notrnuch different than in tlie control areas. By the fourthyear there were it ell-defined, dose-dependent increases
in light penetration (up to sisfold) and precipitation (upto t\vofold) owing to the loss of pine foliage and, at thehighest doses, the loss ot'trees, causing an increase in
grass biomass up to 3.5 times that in the control area. In
the longer tenii. the extension of the grass ground coverin the irradiated area is expected to delay the recoveryof the coniferous component of the forest by suppressing seed germination and seedling survival [S28].
88. These data on thc response of a pine-birch forest
comniunity have been incorporated into a model 10
examine the long-ter~i~consequences of acute radiation

exposure [S19]. An exposure of 25 Gy (less than theLD,, for pine trees) substantially reduces both thenumber and productivity of the pines to minimum
values at 15 years and 5 years, respectively. with slow
recovery thereafter. The birch trees, being more radioresistant, benefit from the reduced competition. andtheir number and productivity increase. although riot
enough to balance tlie loss of the pines. It was predictedthat conlplete recovery to the pre-irradiation state \vould
require more tlian 50 years following an acute exposureof 25 Gy [S 191. Such a result is not surprising. since it
might be expected that a period longer than the average
lifetime of the trees \vould be necessary to regain thestable clima.. state.
89. The outcome of these studies of the acuteracliation response of the pine-birch lbrcst is broadly
comparable Lvitli the results of experiments on otherplant communities, which were reviewed by [I4. W3].
90. The protraction of radiation exposures increases
tlie total doses required to kill plants: for I I \voody
spccies. the LD,,, increased by a factor of 4.3 between
tlie first and eighth years of continuous exposure [S 131.
Gymnosperms (including the pine species), with athree-year LD,, of 46 Gy (5.200 pGy h-I). remainedmuch more radiosensitive than angiosperms. for whichtlie three-year LD,, was 330 Gy (38.000 pGy h'l) (seealso 1141). The I,U, for Pit~usrigiciu increased to 74 Gy
alicr 10 years of exposure (average dose rate of
1,250 pGy h") [S29]. and that for Abies balsunzea
increased to 1 10 Gy after I i years of exposure (average
dose rate of 1,500 pCiy h") and was still increasing[D121. The nu~nbersof balsam fir saplings in irradiatedplots was, howe\ler, greater than in control plots at dose
rates up to 250 pGy h-' over 1 l years [D12]. After I 1
years of radiation exposure, the LD, for plantation
black ash (Frcr~ir7lr.snigra) specinlens planted as twoyear-old saplings had increased to more than 900 Gy ats dose rate greater than 10.000 pGy h-'. All naturally
growing saplings of black ash \yere killed within five
years at exposures of approximately 10,000 pGy kl.but
two older specimens were surviving after 11 years atdose rates of 1 1,000 arid 4,100 pGy h-'; a green ash(Frr~sitlztspetrt7,~yI~~trniccr)
was also surviving after I I
years at a dose late of 5,900 pGy 11-' [D13]. Changes in
canopy cover owing to mortality confirm the relative
radiosensitivities of gymnosperms and angiosperms
ilrter I0 years of chronic irradiation [A4].
91. In mature trees. needle growth is reduced byexposures over 3-4 years at dose rates greater than
3,000 pGy 11-' to /{hies baisatnca [1)12] and over 10
years at dose rates greater than 600 pGy h-' to Pit1zc.s
rigida [S29]. For one-year-old saplings of Pitllrs.sylvesrt.is, needle length was substantially reduced at
7,000 pGy 11-I over a single growing season but wasincreased marginally relative to the controls at lower

ANNEX: EFFECTS OF RADIATION ON THE ENVIROhTMENT

dose rates (<78 pGy 11-I): stem length was reduced at alldose rates, and significantly so at 7,000 pGy h-I [S30].
Two-vear-old saplings of Pinzrs buttkriana showed
reduced stem growth at dose rates greater than
3,700 pGy h-' over the growing season [Aj]. Above
500 pGy h", the percentage of dead buds on Abies
balsat?zea increased rapidly after five years of chronic
exposure [DlZ]. Trunk growth in mature specimens of
Pinza rigida can be reduced by dose rates in the range
400-2.000 pGy h'l over 9 years [W 161 and at dose rates
above 1.700 pGy 11-' over 10 years [S29]. The radiation
response can be intensified by poor growing conditions[S29, W16] or mitigated in trees with large healthycrowns free of competition [W16]. The cambium layer
appears not to be terminally damaged by the irradiation[S29]. Net photosynthesis and CO, exchange in Pittzrs
rigida are poor indicators of darilage fro111 chronic
irradiation at dose rates less than 12.000 pGy ti-' [B20].
92. Chronic irradiation over a nine-year period
reduced the number of mature seeds in Pinus rigid0
cones to 10% of the control values at a dose rate ofabout 1.500 pGy h'l; no cones with mature seed were
found at nine-year accumulated doses greater than
74 Gy [S29]. White spruce (Picea glazrca) pollen has
been found to have an acute LD,, benveen 60 and
90 Gy for seed yield and quality [RG].
3. Shrub species

93. Radiation effects in shrub species can be illustrated by the results of two experiments, one short-term
and the other longer temi. In the short-term experiment,
estimated beta doses from simulated fallout (90Ycontanlinated particles) to the developing flower budsof Viguieraporteri (approximate doses of 30 and 60 Gy
at two experimental sites) induced a significant (2.5fold and 3.6-fold, respectively) increase in aberrant
flowers (estra petals, fasciated flo\vers, incomplete
flowers) relative to control plants. Flowers with additional petals. which constituted 8 1 % of' the aberrant
forms, produced 38% fewer seeds than normal controls,with no significant differences between the values forthe hvo exposures. Seeds from flowers receiving 5 1 Gy
showed a delay in the initiation of germination and a
38% reduction in germination rate; the plants from all
irradiated seeds were, however. apparently normal [M I I].
94. After seven years of chronic exposure, 3 1 shrub
species growing naturally in a mixed boreal forest
showed 5O0A mortality at dose rates ranging from SO0 to
over 60,000 pGy 11": for another 24 species, individuals
were sunriving at the upper end of the range 1014,000 pGy 11.' but in only three cases had single
individuals died at higher dose rates during the term ofirradiation. Where sufficient data were available toestimate it. the 50% lethal dose rate decreased with
irradiation time but for four species appeared to have25

reached stable long-tern1 survival values of 10.000
uGy h-I (Alttus rzrgosa) and 1 5,000 pGy h" (Coq7lus
cornzrta, Ifaccit~ium attgzrstifoliun~ and Vaccittirrm
ngatilloides). Differences in radiosensitivity could becorrelated to some extent with growth habit. e.g.
average mature height, vegetative goivth from shieldedroots, deciduous or evergreen. Regardless ofradiosensitivity, somatic effects were seen in most
species, and those that carried aerial buds through thedormant season showed the greatest number of effects
on leaves, flo~versand branches [D14]. The capacity toregenerate from rhizomes shielded below ground andfrom the bases of damaged stems at ground level.
growth habits that contribute to the relatively highapparent resistance to chronic irradiation in Gqlussacia
baccata and I~'accbiizm~
vacillatt~,appear to derive from
adaptations that i~nprovesurvival in response to a naturalstress. namely, forest fires following lightning strikes[B2 I 1.
4. Herb communities
95. The predominant effect of chronic iuadiation of
herb con~munities is to reduce species numbers(diversity) as the dose rate increases. caused by the lossof more radiosensitive taxa [F7, F8. W121. The
threshold for change was less than 20,000 pGy h" forold field communities [WI?]. and the dose rate toproduce a 50% reduction in the diversity of a plains
short grass community declined with extended exposure
to about 1,000 pGy h" [F8]. Nevertheless, a winter ryeweed community showed little change in composition
below 40,000 pGy h-', although the rye standing crop
was reduced at dose rates down to 10.000 pGy h-' andthe production of fertile rye seed was reduced at dose
rates above 1,000 pGy h" [H9]. Although a number ofherb species. one of which was Erigeron cartadensis,
survived at dose rates up to 130.000 pGy 11-', thereproductive potential was damaged above 20,000
pGy 11'' [W 171. In the longer term. chronic irradiation
slows the rate of successional change [F7]. which may
depend, more than usually, on the adventitious arrivalof viable seed from outside the irradiated area [W12].
Overall, however. herbaceous plants appear to be
somewhat less radiosensitive than shrubs.

5. Lichens
96. The diversity of lichen con~munitieswas reducedby chronic irradiation at a dose rate of 1.1 Gy 11-' over
one year. To survive at all at this dose rate (over9,000 Gy a'') attests to the radioresistance of the lichen
species. An apparent threshold dose rate of 125,000
pGy 11'' tvas found for effects on the composition oflichen comniunities, although relative densities werechanged at lower dose rates. Crustose fornis were moreresistant than either fiuticose or foliose forms. However,these two less ~.esistantforms grew more vigorously in1996 REPORT

areas where the dose-rate range was 26,00096,000 pGy h-' than in the control areas, although thismay have been an indirect response to irradiation.
caused by the collateral loss of the canopy as trees died
off at these dose rates. The total density of lichens also
declined with increasing dose rate, that is, the moreradioresistant species did not colonize the areas vacatedby the more radiosensitive species, but this may be aconsequence of an observation period that was too short
relative to the slow growth rates of these organisms[B22, W 171.
6. Fungi

97. The appearance of the fruiting bodies of macrofungi in an irradiated forest appeared to depend more on
the availability of an adequately nutritional substrate
than on the radiation dose rate. After an eight-year
exposure. mushrooms appeared at dose rates up to
100,000 pGy h-'. puffballs at dose rates up to325,000 pGy h-' and slime moulds at dose rates up to770,000 pGy h-I. These values are likely to beoverestimates of the actual tolerances, as the fruiting
bodies evolve from vegetative organisms, which areshielded to a greater or lesser extent below ground[H 101.

7. Indirect effects
98. A number of indirect effects of radiation
exposures may become apparent in plant communities.
In white oaks subjected to chronic gamma irradiation
there is a dose-rate-dependent gradient of damage in theforn~of delayed bud burst and an extended period of
leafing-out, during which process the leaves are softerand of a yello\vish hue, making them attractive to aphid
parasites. High densities of aphids were observed insome years (1963 and 1969) but not in others; these
densities were. moreover, significantly greater on trees
at dose rates greater than 4,000 pGy h-' than on trees atlower dose rates. It was concluded that other factors,
primarily meteorological, governed tlie presence anddismbution of ovenvintering aphids capable of colonizing the weakened host plants [H 1 I]. lnsect damage did
not, however, contribute to the loss of callopy cover inan irradiated boreal forest [D IS].
99. The induction of direct damage in plants by longterm chronic irradiation is likely to have indirect effects
on the local environment that may then interact with theradiation stress. Loss of vegetation and canopy cover
have been shown to affkct evapotranspiration in an
irradiated oak-pine forest. Close to the radiation source.
\\.hers virtually all the vegetation had been destroyed
afier 1.5 years of exposure at dose rates above 65,000h", tlie cu~nulativc'evapotranspiration was about
85% of that in undamaged forest. The rates of evapotranspiration in the first half of the groning season

increased as the dose rate (and damage) decreased but
became independent of irradiation during a drought inthe second half of the season. The lowest dose rate at
which there was n clear reduction in cumulative evapotranspiration was 4.800 pGy h-', at which point the tree
canopy had been reduced by 50% but the shrub layer
had remained almost undamaged [R7]. A chronic
irradiation dose-rate gradient has also been shown tohave significant effects on litter fall and total organic
matter content of the soil. Even I2 years of exposure
were not sufficient for these changes to reach a stableequilibriu~~~.
At that time. the total annual litter falldeclined continuously at dose rates above 1,500
pGy 11-I,as did the standing crop of litter. The effect of
this reduced organic input was apparent in the humus
standing crop. which showed depletion. relative to
coritrol areas. at all dose rates above 1.500 pGy h-I:
there was, however, a noticeable secondary maximum
in the humus standing crop at a dose rate of
10.000 pGy 11". corresponding to a zone where arelatively radioresistant sedge (C'arcr permnq-lvat~ica)had become established [A6].
100. The devastated area close to the radiation sourcein the chronically irradiated oak-pine forest would be asite where normal successional colonization would be
expected were it not for the continuing radiation esposure. It has been shown that there is a significant
input of wind-borne seed of advcntive herbs. \vhicli are
typical colonizers of disturbed areas [WI 81. and manyof these are sufficiently radioresistant to germinate andproduce young plants that can grow to maturity in thehigh-exposure zone. The capacity of these plants torepopulate the clisturbed area through reproduction was
limited. ho\vever. by two factors. First. the radiation
exposure severely reduced the nornlally profligate seedproduction: secondly. rabbits selectively grazed theplants that were conspicuous in the othenvise barren
area. In combination, these factors retarded the rate ofrccolonization, and the more successful species were
presenl as a few small clumps. These species weregelierally of nom~allysmall stature and thus more likely
to receive adventitious shielding from standing andfallen dead trees or they were perennials with theadvantage of shielded sub-surface buds. It was this latterclinmclcristic that, together with relative radioresistance.
t*avoured a species nor~nallypresent at low density inthe forest. The sedge (Cores pentisylvm~ica)spread
vegetatively and vigorously from the few originalindividuals and seemed likely to dominate the successional pattern to the exclusion of the hardy herbs [W 191.
8. Summary

10 1. Acute lethal radiation doses in plants have been
noted to range from I0 to 1.000 Gy. For some forms oflower plants (mosses, lichen) [lie upper range of theacute lethal dose may be higher by an order of rnagni-

ANNEX: EFFECTS OF RADIATION ON THE ENVIKOhWENT

tude. In general. larger plants are more radiosensitive
than smaller plants, with radiosensitivity decreasing in
the order conife~*oustrees, deciduous trees, shrubs,
herbaceous plants, lichen and fungi [W20, W2 I]. Nonlethal effects are noted at lower doses. for example
severe growth inhibition is noted at 40%-50% of thelethal dose and failure to set seed at 25%-35% of thelethal dose. At doses less than 10% of the lethal dose,
effects are less apparent, and plants maintain a normal
appearance.
102. A range of sensitivities to radiation exposure is
exhibited by the components of plants. ranging from dryseed (least sensitive) to apical meristenis (most sensitive).
Various crop plants show different reductions in yieldfollowing radiation exposures. with further modification
caused by external factors (temperature, liumidity).
Young plants and plants disadvantaged by growing
conditions may show increased radiosensitivity.
Plant species are also variably tolerant to chronic
radiation exposures. In the more sensitive pine species,
dose rates above 3.000 pGy h-' over 3-4 years reduceneedle growth; in one-year-old saplings, needle length
was substantially reduced at 7,000 pGy h" over a single
growing season. Trunk growth was reduced in maturepine trees by dose rates in the range 400-2,000 pGy h-'over nine years. Delayed bud burst and an extended
period of leafing-out was demonstrated in white oaks
exposed to chronic gamma radiation. At dose rates
greater than 4.000 pGy h-' the trees were more
susceptible to aphid infestation.
103.

104. With effects of chronic irradiation of the mostsensitive plants evident at 1.000-3,000 pGy 11.' andsome specific changes noted at 400-2,000 uGy 11-', it issugges~edthat chronic dose rates of less than 400
pGy h-I (10 niGy d-') should have only slight effects insensitive plants but would be unlikely to produce any
significant deleterious effects in the wider range ofplants present in natural plant communities.

B. TERRESTRIAL ANIMALS

I. Mammals(a)Mortality

105. Radiation effects in mammals have been
extensively studied in radiobiological experiments using
laboratory animals (niicc. rats, dogs and monkeys) anddomestic livestock (pigs, sheep, goats, burros and cattle)[BS, B9]. Except in the case of exposure at unusuallyhigh doses, radiation damage or lethality in mammals isdue to disturbances in the haematopoietic system andthe gastro-intestinal mucosa. These cell self-renewal
systems contain stem cells, differentiating cells and27functional end cells. with the stem cells being the mostradiosensitive and thus the predominant influence on
the radiation response. Symptoms become apparent
when end cells are not replaced.
106. Mammals die from damage to the gastrointestinal tract within the first 10 days following
exposure to relatively high radiation doses (midline
doses of 10-50 Gy) ([U3]. Annex G. "Early effects in
man of high doses of radiation"). The intestinal
symptoms (diminished food and water intake. diarrhoea,
loss of fluids and electrolytes, decreased intestinal
absorption etc.) are a consequence of cell depletion in
the intestinal lining due to damage to the survival andproliferative capacity of the crypt stem cells: the normal
continuous flow of mature replacement cells from theclypts to the villi is interrupted. The time course of
events is alniost independent of dose in the range 1050 Gy but differs widely benveen species. The differences in radioscnsitivity behveen species result fioln thecomplex interactions of the sensitivities of the crypt
stem cells and their rates of maturation and progression
from the crypts to the villi. Approximate LD,& for the
gastro-intestinal syndrome are as follows: mouse.
12 Gy: rat, 11 Gy; rhesus monkey, 9 Gy; and dog. 8 Gy
[V3]. The values were determined for particular strainsof these species, and wide variations are known tooccur. However, the approximate species differences(due lo the complexities noted above) might arise fromvariations in intestinal morphology that have to do withadaptations to particular diets, i.e. herbivory. omnivory
and carnivory [V3].
107. Mammals die from bone marrow failure (thehaematopoietic syndrome) within weeks following
whole-body radiation exposures giving midline doses of
1.6- 10 Gy. Tlic ultimate cause of death in different
species is granulocytopenia. thronibocytopenia or
lymphocytopenia [U3]. l'hese conditions are again thercsult of complex interactions of differential
radiosensitivities and cell cycle and maturation kinetics(including stem cell survival) in the various celllineages. Nevertheless. there is an apparent inverse
relationship between the LD,
and the weight of theanimal [U3], and approximate values are 6-10 Gy forsniall matnmals and 1.6-2.5 Gy for larger ones [B8]. For
domesticated animals (cattle, sheep. goats. pigs, burros
and horses) the LD,, lies in the range 1.2-3.9 Gy(midline dose) [KlO]. In addition to the variation in
LD,,,,.
the rate of change of survival with dose also
varies behveen species (Figure I I I). with sonie evidence
that at lower sublethal doses there might be lessvariation behveen species. There has been considerable
errort (e.g. [B 101) to reanalyse experimental results toquantify more esactly species-relevant LD+. 'There are,lioivever, many differences in response between
separate strains of the same species. dositnetric uncertainties and difkrences in conditions of maintenance28

UNSCEAR 1906 REPORTand care of the animals before and after exposures that
can affect response. All species are markedly influenced
by the presence of pathogenic bacteria in the animal.
which reduces survival times and, thus, LD,,s. The
LD,, for mice housed in a genn-free system has beenfound to be about 3 Gy higher than that for mice housed
in a conventional systeni [L4].
108. Protraction of :i given total exposure generally
reduces the extent of iri.jut-y. as it allows mlo distinct
processes to intervene. 1-irst, sublethal damage is reparable at the cellular level. which is particularly importantfor exposures to low-LET radiation. Secondly, cellproliferation can replace lethally damaged cells andmaintain t t ~ ecell population at a new level. which isdetermined by the dynamic interaction between the dose
rate and the rate of cell death and by the total reserve
proliferative capacity.
109. At reduced dose rates (protraction of a given
total dose) of lo\\.-LET radiation, all species show a
gradual increase in LD,,: higher total doses aretolerated. This changing response has been attributed ro
the increasingly effective influence of cellular repair ofsublethal damage at the lower dose rates. As the dose
rate is furthcr reduced. a sharply increasing trend in thevalues for median lethal dose is apparent for mice, pigs.
dogs, goats and sheep; the approximate threshold dose
rates for this change in response correspond to theaccumulation of the LD,, in periods ransing from 0.2
days (mouse) to 9 days (goat). This rapid change inLD,, with dose rate has been interpreted as theconsequence of a shifiing balance in the dynamic interaction between dose-rate-dependent cell loss and cellproliferation and maturation kinetics in rhe haernatopoietic system: the latter processes are under homeostatic control. i.e. their rate constants can alter in response to radiation-induced cell loss. The data for theburro (donkey) and rhe primates do not show any sharp
increase in median Ie~haldose at dose ratcs down to
8.300 pGy h-I (LD,, in 18 days) and 5,400 pGy h-I(LD, in 60 days). respectively. There do not appear tobe any data for LL),,s at dose rates less than
4,000 pGy 11" or for periods of exposure exceeding 60
days, although studies have been made outside theselimits for other purposes.
110. For the survivors of acute doses in the LD,,
range and for organisms exposed to lower acute doses,
it has frequently been suggested that there \s1ouldnevertheless be consequential life-span reduction FFom nonspecific causes, e.%. accelerated ageing or the earlier
onset of the pathological conditions responsible for~iionaiityin the unirradiated population. The available
data have been reviewed ([U5]. Annex K. "Radiationinduced lilt. shortenilig") and the conclusion reachedthat there is little evidence that an observed reduction inlife-span arises from anything other than an accelerated

onset or increased incidence of neoplastic disease: thisconclusion has been confirmed by the Committee's mostrecent consideration of the available data ([U?].
Annex F. "Influence of dose and dose rate on stochastic
effects of radiation"). Analysis of the results for mice
cxposed to x raps or galiirna radiation, including thoseresults that show an extension of life-span at doses lessthan 2 Gy. indicates that the percentage of life-shortening could be most simply expressed by a linear, nontllreshold dependence on dose. 'The slope of the doseeffect relationship yielded a 5% reduction in life-span
per gray down to the lowest doses. The much more
limited data available for the rat, dog and hamster showthat their responses are not very different from that oftlie mouse at doses below 6 Gy, and in this dose range
a factor of 5 would cover the overall intra- andinterspecics variability.
1 1 1. For chronic lifetime exposure of mice to low-LET
radiation at dose rates where haematopoietic damage(bone marrow failure) does not occur. the percentage lifeshortening sho\vs an essentially linear response with dosein the range 0-45 Gy (dose rates less than 3.800 pGy h-I).
Thus, chronic exposure is substantially less effective, bya factor of 7, than acute exposure. Again. there is noevidence that anything other than radiation-induced
cancer is responsible for the increased loss of life-span
relative to the controls [Uj]. At a dose rate of 420 pGy h-I(a lifetime dose to illice of approximately 7 Gy) the
average loss of life-span amounts to 5% (equivalent, forexample, to 20% of the population dying from theconsequences of irradiation at 75% of the normal meanage). Extrapolation of rllese specilic data on thc mouse to
the radiation exposure experienced by a population in acontaminated "natural" environnient is not straightfonvard:(a) natural mortality in a wild population of micesubjected to competition (intra- and interspecies)
and predation is unlikely to have tlie same age
deperldence as observed for control populations in
the laboratory; thus a late, incremental incidenceof turnours is unlikely to have the sanie overall
effect on life-span;(b) estetision to other species, especially those withlonger average life-spans is unjustified; andif
the fertility of the older members of the popula(c)ti011 represents a significant buffer capacity, thenearlier than normal mortality due to radiation
exposure might have a disproportionate effect on
the population at times of stress [F4].
The very limited data available for other species(guinea-pigs. goats and dogs) are insufficient to allow
meaningful comparison; they do. ho\vever, identify
turnour induction as a consequence of radiation
exposure [US].

