Radionuclide Concentrations in Foor and the Environment - Chapter 7 docx

209

7

Effects of Radioactivity
on Plants and Animals

Kathryn A. Higley

CONTENTS

7.1 Introduction 209
7.2 Physics, Chemistry, and Biology of Radiation Interactions 209
7.2.1 Types of Ionizing Radiation 210
7.2.2 Physical and Chemical Aspects of Ionizing Radiation
Interactions 210
7.2.3 Direct and Indirect Radiation Interaction 211
7.2.4 Biological Consequences of Radiation Interaction 212
7.3 Effects of Radioactivity on Individual Plants and Animals 215
7.4 Ecological Consequences of Radiation Exposure 219
7.5 Conclusion 222
References 222

7.1 INTRODUCTION

The literature on the effects of ionizing radiation on plants and animals spans
nearly a century. Early studies of radiation effects on drosophila were used to
determine that it is a mutagen [1]. The primary intent of these early studies was
to better elucidate the nature of radiation interactions to understand their impacts
on people. A consequence of the development of nuclear weapons was the

developing awareness of the existence and global distribution of radionuclides.
Interest grew in understanding where radionuclides went in the environment and
helped support numerous studies of radiation effects on species, populations, and
ecosystems [2]. While the bulk of the studies have focused on the response of
the individual, accidents such as Chernobyl have allowed ecosystem-level inves-
tigations to be conducted. Many of these studies are ongoing.

7.2 PHYSICS, CHEMISTRY, AND BIOLOGY
OF RADIATION INTERACTIONS

Understanding the effect radiation has on living tissues requires that one first
examine the physics and chemistry of the initial interaction. Living cells are

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Radionuclide Concentrations in Food and the Environment

composed in large part of water. The remainder consists of organic compounds —
lipids, proteins, carbohydrates, and nucleic acids [3]. When ionizing radiation
interacts within a cell it rapidly sets in motion a series of events that can lead to
chemical and ultimately biological changes. The subsequent damage can be traced
to the chemical changes that have come about due to the initial interactions of
radiation. The nature and time frame for these events are discussed below. The
magnitude of radiation exposure necessary to cause the effects is discussed later
in this chapter.

7.2.1 T

YPES



OF

I

ONIZING

R

ADIATION

There are two types of ionizing radiation: electromagnetic and particulate. X and

γ

rays are the ionizing electromagnetic radiations. They differ primarily in their
origins (atomic vs. nuclear transitions), but are otherwise similar in properties.
When X or

γ

rays are absorbed in matter, energy is deposited — unevenly and
in discrete packets. The amount of energy is generally sufficient to break chemical
bonds. Hence these radiations are termed “ionizing.”
The other type of ionizing radiation is particulate. The most common partic-
ulate radiations encountered in environmental settings are

α

and

β

particles.

α

particles are highly energetic helium nuclei lacking orbital electrons. They have
a +2 charge when they are initially ejected from the nucleus during decay.

β

particles are highly energetic electrons that originate in the nucleus and may
carry either a –1 or +1 charge.

7.2.2 P

HYSICAL



AND

C

HEMICAL

A

SPECTS



OF

I

ONIZING


R

ADIATION

I

NTERACTIONS

Absorption of ionizing radiation energy occurs through indirect and direct mech-
anisms. Charged particles such as

α

and

β

particles have enough kinetic energy
to directly dislodge electrons and cause ionization of the atoms and molecules
with which they interact. Electromagnetic radiation (X and

γ

rays) is classified
as indirectly ionizing. The radiation must be absorbed in order to transfer its
energy to an electron. The end result is virtually the same — the production of
an excited or ionized atom.
The result of this interaction is the production of secondary electrons with
some kinetic energy (energy of motion). In water, and other low atomic number
materials, these secondary electrons have energies on the order of 10 to 70 eV
[4]. The life span of these secondary electrons is very brief (approximately 10

–15

sec) and during that time they transfer their energy to the surrounding environment
as they move through it. The initial transfer of energy to water results in the
formation of ionized and excited water molecules, most notably H

2

O

+

(ionized
water) and an electronically excited version of water, H

2

O

*

. These are accompa-
nied by free electrons that have insufficient energy (less than 7.4 eV) to cause
any additional excitation.

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Effects of Radioactivity on Plants and Animals

211

Following the initial interaction, the three species that have been created
undergo additional changes. The ionized water molecule can interact with an
adjacent water molecule to form the following compounds:
H

2

O

+

+ H

2

O

→

H

3

O

+

+ OH.
The excited water molecule, H

2

O

*

, can lose energy in two ways:
H

2

O

*



→

H

2

O

+

+ e
or
H

2

O

*



→

H + OH.

This process, although not as rapid as the initial ionization event, occurs in the
time frame of 10

–12

sec. The molecule H

2

O

+

is an ion radical (it is both electrically
charged and contains an unpaired electron). It has a short life span (less than
10

–10

sec) and decays to form the highly reactive hydroxyl radical (OH·), which
has a life span of approximately 10

–5

sec. Once these species have been produced,
they go on to react chemically with their environment, based on diffusion-con-
trolled reaction kinetics [4].