1 12. Acute or chronic whole-body exposure to highLET radiation (fast neutrons) has been shown to be more

ANNEX: EFFECTS OF RADIATION ON THE ENVIROh'MENT

effective than the corresponding ION--LETexposure
regime in producing a reduction in life-span. The relative
biological effectiveness (RBE) is greater, as is to be
expected. for chronic irradiation than for acute exposure[Uj]. These results underline the importance of thepotential internal exposure from contaminant radionuclides that decay by alpha emission. There is a body ofevidence to show that the injection of radioisotopes ofbone-seeking elements (Sr. Pu.Th, Ra and Am) into ratsand dogs results in life-shorteningdue to the induction ofbone tuniours. with tlie alpha emitters being more
effective per unit of absorbed dose than the beta-etnitting
90Sr-?' (although the precise site of deposition is also amodifying factor). In apparent sharp contrast. 2'9Pu
chronically administered to rats results in very littlechange in the life-span compared with the controls.
although there is an increased incidence of marrowdamage, leukaemia and bone cancer [Uj].It is clearly
unportant to identify the appropriate target tissues andorgans and to h o ~ vthe exposure from internal orexternal contaminant radionuclides when attempting toassess the potential impact on the environment.
1 13. The influence of hibernation on the response of
mammals to acute irradiation is complex and depends
on the Stahis of the animals before, during and after
exposure. For the ground squirrel (Citelliis ~ridecenllineutzrs), hibernation induced by maintenance at 5°C
for 2-5 days prior to and during irradiation consistently
provided some protective effect in ternis of increased
mean survival tinie and percentage survival at 30 days.
Thc degree of protection could be modified by the postirradiation maintenance conditions, with immediate
arousal to an active state improving survival relative toanimals maintained in hibernation lor an additional 2030 days [ B E , 34, M21]. The conditions employed toinduce effective hibernation also modified the degree ofprotection. Maintenance for 2-5 days before exposure at
I j ° C . or undisturbed. but closely confined, at 23°C
both improved survival relative to animals maintained
at j°C,which, in turn, survived better than animals
irradiated while nortnally active [B32]. Split doseexperiments have shown that repair of radiation damage
continues during hibernation at 5°C [J4].

113. Some limited data are available indicating thatthe acute effkcts ofradiation in small mammals are lesssevere when experiments are carried out under controlled conditions in the laboratory rather than in thenatural environment, where additional stresses arepresent. Although the LD,, obtained for female cotton
rats was similar for a laboratory study and for irradiatedanimals released into quasi-natural conditions in large
field enclosures, the mortality of rats exposed to doses
less than the LD,, was greater under field conditions[137]. Exposure of house mice and tield mice at theLD,,,, established under laboratory conditions
produced the same and lower survivals, respectively.

29

when the animals were released to field enclosures[G4]. In laboratory studies. the LDjoa,, for the female
house mouse was found to be greater when the treatedanimals were housed singly than when the females were
kept in groups of five [D6]. Although the data were notentirely conclusive. chronic irradiation of pocket micein an eight-hectare enclosure at approximately 420
pGy h-' appeared to marginally reduce their survival
relative to othcrwise similar controls. The survival ofthree field populations (one irradiated and two control)
was less than that of an irradiated laboratory group,
which in turn was less than that of the laboratory
controls. In addition. under laboratory conditions. theirradiated and control male mice survived longer, on
average. than the corresponding females [F3].
1 15. It has to be accepted that the number of mammal
species that has been or. indeed, is likely to be studied
is an extremely limited, and probably atypical. selection
from those extant. Nevertheless the available data eventaking account of substantial interspecies variability,
provide very little evidence that dose rates below
400 pGy h-' (approximately 10 mGy d-') to the most
exposed members of the population would seriously
affect their mortality (and. thus, the death rate inpopulations of these species) from either deterministic
or stochastic responses.
(b)

Reproductive effects

1 16. 'The effects of radiation on reproduction have also
been ~nuchshidied. with most of the results suggestingthat natality is a more radiosensitive parameter' thanmortality in species other than man and, therefore, of
more relevance in an envirotunental context. The
minimum dose required to depress reproduction rates
may be less than 10% of the dose required to produce
direct mortality [W5]. Reproductive effects niay beapparent at doses that cause no other observable responsein the animal. For example. the LD,
in mice is 612 Gy, depending on strain and species. but a11acute doseof 0.08 Gy produced a 50% reduction in the nuniber ofoocytes at their most sensitive stage in newborn mice
1031. Because more immature oocytes are normallypresent than will be utilized for reproduction. tlie 50%
reduction does not translate to a 50% decline in fecundity;
it could, however, conceivably lead to a minor shorteningof the reproductive span [M5]. In male mice, by contrast,
an acute dose of 10 Gy may only temporarily impair
fertility in adults, although it1 young mice (3-5 days ofage), it can induce permanent sterility ([U6]. Annex H,"Genetic effects of radiation"). The differences in
response are a consequence of the quite different
processes of gametogenesis in the two sexes [D2].
There
are also substantial differences in response to the same
dose between species, particularly for oogenesis. withmost species showing greater radioresistance than themouse [C6].

1996 REPORT

1 17. Chronic irradiation probably affects oocyte
viability by different nlechanisms than acute irradiation
at the particularly sensitive stages of oogenesis, as
discussed in the preceding paragraph. The differences
arise from both the timing of the oogonial cell divisionand the limited size of the stem cell pool. In a female
mammal exposed throughout its life, fro111 co~iception
to reproductive maturity, the greater part of the total
dose is likely to be accumulated by oocytes in theresting. immature stage rather than in any particularly
sensitive stages of oogonial cell proliferation. The
effects of chronic exposure are more relevant toenvironmental concerns. The number of immature
oocytes in mice can be reduced by 50% by a dose rateof 130 pGy h-' from tritiated water during the period
19-33 days after conception [D5]. For irradiation fromtritiated water from conception to 14 days after birth,the median lethal dose rate for mouse primary oocytes
was 180 pGy h-', and an RBE of abour 2 (relative tobOCo gamma rays) was estimated. At lower dose rates(and lesser effects) the RBE increased to 3 [D 16, D 181.
In I I-week-old female mice chronically exposed toeither beta radiation from tritiated water or T o gamma
rays for 10 days kvith similar dose-rate profiles. thenumber of priniary oocytes declined exponentially withcuniulated dose. A total dose of 0.16 Gy from tritium
reduced the number of primary oocytes by SO%, and an
RBE of 2 was estimated relative to @Cogamma rays
[D20]. The developing oocytes of the squirrel monkey.
exposed to tritium from conception to birth. sho\ved aneven higher radiosensitivity. with a median lethal dose
rate of 42 uGy h'; neonates that had been exposed to
420 pGy h-' were found to be sterile [D18]. Similar
results have been observed for tritium exposure inmonkeys in the last third of pregnancy [C6] and for
wSr-90Yexposure of mice [ W ]The
. total accumulated
doses \\!ere 40-200 mGy. A total dose of 900 mGy fromwSr-MYreduced fertility in the mouse [R2], and a dose
rate of 3,300 uGy 11.' during the period 20-40 days afterconception produced complete sterility [Rj].
118. The effects of continuous tritium exposure
from either tritiated food or tritiated water on
primary oocyte production in first-generation (Fl)and second-generation (F2) offspring have beenstudied in rats. The numbers of primary oocytes were
determined in 21 -day-old F, and F,offspring that had
effectively been esposed since conception at a dose
rate of 77 pGy h-I. Although oocyte numbers werereduced to similar estents under both esposure
regimes and in both I.', and F2 offspring. the differences from control values were not statisticallysignificant [PIS]. In a second experi~nent, thereduction in oocJ,te numbers in ?-I-day-old F,
offspring was significant at a dose rate of
6 10 11Gy h" derived from tritii~rriin drinking waterand at 200 pGy 11" derived from tritium in food(organically bound tritium) [PIJ].

1 19. I'or mature female rats, dose rates of less than
4.000 pGy h-I lrorn mCo gamma radiation did not affectreproductive ability [B15]. Female mice exposed at
800 pGy h' from conception became sterile at 25 weeks
of age. and those exposed at 4,000 pGy 11'' were sterileat 7 weeks of age [B15]. In eight-week-old female mice
exposed to either beta radiation from tritiated water or"OCo gamma rays for 10 days with similar cumulative
dose profiles and mated after a further 21 days. preimplantation losses increased linearly with dose. This
loss became significantly greater than for the control at
a total dose of' 0.31 Gy for tritium exposure, and an
RBE of 3.5 was estimated relative to WCogamma rays
[Z7]. In young mice, "'Po injected as PoCI, in isotonic
saline was Sound to be preferentially taken up into theovary and uterus. A dose of 37 mBq g-I body weight
was estimated to deliver an average absorbed dose to
the ovary of about 100 pGy over a period of four days,
at which time there was a significant reduction inprimary oocytc survival (79% of control). Comparisonswith other published studies of the effects of gamma
radiation [ 0 3 ] provided an estimate of over 370 for the
RBE. although lower values were found for higher absorbed doses ol'alpha radiation and greater effects [S3 I].

120. l'he testes are also sensitive to chronic exposure,although tlie continuous nature of the spermatogenic
process allows sperm production to be maintained underirradiation, often at equilibrium levels lower than incontrol animals. A dose rate of 570 uGy h" over sevenmonths resulted in the stabilization of the spermatogoriial cell population in the mouse at 80% of control
values. I-lowever, a second study showed that at a dose
rate of 750 pGy h-' over 15 weeks, the stem cell
population maintained control values, although cell
death was occurring [C6. U6]. In male mice a mean
absorbed dose rate of 36 pGy h" to the testes from 39Pu
alpha radiatio~ifor 5-8 months reduced testes mass andspeml output by approximately 10% and 8%.
respectively: an RBE of 10- 15 was estimated relative tothe effects ofmCoganinia rays [S50]. In the rat, a dose
rate of 580 pCiy 11-' reduced the testes weight by 7%
relative to tlie controls after 75 days of exposure.
corresponding to a disruption of the process of spermatogenesis. Cessation of esposure allowed recovery tonear-nonnal values [La]. At a dose rate of 800 pGy h-'liom conception. the I'crtility of male niice was notaffected over the 33-week duration of the experiment[BI 51. 111 beagle dogs, a dose rate of 180 pGy h-'resulted in progressive cell depletion and sterility withina few months, but exposure at 36 pGy ha' over thewhole life clicitcd no respolise [C6]. No more sensitive
terrestrial mammal has been identified [Mj. U4],
although it is accepted that few of the total number of
species have been studied.
12 1. Continuous irradiation at 500- 1,000 pGy h" forat least 10 generritions did not affect the fertility of pairs

ANNEX: EFFECTS OF RADU,TION ON THE ENVIRONMENTof mice from four different strains. as indicated by theaverage size of the first litter [SI I]. This result is notnecessarily inconsistent with the data discussed inparagraph 1 16, because of the lack, noted there, of adirect relationship between oocyte reduction andfecundity. In the environmental context, it is tlie effectof radiation on lhe normal distribution of lifetime
reproductive capacities that is the relevant factor.
Nevertheless, it seems unlikely that a dose rate of
100 pGy h l to the most highly exposed individuals in
populations of wild mammals and, by inference, a lower
will have any
mean dose rate to the whole pop~~lation
damaging consequences for the fecundity of populations as a whole.
(c)

Effects on t h e developing embryo

122. As is to be expected from the degree of cellproliferation and differentiation in progress. thedeveloping embryo has been found to be rather
sensitive to the effects of radiation. Damage at this stageof the life cycle can reduce fecundity and postnatal
survival and, hence, tlie potential recruitment to the
population. The available data, the majority of which
relate to the mouse. \sferethoroughly reviewed in earlier
UNSCEAR Reports [U4. U6] and in a report producedby the Comn~issionon Radiological Protection of theFederal Republic of Germany [C22], so only a briefsummary will be included here. I1 is conventional todivide the temporal development of the mammalianconceptus into three riiain periods corresponding tosignificant differences in the processes in progress inthe embryo: the pre-implantation period, which encompasses the development of the blastocyst; the periodof major organogenesis; and the fetal period. These
divisions are also convenient for the discussion of the
responses to radiation. which differ in nature and degree
benveen the periods, as can be seen in Figures IV andV, which summarize the situation for the mouse [C22].
123. The most conspicuous effect of acute irradiation
during the pre-implantation period is tlie early death ofthe embryo: post-implantation and postnatal death areless important sequelae of such exposure. Similarly,.rrro\vth reduction and nialfonnations are a less frequentconsequence of pre-implantation exposure [C22, Pl31.
Even within the pre-implantation period (up to tlie lateblastocyst stage), however. there are variations in
response. Exposure of single-cell mouse embryos to
2 Gy produced niainly pre-implantation deaths withmany fewer resorptions (post-implantation deaths) andfetal deaths, while similar exposure at the stage of 32-64
cells only produced resorptions [M 181. 'I'he mortality ofthese very early embryos correlates well with thepresence of radiation-induced chromosome aberrationsin the blastomeres [C22]. Doses as low as 0.2 Gy tomouse embryos in virro have been reported to produce
mortality at the most radiosensitive time. prior to DNA

31

synthesis in the pronuclear stage. It has been shown that
there is a tenfold variation in radiosensitivity throughthe different stages of the mitotic cycle and benveen
mitotic cycles in the very early developnient stages. ?heirradiation also disturbs the normal kinetics of progression through the cell cycle. In vivo studies withrodents have provided q~~alitative
confirmation of thesefindings. Notwithstanding the general conclusions given
above. doses as low as 0.05 Gy to the rat in the preimplantation period in one experimental series resulted
only in fetal mor-tality. whereas a higher dose (0.1 Gy)
produced both embryonic and fetal mortality, with thelatter being greater [U4, U6].
124. There appear to have been rather few studies ofthe effects of chronic irradiation during the preimplantation period. The impact of chronic exposure
from internal radiation (tritium as tritiated water) andexternal T o gamma radiation on pre-implantation
mouse embryos maintained in culture has been
investigated [Y I]. The radiation exposures commenced
at the pronuc~ear,early two-cell and late hvo-cell stages,
and survival to the expanded blastocyst stage was usedas the criterion of damage. Exposure from the pronuclear stage showed the greatest radiosensitivity, with
50% survival at an estimated tritium concentration of
4.4 MBq ml-I (corresponding to an estimated dose rateof 10.000 pGy 11-'). The range of tritium concentrations
used does not allow assessing tlie lowest dose rate toproduce an effect. The estimated RBE was not
significantly different Frolii unity. Other experime~its[U4] have shown that tritiated thymidine produces
damage at much lower activity concentrations, underlining the importance for the purposes of dosimetry of
infomiation on tlie relative spatial disposition of theradiation source and the putative target for the biological effect being examined (see also [C22]). The
available data are insufficient to assess whether
protraction of the exposure reduces the effectiveness ofa given dose (the sparing effect), but it should be notedthat the restricted time available for the accumulation of
the dose (pre-implantation periods of 5- 17 days [U1])also limits the potential total dose to this embwonicstage at low dose rates.
125. It has been concluded that the most characteristic(but by no means the only) response to acute irradiation
during the period of major organogenesis is theinduction of nialfonnations [C22. U4. U6]. These
teratogenic effects develop during embryonic and fetal
growth and, if not of lethal consequence. persist into thepostnatal period. 'Ihe time of maximum radiosensitivity
for the induction of malformation in a particular organ(although there may be growth disturbances in otherorgans or the whole body as well) coincides with thesurge in cell proliferation in the relevant precursor
tissue. This is a general finding for the animal species
that have been studied (mouse, rat, hamster. gerbil.

32

UNSCEAR 1996 REPORT

rabbit, monkey, dog. sheep, cattle. pig and marmoset),but the response to a given acute dose strongly depends
on the species and its developmental stage at the time of
exposure. The dose ranges associated with observablemalformations in several species are summarized inTable 8.
126. The dose-response relationships for the inductionof malformations are si-moid and consistent with adeterministic mechanism. Protraction of a given dose
reduces the incidence of each class of malformation
below that expected as a consequence of the same dose
given at the most sensitive stage. Careful experimentswith a particular strain of mouse have shown that doses
as low as 0.05 Gy at the most sensitive stage ofembryonic development (seven days after conception)
can triple the incidence of gross skeletal malformations
IIJ41. Malformations of the central nervous system havebeen particularly studied. and there is little evidence forany pathological responses at doses below 0.1 Gy (inmice. rats and primates) [U4]. Sterility was induced in
36% of female rats esposed to 0.5 Gy as embryos atnine days after conception [U4]. For the relatively lessfrequent effect of embryo lethality, rodents sho\sr an
LD,, of less than 1.5 Gy in the early stages oforganogenesis, after which there is an increase with
development until the fetal stages. which yield values
little different from tlie postnatal LD,,.
127. There appear to be no studies of tlie effects ofchronic irradiation specifically during major or,"an0genesis. A single study of fractionated exposure in rats
(four daily doses of 0.01 Gy at 6-9 days after conception) showed a significantly impaired learning
capacity at four months of age in behavioural tests inwhich perforniance requirements were gradually hcreased [B 191. Mouse enibryos have been exposed tobeta radiation arising from a single injection of tritiatedwater to the mother at 12.5 days afier conception, withthe male offspring being given behavioural tests from
21 days of age. There was evidence of changes inbehaviour, attributed to irradiation. at cuniulative dosesof 0.1 Gy and greater [W26]. Such a response could
lead to reduced viability in the natural environment.
128. During tlie fetal period of developrnerit the mainconsequences of acute radiation exposure appear to bemortality, with LD, values similar to those for postnatal
exposure, and disturbances of growth. Teratogenic
effects become increasingly difficult to detect, althoughdaniage to [he eye, tlic central nervous system and the
gonads appear to be tlic main responses [C22, U4, U6].
Acute exposures up to 2 Gy to developing rats behveen
sis days after conception and eight days after b i d
induced no deficit in the immune response up to 12
weeks of age [PSI. Esposure of rats to 1.5 Gy (10-12
days after conception) caused germ cell killing; testis
weight was reduccd slightly by exposure on day 15 andbecame progressively more pronounced at later times,
with the peak reduction for exposures behveen 18 days
after conception and 3 days after birth [CIS]. The
weight deficit was due to the loss of spermatogenic cells
in the tubules, but the endocrine function of tlie testis
was unarfected. In anotlier study, 2.5 Gy delivered togravid rats on day 20 after conception caused sterility in
70% of the female offspring [K7].
129. Fractionated x-ray exposures (I6 exposures of
0.12 Gy, twice weekly for eight weeks) produced severe
daniage to the ovaries of female bonnet monkeys when
the irradiation was given 77- I33 days after conception
but produced very littlc response when given 48-104
days after conception [Aj]. A single injection oftritiated water to the females on day 13 after conception
was used to deliver total estimated doses of 1.3. 0.6 and
0.2 Gy to fetal mice. At two months of age, all male and
40% of female offspring were infertile at the highestdose, and at three months female fertility was declining.
\vliile there were signs of some recovery in the males[TI 61. It was concluded that doses in excess of 0.5 Gy
were required to affect fertility [U4]. A dose of 3 Gy
delivered to female rats at 18.000 pGy ha' over theperiod 13-20 days after conception affected ovariandevelopnient (smaller ovaries, absence of follicles andcorpora lutea) in offspring, whereas an acute dose of thesanic ~iiagnihldeon day 18 after conception produced
110response [E4].
130. Chronic radiation exposure throughout gestationis the more likely possibility in contaminated naturalenvironments. Esposure of pig embryos togamnia rays at 420 pGy h-I for I08 days during gestation (1 12 days duration) reduced the weight of the
gonatls in the offspring, and at 1.300 pGy h-' both
female arid male offspring were rendered sterile. I-listological esaniination of tlie gonads showed reduced
numbers of gem1 cells at a dose rate of 210 pGy he'[ES]. Rat embryos exposed to tritium (as tritiated water)
throughout development showed significant reductionsin testis weight at an estimated dose rate of 1,300
pGy li", and the ovaries were much reduced or absent
at 2,500 pGy he' [CO]. Exposure of female 111ouse
embryos to tritium (as tritiated water) from conception
to 14 days of age showed dose-dependent reductions intlie numbers of oocytes, with a significant reduction(13%) in primary oocytes per ovary at an estimateddose rate of 10 pGy h-' and a reduction to two thirds oftlie control value at 100 pGy h-I [D7]. A later series ofexperi~iients produced similar results. with theadditional finding that [lie largcst part of the response
was a consequence of the prenatal exposure and that thetritium beta particles were more effective than *Co
gamma rays in producing the damage (an RBE of 1.9;
see also paragraphs I 17- 1 19) [DS]. After irradiation at
420 pGy 11-I during gestation, germ cell numbers werereduced relative to the controls in the following species

ANNEX: EFFECTS OF RrZDIATION ON THE ENVIRONMENT

P I ] : pig (I. l Gy total dose), I% (male), 5% (female):guinea-pig (0.62 Gy total dose), 41% (male), 71%(female): rat (0.2 1 Gy total dose), 50% (male). 90%(female): mouse (0.20 Gy total dose). 7 1% (male). 87%(fen~ale).As noted above, these reductions in germ cellnumbers would not necessarily produce a corresponding
reduction in fecundity.
13 1. A significant reduction in the birth weight(stunting) of female and male offspring was observed at2.500 pGy h-' From tritium exposure (as tritiated water)
during gestation in rats, and the brain weight wassignificantly reduced at 1,300 pGy h'' [C9]. A later
experimental series [C 101 showed significant reductionin brain weight in young born to mothers that had been
exposed to 130 pGy h-' From tritium (3.7 lo4 Bq ml-' astritiated water in drinking water) since their own
conception, through 100 days of postnatal life and the
21 days of pregnancy. Simultaneous esposures tograded concentrations of lead in drinking water showedthat the interactive effects of these two contaminants
were less th'm additive.
132. The relative effectiveness of tritium beta
particles and external '"Cs gamma irradiation in
reducing cerebral development in rat embryos has been
investigated [U4]. The range of estimated dose rates
from tritium was 2 10- 1,600 pGy h", and cerebral mass
at birth was negatively correlatcd with the cumulative
dose during gestation. 'l'he '"Cs gamma radiation wasless effective in producing a response (KBE = 2.1 at
500 pGy 11.' from 'H). A dose rate of 1,300 pGy h-'(60Co gamma rays) reduced the peri- and postnatal
weight of the brain in pigs [U6]. No studies appear tohave been made to determine whether such morphological responses have an associated impairment of
hnction that might be significant in the natural environment: the few data noted in paragraph 126 are, however.
suggestive of the potential importance of this response.
1 . Damage to the developing mammalian embryo
appears to be a potentially significant criterion of
impact From contaminant radionuclides in the naturalenvironment. Dose rates of 420 pGy h-' throughout
gestation produce readily detectable reductions in the
populations of gem1 cells in the developing gonads of anumber of mammalian species. and the lowest dose rate
at which damage has been seen is 10 pGy 11'' fromtritium (as tritiated water in drinking water)incorporated in female mouse embryos. In addition,dose rates of the order of 420 pGy 11-' induce reductions
in neonatal brain weight, although the significance of
this deficit in Sunctional or behavioural terms is
unknown. The wider significance of these responses atthe population level has not been investigated. Even
recognizing that only very limited data are available, it
may be concluded that maximum dose rates of 100
pGy h-' (2.4 mGy d-') to gravid members of a maninia-

33

lian population are unlikely to have any consequences
for the population as a whole from induction of damage
in the developing embryos.
(d)Somatic and hereditary mutational effects

134. The substantial literature on the induction of
nuta at ions (genetic damage) in animals by radiation
exposure has been thoroughly reviewed in previous
reports of the Committee [U2, U3, U4, U5, U6]. The
tern1 mutation encompasses a wide range of damage tothe genetic material. and its consequences depend on
the nature of this damage and also on the site, i.e. insomatic tissue or in genn cells. In many cases. thedamage is severe and incompatible with the survival of
the cell as an entity with proliferative potential; thedamaged cells die either immediately or after rather few
division cycles. This f o m ~of damage is largely subsumed in the discussion above of mortality, effects on
fertility and effects on the developing embryo. Thereremain the lesser forms of damage that are notinconsistent with the survival and subsequent long-term
proliferation of the cells but which. nevertheless. havea potential to harm the host organism. In somatic cells,
the consequence of concern is the induction of cancer[U4];in germ cells, it is necessary to assess the potential
impact on the fitness of offspring in the next andsubsequent generations of animals and the potential
i~nplicationsfor the population [U3].
135. It has alrcady been noted (paragraph 1 10) thatthe chronic exposure of animals throughout their life
reduces life-span, mainly by the induction of malignant
tuniours, although it was concluded that at dose rates
less than 420 pGy h'' (10 mGy d-I) the effect would beslight. The data for animals (mainly rats and mice)reviewed in the UNSCEAR 1986 Report [U4] show that
there is a wide variation in the sensitivity to tumour
induction depending on the tissue and on the species.
Nevertheless. there is a consensus that at the dose rates
likely to prevail in environments contaminated as aconsequence of controlled discharges of radioactive
wastes, a linear dose-response relationship would beappropriate for all qualities of radiation. This limited
database makes extrapolation to other species. particularly those that are long-lived, uncertain. A review ofdata on the effects of chronic exposure to *Sr-MY beta
radiation in beagle dogs showed that cumulative chronic
exposures up to about 7 Gy, either from a single injection to young adults or from a body burden accunlulated
via ingestion fiom the fetal stage (uptake from themother) to 540 days of age. did not increase the incidence of cancer in either the bones or the adjacent soft
tissues. and there was no significant reduction in lifespan compared with controls; this corresponds to anlean dose rate of approximately 60 pGy h-I. There wassome evidence from effects at higher total doses that theage at commencement of exposure and the cumulative

1996 REPORT

dose profile influenced the outcome: for example, thedogs initially exposed it1 zrtero showed haematopoietic
effects and soft tissue cancers that were not apparent indogs cornrnencing radiation exposure as young adults.
Parallel experiments \vitli internal exposure from 226Ra
indicated that at the lowest doses causing a radiationinduced increase in bone sarcoma, the RBE (alpharadiation compared with beta radiation) was about 25[NJ]. In addition, the "OSr body burdens that did not
induce cancer also had no effect on the fertility or
fecundity ofthe dogs. As pointed out above, effects on
reproduction and on the developing embryo are moresensitive criteria. \vhich leads to the requirement forlower maximal dose rates to individuals in mammalian
populations. At lower dose rates the available data
indicate that the incrcniental incidence of radiationinduced tumours is likely to be low and, therefore, oflittle significance at the population level.
136. Radiation-induced genetic changes in either
somatic or germ cells include gross numerical aberrations (e.g. aneuploidy or polyploidy) or structuralaberrations (tnnslocations. deletions, duplications etc.)of the chromosomes as kvell as gene mutations (change
in the nucleotide sequence in the DNA constituting thegene). If these occur in germ cells, they mav betransmitted to the next generation progeny. In mostcases. aneuploidy (at least for certain chromosomes)
and polyploidy arc incompatible with the production of
viable embryos [U4, U5] and would reduce fertility or
fecundity. Such effects would be included in the effects
described above on reproduction and on the developing
embryo. Both aneuploidy and polyploidy occur spontaneously in the oocytes and early embryos of a numberof niarnmalian species, and there is evidence that theincidence increases with maternal age [Uj]. Exposureof female mice to acute doses of 0.02-0.16 Gy produces
no change in the incidence of either aneuploidy or
polyploidy [hlO]. The data for male mice indicate aslight possibility that the incidence of aneuploidy inoffspring may be increased by the irradiation of spermand spermatids, but there is no evidence that there isany effect from the irradiation of spermatocytes andspermatogonia [U5]. In the female Chinese hamster anacute exposure of 2 Gy is necessay to produce
cytogenetic evidence for a marginal increase in theincidence of aneuploidy. Male northern field voles
exhibit increased diploidy in spermatids, which isdependent on dose in the range 0.25-2 Gy [Uj]. It has
also been noted that any effect that depleted the oocyte
popi~lation(e.g. irradiation during embryonic development) could advance the maternal age effect for
aneuploidy [U4]. Clear evidence has been presented ofliyperliaploidy and structural ano~naliesin metaphase 11
oocytes from young adult mice that had received
gamrlia-ray doses of 1, 2 and 3 Gy at a dose rate of
6,000 pGy h-' between 4 and 8 weeks of age [GlO].
Although the chromoso~iieaberrations reported areprobably not con~patiblewith survival. lesser degrees ofcytogenetically undetectable damage may have beenpresent that could result in viable (but, perhaps. less fit)
offspring. There appear to have been no studies of theeffects of longer-term, lower-dose-rate exposure.
137. Keciprc?caltranslocation (the niutual exchange ofDNA between two non-homologous chromosomes) is
the structural rearrangement that has received mostattention. In the various rodent species that have been
investigated. the induction rate in stem cell sperrnatogonia (assessed in cytological preparations of descendent spcnnatocytes) is 0.0 1-0.03 Gy-' at total doses
up to 3 Gy of acute low-LET exposure [U3]. Alpha
irradiation of male mice for 5-8 months from "9Putaken up into the testes (36 pGy h l ) increased theincidence of reciprocal translocations (derived from
irradiated spennatogonia). acentric fragments (fromirradiated spermatocytes) and dominant lethality(determined from post-implantation embryo mortality);an RBE of 22-24 relative to '"Co gamma radiation was
estimated [SjO]. In non-human primates the induction
rate was 0.0 1-0.078 Gy" at doses up to 1 Gy [M 191.
The magnitude of the potential sparing effect of lowdose-rate exposure appears to be species-dependent, andthe incidence could be lower by a factor of 3- 10 [U4].
The gametes resulting i'rorn a spermatogonial stem cell
containing a reciprocal translocation are produced(assuming ranclom segregation through n~eiosis)in the
proportions 1 : 1 :2 of balanced-normal, balanced-translocated arid unbalanced, respectively [S21. U6]. The
mortality associated with the output of sperm with anunbalanced chromosomal constitution would be included in the reduction of fertilitylfecundity noted
above. I'or on'spring heterozygous for the translocation,d ~ totale production of gametes will have chromosome
constitutions in the proportions given above, so theseoffspring would be expected to be semi-sterile (and areoften found to have even lower fertility) [U6]. The
likely low incidence of such individuals means that theconsequences for the overall fertility of the population
would be less than the consequences arising from thedirect effects of radiation on gametogenesis. Experiments with female mice have shown that the greatniajority of chroniosomal aberrations induced in preovulatory oocytes were eliminated through pre-implantation and early embryonic mortality. Again, the effects
on fertilitylfecundity would be included in the responses
already discussed.
138. The final class of genetic changes includes genemutations that are inlieriled ill a simple Mendelianfashion. Detectable by tlieir phenotypic expression in
the offspring of irradiated parents or by conducting
appropriate breeding experiments. they include recessive visible, recessive lethal, dominant visible.
dominant skeletal and dominant cataract mutations. The
available data perniit estimates for specific types ofANNEX: EFFECTS OF K4DWTION ON THE ENVIRONMENT

mutation. For instance. at doses up to 6 Gy, recessive
mutations at seven specific gene loci in the mouse are
induced at a rate of about 5 10.' Gy-I locus-' at a dose
rate of 5.000 pGy h-I. and dominant mutations causing
either skeletal abnormalities or cataracts are induced at
rates of 4 10" Gy" garnetc-I and 2.6 10" Gy-' gamete-'.
respectively. at low dose rates [S2 1, S43, U71.
139. Acute. sublethal whole-body irradiation of malemice or localized testicular irradiation over a number ofgenerations has been shown to reduce the reproductive
fimess of subsequent unirradiated progeny [Gj. G6,
S321. This has been attributed to the accumulation ofrecessive mutations that, even in the heterozygous
condition. combine to produce the observed response.
The mean sunrival time under chronic irradiation(50,000 pGy h") of mice with accuniulated ancestralpaternal irradiation was also lower than in controls, andsimple breeding tests appeared to indicate that thecharacteristic was recessive in nature [S32].
u140. Classical population genetics assumes that somemutations arising from increased radiation exposure
would lead to a reduction in fitness (even for recessives
present in the heterozygous state) and therefore have an
adverse impact on the population. Selection pressure
would tend to eliminate the induced mutations from the
population over a number of generations inversely
related to the specific reduction in fitness. At somestage (with constant. radiation exposure of the
population over time) a new equilibrium between
mutation arid selection would emerge, with a slightchange in the population age-dependent mortality rate
owing to the genetic changes. Laboratory studies ofirradiated populations have not shown unambiguous
evidence for reduced fitness from an increase in theincidence of this class of radiation-induced mutations[B17. G9, U7]. While tlie available data suggest a very
limited mutational impact at the levels of radiation towhich wild populations in contaniinated environments
are likely to be exposed, it should be noted that thegenetic constitution of these laboratory populations israrely comparable to that of their wild cousins. In thesecircumstances, the finding should be extrapolated to thenatural environment \vith caution.

-

14 1. There have been a nu~iiberof investigations ofpossible genetic damage in the sonlatic cells of
mammals subjected to increased irradiation from
Chernobyl fallout (prilnnrily caesium radionuclides).
The incidence of micro~iuclei(inclicative of the presenceof acentric chroniosonle liagments) in the erythrocytesof*\vild house mice was Iound to be increased, relative
to earlier controls, duri~igand after tlie fallout from the
Chernobyl accident at a site north of Rome. Italy, where
about 1 kBq m" ot""Cs was deposited. The frequencyof micronuclei was found to be positively correlatedwith the IJ7Csbody burden (up to 45 Bq kg"). Although35

no quantitative dosimetric data were given, it was
concluded that the dose rate implied by the body burden
was insufficient to account for the increased numbers of
rnicronucleate cells [CI I]. It could only be suggested
that the (unknown) dose rate from external sourcest~iighthave provided the necessary additional exposure.
The external dose rate from "'Cs (even including 13JCs),
however, would probably have been within the normal
variation in the natural background radiation at thislocation. Indeed, dose estimates from a subsequent
study [C12] confirm that the total dose (external plus
internal) from '"Cs and "'Cs would have been only
about 5% of the natural background dose rate.
142. A second study by the same researchers was
conducted in areas of much higher Chernobyl fallout in
Sweden. The bank vole (Cle~l~eriono~~ys
glareoltcs) tvas
used as the experimental animal, and estimates werernade of the dose rates from internal and externalsources of both "'Cs and "'Cs. The beta component of
the radiation from internally deposited caesium
radionuclides \vas the major source of exposure (52%31%). with external gamma irradiation providing mostofthe balance. Tlie estimated dose rates (in addition to
0.1 7 pGy h-' assumed for tlie natural background) at thefour sampling sites were 0.01, 0.2, 1 and 1.5 pGy h-'.
Tlie body burdens of 'I4Cs and "'Cs showed substantial\ariation at each site (coefficients of variation in therange 62%-138% for n = 22-38 animals). and the dose
rates received by the individual animals would therefore
be expected to show a similar substantial variation (thelonger-term accumulated doses might show lesslariation owing to fluctuations of individual bodyburdens over time). The incidence of niicronucleate
erythrocytes, although varying greatly in any given
esposure group, correlated well with the mean dose rate
[C 121. Ludwiko\v [L 1 I], however, was unable todemonstrate such a clear-cut dose-response relationshipfor the incidence of micronuclei in larger numbers ofperipheral blood cells (rather than bone marrow cells)
in a laboratory study employing the same species.
143. The incidence of chromosonle aberrations wasdetermined in the peripheral blood of semidomesticated reindeer living in areas of Nonvay withdiffering degrees of Chernobyl fallout contamination. If
age is disregarded, the frequency of aberration was notcorrelated with the incremental dose rates estimated forthe different areas. In calves from the mostcontaminated area, \vhel*e dose rates were about 8-9
j~Gy11-I in 1986- 1987, falling to 4-5 pGy 11.' in 19891990. the incidence of two break events (dicentrics,
lings) was, however, significantly higher than in calvesfrom other arcas, and for this area tlie reindeer born in1986 showed a higher incidence than older animals. In
a positive control experiment in which 7-8-month-old
reindeer calves were fed 134Csat four different rates for
23 weeks, there was a significant dose-dependent

36

UNSCEARincrease in chromosome aberrations relative to thecontrols [R8].
144. A range of data lias been obtained concerning
the genetic darnage induced by increased radiation
exposure of the germ cells of male wild house rnicecaptured at different sites within the 30-km zone of
the Chernobyl nuclear power station. The external
gamma-radiation dose rates at the capture sites were in
the range 0.2-2,000 11Gy h-' (if the data given above
for the bank vole are applicable. the total dose rate,
inclusive of internal exposures. might be greater by afactor of 2-5). Wild niale mice were rnatcd to femalesof a laboratory strain to determine the incidence ofdominant lethality (embryonic mortality). For niales
captured in 1986 there was no consistent relationshipbehveen dose rate at capture (0.5-500 pGy h") andobserved embryo mortality. In the follotving year. in
addition to the three sites used previously, another sitewith higher dose rates was san~pled.There, at dose
rates of 1.700-2,100 11Gy h-I. two of tlie captured
males produced no offspring and were concluded to besterile. and the remainder showed a period of
temporary infertility and reduced testes mass, which.
however. recovered with time after capture. The onlj
group for which embryo mortality (post-implantation)differed significantly from the rather uniform overall
picture consisted of tlie litters sired by males within
two weeks of capture from the high-dose-rate site, i.e.
litters resulting from sperm which were at the postmeiotic stages at the time of irradiation [S22]. For all
the mice collected at the three or four sites in 1986
and 1987, respectively, there was a dose-ratedependent increase in the incidence of reciprocaltranslocations scored in spermatocytes at meiotic
rnetaphasc I [S22].
145. The results of these four studies [C I I , C 12, R8,
S22] confirm that incremental exposure fromcontaminant radionuclides will, as expected, induce
genetic changes in both somatic and germ cells in
populations of wild manimals. The rather limited natureof the dosinietric data provided makes it difficult tocompare these results with the outcome of laboratory
studies. In addition, the reports provide no indication of
the consequences of the damage for the respective
populations. At the two most highly contaminated sites
in the Chernobyl 30-km zone, the total dose rates arelikely to have been greater than those suggested inparagraphs 126 and 133 as limits for the maximally
exposed members of populations in areas subject tocontrolled contamination From waste disposal practices.
I t may be concluded that the lower dose rates werecompletely consistent with the survival of the
populations, although it would be desirable to havemore data, particularly on population attributes.
including such 13ctors as immigration from areas oflower contarninat ion.

2. Birds146. A review of the effects of ionizing radiation on
birds was compiled by Mellinger and Schultz [M2].
Wild birds appear to exhibit LD,, values that are in thesanie general range as small mammals (5-12 Gy).
Doniestic poultry are reported to exhibit an LD,,,, of
9 Gy [B2].
147. Studies of radiation effects on the young of three
species of wild birds, tree swallow (Tachycitieta
hicolor), eastern bluebird (Sialia sialis) and house wren
(7i.ogloc!r-tt.s uedon), showed progressively reduced
groivtli following acute doses to hatchlings of 0.9 to
6 Gy 1221. Tlie young birds were irradiated andreturned to their nests in the field and observed over tlie
16-day period until fledging. There was no radiationinduced mortality during the nestling period. No
observation could be made of possible life-shortening.
Doses of'4 and 6 Gy had statistically significant effects
on bocly riiass. with reductions of 10% and 137'0,
respectively, and also on primary feather length andfoot length. A dose of 2.6 Gy had less effect, and
0.9 Gy had little effect on initial o w t h anddevelop~nent[Z2]. In subsequent similar experimentswith tree swallows. the growth data were fitted to thevon Bertalanffy growth model. Tlie parameter values
liom this fit showed that doses of 2.7 and 4.7 Gy to the
newly hatched nestlings produced significant growthdepression, particularly in body mass: the irradiation
also influenced the developnient time [Z4]. In domestic
fowl irradiated at 2 days of age. the growth rate over thesubsequent 30 days was reduced at all doses but only
significantly so at doses greater than 6.7 Gy [B6].
148. I'ro~ii limited data it lias been suggested that the
juveoile bird is liiore resistant to radiation than the adult1221. The lethal dose for the eastern bluebird nestling isgiven as 30 Gy [\V4]. In yoling chickens exposed at age
3-4 days. however, the LD,,was determined to be
7- 1 I Gy (exposure time less than 1 hour) and 12-20 Gy(exposure tinie of 24 hours) [S3].
I . 'Ilie effects of acute radiation on the developing
avian embryo have been investigated for the blackheaded gull (Larirs ridih~inhis) and the domestic
chicken [PG]. The eggs were irradiated at day 10 ofdevelopnient and incubated artificially. The LD,& athatching for the two species were determined to be 1213 Gy and 9 Gy, respectively. For the developing trees\vallow (T~~cl~ycineta
hicolor) irradiated at days 7-8
and incubated naturally. total doses up to 3.4 Gy did notaffect Iiatching or fledging success, but the tinie tohatching increased and growth was depressed at doses
greater than 1.6 Gy [Z3].
150. No data appear to have been obtained at acutedoses less than 0.5 Gy, Out for most of the responses

ANNEX: EFFECTS OF RADIATION ON THE ENVIROhMENT

that have been studied, damage is detectable only athigher doses. Studies of effects of chronic exposures arelimited. The nesting success of birds was studied infield experiments with chronic irradiation from large
gamma-ray sources. Exposure rates of 8,400-42,000
pGy h-' caused embryonic mortality [R7,W 14, 221,while no apparent effects were detected at 30260 pGy h-' [ZS]. Tree swallows (Tuchycineta bicolor)
occupied nesting boxes independently of radiation exposure in the range from natural background to
6 pGy 11". The breeding perfomlance over the season
was unaffected by the radiation exposure. and the
production of fully-fledged young was comparable with
controls. These results indicate that the population isunlikely to suffer adversely at annual doses up to
50 mGy [Z6]. Chronic irradiation of developing chicken
embryos at dose rates greater than 10,000 pGy h" until
hatching destroyed the process of spermatogenesis andprevented the production of any resting oocytes,
effectively sterilizing both sexes [M121. Thus, while thechronic dose rates causing effects on embryonicdevelopment in birds (8,000-10,000 pGy h-') have been
determined, the minimum dose rates that may cause
other clearly evident effects have not been.

3. Reptiles a n d a m p h i b i a n s
1 5 1. Studies of rcptilcs and amphibians suggest thatthese groups may have a radiosensitivity similar to thatof niammals and birds when the observation period isappropriate for registering the incidence of radiationinduced mortality. Frogs, salamanders, turtles, snakes
and lizards vield LDo values of 2-22 Gy. The cause ofdeath has usually been identified as damage to thehaematopoietic system. with mean survival times after
irradiation ranging up to 190 days [ C l j , C14, D9.
T 121. For one species of lizard (Ufu sfo~lsbtiriana)hvo
separate studies gave LDS,, values of 10- 12 Gy [D9]and 17-22 Gy [T12]. Differences in radiation quality.
dose rate and maintenance conditions were offered as
explanations for the different results [T12]. In
addition. since it is not evident from the data presented
that the short observation period encompassed all theacute radiation mortality. the lethal dose may havebeen overestimated. An acute esposure of 50 Gy
caused temporary sterility in nialcs of this species oflizard, but recovery to normal proportions ofspermatogenic stages was well advanced by day 48
after exposure [D9]. Exposure of adult males andfemales sampled from a natural population to an acutedose of 4.5 Gy to the gonads (head and thorax
shielded) resulted in a substantial reduction after
release in the production of offspring in the year ofirradiation. This in turn reduced the density of adults
in the following year (i.e. there was no compensating
increase in survival), but by the second year both
natality and population density were recovering tocontrol values [TI 31.

35152. An acute dose of I0 Gy was found to be 100%lethal for four species of amphibians. although only one
species showed an L D 5 J 0less than 10 Gy. Using data
fiom the literature for two other amphibian species andestimates of the interphase chromosome volume andassuming a linear relationship behveen interphase
chromosome volume and radiosensitivity, LD,valuesin the range 8-36 Gy were calculated. Extending theassessment period to enconipass all the radiationinduced mortality (up to 200 days for one species) at
total doses less than 10 Gy yielded lo\verestiniates for
LD,, values, in the range 0.8-7 Gy. The interphasechro~nosomevolume appears to be a potentially usefulindicator of radiosensitivity [S33]. Adult toads.
juveniles and tadpoles showed different radiosensitivities, with estimated LD,,, values of 24 Gy.
111Gy and 17 Gy, respectively. After extending theobservation tinie, the adult LD,,declined slightly to
18 Gy, but the sensitivity of the juveniles and tadpoles\{as much increased. with both showing an LD,,,, of
0.1 Gy. In addition. irradiated tadpoles failed to metaand
rnorphose [L91. A toad species exhibiting LD,,,
LD,,,, values of 22 and 20 Gy, respectively. showed
greater survival after 15 Gy if they were allowed tohibernate than if they were kept active. An acute dose of
I5 Gy to a natural population as they emerged fiom
hibernation in the spring had little impact on breeding
activity. feeding or preparation for hibernation thefollowing autumn. There was, however. a marked
reduction in survival, independent of age and sex, in the
population errierging from hibernation one year afier
irradiation [T 181. A single report [B 181 provides
evidence for the induction of abnormalities in. andreduced survival of. offspring after paternal exposure oftoads to acute doses of 3-20 Gy.
153. There are relatively few data on the effects ofchronic irradiation on reptiles and none, apparently, foramphibians. The data for lizards were obtained in field
experinients with large gamma-ray sources. A
population of Uta sta~~sbliriu~laexposed to average
tissue doses of 830 pGy h" showed a sex ratio. a
maximal life-span and an age distribution that were notsignificantly different from those of control populations
over a period of five years [T8]. An earlier study of thesame system had indicated differences behveen
irradiated and control lizards in growth (length andweight) of young of the year, but this response could
not be confidently attributed to the direct effects ofradiation exposure; an indirect effect mediated byda~iiageto plants was suggested as one possible cause.
but non-radiation environniental factors could also havebeen involved [T14].
154. Observations have also been made of hvo otherlonger-lived species of lizard, Crorap~vrliswislizenii
and G7e1~ridopl7orzcsrigris. that received approximate
annual exposures of 4-5 Gy and 2-2.5 Gy, respectively.

38

WSCEXR 1996 REPORTin the irradiation facility [T15]. After 3.5 years of
exposure, demographic data and the failure of mature
female Croraphytus to assunie reproductive coloration
indicated a lack of reproduction in this species. Direct
observations after 5.5 years of exposure showed that theovaries had regressed completely. At this time. one ofthree irradiated males was also found to be sterile.
Control males and fe~ilalesof the same age werereproductively normal. Similar responses became
apparent in Cnearidophorri.~some hvo years later thanfor Croi~~pl~~.rris;
the delay simply retlects the lower
average dose rate experienced by the latter species.
These results underline the significant degree to which
demographic (and behavioural) factors determine therelative responses of populations of animals to a given
degree oTclironic radiation exposure [Fj, T15].