7.2.3 D

IRECT



AND

I

NDIRECT

R

ADIATION

I

NTERACTION

Radiation interactions within cells are typically characterized as direct or indirect
in nature. This characterization stems from the historical assessment that DNA
is the principal target of concern with regard to radiation damage [3–5]. When
radiation interactions occur in the cell, they may do so directly with the atoms
of the target or with other atoms or molecules in the vicinity. For

α

particles,
which are considered high linear energy transfer (LET) radiations, direct action
is the dominant process by which the critical targets are affected. Sparsely or
indirectly ionizing radiations such as

β

particles and X or

γ

radiation produce
free radicals that can then diffuse and damage the critical target. This mode of
delivering radiation damage is called indirect action. It accounts for roughly two-
thirds of the damage caused by sparsely ionizing radiations [4].
Although DNA has generally been viewed as the most important target from
the perspective of radiation damage, there is a wide range of molecules within
the cell that can be adversely affected. These molecules vary in both size and
molecular weight, and they too are impacted by the same direct and indirect
effects of radiation discussed earlier. Broken chemical bonds, cross-linkages, and
conformational changes are the resultant products of radiation interaction within
the cell [4,5]. These altered molecules may hinder the molecule’s biological
function. For example, a change in the orientation of an enzyme or protein (a
conformational change) could limit its ability to perform a function in a metabolic
pathway. The result could be the interruption or cessation of certain functions [5].

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Radionuclide Concentrations in Food and the Environment

7.2.4 B

IOLOGICAL

C

ONSEQUENCES



OF

R

ADIATION

I

NTERACTION

The consequences of ionizing radiation interaction can be seen at all levels of
biological organization (molecule, cell, organ). However, it is important to note
that while events may transpire at the molecular level, impacts do not automati-
cally flow through to the higher levels of organization (individual, population,
community, or ecosystem) [6–10].
When DNA is considered the critical target, the impacts of concern are the
nature and extent of damage caused by charged particle tracks (or resultant
chemical species). Single breaks in a strand of DNA, as well as ruptures in both
strands (double-strand breaks), are the immediate products of ionizing radiation
interaction within cells. As previously noted, ionization produces highly reactive
products that break chemical bonds, including DNA molecules as well as cell

membranes. Cell killing, mutation, and carcinogenesis are the longer-term con-
sequences of these events. However, to complicate matters, many living cells
have systems in place to repair damage to the DNA [11].
There are several characteristics of radiation that are important in determining
the extent of the biological response. These include
•Type and energy of radiation (e.g.,

α

,

β

, or

γ

). As noted previously,
these can be densely ionizing radiations (i.e.,

α

) that directly impact
critical targets, or sparsely ionizing radiations (X or

γ

rays, or

β

par-
ticles), which have an indirect effect as their principle mode of radiation
damage. These radiations are not the same with respect to their effec-
tiveness in causing biological damage [12]. An absorbed dose of

α

particles, for example, can cause more biological damage than an equal
absorbed dose of photons. In translating absorbed dose to a measure
of biological effect, radiation “weighting” factors have been developed
for humans. They have been assigned a value of 1 for photons and
electrons and 20 for

α

particles. However, they account for the potential
to cause cancer, a stochastic effect, and do not address deterministic
effects. Data on deterministic radiation effects for

α

particles have been
reviewed and evaluated by the International Commission on Radiolog-
ical Protection (ICRP) [13] and appear to lie in the range of about 5 to
10 [12]. A weighting factor of one is typically used for electrons and
photons, even for deterministic effects.
• Spatial distribution of delivered energy, both micro- and macroscopic.
At the macroscopic scale, the physical unit that describes energy dep-
osition is the absorbed dose (in Gy or rads). It is defined as the average

energy absorbed in a target tissue or organ divided by its mass. How-
ever, this average value does not depict the enormous variability in
energy deposition that occurs at the microscopic (e.g., cellular and
molecular) level due to the stochastic nature of energy deposition
events.

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Effects of Radioactivity on Plants and Animals

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•Total dose (energy per mass) delivered. With moderate to high doses
of sparsely ionizing radiation (greater than 100 mGy), cells and tissues
receive a nearly uniform exposure [14]. However, for substantially
lower doses (approximately 1 mGy) more than a third of the cells
remain undamaged [11]. The number of cells struck by an ionizing
event depends significantly on the radiation energy as well as the type
of radiation (i.e.,