4. Invertebrates
155. A very large database exists for radiation effects
on invertebrates, especially on insects. O'Brien and
Wolfe [OI I prepared a monograph on tlie subject andconcluded that insects are. in general, far less sensitive
to radiation than vertebrates. l'his conclusion should betempered by the following considerations concerning
differences in physiology and in life cycles. For thevertebrates, there are more or less clearly definable
ranges of acute absorbed dose for which tlie postirradiation survival time is relatively independent of anincrease in dose and that correspond to the induction ofdamage in specific organs or cell systems (in order ofincreasing dose and earlier expression tiriie, these are
the bone marrow. intestinal and neurological syndromes) ([U3], Annex G). For the mammals. there isvirtually no acute (short-terni) radiation mortality atdoses below those that affect the haematopoietic
system, and essentially all the mortality from bonemarrow damage is expressed within 30 days; hence theLD,,,,, is justified and commonly employed as acomparative measure of radiosensitivity. As noted inparagraph I5 I , longer times (up to 190 days) arenecessary to encompass the (low-dose) acute mortality
in reptiles. A similar qualification on the use of LDiajo
values has been made with respect to aquatic organisms[W151. The presence of substantial physiologicalvariations behveen thc different groups of organisms
for all its practical convenience,means that the LD,,
provides an insecure basis for comparing radiosensitivity across a wide taxonomic range. This is not to
say that there are not very real differences in radiosensitivity but that thesc might not be as great as they
appear from the coniparisons made so far. For example.
the apparent low radiosensitivity of many adult insects
has been ascribed to the fact that very little cell divisionand differentiation is in progress. i.e. there is no direct
physiological basis for the equivalents of the bonemarrow (Ii;~ematopoietic)and intestinal syndromes. In
these circumstances it may be that tlie appropriatecomparison should be with the ~ieurologicalsyndrome
in mammals. for which a lesser differential radiosensitivity would be apparent.
156. The life expectancy of 12 species of arthropods( I I insects and I isopod) were significantly reduced atdoses greater than 80 Gy. and for 6 species a 50%
reduction in mean life-span was induced by doses
behveen 20 and 40 Gy [ M l j ] . Acute irradiation of
invertebrate populations in soil samples showed that thesurvival of the ~llajorityof the identifiable taxonomic
groups was less than 50% of the control values at acutc
doses less than 100 Gy [E6]. In both studies thequalitative observation was made that the radiosensitivity of the organisms increased with theiractivity. Adult earthworms (Eiseniafoerida) were foundto he less sensitive to acute irradiation (LD,,,
about
650 Gy) than juveniles, for which growth wascompletely inhibited at 100 Gy, and developing
embryos, for which 20 Gy delivered soon after the ova
were deposited in the cocoons (i.e. early inembryogenesis) significantly reduced hatching success.
A dose of 20 (iy to mature adults also affected thehatchability of uggs produced subsequently. dependingon the time between irradiation and egg deposition[S34]. A second species of earthworm (Lurnbriczis
terresrris) also appeared to be unusually radioresistant,
will1 an LD,,,,, of680 Gy for acute gnnima irradiation
at a dose rate of 290 Gy 11'' [R3]. The LD,,for pillbugs (terrestrial isopod crustaceans) was about 300 Gy.
but after 60 days, when essentially all of the acutemortality had been expressed. the median lethal dose
Iiad fallen to about 50 Gy. The survivors of the latter
exposure grew and moulted nom~ally,and one fenialc
laid eggs that developed into fertile adults PSI.
157. The reproductive tissues in adult insects are one
system in which significant cell division. i.e. gametogenesis, is in progress, and these tiss~~es
can be damaged
at much lower acutc doses than those leading tomortality. This circumstance fornis the basis for the
production of radiation-sterilized but othenvise
perfectly viable male insects in large quantities forrelease in pest control programmes. Three examples
from a voluminous literature will serve to illustrate thekind of data available. The exposure of mature pupae or
adult codling moths to 300-400 Gy completely sterilized
the females and reduced male fertility to less than 10% of
control values without seriously influencing behaviour
except for substantially reducing sperm competitiveness.
I7iis reduced male fertility lessened the impact of released
irradiated malcs on population growth unless a highsterile:wild malc ratio of 20:l was maintained. Doses
below 250 Gy had a smaller effect on male fertility (1 5%
ofcontrol), but the males showed ~iiuchimproved overallniating competitiveriess (sperm competitiveness,s;itisfaction of female mating drive and induction ofnorrnal oviposition), \vith the added advantage that thereANNEX: EFFECTS OF RADIA,TION ON THE ENVIICONMENT

was an increased incidence of infertility in othenvise
normal F, males. The release of irradiated males when thenatural population was emerging ffom ovenvintering andagain in mid-summer provided effective control but did
not eliminate the pest [P9]. Similar results were obtainedin the case of the spruce budworm [E7]. The red palm
weevil was found to be much more radiosensitive. as
15 Gy to one-day-old males induced 90% sterility. The
effectiveness of these males in population control wasagain limited by a decline in mating competitiveness,
otving partly to a 10%-20% reduction in adult longevity
and partly to reduced sperni production [R9]. In all threecases it is clear that even drastic radiation effects on the
reproductive capacity of a proportion of the individuals in
the population would have only a limited effect on the
total population unless they were being induced
extensively in space and time.
158. Like the reproductive tissues in adult insects,
juvenile insect forms are much more sensitive to thelethal effecis of radiation, as would be expected fromthe high cell turnover rates in these age classes. Thesefindings reduce. but do not eliminate. tlie extent of thedifferential radiosensitivity behveen vertebrates andinsects. Many factors have been shown to modify the
response of insects to radiation; it is, however, very
unlikcly that insect species more sensitive thanvertebrates to either the lethal or (more important in theenvironmental contest) the reproductive effects ofradiation will be discovered.
159. Some relatively high LD,$ in insects have beenreported after short observation periods (e.g. at 1 day orwithin 3-4 days). Latency periods of these lengths may
occur before damage is observable [VI]. Dose-rate
effects have also been reported. For example. tlie LD,,in young adult crickets (Achern clomc~ticrrs)is about
50 Gy for dose rates above 2 Gy h-I. At 0.3 Gy h-',however, a 50 Gy dose causes only 10% mortality in 20
days [V3]. Larger. longer-lived insects may be moresensitive than smaller, shorter-lived one.
160. There may be considerable differences in sensitivity in the different stages of insect gro\vtli. In general,
radiosensitivity decreases as development proceedsfrom egg to adult stage. Van Hook [Vl] reported theLD,for eggs of the grasshopper ~\felut~oplus
sat1gzl~trit1ipe.s
to be 4 = 1 Gy and the first nymphal instar
to be one third less sensitive. The LD,,,s
for thevarious stages of groivtli were 13 Gy (first and third
instar), 7 Gy (second instar) and 8 Gy (fourth instar andadult) [V I]. For the soil arthropod Collenibolu, tlie egg
is I0 times more sensitive than the adult. The LD,,
values were reported to be 150-300 Gy for the adultinsect, 130-230 Gy for the juvenile stage and 15 Gy forthe egg [S6]. An exposure of 30 Gy had little impact on
Collembolu population growth over rhree generations(1 6 days), but 70 Gy delayed the commencemerit of the39

exponential growth phase and at 16 days the population
size was approximately half that of the controls [A7]. In
invertebrates as well as mamnials, populations may be
more affected by reduced fecundity and egg mortality
than by tlie death of irradiated individuals,
5. Summary

16 1. Data on radiation sensitivity of terrestrial animals
are dominated by data on mammals. the most sensitiveareclass of organisms. Acute lethal doses (LD,,,)
6- 10 Gy for small mammals and 1.5-2.5 Gy for larger
animals and dornesticated livestock. When a total doseof similar magnitude to the LD,,, is delivered over the
lifetime, for example 7 Gy to the mouse (420 pGy h*',or 10 mGy d-I), tlie average loss of life-span has been
estimated to be about 5% and would result from theinduction of neoplastic disease [Uj]. There is substantial interspecies variability but, in general, little
indication that dose rates below about 400 pGy h" tothe most exposed individual would seriously affectmortality in the population.
162. Reproductive capacity is more sensitive to theeffects of radiation than is life expectancy (mortality).
The reproductive rates of mammals may be depressedat doses that are 10% of those leading to mortality.
Some loss of oocytes may occur at 1% of the lethaldose, but because of excess oocyte production,
fecundity should be affected to a lesser extent. Exposedfrom conception to a dose rate of 800 pGy h", mice canbe made sterile at 25 weeks. In the most sensitive~nanimalstudied, the beagle dog. 180 pGy h-I caused
progressive cell depletion and sterility within a few
months, but exposure at 36 pGy h-' over the whole life
produced no damaging response. It is concluded that aradiation dose rate of less than 40 pGy h-' to the most
exposed individual in a population (and most probably,
therefore, a lo\ver 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 effects on
fertility, fecundity or the production of viable offspring.
163. Radiation effects in birds have been shown to be
similar to those in small mammals. Reptiles and invertebrates are less radiosensitive, although physiologicaldifferences begin to make more direct con~parisonswith
other species less appropriate. The chronic exposure of
one short-lived species of lizard in enclosures has
sho~vnno evident effects over 5 years at 830 pGy h'l. In
two longer-lived species of lizard, some individuals
were made sterile after 3.5 years at 630 pGy h-I in one
species and after 5.5 years at 2 I0 pGy h-' in anotherspecies. Adult invertebrates are seemingly quite
insensitive to tlic effects of radiation exposure in termsof induced mortality. but gametogenesis, developing
eggs and juvenile stages are more sensitive.

UNSCEAR 1996 REPORT40

C. AQUATIC ORGANISMS
164. There have been a number of reviews of thestudies of the effects of ionizing radiation on aquaticorganisms [A2, B4. CI, El, 12, 13. NI. N3, P4, T6,
W9]. A number of these were prepared specifically toprovide a basis for assessing the potential effects ofdischarges of liquid radioactive effluents on aquaticorganisms in their natural environment 112, 13, N 1, N3,
W9]. In consequence of these many reviews, it does notseem necessary to repeat the exercise here; there havebeen no more recent reports of results that would alter
the general conclusions. I t will be sufficient. therefore.
to mention the relevant conclusions, accepting that the
supporting evidence has been thoroughly examined.
165. I t has been concluded that, among the many nonmammalian phyla represented in aquatic environments.
fish are the most sensitive to acute radiation exposure;the developing fish embryo is particularly so. The
LD,, values for 10 marine invertebrates \\..erefound to
be in the range 2- 1,500 Gy: extension of the assessment
period to 60 days reduced this range to 2-680 Gy, andthe median lethal doses for the apparently mostradioresistant species were still declining [E8. W 151. A
similar situation was found for SLY species of marine
fish, in which tlie range of LD,,s declined from I I 56 Gy at 30 days to 9-23 Gy at 40-50 days [WI S]. Thel,D,,s for developing fish embryos can, however, bemuch lower. Irradiation of silver salmon embryos at thesingle-cell stage yielded estimated LD5,,s of 0.30 Gy at
hatching and 0.16 Gy at a larval age of 90 days; theradiosensitivity decreaqed with embryonic development[B23]. Other fresh-water fish that have been studied
appear to be less sensitive [W9]. A single LD,, value of
0.09 Gy was determined for a maline flatfish species(the plaice) irradiated at the blastula stage and assessedat metamorphosis [W22]. When account is taken of
their poikilothermic nature and generally loivermetabolic rate, fish appear to be somewhat moreradioresistant than marnrnals, but there is substantial
overlap in sensitivities. While no data are available forthe marine mammals, there is no reason to suppose thatthey would exhibit radiosensitivities substantiallydifferent from those of'terrestrial mammals.
166. Exposure of adult female loach (family Cobitidae, related to the carps) to whole-body exposures of
2.5. 5.0 and 10 Gy produced only very slight effects inmature oocytes at the highest dose. For an exposure of
20 Gy, a clear response was obtained in both developing
and mature oocytes; a lesser response mas obtained by
cxposure of the head alone (i.e. the ovary was shielded).
and this was amibutcd to a radiation-induced reduction
in gonadotropin secretion from the pituitary gland [E9].
Doses as low as 1 Gy caused a temporary reduction intestes weight in rnaturc rnedaka (rice tish. 0r)zias
lot$~cs).and slight effects on sperrnatogonial prolifera-tion were detected histologically [Kl I]; the sterility
induced by acute doses of 5 and 10 Gy was temporary,
and recovery was well established at 60 days after
irradiation [H 12, M 141.
167. In developing riiedakaembryos. the sensitivity ofthe primordial germ cells (as indicated by the number
present at hatching) decreases with time after fertilization, but 20 Gy at all stages produces a substantial
reduction. At tlie most sensitive early stage the numberof germ cells at hatching is exponentially related todose, and 5 Gy produces a significant reduction. In
those embryos that survive a 20 Gy dose at the earlystage. the reduced number of germ cells present at
hatching proceed to differentiate fairly normally intospe~matogonia (through mitotic proliferation) andoogonia and oocytes (through mitosis and meiosis): thegreater number of germ cells that survived 20 Gy late inembryonic development were, however, inhibited fromprogressing into differentiation [I 101. In normal female~riedakafry the total number of germ cells increased
niarkcdly immediately after hatching. with oogonia
generating oocytes in various stages of meiosis. An
acute exposure of I0 Gy hvo days after hatching prevented the normal proliferation of germ cells. and at I0
or 15 days after hatching. the irradiation reduced thegerm cell population at all developniental stages. Regardlcss of the tirning of irradiation, there was a substantial reduction (by a factor of about 6) in total
numbers of germ cells [I1131. Esposure of embryos to
10 Gy on the last day before hatching had no effect on
the numbers of female germ cells at hatching but
delayed the commencement of proliferation and maturation: signs of recovery towards control values occurredby day 20 after hatching [H14]. In contrast to thesefindings, the primordial testes became more sensitive asembryonic development progressed. as indicated by theincidence of sterility and ovo-testes at 70 days after
liatching. An exposure of 50 Gy on the day before
hatching produced an incidence of'approximately 50%
equally divided between complete sterility and ovotestes [EIO]. The rainbow trout seems to have a similarradiosensitivity, with exposures of 6 and 8 Gy late inerribryonic development producing a greater than 50%
incidence of sterility [K12]. Thus, the primordial
gonads in the developing fish embryo and the newly
hatched fry have been found to be some\vhat moresensitive to acute radiation exposure than the adult fish,
a situation like that in mammals.
168. There have been few studies of the lethal effects
of chronic radii~tionexposure in aquatic organisms.
Exposure of Pl~~,sa
lre~erostropha(a fresh-water snail)at 10.000 pGy h" over the 21 week life-span underlaboratory conditions (total dose 45 Gy) had no
significant effect on mortality [C 161. Cumulative dosesof 80-88 Gy at 9,000- 10,000 uGy h-' had no effect on
the survival of juvenile marine scallops and clams

ANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT[B24]. 4 dose rate of 720.000 pGy h-' froni 60Co
gamma rays, giving a median lifetime dose of approximately 120 Gy, had little effect on the age-specificsurvival of Daphtziaplrltx populations receiving a fixed
per capita food supply, and there was little effect on life
expectancy at birth at tlie higher dose rate of 760,000
pGy h-' [M15]. However, in food-limited populations ofDaphnia (that is, populations under additional stresscompeting for food). the total death rate. including
prenatal mortality, was increased at 35,000-45,000
pGy h-' [M 161. The ~nortalityof blue crabs (Callitzectes.sapidus) was greater than that of the controls after 50days exposure to T o gamma rays at a dose rate of
290,000 pGy h-' (total dose 330 Gy), whereas a dose
rate of 32,000 pGy h-' had no effect [E I I].
169.

Exposure of medaka to tritiated water or external
gamma radiation during embryonic development

137cs(average 9.1 days from three hours after fertilization tohatching) at dose rates behveen 18,000 and 79,000
pGy h-' had little effect on hatching rate. Larval survival to one month of age was, however, consistently
and significantly decreased at dosc rates above 35,000
pGy h-' for tritium beta particles and at the highest dose
rate for gamma rays. The incidence of vertebral
anomalies was increased for all dose rates from I3'Cs(i.e. >18,000 pGy h-') but only at dose rates above
35,000 pGy 11-' froni tritium [H 161. Dose rates in therange 14,000-54,000 pGy he' from 'OCo gamma rays tonlosquito fish (Gumbztsia M n i s ) at either I5 or 25°C
for 40 days (total doses 12-50 Gy) induced no increased
mortality relative to the controls [C17]. Limited data(small samples) have also been obtained for the guppy(Poecilia relicvluto). Six pairs of fish esposed to "'Cs
gamnia rays at 13,000 11Gyh*'for 238 days (72 Gy total
dose) experienced no mortality. For pairs of fish at thelower dose rates of 4.000 and 1.700 pGy h-' (77 1 and974 days. respectively). the onset and estent of malemortality (470 days and 6 of 9; 230 days and 4 of 10.
respectively) diffcred from the controls (520 days and3 of 12). For the females, there were no deaths among
the controls, 1 from 10 (570 days) at 1,700 uGy h'' and2 from 9 (onset at 450 days) at 4,000 pGy h-I. Becauseof the small numbers involved, these results provide no
more than an indication of possible radiation-induced~iiortality[W9].
170. Small groups of the marine polychaete wonn
Ophq~otroclradiudemo, which is hermaphroditic but
not self-fertile, were esposed to chronic "'Cs gamma
radiation (1,700,3,200, 7.700 and 14,000 pGy 11-I)overseven generations and the breeding performancerecorded. No effects were seen on growth rate or time
to first egg laying, but the reproductive performance
was affected in all generations. In generation 1, thenumber of egg sacs, eggs and larvae produced were
only reduced at thc highest dose rate, but in generations
2 and 3 the reductions were clearly dose-rate-depen-

41

dent: by generation 7 there was a clear tendency towards recovery at the three lower dose rates (thepopulations at the highest dose rate went to extinction
in generation 3). The lowest dose rate to produce asignificant effect. reduction of larvae in generation 2.
was 3.200 pGy h" [K 131. A si~iiilarexperiment with themarine polychaete wonn Nea11thes arcnaceodenrata
recorded significant effects on reproduction in generation 1 at a dose rate of 17.000 pGy h-' but not at 2,100
ltGy k',and there was little difference in the responses
to equal total doses of either acute or chronic exposure[H 171. An exposure to "Co gamma rays at a dose rateof 11,000 pGy h" significantly reduced total egg
production over 12 weeks (total dose 22 Gy) and 14~rreeks(total dose 26 Gy) by Physa heterostropha in hvo
replicate experiments; dose rates of 20.000-250,000
pGy 11-' were progressively more damaging. In the firststudy, the egg production rate recovered towards control values behveen 12 and 24 weeks at 11,000 pGy h-'[C18, C 191. In Daphnia populations not competing forfood and chronically exposed to gamnia radiation.
reduced fecundity was considered to be the cause ofj~rogressivereductions in population birth rate withincreasing dose rate above 220,000 uGy h" [Ml 51. Ln
populations receiving a constant total food supply (i.e.
in competition), fecundity appeared to increase veryslightly. although overall population size declined withincreasing dose rate up to 180.000 pGy h-I. l'his was theniaxinium dose rate at which populations appeared to beable to maintain themselves indefinitely, and it was
concluded that the slight increase in fecundity was dueto the increased food available to each individual andthat this partly balanced the radiation damage [M16].
171. An earlier review [W9] concluded that minor
effects might be expected in gonads of fish irradiated atdose rates greater than 1,000 pGy h-I. More recent
studies have provided additional information. Males
from mixed-sex populations of Anieca splendens
irradiated at an average absorbed dose rate of
7.300 pGy h" ('I7Cs gamma rays) showed disruption of
spennatogenesis at an accumulated dose of 0.95 Gy andwere rendered sterile at 9.7 Gy. The secondary spennatogonia were the most radiosensitive stage, while thepriniary spemiatogonia were the most radioresistant. notbeing completely eliminated until a total accun~ulated
dose of 16 Gy. The testes of males that had received
total doses of 3.9 and 7.0 Gy but had been allowed torecover without further exposure for 125, 174 and 236
days sho\ved a multi-lobed appearance at dissection.
Histological examination showed that the individual
lobes consisted of regenerated testicular tissue (allstages of spermatogenesis present) separated by sterile
scgnients consisting solely of Sertoli cells. Quantification of the recovery \vas difficult. but in the fish thar
had received 3.9 Gy it was estirnated to be 85%-90% of
the controls after both 125 and 174 days ol'recovery.
and for tlie fish receiving 7.0 Gy it was estimated to be

42

UNSCMR 1996 REPORT

5%- 10% at 125 days and 60%-70% after 236 days ofrecovery. The development of damage in the ovaries ofAmieca splei~der~s\sfas less easy to quantifv than that in
the testes. mainly owing to variation benveen individuals, but the final result was no less clear cut. Snlall
resting oocytes started to decline in number after
accumulating 6.9 Gy and had disappeared completely
after 18 Gy. A reduction in maturing oocytes became
apparent at I2 Gy, and they declined to zero after
29 Cy. Twenty-five young fish. born on day 74 of theexperiment and having accu~nulated14 Gy as gametes
and developing embryos. were removed from theirradiated aquaria and reared to maturity. Examinationof the fish at an age of 400 days, by which time themales \\ere showing normal secondary sexual coloration, demonstrated that there had been no gonad
development in either sex [R 101.
172. The effects of chronic irradiation from tritium
beta particles (as tritiated water) and "'Cs ganima rayson the developing gonads has been investigated inenlbryos of medaka [E 12, H 151. At hatching the maleand female gonads are indistinguishable, but the numberof gcrni cells present can be determined. Beta radiationfrom tritium appeared to be more damaging than IT7Cs
ganima rays, with accumulated doses of 2.0 Gy (8,000
pGy h") and 3.5 Gy ( 1 5,000 pGy h-I). respectively,
required to reduce gelm cell survival to 50% of thecontrol value with no apparent threshold; this corresponds to an RBE of 1.8 for tritium beta radiation
relative to "7Cs gamma rays. A combination of agenetic marker and hormone treatment permitted an
examination of the sensitivity of the female germ cells
alone. The 50% survival doses \ifere 1.4 and 3. I Gy forbeta particles and garnma rays, respectively (RBE =2.2). and b> implication, the fernale germ cells weremore radiosensitive tlian those of the male [E 121. The
effect of these tTeatrnetits on the fertility and fecundityof the resulting adult fish has also been investigated. In
females irradiated as embryos and mated to unirradiatedmales, the number of ovipositions and the number of
fertilized eggs per tish decreased with increasing doserate, with 50% reductions at approximately 4 Gy
(17.000 pGy h") and 15 Gy (63,000 pGy 11") for beta
and garnma irradiation, respectively (an implied RBE of
approximately 3.8). For irradiated males mated tounirradiated females there was little consistentdifference between the radiation qualities in reducing
reproductive capacity. and for both radiation types a
50% reduction was apparent at approximately 5 Gy
(2 1,000 pGy 11-I) [I 1151. None of these results isinconsistent with the expectation of minor effects ingonads of fish irradiated at dose rates greater than
1,000 pGy h-' [W9].
173. The li~nitedinfom~ationon the mutagenic effectsof radiation in aquatic organisnls was briefly reviewed[W9]. and it was concluded that the sensitivity of theseorganisms WilS similar to that of ihe much more
intensively st d i e d mice and b i t flies. Recent
investigations of mutation induction at a single specificlocus in the pregonial and gonial germ cells of the zebra
fish appear to indicate that this species, at least, might
be considerably more radiosensitive than the mouse. It
was deduced that most of the mutations were due tolong deletions and suggested that they occur relatively
frequently in pregonial cells because the rapidity of cell
division reduces tile possibility of repair [C20. W231. A
second specific locus test system has been developed
based on the fact that strains of the medaka
lio~iiozygousrecessive at either 1 or 3 autosomal locihave a phenotypic expression (colour or lack thereof)[hat can be recognized in the first half of embryonicdevelopment through the transparent egg membrane.
The incidence of dominant letllals (per gray per gamete)from exposure of medaka sperm appears to be similar tothat f ~ o n iexposure of the mouse. but the spermatids
appear to bc less sensitive. Many of the observed
radiation-induced colour mutants tvere not viable (i.e.
they were also carrying dominant lethal mutations). As
in the mouse. however, some of the colour mutants wereviable, showing that thc n~edakasperm. spemmatids andsperrnatogonia have a radiation sensitivity for mutationinduction similar (i.e. within the uncertainties) to that in
the corresponding spermatogenic stages in the mouse
IS441. A stutly of the production of chromosome(mainly chromatid) aberrations in cultured blood cells
from the central rnudminnow (Urnbra lit~ii)by exposure
to either tritiated Ivater in tlie culture medium or chronic"'Cs gamnla irradiation showed these cells to besome\vhat less radiosensitive than human lymphocytes(by a factor of npproxirnately 5), and a value of 1.9 wasestimated for tlie RBE [S35].
Among aquatic organisms. fish are
174. S~rr~rnr(~ty:the most sensitive to the effects of radiation, anddeveloping fish e~iibryosare particularly so. The LD,,
for acute irradiation of marine tish is in the range 1025 Gy for assessment periods of up to 60 days following
exposure. The upper elid of the range of LDj, formarine invertebrates has been found to be several
hundred gray. Embryos. on the other hand. are affected
at much lower doses, e.g. LD,,of 0.16 Gy for salmon
cm bryos [Hz3 I.
175. For chronic exposures, dose rates of 10,00030,000 pGy h" have had no effect on mortality forsnails. marine scallops, clams and blue crabs. Dose rates
sornewliat above this range had some effects in foodlimited popu1;itions of Dupliriiu p u l a . Short-term (40days) exposure of mosquito tish at dose rates in therange 14,000-54,000 pGy ti-' sho\ved no radiationinduced mortality, but for the closely related guppy,
there was some indication that long-term esposure(>470 days) at dose rates above 1.700 pGy h-' reduced
the normal lifc-span, particularly for males.

UNSCEAR 1996 REPORT

44

radiosensitivity. The observed effects of chronic gamma
irradiation on six species of \+roody plants in theirnatural environnient were compared with predictions
based on chromosonle number and cell nucleus volume[W24]. In terms of a 50% reduction in shoot growth
relative to controls, the prediction consistently underestimated the radiosensitivity of the plants, often by alarge margin. On the basis of the dose rate required to
produce greater than 90% mortality, the prediction
overestimated the radiosensitivity of three species,
although not by a significant margin, and underestimated the sensitivity of the remainder. in t\vo casesby a factor of at least 5. Two factors were put fonvard
as having significantly contributed to the observed
general increase in ~-adiosensitivity: (a) the stresses
associated \I ith the natural environment and (b) the factthat the prediction was developed from a (broad-based)
general correlation based on data for both tvoody andherbaceous plants, even though it was recognized that,r generally moreother things being equal. the f o m ~ e aresensitive than the latter [W24].
18 1. The correlation of radiosensitivity with molecularor cellular characteristics has been extended to mutations, and it has been suggested on the basis of
empirical evidence that the fonvard mutation rate p?r
locus per unit dose of acute radiation might be linearly

dependent (within a factor of 3) on theDNA content of
the haploid genome [AS]. The conceptual basis of thisrelationship has, however, been severely criticized[S42] on the grounds that the studies underlying theapparent correlation employed differing genetic endpoints that were not directly equivalent to specific locus
mutations and detection systems of varying sensitivity.
In addition, it was pointed out that intra-locus mutation
rates are not found to be correlated with the apparent
DNA content in specific salivary gland chromosome
bands (identified with loci or coniplenientation groups)
of Drosopltilo nrelartogasrer. leading to the conclusionthat not all the DNA in a band represents a target forradiation-induced mutations of the type detected
experimentally. It was concluded that these factors
weakened the validity of the hypothesis developed byAbrahamson et al. [AS].
182. In summary. it may be stated that although there
is suggestive evidence for correlations between specificcharacteristics of the nucleus and nuclear components
and a variety of indicators of radiation-induced damage,none of these correlations has been developed to thepoint where it could reliably be used to predict. from therelatively small experimental database. potential
radiation effects in the wide variety of organisms likely
to be present in a contaminated area.

Ill. EFFECTS OF RADIATION ON POPULATIONS OF PLANTS AND ANIMALS
A. STUDY LIMITATIONS
183. Literature on radiation effects in an ecologicalcontest began to appear in the early 1960s. Althoughsome of these research programmes were terminated by
the early to mid- 1970s because of changes in funding
priorities. investigations continued into the 1980s in a
few countries. such as Canada, France and the former
Soviet Union [D I , I:I , G3. K2, M3, S4].
184. The general approaches to studying radiation
effects on populations and comnlunities (assemblages of
populations) have included large field irradiation
facilities. observations at nuclear test sites and in areasof high natural background radiation or contamination,
the release of irradiated individuals to the environment,
the esperimental application of radioactive particles,
ant1 the irradiation or contaniination of laboratory
systems or microcosms. Each of the above approaches
has its advantages. but most suffer from a lack of
ecological realism or from dose levels insufficient toproduce unequivocal results.
185. The expense and difficulty of doing a nieaningful study of radiation effects on plant and animal popu-

lations and communities in their natural environnientmakes it in~possibleto provide information on a large
number of species and community types. For example,
studies have been completed on coniferous anddeciduous forests, certain shrublands and grasslands, a
tropical rail1 forest. herbaceous old fields and mosslichen communities [W3]. However. little work appears
to have been done on aquatic plant communities or on
Arctic or alpine tundra, taiga. savannah or desert
communities. Also. very little work has been done on
the interaction of radiation with other stresses or agents.
This may be a serious omission in light of the multiple
forms of pollution that threaten many contemporary
populations and ecosystems.
186. Other areas that have received very little
attention include the possible long-temi effects ofchronic. low-level radiation and the patterns of repair
and recovery I'ollowing radiation damage. It may takeconsiderable time for damage from low-level chronic
irradiation to be expressed at the ecosystem level, andmost studies are short tenil. Several studies have looked
at repair arid recovery for a few ycars, but manysystems require a decade or even much longer tocomplete their recovery from severe daniage.

ANNEX: EFFECTS O F RADJA,TION ON THE ENVIRONMENT

187. Despite these and other shortcomings in thegeneral database. sufficient information is available topredict, within broad limits. the effects of ionizing
radiation on at least a reasonable sample of the populations and comrnunitics in terrestrial and aquatic
environments. However. this prediction must rely on
adequate dosimetry, which is often difficult to achieve.
For example, the calculation of doses to thc criticaltissues of higher plants following atmospheric deposition of radionuclides is a complex, difficult task andsub.ject to considerable variability and uncertainty.
188. Ecosystems can be large and complex with many
species of organisms, or they can be relatively simple
with only a few species of organisnis constituting asimple food-chain. The number of organisms in a
population may be altered by changes in environmental
conditions, or species niay be completely replaced.
189. General characteristics of diminished ecosystem
functioning under erlvironmental stress have been
identified [R4]that may also apply to radiation stress:(a) loose cycling of nutrients. (b) changes in primary
production, (c) reduction of species diversity, (d)retrogression, as opposed to natural succession. (e)reduction in the average size of organisms and (f) other
distress, such as increases in disease incidence. The
stages in ecosystem response to stress are initial effects
on sensitive parts, coping mechanisms to co~mteracting
the stress and ecosystem rebalance or breakdown. It is
not easy to predict specific effects in diverse ecosystems, which are usually under multiple stress. andfurther observations in contaminated environments areneeded to increase knowledge and experience.

190. In the specific case of continuing exposure to
low-level irradiation, Woodwell and Houghton [W25]concluded that the response of a temperate oak-pine
forest (and other plant communities) is (a) systematicand predictable. (b) common in nature, (c) cuniulativeand progressive over an indefinite period measured in
decades. (d) measurable in stages and (e) best characterized by the concept of "impoverishment". By"impoverishment" is meant the loss of large. long-lived,
slowly reproducing species with replacement bysmaller, opportunistic, short-lived species with highreproductive rates. These are readily recognizable as theweeds and pests of conimon currency and are typical of
all disturbed habitats. In ecological terms, impoverishment is the reverse of' succession, and it frequently
appears to be a niorc rapid process [W25].
19 1. One of the problc~nsin evaluating the effects ofradiation on populations and ecosystems is to detemiine
which parameters to measure and how radiationinfluences them. 'Typically measured attributes at the
population level include numbers of individuals,
mortality rate, reproduction rate and mean growth rate.

45

In general, measurable changes in populations andcommunities require rather severe effects at the cellularand individual organism levels. For example, alterationin the structure of a biotic community requires a change
in the component populations. which in turn rcquires
widespread mortality andlor reduced reproduction ofindividuals [W3]. In the same way, genetic or somatic
mutations that can be produced by lower levels of
exposure may have little or no impact on population orcommunity performance because of natural selection[B3, M4, N2, P1, T6] and the convergence of genetic
information among adjacent populations [RI]. For
example. in organisms whose reproductive rates are
kery high and on which selective pressures are strong,
the value of one or even many thousands of individuals
to the population may be rather insignificant [12, T6]. Insuch populations, normally a small fraction of theindividuals will mature and perpetuate the gene pool,even in the absence of radiation or other stresses. In
most species. genetic information that is altered byradiation is extremely unlikely to be perpetuated in the
population. even though it may not be immediately
lethal at the individual level.
192. Radiation effects at the populatio~i and conimunity levels are manifest as some combination of
direct changes due to radiation damage and indirect
responses to tlie direct changes. This seriously
complicates the interprclation of radiation effects onorganisms exposed in tlie natural environment. The
wide range of radiosensitivities of the organisms thatmake up most natural communities creates a situationin which, if doses are such that the sensitive species but
not the more resistant ones are affected. the latter may
gain a significant competitive advantage and perhaps
increase in abundance or vigour [W12]. This could
erroneously be interpreted as a hormetic response. Sucha response might not 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.

193- Individual populations of organisms, and thecommunity as a \\,hole. may be altered by radiation
exposure only as a consequence of dependence on amuch more ndiosensitive species for food or shelter. For
example. many plant species in a pine forest would belargely unaffiectcd by an acute dose of 10 Gy. but the pinecomponent would probably experience severe mortality[ W I I]. This would cause both positive and negative
perturbations in tlie populations of other species notdirectly damaged by thc radiatiori exposure. Because ofsuch indirect responses, in any situation where all the
species in a community have been exposed concurrently,
great care will be necessary to identify the species mostdirectly affected by the irradiation.

194. Changes in the composition and structure ofvegetation lead to changes in the animal population [C2.

46

UNSCEAR 1996 REPORT

H2,W131. Such changes could also involve interrelated
populations of animals (predator-prey or host-parasite
relationships), but these are more difiicult to demonstrate. Numerous and extensive changes in the chemicaland biological properties of the soil can occur as anindirect effect of radiation damage to vegetation. Recent
work in France has denionstrated these kinds of changes
clearly [C4, S2. T4,1'20] (see also paragraph 2 15).
195. Relevant information concerning the effects ofincreased chronic radiation exposure of populations ofwild organisms is beginning to become available from
two additional sources. the two large-scale accidents
that occurred in the fomler Soviet Union: the one in1957 at a nuclear waste storage site near Kyshtym in thesoutheastern Urals and the other in 1986 at tlie
Chernobyl nuclear reactor in Ukraine. Apart from theimmediate. effectively acute radiation response
observed in plants and animals near the release points
for each of these accidents. there have been continuing
studies of the effects of the longer-term chronic
radiation exposures. The results of these studies are
summarized in Section I1I.D.
B. EFFECTS ON PLANT POPULATIONSAND COMMUNITIES
196. Studies of radiation effects in natural plant
conimunities have beer) more or less limited toterrestrial systems. The characteristics that have beenmeasured in relation to the stress of ionizing radiation(grotvth-fonn). species
include physiognomy
composition. species diversity and vegetation cover andproduction [W3]. At tlie poptilation level. parameterssuch as density or frequency of occurrence. gro~vthandvigour, mortality, reproduction, phenology andmorphology are often measured [G2, 021. Effects on
individuals or components of populations can give someinsight into potential changes at the population andecosystem level.
197. Some specific measures of change in plantcommunities that have been used to investigate thepotential effects of radiation include the coefficient ofcommunity, siniilarity. diversity and biomass. The
coefficient of comn~unityis a parameter calculated froma list of species present in an irradiated area and acontrol area, or in one area before and after theirradiation. This pararneter is designed to detect changes
in species composition resulting fro111 the eliminationand possibly replacement of populations. Similarity islike the coefficient of community, except that therelative abundance of individuals within each species is
considered as well. Diversity is a measure of the number of species within a community and the evenness ofapportionment of individuals among tlie species. Boththe loss of individuals and tlie loss of species wouldchange the diversity. Biomass is a measure of the massof biological tissue per unit area. It may be estimatedfor individual populations or for entire comnlunities.
and owing to sublethal alterations in growth. it canchange without a loss of individuals or species. These
parameters are defined more precisely in various
publications [G2, W3. W6], and more complex indicesand means for analysing change are available [G7].
198. An example of radiation effects in plantcomn~unitieshas been seen in a stud) in a graniteoutcrop ecosystem common to the southeastern UnitedStates [MG]. Tile composition of this ecosystem isrelatively simple, and there are \tell-defined boundaries.
One such system was treated with simulated fallout
particles ("Y). and effects of the beta irradiation wereobserved over a 60-day period [M6]. Accumulated
doses were measured with thermoluminiscent dosimeters at the ground surface and at 40 cm height. theaverage height of tenninal buds of the summeldominant plant. 1'iguier.a porteri. The mean doses in
hvo experimental systems were 40 Gy and 70 Gy. with
20% higher doses at the ground surface and 20% lower
doses at the 40 cm height.
199. In these irradiated systems. there were no
obvious changes in appearance of the experimental
plots: rather close observation and measurement \+ere
required to detect effects of the radiation exposures.
Only one change in the 40 plant species constituting thisecosystem was noted that could be related to theradiation exposure. A sedge, B~1bost)ili.scapilluries,
decreased by 17% in the 70 Gy community but
increased by 12% in tlie control and 40 Gy conimunities[MG]. Other sh~dieshad shown this plant to be relatively
radioresistant but because its growring apices are close
to the ground, it may have retained high densities offallout particles in close proximity to sensitivemeristems. Thus, the geometry of the radiation field is
an important consideration when llterpreting theobservations.
200. In the main species, I'igiriera porleri, in tlie
70 Gy community, 46% of all terminal buds died,resulting in a 37% height reduction: however. there wascompensatory lateral branch development. In this plot,
community biomass was reduced by 16% owing todecreased production of flower and ste~iibiomass. but
leaf bio~nasswas similar to control levels [MG]. An
additional obsc~vationwas that beta radiation was tulice
as effective as gamma radiation over comparable
periods and equivalent total doses [MG].
20 1. The effects of chronic irradiation on h e microalgal population in soil have been examined [F9]. 'The
micro-algae appear to be relatively radioresistant, eventhough some part of the observed change might havebeen atlributable to the gross effects (mortality. much
reduced litter fall etc.) of radiation on the higher plants

ANNEX: EFFECTS O F RADUTIOK ON THE ENVIRONhlENTin the zone examined, i.e. the change was partly anindirect response. The total number of taxa that could be
isolated from the soil saniples did not appear to change
markedly with dose rate up to the maximum delivered(approxinlately 1.7 Gy h-'). Above a threshold ofapprosinlately 0.3 Gy h". however, eukaryotes were
replaced by prokaryotes. Estimates of tlie coefficient ofcommunity and percentage similarity (relative tounirradiated controls) were consistent in showing athreshold for decline at approximately 0.4 Gy h", 50%
reductions at about 0.9 Gy h" and extrapolation to zeroat 2.5-3.0 Gy h-' [F9].
202. Chronic irradiation also had a substantial effecton the populations of microfungi at the base of thehumus layer in an oak-pine forest. Where higher plants
persisted, i.e. in the intact oak-pine forest, and where
the dose rate at the sampling depth increased from lessthan 400 uGy h" to about 8,000 pGy 11-'. there appeared
to be little direct effect of radiation on the microfungi.
The fungal species isolated were typical of podzolic
soils in mixed conifer-hardwood forests and \\.ere
dominated by eight ~norphologically complex tasa
(71% of isolates but only 5% of the species). There wasalso a consistently high concentration of about lo5
viable spores per gram of dry soil. At the edge of thesedge zone. where the dose rate was about 30.000
pGy h-I, the concentration of viable spores fell to
1.6 1O4 g-' dry soil, but the species diversity increased inthis transitional band between the endemic forest
populations and opportunistic pioneer species, and there
were few dominant fonns at low densities. Closer to theradiation source. where there were no higher plants. thedistribution of the microfilngi was related to the radiation gradient. The viable spore density. the coefficientof community and the incidence of niorphologicallycomplex taxa all declined. At the highest dose rate,
about 0.75 Gy hl, the viable spore density was reduced
to 500 g-' dry soil and the population was dominated bysterile, slow-gro\ving forms of morphologically simple
yeasts [Gal.
203. Based on the results of several investigators.
Whicker and Schultz [ W j ] summarized the effects ofradiation on major plant communities of North
America. The results given in Table 9 are the doselevels that give minor, intermediate and severe effects
following short-term (8-30 day) exposures. Minor
effects are considered to include changes in productivity
and reproduction, from which rapicl recovery would be
expected after the radintion stress has been removed.
Interniediatc effects include chi111gt.sin species composition and diversity through selective mortality ofmore radiosensitive species. Recovery could take placethrough processes of plant succession requiring one toseveral generations. Severe effects are those thatdrastically change the species composition by causingmortality of all or nearly all the higher plants. Recovery

47

inay be slow. requiring decades or even centuries if
there has also been extensive leaching of soil nutrientsand erosion. To estimate the chronic exposures thatwould be expected to result in comparable effects, thedose ranges in the Table should be divided by 25- 100 togive daily dose ranges.
204. The plant communities included in Table 9 arelisted in approximate order of sensitivity, fromconiferous forests to moss-lichen coniniunities. The
greater radiosensitivity of the coniferous forest iscorrelated with the large chroniosome volumes of pinetrees. The other communities listed in Table 9 are much
more resistant because they are dominated by moreresistant species having generally smaller chromosomes. Lichen-dominated co~nmunitiesare exceptionally resistant [GI]. This resistance may be explained bydiffuse centromeres and asexual reproduction as well as
by small chromosonies [W3].
205. The general capacity of plant communities to\jfithstand environmental stress (low rainfall. hightemperatures) also enables them to withstand low tomoderate radiation stress. There may be alterations incommunity stnlcture (species abundance changes) andmorphological changes in individual plants (lateralbranch development), depending on the total radiationstress, but the compensations are generally such as tomaintain a normal energy balance. While it is possible
for radiation stress to induce systeniic defence
mechanisms in individual plants that could incrcase
their potential to respond to secondary stresses such as
pnrasitic fungi, it should also be pointed out thatapparent similarities in plant regrowth and recovery.
after either radiation exposure or some other form ofstress, may be superficial and conceal the existence ofstress-specific responses.

C. EFFECTS ON ANIMAL POPULATIONSAND COMMUNITIES
206. The impact of radiation exposure on an animal
population is likely to be a complex combination ofeffects within individual animals (direct effects) and thepositive or negative effects of the responses of the otherbiological components of the environment with whichtlie population normally interacts (indirect effects).
Where there is a close coupling between two species,
e.g. plant-herbivore, predator-prey or host-parasite, it isvery likely that their responses to chronic low-level
radiation (whetlicr similar or different at the individuallevel) will be modified at the population level byinterspecies interaction. The direct effects of irradiation
measured in animal populations have included changes
in the birth rate, the death rate and. in combination. theintrinsic rate of natural increase [F?]. Because areduction in reproductive capacity has been considered

UNSCEAR 1996 REPORT

18

to be a more limiting end-point than mortality, in termsof the maintenance and survival of the population.
changes in fertility anrl fecundity have been measured
and the response at the population level estimated using
an appropriate model of population dynamics. The
published s~udieshave rarely. however, taken accountof the influence of either intra- or interspecies
interactions or factors other than radiation.

1. Terrestrial e n v i r o n m e n t
207. Because animals are mobile, it is difficult to
conduct field studies of radiation effects. The use of
enclosures to retain animals in exposed areas may
unduly restrict their movement, feeding and behaviour.
causing effects in addition to those under study.
Investigations in areas of high background or in more
widely contaminated areas may be less affected byspatial limitations.
208. Notable effects in animal communities can result
from changes in vegetative cover, particularly for
insects. As vegetation dies in highly irradiated areas,
herbivorous insects and their predators disappear andare replaced by species subsisting on dead and decaying
material. Aphid increases were noted in irradiated oakpine forest on L.ong Island. New York. the insects
perhaps having been attracted by the altered quality or
appearance of tlie oal< leaves [W 131. Bark beetles
invaded an irradiated tropical forest in Puerto Ricowhen natural defencu processes in the trees aere
weakened [ S 5 ] . The prcsence of moribund pine trees in
the high-dose-rate zonu of a chronically irradiated oakpine forest provided an ideal substrate for colonization
by bark beetles and other xylophagous insects.
Moribund trees were licavily attacked by hvo species ofbark beetle irrespective of the ambient radiation doserate, but the ensuing clcgree of developmental success
was inversely correlated with dose rate. At aboke
200.000 pGy h" the adults attacked the trees and began
excavating galleries but were killed before they could
complete the task of preparing cavities for eggs orlaying eggs. Between 40,000 and 200,000 uGy h-', theegg cavities were completed but there was no egg hatch,owing either to infertility or damage to the developing
embryos. In the range 30,000-40.000 pGy h-I, where
eggs hatched, there was total larval mortality; at 20,00030,000 pGy h-I, there was low larval mortality but all
the pupae died. Between 10.000 and 20.000 pGy h-'there was some pupal nlo~talityand some adult emergence, anrl bclow 10,000 pGy h-' adult emergence was ashigh as. or higher th:~n. normal. Within this overall
picture there \\!ere also interesting observations on theinfluence of inlcrspecies con~petitionwith other xylophagous insects: those species with more protracted life
cycles tended, at any given dose rate. to be at a competitive disadvantage. The importance of shielding, in thiscase between distal and proximal segments of thetrunks. was also noted. Lastly, it was concluded that if
pines were debilitated by a short-term but spatiallyvariable radiation exposure, then the less-radiosensitive
bark beetles could. owing to tlie availability of many
suitable feeding and breeding sites. reach epizootic
proportions arid fi~~tller
damage and kill trees that would
otherwise have survived [B25]. These findings show
how iniportant it is to appreciate the overall context ofradiosensitivities and interactions between species whenassessing potential environmental daniage from chronic.
low-level irradiation.
209. Density-dependent responses play an importantrole in modifying the impact of radiation. Such compensation and adaptation in populations is not apparent
in laboratory experiments on individual organisms.
Studies of lizards irradiated in a nine-hectare desert
enclosure in Nevada in the United States showed
impaired fertility and altered population levels [TS, T9].
Species response depended on life-spans. time of sexval
maturity and population age distributions. One shorterlived species of lizard, Uta s~ansburiana,was able tomaintain population nunibers in spite of appreciable
proportions of sterile older females, apparently because
the young ani~ilalssurvived better [T9].
2 10. Radiation effects in exposed animal populations
have not been readily apparent. For example. studies of~namnialson the dry bed ofthe retention pond at WhiteOak Lake. near Oak Ridge. Tennessee, United States
could not ascribe any effects to radiation exposures[D3]. Lifetinle doses to tlie wild rodents were probably
2-3 Gy [T9]. 'Iiie study of lizards in the irradiatedenclosure in Nevada revealed no differences in bodyweight and no fonii of tissue pathology. although somechanges occurred in ovaries and oviducts ofcontinuously irradiated lizards at annual gamma dosesof2-5 Gy ['f9]. In all species of lizard in which female
sterility was observed, the amount of body fat wasincreased.

2 1 1. In a region of high natural background radiationin the former Soviet Union, abnormalities, decreased
body fat and reduced fertility were observed in
mammals living in close contact with soil (i\.licrotw
oeconon~rrs,Tulpu ezrropaeu, rlrvicola tcrrestris, L~itrc~
llttra and S o r a arunelrs) [MI]. The dose rates wereabout 80 pGy 11-I,or 700 mGy aA'.Since results at suchlow dose rates have not been obtained in laboratory orother field studies, tlie validity ol'the dose calculations
has been questioned 1'1'01.
212. In France, definite effects on reproduction infemale mice maintained in captivity at a site where theexternal background was about 80 pGy h" weresuggested by Leonard et al. [ L I, L2, L3]. In the same
shldy. rabbit lymphocytes sho\ved an increased numberof unstable chromosome aberrations. I t is possible,

ANNEX: EFFECTS OF RADIATION ON TIiE ENVIKON.MENT

however, that internal doses. which were not calculated,
contributed substantially to the total dose.
213. Radiation effects in populations of soil invertebrates were reported by Krivolutsky [U].
Variousradionuclides, including "Sr. "'Cs, 10"u, 9'Zr, 2 3 9 Pand~
"6Ra. were added to the soil in small plots. At various
intervals thereafter. the numbers per square metre ofseveral types of soil invertebrates were determined insmall ecosystem plots. Dose rates that apparently
produced reductions in animal numbers \vere generally
q ~ ~ ihight e (420-42,000 pGy h-I): however, sorne effects
were reportedly observed at dose rates of around
100 pGy h-I. The most sensitive organism observed was
the common earthworm.
214. An apparent response by ants to chronic
irradiation has been observed in an oak-pine forest at adose rate of 80,000 pGy h". A thriving nest was
identified prior to the commencement of radiation
exposure. Over three years of irradiation, the number ofants in the colony declined (in part by emigration to asecondary colony further from the source in the firstyear), fewer individuals (and eventually, none) wereseen on the burned pine stump forming tile centre of thenest mound, and less plant debris was collected tomaintain the nest mound. At the end of the period thecolony appeared to increase in number, and a 1.25 m
subsoil surface pathway covered with litter had been
formed leading at an angle away from the radiation
source: the runway was lost at 29 m from the source(dose rate of around 28,000 pGy h-I). and no secondarycolony was found. The ants used this pathway
exclusively for travel to and from the nest. Because thevegetation canopy and its dependent populations ofinsects (ant food) were reduced as early as the first year.
at least some of the responses (emigration and Coraging
further from the source) could be attributed to a decline
in the food supply, but the decline in the habit ofcollecting plant debris to maintain the nest could mosteasily. albeit speculatively. be attributed to radiation
avoidance [B26]. Over an 18-year period of chronic
irradiation of a Mediterranean oak forest, the number ofant colonies was reduced in areas where dose rates weregreater than 5.000 pGy h". Although the n~lmberof
species was little changed, the species conlposition wasaltered. Three species (of which two were not present at
the beginning of the irradiation period) were found near
the source at dose rates greater than 100,000 pGy h-I.
The changes in the ant fauna were mainly attributed to
the loss of vegetation canopy, but direct effects ofradiation could not be discounted [PI 01.
2 15. Two to three years after chronic irradiation of aMediterranean oak forest there were changes in the
populations of insects that could be attributed to bothh e direct and indirect effects of the exposure. Small
insects of the order Psocopreru (booklice) were49

substantially increased in numbers in the dose rate range
14,000-38,000 pGy h-I, and even at approximately
100,000 pGy 11'' the increase, although less, was still
greater than in the control area. It was suggested that
this increase was due to an increase in food supply(unicellular algae) in response to higher light levels
following radiation-induced leaf loss in the canopy. In
contrast. the populations of springtails (order Collembola) declined with increasing radiation exposure andaccumulated dose [B27, PI I]. In addition. later studies
showed decreased overall activity in the soil systemfollowing a reduction in the microbial population [Ti9].
Near the source, where all the trees and shrubs had diedand been replaced by small, more radioresistant annual
plants. the litter input to the soil was negligible. Unlike
in a temperate oak-pine forest [W24] the rate of loss ofexisting litter declined with increasing dose rate, but inboth environments the total organic matter content of
the soil decreased with increasing dose rate [P12. TI 9.
1'201. Although the normalized oxygen consumption
rate of the highly irradiated soil was also lower than in
the control, the specific respiration (CO, production
normalized to unit soil biomass) was slightly higher
than in the control: the NO,- content of the irradiatedsoil was generally higher. o~vingto a reduced microbial
requirement [P12. TI91. While the cumulative consequences of the chronic irradiation, both direct andindirect. are clearly complex. it is nevertheless true that
all the observed responses stemmed from the initialdamage to the most radiosensitive components of thesystem. the trees and shrubs; at lower dose rates, where
the higher plants were much less affected. there were noconsequential indirect responses [PI'].
2. Aquatic environment

216. A number of aquatic field studies wereconducted at sites of enhanced environmental radiationfrom anthropogenic sources [Wj]. Examples of suchsites include the Irish Sea in the vicinity of the Sellatield facilities: the Animas River near Durango,
Colorado, United States, where uranium milling waste
once entered the river; and a radioactive waste retention
pond at the Oak Ridge National Laboratory in the
United States. An extensive review of research on theecological effects of nuclear testing was made by
Templeton et al. [T6] for test sites in the Pacific.
Several investigations were completed for marine
d atolls [Bj, H1. W1, W2]. The
organisms a r o ~ ~ nthe
effects of the testing programme could not, in general.
be ascribed solely to radiation because of concomitanteffects of environmental disturbance. The recovery
processes follo\ving the testing programmc were relatively rapid, and deleterious effects on marine andterrestrial populations were not persistent. presumably
because of the rapid declines in the intensity of radiationand other impacts and tile recolonization of damased
areas by healthy individuals from distant locales.

1996 REPORT

2 17. Ponds, ditches and streams on the Hanford
reservation in tlie United States in the past received avariety of radioactive wastes, resulting in radiation dose
rates at the sediment-water boundary of up to 44.000
pGy h-' (measured with LiF thermoluminiscent dosimeters). Although diversity was occasionally reduced:
there were no consistent differences between thecontaminated ponds and streams on the Hanford siteand off-site reference locations. Across the sites
examined, it was not possible to demonstrate any
correlation between the variation in radiation dose rates
arid the biological paranieters investigated, i.e. rates of
periphyton and invertebrate colonization (colonizationpressure) and a range of diversity indices: individuals perunit area, species richness, community diversity andspecies evenness [E 131.

2 18. At the Savannah River site in the United States anumber of catchment basins have received low-level
waste from fuel reprocessing activities, leading to relatively high cumulative inputs of 'H,8g*Sr and 134''37Cs.
Nanrral populations of slider turtles (Pselide~~ys
scripta)inhabit the ponds and, because they are known to be longlived, could have accumulated relatively hidl total doses.
The technique of flow cytometry has been used toinvestigate the potential genetic effects of accumulated
radiation esposure by measuring the coefficient ofvariation of the distribution of DNA content (at the GI
phase in the cell cycle) of nuclei isolated from red blood
cells. The mean coefficient of variation estimated frommeasurements of 16 exposed animals was significantly
greater (and hence indicative of a gain and loss ofchromosomal DNA) than that estimated frommeasurements of 6 control animals. For 4 other exposed
animals there \iras clear evidence of aneuploidy~nosaicismin the fonn of G , DNA peaks with eitlier a
distinct shoulder or an adjacent peak; the finding that 4 of
20 exposed turtles exhibited aneuploidy mosaicism.
compared with 0 of 6 controls, although suggestive of aneffect, did not reach statistical significance (p > 0.05)
owing to the small sample size. Insufficient data were
provided to permit dose rates to the animals to be
estimated (in a separate study, however, the dose rate tonrrtles in this environment from internal sources wasestiniated to be not greater than 240 pGy h-' [Nl]):however. the exposed males (n = 10) revealed a significant (p < 0.10) positive correlation behveen the coefficient of variation in G,DNA content and plastron length(size). This might be indicative of increasing coefficientof variation with age (and therefore possibly withaccumulated dose). A similar analysis for exposed
females (n = 6) was non-significant, as tvas that forcontrol males; there were too fetv control females tocomplete the analysis. Again, the presence of other,potentially mutagenic contarninants (chromium andmercury) clouds the picture, and these data represent nomore than qualitative circumstantial evidence for a radiation response in a contaminated environment [B28. B29J.

21 9. The sensitivity of developing fish embryos was
cxlensively st~rdied following the experiments of
Polikarpov 11'41, which had indicated that developing
fish eggs were sensitive to minute quantities ofradionuclides in water. In their review of the subject,
Blaylock and Trabalka [B4] concluded that none of theexperiments s,upport Polikarpov's contention. and
Woodhead [W9] attributed the conflicting results to thedosimetric problenis encountered in this type ofexperiment.

3. Summary
220. Radiation effects on populations of organisms
have been examined in large field irradiation studies. inexperimental enclosures and in observations in areas
with high naniral background, contamination fromwaste disposal or accidental release of radionuclides.
There are inherent limitations in obtaining informationon the large number of species and community types
making up the biosphere, on the interactions of themany different environmental factors of both naturaland antliropogenic origin and on the long-term nature of
successional and generational effects. In addition, there
are difficulties in providing adequate dosimetric
information for complex distributions of sources andmovements of organisms within the environments.
221. 'rile exposure to radiation of a naturalcommunity, which comprises organisms with a wide
range of radiosensitivities, may result in direct damage
only to the more sensitive species. Other species may be
indirectly affected. for example by loss of habitat orgain of competitive advantage. For any stress to an
ecosystem. such as radiation exposure. there may be acomplex and long-term sequence of disruption,aclj~rstn~ent
and rebalancing.
222. Coniferous trees of the genus Pi11ti.shave beenfound to be the most sensitive of the plant species
studied following either acute or chronic irradiation. andplant communities including these species are the mostradiosensitive of the plant comn~unitiesfor which data
are available. In general terms, a forest in which pines
are tlie dominant (or codominant) species would
probably suffer niinor effects at total short-term dosesof 1-5 Gy or at long-tenn chronic dose rates of 4004,000 crGy 11-'. In this context, minor effects are small
clianges in productivity and reproduction. from which
rapid recovery would be expected following removal oftlie radiation source. Severe effects in the coniferous
forest could occur at acute doses of more than 20 Gy or
at long-terrn chronic dose rates in excess of
40.000 pGy h-'. Severe effects would include mortalityof almost all higher plants. and the ecosystem would
recover, if at all, only over time periods of decades or
centuries. Other types of plant community canwithstand doses or dose rates at least one order ofANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT

magnitude greater before demonstrating corresponding
effects (Table 9).
223. The radiosensitivity of individual organisms isbut one factor in determining population effects fromradiation exposure. and observations in the laboratory
may not apply exactly to the environment, where there
are additional stresses from conipetition, predation andthe like. Some compensation for radiation-induced
reductions in either survival or reproductive rates may
be possible. but there are numerous indirect effects that
could be of overriding importance.
224. Changes in vegetative cover can affect animalcommunities. When plant species die in highly
irradiated areas. the food supply of herbivorous animals
and insects and their predators is reduced. The animals
may disappear and be replaced by species subsisting ondead and decaying material. Aphids were attracted to an
irradiated oak-pine forest, and bark beetles invaded
trees in a tropical forest when the natural defence
processes were weakened. The insects may further
damage and kill trees that might have othenvise
survived.
225. Because of the compensation and adjustment thatare possible in animal species. it is considered unlikelythat radiation exposures causing only minor effects inthe niost esposed individual would have significant
effects on the population. Reproductive changes are amore sensitive indicator of radiation effects thanmortality. and rnamnlals are the most sensitive animalorganisms. On this basis. chronic dose rates of less than
100 pGy h" to the most highly exposed individuals
would be unlikely to have significant effects on mostterrestrial animal communities (see paragraphs 121 and133). It has also been concluded that maximum dose
rates of 400 uGy h-' to a small proportion of the individuals in aquatic populations of organisms would nothave any detrimental effect at tlie population level(paragraph 176). These conclusions refer to the effectsof low-LET radiation. Where a significant pan of theincremental radiation exposure colnes from high-LET
radiation (alpha particles), it is necessary to apply anappropriate radiation weighting factor to this componentof the absorbed dose rate and to use the total weighted
absorbed dose rate for the assessment of potential
radiation effects.
D. EFFECTS O F ACCIDENTS
226. T\vo major accidents in the former Soviet Union
have provided opportunities to observe radiation-relatedchanges in plant and animal communities. Any accident
is likely to be unique in tenns of the quantity andcomposition of the radioactive material released, thetime course of the release, the dispersal and deposition
patterns governed by local and regional nieteorological51

or hydrographic conditions and the biogeochemical
character of the areas subject to contamination. Where
long-lived radionuclides are released, biogeocheniical
processes will determine the long-term behaviour andredistribution of the radionuclides in the environment.
Given the multiplicity of factors, it is to be expected thatany accident will yield new radioecological inforrnation. It is also true. however. that the primary concern
following an accidental release of radionuclides will beto ensure that the radiation risks to hunian populations
are controlled and minimized. An inevitable corollary
is that the only environmental information likely to becollected is information immediately necessary to meetthis concern. which will therefore be more or lessdeficient for the purpose of developing a complete
radioecological description of the situation. The larger
the incident and the greater its potential human impact,
the more limited will be the resources available tocollect radioecological information in the early phasesof assessment and damage limitation.
227. It is particularly the case that the data required todevelop estimates of tlie radiation exposure of wildorganisms. that is. the space- and time-dependent
variation of the radionuclide concentrations (especiallyfor the short-lived isotopes), both within the organisms
and in their external environment immediately following an accidenl. will not be known. These variations
will result in stlbstantial intra- and interspecics inhomogeneities in exposure and will pose considerable
difficulties for establishing a clear and reliable relationship between cause (the accuniulated radiation dose)and any observed effect. In practice. it is likely that
estimates of the dose rates in the early period following
the release would be made retrospectively by extra~olationand calculation from the observed distributionof contamination densities of the longer-lived radionuclides, a knowledge of the relative quantities of theradionuclides released and niodels of radionuclide
behaviour in the environment. Such dose-rate estimates
are inevitably imprecise and could be subject tosignificant systematic error.
228. Aside Srom the radioactive half-lives. otherradionuclide-dependent factors significantly affect thepotential radiation exposures received by wildorganisms. These include the chemical identity of theradionuclide. which influences its environmental
beliaviour and its radiation characteristics (alpha. beta
or garnrna emissions). which profoundly affect the
spatial dose field from any given source distribution.
Additional complicatilig factors are tlie highly variable
habits and target geometries of the \vild organisms.
These range, for example, from soil bacteria to singlecelled algae and protozoa and include a wide variety ofterrestrial and aquatic invertebrates, manimals (shrews
to deer) and large deciduous or evergreen trees. If aradioactive aerosol is released, plants provide a very

1996 REPORT

high surface area to mass ratio (compared with animals)
for deposition/adsorption. Because the leaves, flowers
and terminal buds of plants are responsible for both
energy absorption and growth and reproduction. acoincidence arises between radionuclide accumulation(and hence radiation dose) and potential radiosensitivity. Other examples of coincidence are thesurface litter layer and its populations of invertebrate
decomposers. and the surface sediments and benthic
organisms in aquatic systems.
229. Depending on the quantities of specific radionuclides released in an accident, the radiation exposures
might range from low (a few multiples of the natural
background) to high (absorbed doses greater than about
1 Gy). More importantly. for the higher total doses.
different phases of biological response ma) be
distinguished. Initially, and particularly if short-lived
radionuclides make up a significant proportion of therelease. there might be an acute phase in which total
doses sufficient to produce immediate or relatively early
detectable biological responses are accumulated. In theintermediate phase. dose rates become lonrer owing todecay of the short-lived radionuclides and possibly, but
not necessarily, owing to the redistribution of thelonger-lived radionuclides by natural processes. In thisphase the slower accumulatio~lof radiation dose may
still result in total integrated doses sufficient to prevent
recovery of organisms damaged in the initial phase or tolead to the appearance of medium-term damage. In the
final, long-term phase, post-irradiation recovery (andadaptation) becomes apparent. provided that the initialand medium-tern1 damage have not been large enoughto radically alter the population or community structure.
It is important to be aware, however, that suchdescriptions can be no more than qualitative.

1. The accident in t h e southeastern Urals
230. The accident at the Mayak nuclear materials
production complex east of the town of Kyshtym in thesoutheastern Urals occilrred on 29 September 1957. A
fault in the cooling system of a concrete tank containing
mixed. highly active nitrate-acetate wastes led to a large
chemical explosion. Appt-oximately 74 PBq of fission
products nere released as an aerosol that moved
northeast. Approximately 95% of the activity was
associated with radionuclides having half-lives of one
year or less ('"'Ce, "Zr-"'Nb and Io6 Ru), while theremainder consisted almost entirely of T r . More than
15,000 km' of territory were contaminated with 90Srat
a density of greater than 3.7 kBq m-' (hvice that fromglobal fallout), and this included 1.000 km2 at over
70 kBq m-' and 120 km' at over 3.7 MBq m-' [N6].
23 1. The greater part of the total dose to wildorganisms was delivered within the first year of theaccident: during which time the contamination density(total Bq 111") decreased through decay byapproximately 66% (see Table 10) [T21]. At the time ofdepositiori the decay energy from beta radiation wasapproximately three times greater than that fiom gamma
radiation. which meant that the dose-rate distribution in
space and time in the contaminated area (forest.
tneado~v,swi~rqp,lakes, rivers and agricultural land)closely followed the detailed deposition pattern and thesubsequent redistribution of the radionuclides byenvironmental processes. Estimates of the dose rates tovarious components of a pine forest (normalized to a
"Sr contamination density of 1 MBq m-') are given in
Table 1 1 [T17]. Because an area of approxin~ately
120 km' was contaminated with "Sr at a density greaterthan 3.7 MBq m". it is very probable that a wide variety
of wild organisms would have received total doses atwhich acute effects might be expected.
232. The main part of the radiation exposure (and,usually. the highest dose rates) was delivered by theshort-lived ( t , < I year) betdgamma emitters g"r-gSNb.
'0bR~-'06Rh
and '""Ce-'"Pr and occurred in the autumn
and winter immediately following the accident, whenthe metabolic activity of the \vild plants and animals\$as generally much reduced. This apparently increased
radioresistance, in that the exposure had relatively little
immediately visible impact. As a corollary. however,repair processes, which are dependent on metabolic
activity, were drastically inhibired, and the difference in
effectiveness between acute and chronic exposure waslargely eliminated. Thus when metabolic activity
resumed in the spring of 1955, the effects of the chronic
irradiation (effectively equivalent to an acute exposure)became apparent and were more closely related to thetotal accumulated dose than to the dose rate [T17].
Estimates of the dose rates (nonnalized) and total doses
accumulated during the acute period (autumn 1957 andwinter 1957-1958) to a variety of organisms in thecontaminated area are presented in Table 12. By the latespring of 1958, the dose rates to the majority oforganisms had been reduced by radioactive decay andradionuclide migration, although the latter factor meantthat there were also some exceptions. e.g. populationsof inverlcbrarcs in the leaf liner and at the soil surface
and small rodents. From that time on. the radiation
exposure was genuinely chronic, and repair processes
were largely able to accon~modateand mitigate theradiation damage [A14, S491.
233. Vie major damage to the environment following
the southeastern Urals accident was seen in the local
forests. This was due to the coincidence of a highcapacity for intercepting the active aerosol. a relatively
slow clearance of the deposit and a relatively highradiosensitivity, especially in the case of coniferous
trees [A9. A10, S20. T22, W3]. Pine trees that had
accumulated total absorbed doses estimated to begreater than 30-40 Gy during the autumn and winter ofANNEX: EFFECTS O F RADIATION ON THE ENVIRONMENT

1957- 1958 sho\vcd radiation darnage, a desiccation of
the needles in the cro\vn. the following spring [K23].
The damage appeared initially in the lower and middle
parts of the canopy, because the active deposit had beencleared more rapidly li+onlthe upper canopy by windand rain, but by tlie autumn of 1959 the pine trees had
died completely (tlie absorbed dose to the bud apicalmeristem was estimated to have been greater than 1520 Gy). At lower, sublethal doses (greater than 5 Gy).
yellowing, desiccation and partial shedding of needles,
defects in the development of new needles. inhibition ofshoot development and trunk growth and reduced seed
and pollen viability were observed in the two seasonsfollowing the release. Birch trees showed lower radiosensitivity, with lethality apparent at estimated absorbed
doses greater than 200 Gy and sublethal responses,
comparable to those described above for pine trees.
being observed at lower total doses (greater than 50 Gy)
received in four years following the accident. One
characteristic sublethal effect in the trees was a clear
shift in the timing of development: delayed sprouting of
new leaves in the spring and earlier leaf fall in theautumn. In severely damaged trees (100-200 Gy) the
delay in bud burst amounted to an increase in the
integrated time-temperature product of 30 "C-days. In
1960, this corresponded to a delay of 7-9 days and in
1961. 4-5 days. Five years after the accident thedevelopmental delay began to decrease. and afier sevenyears the onset of bud-burst had returned to the normal
time. The data on the responses of pine and birch trees
to irradiation in the contaminated area of thesoutheaster11 Urals arc summarized in Table 13.
234. Following the acute phase in the tirst year after
the accident, the dose rates dropped to long-term,
relatively low levels, and the forest began to recoverthrough both vegetative processes and seed germination. The intensive production of side shoots evenrestored the crowns of severely darnaged pine and birch
trees, which had lost up to 95% of their needle or leaf
cover and suffered a complete growth check. After 8- 10
years. irradiated and urlirradiated trees were indistinguishable in superficial appearance and trunk growth
had been restored. In areas of wSr contamination
density above 1,000 MBq nl", where pine seeds hadreceived radiation doses greater than 20 Gy, thegermination potential was lost, but at an intermediate
dose of 6 Gy (300 MBq ~n**)sorile pine seeds reniained
viable and developed. 'The growth rate of pinc seedlings
was. however, dependcnt on the ambient radiation field.
and an absorbed dose of20 Gy or more during the firstseason severely restricted development. In areas ofcontamination density below 100 MBq m", fullrecovery through seed propagation was possible [T23].
235. Radiation damage was noted in the first year
after the accident in all 20 herbaceous plantcommunities that were recognized in the contaminated53

southeastern Urals region. The damage wasconsiderable where *Sr contamination densities wereabove 130 MBq m" but slight where they were 1826 MBq m-'. The most sensitive herbaceous species
were those with domiant buds at or near the soil surface(hem icryptophytes and han~eophytes).These species
disappeared from plant communities wherecontamination densities were greater than 1826 MBq m" and were replaced by species with dormant
buds either below ground or high above the surface andby species with short life cycles [B3O, S36].
236. The long-term effects of increased chronic
irradiation on the soil alga Chlorella vzrlguris were
investigated in the contaminated zone. Samples of algae
were collected in years 5. 6, and I I after the accident
from areas contaminated with T r at between 0.04 and1.300 MBq m-*(equivalent to absorbed dose rates in therange 45,400 pGy h") and tested for changes inradiosensitivity in response to an additional acute doseof 300 Gy. At all wSr contamination densities anincrease in radioresistance tvas observed. by a factor ofup to 1.5-2 at intermediate densities. At the highest
environmental dose rates it was concluded that theinduced genetic load of mutations had reduced
population viability. Over the 1 I -year study period thechanges in radiosensitivity apparently stabilized in thealgal populations sampled IS37, S381.
237. Becausc they were subject to some of the highest
long-term dose rates, as the deposited radionuclidcs
accumulated more or less rapidly in this zone, theinvertebrate populations inhabiting the litter andunderlying surface soils in the birch forests of thecontaminated area of the southeastern Urals have beenstudied in some detail [K15]. Eleven years after theaccident. in an area where WSrcontamination was 165340 MBq m", the total mesofauna densities were lessthan half those in control plots. The most severely
affected group was the saprophages (phytodetritivores:
earthworms and millipedes). It was concluded that this
response arose from the enhanced radiation exposure
aitributable to their relatively sedentary lifestyles rather
tlian from any intrinsically greater radiosensitivity: themore mobile predatory species showed a lesser response(Table 14). Although enhanced radiation exposure wasconsidered to be tlie probable cause of the observedchanges, other ecological factors could not be excluded.
A second survey was made 30 years after tlie accident
to obtain comparative data. Overall. the total density oforganisms and their biomass remained depressed, atabout 30% of the conlrol values. The earthworms
showed solne recovery between 1969 and 1988
(Table IS), but it was notable that juvenile individuals
were underrepresented in the irradiated population. The
numbers in the other major groups also remained
depressed relative to the controls: the phytophages, at
16% of control values, had declined since 1969. while

54

UhlSCEAR 1996 REPORT

the predatory beetles, at 6 1% of control values, showed
little change overall. although there was a decline in oneof the tsvo taxa studied and a recovery in the other.
238. At the same density of radionuclide contamination (deposition on tlie ground). different species of
insects and other invertebrates receive different
radiation exposures depending on the specific variationsin their behaviour and habitat at particular stages of
their life cycle, and for a given radiation dose there will
be a range of radiation responses as a consequence ofinterspecies and age-dependent differences in radiosensitivity. The invertebrate species most likely to beaffected by a radionuclide deposit are those whose early(pre-adult) stages of life are spent in the forest litter andsurface soil. although length of life cycle is also asignificant determinant. It has been concluded that asignificant reduction in invertebrate numbers and loss of
species from the typical leaf litter communities on theforest floor can be expected at a wSr contaminatiorl
density of 3.7 MBq m-' [G 121.
239. Populations of small rodents (dark field mouse:
Microtlrs uprestis; red bank vole: Cletl~rionor~nrs
rurilis;and wood mouse: Apodetnlrs ~ l v a t i c u salso) attracted
attention in the contaminated zone. Populations wereisolated in large open-air enclosures and studied formore than 40 generations. In an enclosure with an initialwSr contamination density of 44 MBq m-', the estimatedabsorbed dose rate to the rodent skeleto~idecreased
from 340 uGy h-' in 1962 to 20 pGy h-' in 1981.
Control enclosures \\.ere established at the periphery of
the contaminated zone. In the early part of the study.
when the dose rates \\.ere highest, a number of changes
were observed in rodent populations in the contaminated enclosures: the death rate increased andindividual life-spans decreased owing to accelerated
ageing of the older animals; the reproductive performance declined owing to increased embryo loss and ashift in the timing of, and a decrease in, the reproductive
span; the incidence of ecto- and endo-parasitism
increased: the susceptibility to predation increased:
there were changes in behaviour, e.g. a decrease in thenumber of individual habitation sites used by the dark
field mice; individual animals appeared to have greater
tolerance of stress. e.g. wood mice proved to be moreresistant to a phlrsical load such as swimming:
individual animals showed a lower rate of osygeli
consu~nptiori(considered to be an adaptive response):
and, very clearly, there was an overall increase in thevariability of most population and individual morphophysiological attributes [I13, 114. 1151. In bank voles
and wood mice living at sites with mSr contamination~ , incidence of aberrations
densities of 19-63 MBq ~ i i -thein bone marrow cells increased over the 25-30
generations after the accident, i.e. \\.it11 increasing
cumulative dose. Individuals from contaminated sites
showed greater radioresistance to single injections of

75- 185 kBq "Sr per gram body weight than did the
Despite all these changes, apparently
controls [D17].
attributable to the increased radiation exposure, therodent populations hi the contaminated ericlosures havesurvived for many generations, and it has beenconcluded that there has been some homeostatic
adjustment or adaptation to the increased irradiation.
240. At the time of the southeastetn Urals accident
some fann animals in the contaminated area were still
grazing in the fields. although relocation to barns andstables had been in progress. At three sites close to therelease point, where the total radionuclide contamination density 20 days after the accident was behveen 930
and 1.100 MBq m", the external dose rate to farmarii~tialswas high (Table 16), as was the intake ofradionuclides from contaminated grass and subsequent
incorporation into tissue (Table 17). Estimates of theabsorbed doses over 12 days to different segments ofthe gastro-intestinal tract (up to 50 Gy) and the skeleton(up to 2 Gy) of cows and sheep are given in Table 18.
At these doses the symptoms of acute radiation sickness
arid the gastro-intestinal syndrome (mucosal bleeding.
diarrhoea and Ieukopaenia) appeared. and the animals
began to die 9-12 days after the accident. Where thetotal radionuclide contamination density was
170 MBq m-', resulting in an external dose rate fromgamma radiation of up lo 920 pGy k'(a total dose of
0.13 Gy in 12 days) and absorbed doses from internal
contamination of 4.2 Gy to tlie rectum and 0.1 5 Gy totlie skeleton, no animals died within six months of theaccident. Over a period of 120 days the total radionuclide concentration in some of the tissues of theanimals had decreased by up to 75%. but those in theliver and skeleton had increased (Table 17). Those
animals from this area that were relocated outside die
contaminated zone did not differ from the controls in
ternis of subsequent mortality or reproductive perforrnance, and there was no firm evidence of an increase interatogenic effects [A 1 I, B301.
241. Rather less information has been provided
conce~iiingrhe effects o r the contamination on aquatic
systems. A study of fish populations (pike. perch. roachand golden and silver carp) was made in two lakes 1415 years after the accident. Although no dose rateestimates are given. the concentration data forand'"Cs in water and fish tissues, together with data fromprevious studies [Nl]. suggest that at that time the total
absorbed dose rate might have been a few thousand~nicrograyper hour, mainly from I3'Cs incorporated into
the lake sediments. for which no data are given. NO
effects. compared with controls, were noted for
reproductive performance or morphological characteristics [M 171. The general conclusion has been drawnthat there are no observable genetic effects in fish atdose rates below 400-1,200 pGy h-I, although underadverse environmental conditions, the threshold might

ANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT

be lower by a factor of 10, particularly for developing
fish eggs [S37].

2. T h e Chernobyl a c c i d e n t
242. The accident at the Chernobyl nuclear power
plant occurred on 26 April 1986. A brief account of theevents leading up to the accident, the time-course of therelease of the radionuclides and the initial atmosphericdispersion was given in tlie UNSCEAR 1988 Report([U3], Annes D); further details on the cause of theaccident are given in [I1 I]. A wider range ofradionuclides than in the southeastern Urals accident
was released in this accident because the reactor corecontained an operational inventory of fission andactivation products at the time. The total release,
exclusive of noble gases. was estimated to be 2 I EBq[I I I]. The variable time-dependency of the release rates
for the different radionuclides and the changing
nieteorological conditions over the 10-day release
period resulted in very inhomogeneous deposition
patterns. Not including the 30-km exclusiori zone, anarea of approximately 2.4 104 km' was contaniinatedwith I3'Cs at a deposilion density greater than 200
kBq nis'. with 5.710 km' at greater than 600 kBq rn"
and 1,360 km' at greater than 1.5 Mbq m" [I 121.
Within the exclusion zone the contamination density
niay have been more than hvo orders of magnitude
greater in limited areas 1K141.

*

243. From the point of view of potential effects on theenvironment, the main differences between the
Chernobyl and southeastern Urals accidents were thetime of occurrence and the quantity of activity released.
The Cheniobyl accident occurred in late April, just as
wild plant and animal populations were entering tlie
accelerated growth and reproductive phases of their life
cycles. i.e. when they were at their most radiosensitive.
Other differences, such as the extended (I 0-day) periodof the release and the radionuclide composition weregenerally of less significance. As indicated in paragraph
230, three main phases of the radiation impact on theenvironment were discerned [K3]. In the first. 10-20
days following the accident. essentially acute exposures.
in large part from vapour clouds. were delivered toorganisms close to the power plant from the large
quantities of short-lived radionuclides ('"Xe, "'I and%lo) released. The second phase estended through thesummer and early autumn of 1986, \+-hen despite adecline in dose rates at the soil surface to 25%-20%(and sometimes to as low as 10%) ofthe initial values,
damaging total doses were accumulated. In the third andon-going phase of chronic exposure, dose rates are lessthan 10% of the initial values and are derived mainly
from "'Cs and "'Cs contamination. Approsinlately
80% of the accumulated exposure was delivered within
three months of the accident, and over 95% of this wasdue to beta radiation [S39].

55

244. Within hvo weeks of the accident, lethal effects
were visible in pine trees close to the damaged reactor.
In this zone of 500-600 ha the trees were estimated toliave received doses in excess of 80- 100 Gy. i.e. doses
greater than the acute LD,, mostly from beta radiation.
Although the trees were nioribund. there was someevidence initially of root survival. The deciduous trees
in this zone suffered partial damage. A second zone. ofzpprosimately 3,000 ha, received estimated doses above
8-10 Gy, and dieback of new vegetative shoots of pinetrees was apparent, needles and buds were damaged anddeciduous trees showed morphological changes. In a
third zone of 12,000 ha there kvere moderate effects:
coniferous trees received doses estimated to be 3.5-4 Gy
and showed various morphological changes. including
growth suppression and needle loss, reduced
reproductive capacity and genetic damage during 1986
and 1987. There was some evidence of minor
abnormalities in growth. morphology and reproduction
throughout a large part of the 30-km exclusion zone
[K24, K25, S4 I]. The data on radiation doses in the fourzones are summarized in Table 19. It should also be
noted, however, that the distribution of absorbed dosein the tissues of trees could be markedly non-uniform
owing to the presence of hot particles in the fallout fromthe reactor. These particles, containing mainly
y'Zr-93Nb,'06Ru,134C~,'37C~
and '"Ce, were of irregularshape (2-10 to 30-40 pm) and were found sticking to
the wasy or resinous covering of pine needles. It has
been estimated that the additional absorbed dose fromthem may have been an order of magnitude greater thanthe external garnma-ray dose [K25].

245. The radiosensitivity of spruce trees was observed
to be higher than that of pine trees. At absorbed doses
as low as 0.7- 1 Cy. spruce trees showed disturbances inneedle morphology, bud developnlent and shoot growthiu 1986. In 1987, the trees developed large apical shootswith needles 35-40 mm long and eshibiting a variety ofstraight. t\visted and curved forms [ U j ] .

246. The efkcts noted in the pine trees were mainly
deterniined by the initial acute (over a period of days)
esposures. During the summer of 1986. as dose rates
declined, there was continuing inhibition of growth owing.
mainly. to ~neristemdamage and the reduced synthesis ofzrowth hormones; new growth wvs also evident, dependent
on the accumulated dose. By the spring of 1987 stems andleaves were actively growing. although some morphological changes \Yere noted in trees that had received doses
greater than 2-2.5 Gy. With an overall decline of dose rates
to less than 10% of initial values and a relative stabilizationof the exposure from internal sources. growth of trees
continued and by 1988- 1989 was apparent even in thesecond zone (Table 19)uw].

217. The reproductive organs, female (seed) and male(pollen) cones, of the pine trees showed the greatest

56

UNSCEAR 1996 REPORT

radiosensitivity. In 1987, at doses of 0.7- I. l Gy, theincidence of chromoso~ne aberrations in microsporocytes (the premeiotic stage of pollen production)
was more than three times the natural level, and theviability of the resultant pollen (tested by in vifroge~niination)decreased by 30%. The female gametophyte, a small, rnulticellular (approsimately 2,000 cells)organ that arises from a single haploid cell (themegaspore) following meiosis and produces 2-6 ova,
was also found to be very radiosensitive. In 1988. as canbe seen Srorn Table 30, there was some evidence forrecovery [K25].
248. In ttie summer following the accident, disturb
ances tvere noted in ttie process of ga~netogenesisin
crop plants. and grain yields were reduced by 50%[S40]. Dose estimates to the affected plants are notavailable. Within the 30-km zone around tlie power
station, where the initial dose rates to herbaceous plants
had ranged from Z to 8,000 pGy h'l, there \\'as nocorrelation in 1988 between the contamination densityand effects in seeds of different species, as measured byseed niass and aberrations in root cells from germinatedseed. In contrast, seeds of Platttago latzceolu~ushowed
increased sensitivity to additional radiation exposure[Tj].
249. In 1986- 1987 a marked reduction was observedin tlie nurnbcr of species in the litter niicroarthropod
communig of the forests of the 30-km zone; the impact
was less pronounced Sor the soil microarthropods andthe larger invertebrates. At an estimated total dose of
30 Gy, no changes were noted in adult animals, but the
numbers of juvenile stages were seriously depleted. In
the succeeding 2 - 2 3 years the populations recovered[K16]. Immigration of individuals from outside thezone contributed significantly to the recovery of theinsects, and larval abundance reached near-normal
levels [MI]. Within tlie 10-km zone changes in thenumbers of bvood lice (Crustacea, Isopo~Iu)persisted
until 1988- 1989 [KI 71.
250. Within the 30-km zone it was estimated that theradiation doses to small rodents over the acute phase(up to mid-May) may have reached 880 Gy (20 Gy
from gamma rays and 860 Gy from beta radiation),
which would have been lethal [T7]. An increase inmorphological variability was noted over I0 generationsin populations of bank voles in the contaminated regionof Mogilev, Belarus. In addition. individual animals
showed lower oxygen consumption, increased tolerance
to stress and an increase in radioresistance; it was
concluded that all these changes were syniptomatic ofan adaptation lo the increased radiation esposure [17.
KIS, K 191. The responses here parallel those observedin rodents inhabiting the contaminated area of thesoutheastern Urals (see paragraph 240). Biochemical
studies of rodents captured in the summer-autumn of1987 in an area where they were receiving a dose rate of
1.500-2,000 pGy ti" from external gamma radiation
showed disturbances of membrane lipid oxidation whencompared with animals exposed at 2- 10 pGy h-' [K26].
The range of radionuclides present in the deposit on
pasture ~neantthat the consequent exposure of farmanimals was far from uniform; for example, cows
grazing open fields for 240 days following the accident
were estimated to have received doses to the thyroid.
the gastro-intestinal tract mucosa and the whole body inthe ratio 230:2. I: I , and it was suggested that the thyroid
exposure might well have contributed to the observed
niorbidity and mortality [A 121. There was no evidenceof teratogenic effects in domestic animals outside the
30-km exclusion zone.
25 1 . In populaiions of brown frogs (Rnna a t v d i . ~Nills) in coniaminated areas close to the Chernobyl
power plant. a decrease in male fertility (spermatogenesis) was identified as the only effect that could beunambiguously attributed to the increased radiation
esposure (dose estimates are unavailable). In the springof 1987 more than one third of the egg clustcrs
deposited were wholly or partially infertile. In eggs thatwere fertile. so-called partial division was observed asa consequence of the anomalous behaviour of the malepronucleus and/or the anomalous replication of thechromosomes. In controls. the proportion of clusters\vilh infertile eggs was less than 1.5%. In 1988 theproportion of partially or completely infertile egg
clusters remained high (27%), but this declined to astable incidence of 3% from 1989 onwards. No effects
were detected in the processes of either ovogenesis orembryonic development [C21]. An increased incidence.
compared with controls. of cells with cl~rornoso~rie
aberrations was Sound in tissues sampled from frogs in
the 30-km zone in 1987 [K27]. In frogs inhabiting areas
in Belarus with contamination densities of 1802,200 kBq nl-' of '"Cs and 3.7-96 kBq m-' ofgoSr,theclironiosome aberration rate in red bone marrowf cells
was found to be greater by a factor of 2- 10 in the period
1986- 1989. The estimated absorbed dose rate of 0.27.1 pGy 11-I Srom wSr-wY was considered to be thepriniary cause [EIJ]. Chromosome aberrations werealso observed in Chiro)~omidlarvae collected from thc
Cliernobyl power station cooling pond and from small
ponds near the village of Yanov, within 10 km of thepower station [P 191.
252. The cooling water reservoir of the Chernobyl
nuclear power plant received a substantial input ofradionuclides as a consequence of the accident.
Estimated inventories for the end of May 1986 aregiven in Table 21 [K27]. Maximum dose rates toaquatic animals from external sources (water, particulate material trapped on aquatic plants and sediments)
were estimated, using established methodologies, to be
4,200-8.400 pGy 11.' in 1986 (1 0' tin~csgreater than the

ANNEX: EFFECTS OF RADIATIOY ON THE ENVIRONMENT

natural background dose rate) [I2. 19, K28]: theestimated dose rates fiom radionuclides accumulated intissues were lower, in the range 80- 120 uGy 11-I [K20].
In 1987 it was estimated that the external dose rate had
fallen to 1.300 pGy h-I [PIS], and in 1989 radionuclides
within the fish were a more significant source of
exposure (30-1,300 uGy kl) than gamma radiation fromexternal sources (0.4-83 pGy h-I) [LIO]. For bottomliving fish of the 1985- 1986 year class. the accun~ulated
dose from internal and external sources was estimatedto have reached 10 Gy by 1991, with over 50% having
been received in the three-year period 1986- 1989 [K24,K29. KjO]. Radiation-induced damage was observed intlie gonads of fish surviving the accident and in
subsequent generations (see Table 22) [B33. W 2 ] .
Over the period 1989- 1992, 5 of the 70 silver carp
(HypophthalinichrI~ys11101itrix)examined were sterile.
and 35% of females and 48% of males showed gonad
abnormalities, including degeneration of the gametogenic cells. The high dose rates experienced by benthic
animals from radionuclides acc~lmulatedin the reservoir
sediments produced reproduction dishlrbances in bream(Abranlis brama) and silver bream (Bliccn bjoerilka)
and in colonies of molluscs [K24, S41].

3. Summary
253. The effects on ecosystems of radiation esposurescaused by the accidents in the southeasteni Urals and at
Chernobyl in tlie fortner Soviet Union liave been
analysed. Each accident was unique. clearly so withrespect to the radionuclides emitted, the time course andseason of the release, but also with respect to tlie local
and regional environmental co~iditions influencing
dispersion and deposition. The highest doses resulted
fioni the acute phase following the accident, until many
short-lived radionuclides had decayed. The measurements were most limited in this important phase, andthe dosimetry was most complex.

57

254. There are considerable problems in making
accurate estimates. particularly retrospectively, of thetotal absorbed doses received by the wide variet). oforganisms inhabiting the areas contaminated by the two
accidents. There were substantial variations in the dose
rates over time. both between the two accidents andbehveen the accidents and controlled experimental
studies. Despite these admitted and considerable uncertainties, it must be concluded that the observed environmental consequences of the accidents are generally
consistent with the results of experimental Lvork either
under controlled laboratory conditions or employing large,
sealed gamma-ray sources in the natural environment.
255. General features of species radiosensitivities werenoted in these accidents. Coniferous trees were mostsensitive. deciduous trees less so. Herbaceous species~ i t hdormant buds at or near the contaminated soil
siu-facewere most affected and were replaced by species
with buds either below or high above the soil surface andby species with short life cycles. Populations of soil
invertebrates received high doses in highly contaminatedareas, and their numbers were depressed even 30 years
after the accident in the southeastern Urals. The observed
effects on fecundity and fertility under continuing chronic
i~radiationconditions are to be expected and. for theparticular cases of fish and molluscs in the cooling water
reservoir of the Chernobyl power plant. could have been
predicted fiom available infomiation. There has been noreport of a local (i.e. isolated) population of a single
species having been eliminated as a consequence of theradiation exposure. Populations of small rodents havebeen isolated in large enclosures and studied for morethan 40 generations. Radiation-related effects have been
observed, along with sonie homeostatic adjustment or
adaptation to [he altered conditions. There is evidence ofrecovery. in marly instances. from the initial acute-phase
responses, and in all areas the populations continue tosurvive under long-term chronic irradiation.

CONCLUSIONS
256. All living organisms exist and survive inenvironments where they are subject, to a greater or
lesser degree, to the natural radiation background and,more recently. to man-made contamination from global
fallout following atniospheric nuclear weapons tests. At
times. and generally in restricted areas. therc are
additional increments of radiation exposures either from
authorized (controlled) discharges of radioactive wastes
to the air, ground or aquatic systems or from accidental
releases. In tlie majority of cases there have been noapparent effects in wild plants and animals from these
additional esposures. Followirlg severe accidents.

liowever. damage has been observed in individualorganisms and populations, and long-term effects could
develop in communities and ecosystems from tlie
continuing increased chronic irradiation.
257. The available data on the exposure of wildorganisnis to radiation from the natural background andfrom contaminant radionuclides are relatively limited.
They relate to a very restricted variety of organisms,
although for tlic marine environment they do provide a
reasonably representative picture of the range of doserate regimes likely to be esperienced. Because the58

UNSCEAR 1996 REPORT

estimates are largely derived either fro111 localizedmeasurements of the concentrations of radionuclides
within the organism and in its immediate external
environment or from niodels that assume an equilibrium
state, there is very little information on the te~nporalvariation in dose rates to be expected from short-term
fluctuations in discharge rates, differing stages in thelife cycle, changes in behaviour and short-term environmental factors such as seasonality. It is thus very
difficult to estimate from the available data the total
doses that are likely to be accumulated over specificstages of the life cycle. e.g. during embryonic development or up to reproductive age.
258. For both terrestrial and aquatic environnients.
there appears to be a significant contribution to thenatural background dose rate from alpha radiation. For
the fernier tlie main source appears to be "'Rn and its
short-lived decay products, and for the latter the main
source is "'Po. Owing to the short range of alphaparticles, the absorbed dose rates are tissue-specific, andthe results underline the crucial need for riiore detailed
information on the distribution of the radionuclides
relative to the biological targets that might beconsidered important (e.g. the developing embryo or the
gonads) if accurate estimates of background radiation
exposure are to be made. The usual range for the
background radiation exposure is up to a few microgray
per hour, but in exceptional cases (e.g. the liepatopancreas of a small pelagic marine shrimp) the absorbed
dose rate may be as high as 150 pGy h".
259. It is accepted that the release of radioactive wastes
to the environment is likely to increase tlie radiation
exposure of wild organisms. For discharges to theatmosphere, to a landfill or to surface waters, thepublished assessments reviewed in this Annex indicatethat the radiation exposures to some (but not all)individuals in endemic wild populations could reachabout 100 pGy 11'. in general; in exceptional cases.
depending on the quantities of specific radionuclides inthe \vastes. absorbed dose rates might reach several
thousand microgray per hour. In a v e n limited numberof instances the dose rates estimated fro111measured
concentrations of radionuclides in the contarninatedenvironment have been broadly confirmed by in sitr~
measurements employing dosimeters attached to theanimals.
260. The dose rates in the environment following an
accidental release clearly depend on the quantities of
specific radionuclides involved, the time-scale of therelease, the initial dispersal and deposition patterns, andtheir subsequent redistribution by e~ivironmental
processes over time. I t is equally clear that these
accidental releases havc the potential to generate muchhigher dose rates and higher total doses in theenvironment than do nor~iialoperations. Sucli was thecase following the accidents in the southeastern Urals
and at Chemobyl. where numerous studies haveindicated that trees (and. by reasonable extension. otherorganisrns) close to the release points could haveaccumulated doses up to 2.000 Ciy arid 100 Gy at thetwo accident sites. respectively. over relatively shortperiods of time. At both sites, longer-term chronic
esposures from the deposit of longer-lived radionuclides have continued to be significantly higher than
exposures from controlled waste disposal.
26 1. Froni thesc data it lilay be concluded that it is the
responses of plants and anirnals to chronic radiation
exposures up to a rnaximuni absorbed dose rate of 1,000
pGy h-' that are of interest from the viewpoint ofproviding a basis for assessing the environmental
impact of controlled radioactive waste releases: inpractice. infomiation at lower dose rates. up to 100
pGy 11". would probably be sufficient in the greatniajority of cases. For accident situations, whereexperience has clearly demonstrated that initial dose
rates can be high enough to allow accumulating lethal
doses in relatively short periods (days). data are needed
to provide the basis for predicting the progress ofenvironmental recovery at generally lower. long-term
chronic dose rates, down to the upper end (1,000
pGy h-I) of the range of interest for assessing waste
disposal practices.

262. There is a wide range over which organisms are
sensitive to the lethal effects of radiation. A generalclassification has been devised based on the interphaseclirolnosome volume of sensitive cells. These and otherresults of experiniental i~radiationssliow n~ammalsto
be most sensitive, followed by birds, tish. reptiles andinsects. Plants show a wide range of sensitivity thatgenerally overlaps that of animals. Least sensitive toacute radiation esposures are mosses, lichens, algae andmicro-organisms, such as bacteria and viruses.
263. Sensitivity of the organism to radiation depends
on the life stage at exposure. Embryos and juvenile
fonns are nlore sensitive than adults. Fish embryos. foresample, have been sliown to be quite sensitive. The
vi~rious developmental stages of insects are quite
reniarkable for the range of sensitivities they present.
Overall, the available data indicate that the productionof viable offspring through gametogenesis andreproduction is a more radiosensitive population
attribute than tlie induction of individual mortality.
264. In the most sensitive plant species, the effects ofchronic irradiation were noted at dose rates of 1.0003,000 pGy h-'. It was suggested that chronic dose rates
less than 400 pGy h" (10 niGy d-I) would have effects,
although slight. in sensitive plants but would be unlikely
tu have significant dclcterious effects in tlie wider range
ol'plants present in natural plant communities.

ANNEX: EFFECTS 01: RADIATION ON THE ENVIRONMENT

265. For the most sensitive aninlal species, man~~nals,
there is little indication that dose rates of 400 pGy h-' tothe most exposed individual would seriously affectmortality in the population. For dose rates up to anorder of magnitude less (40-100 pGy h*'), the samestatement could be made with respect to reproductive
effects. For aquatic organisms, the general conclusion\+-asthat masimuni dose rates of 400 pGy h-' to a sn~allproportion of the individuals and, therefore, a lower

59

average dose rate to the remaining organisms wfould nothave any detrimental effects at the population level. The
radiation doses necessary to produce a significant deleterious effect are very difficult to estimate because oflong-term recovery (including natural regeneration andthe ~nigration of individuals from surrounding lessaffected areas), compensatory behaviour and the many
confounding factors present in natural plant and animalcommunities in both terrestrial and aquatic environments.

-

-

-

---

-

-

Table I
Internal dose rates to leaves a n d needles of trees from natural radionuclides in the plant material

[Jll
-

1

I

1

Dose rare per ~tnilconcenlrariot~(nGv 11" per i33kg"la0.0033
0.028
0.039

I

1

P. Y

2.42
0.057
2.76
2.7 1
2.76
11.1

0.13
0.068

3.07
2.32
0.13
6.42
12.10
a
b

Includilig decay product.
Illcl~rdi~ig
short-lived tlcc;ly products in rijuilihriurn \vith the palcrll ~;~tlionucliile.

-

.

--

Table 2
Dose rates to leaves a l ~ t lrleeclles of trees from natural backgrort~ldradiation

SourceCosmic mdialion at sea Isirrl
Terrc'strial gamma radialionaI-roni cosmic-ray nc'utrolis.

.

.4 bsorbeti dose rare
(pGy 114)

- -

0.12

XhNES: EFFECTS OF RrZDlA'rION ON THE ENVIRONhlEN'S

61

UNSCEAR 1996 REPORT

62

Dose rates to leaves and needles of trees from noble gas radionuclitles in air[JII

Rodionrrclrrle

a

I

I

Including decay products.

I

Effectir8ccrlerjy(Ale 1')DL'CUJ
nlde

'

l

-

.

- External

.

ot

per I

o e ~ r o o I n air(lO" GI Ir" per- By m")1-

A

Inten~al-1

hNNEX: EFI-ECTS OF RADIATION ON THE ENVIROh'hlENT

63-

Table 5
Ertirn;~teddoses to ierres a n d needles o f t r e e s from normalized discharge to t l ~ catmosphereof noble gases iron1 nuclear reactors

1
I~c~dro~~rtcl~deI--

r t n / eclrschurgt, "/TBq (G K' a).']

I

I

1

11 I

(

'

u

1

A brorbed dost
per unrt energ). generuferl1[pGy (G J'f u).']-DO.^ f i ~ d o Ir

hrtegrc~ft'dco)~cettrrufio~
illtrrr rr/ I km-

[nGy/t/;~,cr By 1t1 '1

I'rcssorized water reactors
Ar-4 l
Kr-85m
Kr-85
Kr-87
lir-88
Xe-131111
Xcl33lll
Sc- 133
Xc- 135111
XC-135
Xe-138I

Iioiling w:itele reactors
Ar-l l
Kr-85rn
Kr-85
Kr-87
Kr-88
Xe-13lrn
Xe- 133111
Xe-133
Xe-I 35111
XC-135
Sc-13s

1

Total

-

2.6

-

Gas-cooled reactors
Ar-l l
a

h
c

2150

l 80000

Ilata from IJNSCEAR 1993 Report [LI?].
,Issun~csdispersion factor 01'3 10" R q s ~ n "11cr Uq [UJ].
Prom Table J [J I].

0.69

120

UNSCEAR 1996 REPORT

64
--

--

-

-~
-----

Table 6
Estimated dose rates to organisnis from controlled discharges of ratlionuclitles that would each resultin a dose rate of 1 rnSv a" to man residing in the same environment
I [I4,NI]

1

1 -

--

I

-

I

-

__

---

~
1

Zr-95
Tc-99

ti

1-131
CS-137---

Ka-226 "U-235 "
U-238 "
Pu-239.Am-241

"
'

a

b
c
d

Doserote (pGy h')
--

-

14-3
C-14
P-32
Co-60
ST-90

I

-

-

A11i111als""-L -- I'liulrs "- -. ---Discharges to atmospliere.
Don~csticsheep.
Discharges to Hater (lakes).
I ligh-LET radiation.

5.8
18
32

5.8
II
28

2.0
38

0.042
2.0

I .I
5.4

0.058
3.1

i--

-

Fish '
-

0.59
4,8
0.53
67

3.8
-

!

I

-

--

-

-

Radion~tclide

i

--

-.-

I

-

I

0.073

!
I

0.72

0.00052

-

-;:;

4.7
0.49
0.7 1

--

ANNEX: EFFECTS OF RADLATION ON THE ENVIRONXIENT
-

-

65

-1

1 Table7

I Cumulative absorbed doses in ;~griculturalaninlals following single intakes of radionuclides a n d for similar periods

1 of c l ~ r o n i cintakes of r:ldionuclides
1 IK91
I

mitnalI

species

Type o/espo.\t\lrre"

Ctrmulative absorbed dose (pGy)

1
Alier

--

I

cattle1

SheepSingleChronic--.

-

SingleChronic

'

.
Swine

SingleChronic

CattleSingleChronic

.

.

I

.
-

I

Sheep

SingleChronic

Swine

SinglcChronic

CattleSingleChronic

I

Sheep
1

Swine

a

b
c
d

SingleChronic
SinglcChronic

Intake ol' I kBq on the lirst day for both single and chronic exposures; for chronic exposure the intakes declined according to theradioacthe decay rates; radionuclides administered orally in experimental setting.
Absorbed dose in thyroid.
Absorbed dose in bone.
Absorbed dose in muscle.

IIlh'SCEAR 1996 REPOICI'66-

I Table 8
Absorbed dose a n d pcriod in organogenesis for radiation-induced, externally tletectable malformations
1

[C211

~

Kudiuse~~sdlr
organ..lirirr~af
speci2s,\iabl blducriott period(days afier cor~ceplion)

Lu11,esrreported doselo cause effect.\lab1 dose rarlge

hlouse (strain-depentienr)
Rat

8-13
9-11

0.25 (iy0.50 Ciyh

1.0-2.0 Gy
1.0-2.0 Gy

hlouseKat
I lamster
Rabbit

7-8
9-10
S-Y
-10

I

1 Central r~ervoussystem
Eye

I

'

I

1

I

1 blouse

7-10
9- 12
7-8
9-1 I
8-12

Knt
I-lan~sterKabbitklonkeys-.

II

0.5 Ciy
1.0 Gy.-to catrse effect '-.-1 .O-2.0 Gy
1.5-2.5 Gys2.0 GysJ.0 G)>2.5 Ci)-- -hlouseSl~cepCattle-1---

XlouseRat, l lnrnsrer
.u

b

Dog
A

Single x-ray exposure.
I-listological findings from 0.1 [o 0.4 Gy

I Table 9I

Dose levels from s h o r t - t e r m irradiation producing d a m a g e to p l a n t cornr~ltlnities"

I Iwj]
Dose rartge lo j ~ r o c ~ ~ c e(@I)_
cts
Severe effccfs-

Coniferous forest
Deciduous forest
Shruhlanll'l'roliical rain forest
Kock outcrop
Old field
Herbacro~~sI'orcst unders~orey(;rassland
Clerbaceous invadcrs
hloss lichenu

1-10
10-10010-50-10- 100
80-10030- 100
200400so-100400-600
100-1.ooo

Exposures of 8-30 days. Dose r;inge may he 2 4 limes lcss for more acute exposures. Equivalent daily dose ranges for chronic
el'fecu are I X I X oftllc listed values.

IANNEX: EFFEC'I'S OF RADIA'I ION ON TIIE ENVIRONhlENT

67

1, Table 10' P r i m a r y composition o f radionuclitles deposited i n a contaminated area following the southeastern Urals accident

v-21I

--

- -

-

--

-

Table 1 1
1 C'erticnl distribution of dose rates from betn :tnd gamma radiation to components o f a pine forest i n an area
I o f contaniination fro111the southe:~sternUr:~lsaccident norllialized to deposition density o f "Sr o f 1 hlBq 111-'[T 1 711.h~lotlrlts
uJer
depositionr,I1 soil surface

I

--

- .
At litter sutj4ace(2 ctn)rlhsorbccldo.~erare ( ~ C It.')
I
-

-

--

-

I

I

A! borrom part ofn m n r (3 m)A

Ar nriddleparr ofcrotrns (6-7 m)--.

Ar topparr oj
cro\trns(9-10 m)
I

1

UNSCEAR 1996 REPORT

68

Table 12
Normalizetl radiation dose rates to organisms during the acute period following t h e accitlent in the southeastern[7'17]

1('onrpotrrrrl, loccrrionor specific typeojorganism

Orgar1ist~l

--.

-

-

~

Pine trees

I3ud meristernSeeds in the canopy.
. Scetls on thc -soil
Birch trees-

I lerbaceous plants-.
Soil invcrtebratcs

Bud rneriitem
Seeds in the canopy

830-1 -300
420-830--I)orn~;intbuds\eeds on the soil

01.2008301,200

A

In the leaf litter;It I crn depth in the soil-

\lamnlals
-

Birds

a

-

-

-

-

:Vortnc;lized closes( p e ri ft iS

-

3-5
2-3
0.5-1
- - -- -,\taximrrrn doses nearrelease pobrr (Gj3.

--

20-2000.5-2
0 3-0.7
.
-

-

---

0-10
2-10

I

-

--

l.arge herbivores (GI mct)
Sir~allrodents (\\-hole body)(GI tract). C;lrnivores- -11,300-2,100
830-1.300-120-830--

fi..f hsorbed closes drrririg (lie acirre period,\iarfinut~rtror~nuli;ed
abswhed dose rdes
(pGy h-!per dfBq tn'? Y'l.Sr)

0-2,000
70-2.000I

31003000420-

Sin;~lI,ovenvintering
C;~riiivorous.ovenvintering((;I tract)-30-1 00-

830- 1.300
Jzo

1

2-3
I

50100
30-100'file dose rates h;tvc hcct~normalized to a strontium-90 contunination density of I hlBq nl'?, ~ ~ C ~ I I Ithere
S L I was a relatively constantrelationship bct\rccti ;III the radionuclides throughout the deposition.

Table 13
Radiation damage to trees in the contaminated area o f t h e southeastern 1Jr:lls

A wrage absorbed dose (Gy)---Radiobiological eflecr-

Jhrcedles

Bud merirrem

5-10

21

-

--

-

Pine: desiccation of needles in the lower part of the crotrn, nonviability ofpollcn aritl sccds, reductior~in growth incrcrnent
Pine: desiccation of 95% ofthe crown. growth retardation
-

10-20

5-10

--

Pine: complete death (LD,,,,)

--- -

-

-

-

40-60

Birch: desiccation ol'the upper storey in 1% of trees, up to 30%
reduction of young growth. low germinatioli capacity of seeds,
reduction in gro\bt11 increment

100- 1 50

Birch: desiccation ol'lhc upper storey in 30% oftn'es, up to 75%
reduction o f young grcn\th (LD,,,)

-

- .

1

-

-

--

--

I

ANNEX: EFFEC'I'S 01.. RADIA'TION ON THE ENVII:ONI1EN'I'
- -

-

-

-

-

-

69
-

--

T a b l e 14
, Numbers of the main groups of soil mesofauna in *Sr-contaminated a n d control sites in t h e southeastern Urals
I IK151

Ab.tolrrte
r~ri~rher
per trr'.

Species

Sapropha~eProportionof cott~rol-

Earth\vorrns
hlillipedcs-- Total-

Snailslslugs
I lcrhivorous insect I m a e'I'oral
.

-

~

I

--

Spiders
Insccl larvae
Bcctles
Centipcdcs-

Tori11

-

-

-

--

-

--

-

T a b l e 15
C h a n g e s in numbers of the main groups of soil rnesofauna in ' O S r - c o n t a n ~ i n ~ t esites
d in t h e southeastern Crals[K l S].-it con/rmrinatcd
site
- -~
-

Conrrols---

2 5 . 5 i 10.7
12.3 * 5.1,~~~

Saprophqc
E,uth\vorms
-

-.

-

I'hytophngs

Click becllcs\\'eevils
-

-

I

Other

*

-

-

.-

4.3 1.8
1.8
-i0.7
--

-

-

1.itllobiidae
Diptera--0.3 i 0.1
2.0 0.6

2.0 i 0.8
2.0 i 0.6

*

~

0.10
0.24

,

0.15
No difference

Table 16Degree of contamination ;~ntlexternal dose rates a t sites where farm animals were grazing following the accident
in t h e southeastern IJrals
[All1

'

I

Cottcenrronon ojbera
emrrfers rrr grcss@'Bykg2-&-

Extc~ntaldose rareur I m({I G j ~ h - ' ) -.-lbral absorbed doseover 12 days

GY)

1

UNSCEAR 1996 RIII'OlCl'

70

Table 17
Total concentr:ition for a11 radionuclides in animal tissues near sites of the accident in the southeastern Urals
[All1

Lrrnp
. -

Co\v
Co\r fetus
Goat
Sheep
Gecse
' Hens
.

-

300

1

30

1

::: i

I.her

I

hidt~ey

SkeletonLarge
intestineI

fiolherr

Site I '

--

I

3.2

I .2

-

I

I

3
3

-

Site 4 '

-

--

co\r
Day I IDay 120
SlicepDay I IDay 120
CicescDay I iDay 120
Hens
Day 1lDa, 120
uContan~inalcdsircs dclincd in 'fable I6, Table 18
Estimated absorbetl (lose over 12 days to different segments of tlie g:istro-intestinal tract :ind to the skeleton of
sheep and cows :it tliree sites contamin:~tetl by the accident ill tlie soutlieastern llrals[All1

11 hsorlletf dose (G}yp--

Srte l-1

Segment of Cil tmcr
Rumen ( 1 )Run~m(2)Omasum.4bomasunl
DuodcnumJijsnurn
Ileum
Large colon
Small colon
Rrituln
Skeleton

Srfd

S I I 3~!

Site I--.TI/~! ?

--Sire 3. -I

ANNEX: EFFECTS OF RADIA'SION ON TIIE ENVII<ONbIENT

71

T a b l e 19

I

, Distributiori of radiation damage in the forest :around Cllernobyl n ~ ~ c l epower
ar
pllnt
K25]

w.1.

/Ihsorhed dosr,
1
I.Leti~alzorlc. 4 km'

I

1Complete cleat11 of'pir~ctrces
Partial damirge of deciduous trees

1

Death of most prouth points, partial
diebach of' coniferous trees
hlorphologicnl changes ill deciduous trees

- ,-

- -

Sublethal rone. 38 hm'

1

! -

-

-

-

a-

frorrr exlemcrl
gamma radiariorr(GY)-

Ihsorhecl close
rule
on I October 1986

'
.----

11 I )

10-20

--

-

I

1-5

20-50

500-2.000- -0.>-1.2

-

p~

-

- -

50-100-Disturbances in groivtli arid reproductio~~.
morphological disturb:rncesin coniferous trees
-

-

.,

I

--

-

- -

-

I

( 9
- -

2,000-5.000

-

-

/

-

Zone of medium
Suppressed reproductive ability. desiccateddamage. 120 kni'
- .
.- needles, morphological changes
Zone oSn~inordamage

Ah.vorbd dose
irr t~eedles

.-.

c200

A

<I0
.

-

-

-

T a b l e 20
C h r o n i o s o n ~ a laberrations a t nieiosis in pine microsporocytes in an ;area close to
the Chernobyl nucle:~rpotrer reactor

[K35]

I

Esrirnrrted
absorbed dose

((3)
.
. -

,

0.7-1.1
1.7-2.3
Control,\irrnber o/cL~II.F
atm(vsed
.

1987

.

4.200
6.300
3.000

I

--

-

1988
--

.

1.800
1,200
1 .000

22.0
30.2
2.7

11.4
9.6
5.8

' f a b l e 21
Estimates of quantities of radionllclides in the Cliernohyl nuclear power plant cooling pond on 20 hIay 1986

[U7]

I

Radiorrrrclrdr

1

Cs-137
Cs- 1.14
Cr- I44
Cr-I11
Ru-106
Ru- 103
Zr-95
Sb-95
Ba-I40La-I 1 0
1-131
Er-00

I
-

-

UNSCEAR 1996 REI'OKS

72

Tnble 22
Effects of radiation on silver c a r p fish s u n i v i n g in t h e c h e r n o b y l nuclear power plant cooling pond
I after the accident

18331
Proporriotl ojfih wirh abnormaliries
11' 1 gerrerarive cells (4)Year offirr~ales
-

-

-

1989
1990
1991
1992
Toral

1

C'azed silver carps "

'

--

/

17
II

1

9

3
10
-

-

-

-

2
3

8
6
7
4

25
-

-

0
0
5
- -

1

16

1

7
70

(Incaged silver carps
-

-

2'
-

u

b
c

Conlined in aquaculrure pens.
At 1;rrge in the cooling pond.
Partial sterilily.

-

l9
- --

- -

-

I

-

1

.\foles-I

ANNEX: EFFECTS OF RADIATION ON THE ENVIRONMENT

73.hloncrliy in 50% r~fplanrs +Srvrrc. gro~vth irlhibitiorr.-f-FIor(r1 inhibirir~nr Poflrrt .s teriliry
Aior~c~li!,'in 10% c~f'~~1r111r.r
Yield mduced by 50'h---aFc~iittruto .>el.wed-&
Meld rrdrrrrd / ~ y10%+-

Nonrual appeorcrncr

I
0

10

I

I

I

I

I

I

20

30

40

50

60

70

P E R C W . 4 G E OF LETHAL DOSE

Figure I.
General range of radiation respome in hc.rbaceous plants in compi~risonro the lethal dose (LDIo0).
is81

Figure 11.
'l'he acute lethal rsposurc to high-dose-rate, low-LET r;~tliationin relation
to the volume of intcrph:~sc (non-dividing) chroniosornc.s of angiosperms.
[S12]

80

UXSCEAR 1996 REPORT

74

I

2

3

5

1

7

6

8

DOSE (Gy)Figure 111.
Rlidlinc close-survival curves for various species of arlinlels irradiated bilaterally.
lTlUl

Lare < [ f e ~ t . ~CANCER AND LI-UKAI-:MIA.......................
FUNCTIONAL DISORDERS

t------,DLSORDWED CELL MATUKA'IION/GROWTH INHIBITION

I

1;igure IV.
Prenatal phases for indueti011of rarliation cf'fects i l l the ~ n o ~ l s c[caq

hrlg-lertn
tt~(itrtr(ifiot~
t1isorder.v

ANNEX: LFFECTS OF IMDIA'I'ION ON TIjE ENVIRONMENI'

75'rI\IE AFI'ER CONCEPI'ION (days)
Figure V.
Relative occurrence of intrauterine irljuries in the louse after acute x irradiatio~~with 1.9 Gy. For irradiation follo\sring
day 14 after conception. there is no radiation-induced injury, and the spontaneous rates are obsened.
[C221

-

0 RAN viruses
D!VA virrrses
A DNA viruses
A Viru.re.r. hucreria, vcutr
Yeu~t,bacteria, r~ra~~ln~als
Bacteria. algae, u1ttp1rihicu1.r
0 Bacteria. plants

Algae. ferns

Figure VI.
Cell radiownsitivity based on correlatio~lbetween D, (379 sur\'ival dose) and chromosome volume.
[Sl]

UNSCEAR 1996 IEPORT76

I

VIRUSESMOLLUSCS

1PROTOZOAI

BACTERIA
MOSS, LICHEN, ALGAE

1

1

CRUSTACEANSI

REPTILES

1

AMPHlBLZNS

I

I

FISH
HIGHER PLANTS

I

I

I

INSECTS

BIRDS

I

/

h.IAMMALS
I

I

I

10'

I o2
ACUTE LLTHrZL DOSE (Gy)I o3

Figure VII.
.4pprosi111ateacute lethal dose ranges for various t:isoncrrnic groups.
ISl. wsl

Bickham. J.W.. R . G . Hanks, h1.J. Smolen et al. Flaw
cytometric analysis of the effects of lo!\.-level radiation
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Rurnazyan, A.1. (ed.). The Results of Investigation andExperience of Liquidation of the Land \vitli Fission I'roducts
CIS
of Uranium. Energo:~tomizdat, h.iosco\v. 1990.
Begg, F.H., h.1.S. Rauter, G.T. Cook et al. Anthropogenic "C
as a tracer in western UK coastal waters. p. 52 in:
C19
Radionuclides in the Study of hlarine Processes (P.J. Kersha~v
and D.S. Woodhcad. eds.). Elsevier Applied Science,
London/hrew York. 1991.
Barr. R.E. and S.J. Musacchia. The elrect of bodytemperature and post-irradiation cold exposure on theradiation nsponsc of the hibernator?Cirellrcs rrunidecen~li~reatus.
Radial. Res. 38: 137-448 (1969).
Bclova N.V.. B.V. Verigin. N.G. Emelianova ct al.
Radiobiological analysis of silver carp (Hypoplrfltuln~icI~~Ir~~~s
nrolitrix) from the Chernobyl NPP cooling pond in the postaccident period. I. The statc of thc reproductive system of fish
sunqiving the accidc~it. Vopr. Iclitiologii 33(6): 814-828(1993).
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Oceans and Coastal Waters, Volume 113 (0.Kinoc. ed.).
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in a chronic gamma radiation field. Am. hlidl. Nat. 8912: 416(1973).
Casaren. A.P. Radiation Biology. Prentice-tlall. Englewood
Cliffs, New Jersey. 1968.
Caster, R. E~~olutiondcs activitis microbierincs dans cn
ccosyst6me ~nediterraniensoumis B une irradiation gamma
chronique. Etude p:~rticulit!rc des transfens azotCs p sniarrluage isotopiquc. CEA/R-5402 (1987).
Coughtrey, P.J. Effect of ionizing radiation on native plan1
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Committee on Biological Effects of Ionizing Radiation (BEIR
Ill). The EfTects on I'opulations ofEsposurc to Lo\\' Levels of
Ionizing Radiation: 1980. United States National Academy of
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CIO Callill, D.F., L.W. Rciter. J.A. Santalucito et al. Biologicalassessment of corltinuous exposure ro tritium and lead in therat. p. 65-76 in: Uiologic:~land Environmental Effects oflowlevel Radiation. Volu~rie2. IAEA, Vienna 1976.
Cristaldi, M., E. D'Arcangelo, L.A. lrradi el al. '"Csdetermination and mutagenicity tests in wild . \ ~ I L SIIIIISC~~~IIS
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Pollut. 64: 1-9 ( 1990).
Cristaldi. hl.. L.A. leradi, D. hlascanzoni et al. Environmental
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:~mphibii~ns.

Coffigny, 1-1. and C. Pasquier. Etude chez Ie rat adulte deseffrts d'une irradiation pre- ou post-natale de 150 rads. Trav.
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Cosgrove, G.E. and U.G. Blaylock. Acute and chronic
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