α

,

β

, or

γ

).
• Rate at which the dose is delivered. It is well known that dose response
can be modified by changing the duration of exposure [5]. The biolog-
ical effects from low-LET radiation are smaller when low dose rates
are used than for higher ones (0.5 to 1.0 Gy/min). Fractionation also
can reduce the impact. High-LET radiations, because of the direct
nature of the damage they inflict, do not show the same degree of dose-
rate response.
Radiobiological studies have shown that, in general, cells most sensitive to
the effects of ionizing radiation are those that are undifferentiated, well oxygenated,
are highly metabolically active, and rapidly reproduce. In mammalian cells, the
most sensitive are spermatogonia and erythroblasts, epidermal stem cells, and
gastrointestinal stem cells [3,4,15,16]. The least sensitive are the highly differ-
entiated and mitotically inactive nerve cells and muscle fibers. Interestingly,
oocytes and lymphocytes are also very sensitive, although they are resting cells
and consequently do not match the criteria noted earlier. The reasons for their
sensitivity are unclear.
There are also several areas of radiobiological research that are challenging
our fundamental understanding of radiation damage at the cellular level (where
DNA has historically been viewed as the principal target of concern). Three of
these areas are
• Genomic instability. Also known as genetic and chromosomal insta-
bility, it refers to genetic change occurring serially and spontaneously
in cell populations as they replicate. The concept of genomic instability
is that radiation can induce a genome-wide process of instability in
cells. This instability is transmitted over many generations of cell
replication, leading to an enhanced frequency of genetic changes occur-
ring among the progeny of the original irradiated cell [17]. The phe-
nomenon has been observed with cell systems

in vivo

and

in vitro

and
for low- as well as high-LET radiation [18]. These effects have been
noted not only in cells that have been hit by ionizing radiations, but
by adjacent, unirradiated cells (see the section below on bystander
effects). While genomic instability is generally accepted, there are
many unanswered questions concerning the mechanisms, in particular
how it is initiated and how it is maintained over many generations of
cell replication [17,18].

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Radionuclide Concentrations in Food and the Environment

• Bystander effects. The conventional model of radiation-induced dam-
age requires damage of DNA either from direct interactions of radiation
or from free radicals created nearby. Recent studies have demonstrated
damage (such as altered gene expression) occurring in cells not directly
exposed to radiation [18,19]. This is known as the bystander effect.
There is evidence that this damage may be a consequence of intercel-
lular signaling, production of cytokines, or free radical generation. It

is also thought that these effects are related to inflammatory-type
responses. The significance of the bystander effect as it relates to
organisms and environmental consequences of radiation exposure is
not yet known [17,18].
• Adaptive response. The technical literature contains an increasing num-
ber of studies that show that adaptive protection responses occur in
living cells after single as well as protracted exposures to X or

γ

radiation at low doses [20]. This has been observed both

in vivo

and

in vitro

and has been documented across a wide range of organisms
from bacteria and viruses to plants and animals. Two types of protection
are identified. One prevents and repairs DNA damage, the other
removes damaged cells. The adaptive response mechanism is not
immediate, but develops, presumably in response to physiologic stress.
It manifests within hours and may persist weeks to months. However,
there are no strong data supporting adaptive response following expo-
sures to high-LET radiation [5].
By convention, the delivery of radiation dose has been categorized as acute
(short term) or chronic (protracted). The resultant impacts of exposure are further
apportioned into deterministic or stochastic effects. There is some confusion in
the application of the terminology, as well as imprecision in describing both. In

general, large radiation doses (the definition of large depends upon the organism)
delivered within a short period of time (an acute dose) leads to short-term, acute
(deterministic) effects. The expression of acute effects does not preclude the later
occurrence of stochastic impacts (stochastic meaning an effect for which the
probability of occurrence, rather than the severity, is a function of dose without
a threshold). The most notable stochastic effects are cancer and genetic effects.
Impairment of reproductive capability is one example of a deterministic effect
[21]. A more severe one is death. Many effects, such as skin reddening or sterility,
only appear when a threshold dose has been exceeded. There are also confounding
factors (noted earlier) such as total dose, dose rate, fractionation, and partial body
irradiation that can alter an organism’s response.
Protracted (chronic), lower-dose radiation exposures that do not exceed the
threshold for deterministic effects can still lead to increased probability for
stochastic impacts. The definition of chronic depends on the life span and metab-
olism of the receptor, but it is generally on the order of days to weeks (or longer).
Chronic irradiation effects data are generally given in terms of the daily dose
(e.g., mGy/day) rather than the total dose (e.g., Gy).

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Effects of Radioactivity on Plants and Animals

215

7.3 EFFECTS OF RADIOACTIVITY ON INDIVIDUAL
PLANTS AND ANIMALS

When radiation effects at the level of the organism are examined, it becomes
apparent that radiosensitivity generally increases with increasing organism com-

plexity [2,21,22]. The generally accepted hierarchy of radiosensitivity to acute
radiation doses has mammals, including man, among the most radiosensitive, and
primitive organisms (bacteria, protozoa, viruses) among the most resistant [2].
Extrapolations and generalizations of effects must be made with caution.
Even within similar species, radiosensitivity can vary by more than an order of
magnitude [21]. During the course of their life span, individuals may also exhibit
a range of radiosensitivities, based on a number of factors, including age, health,
and genetic predisposition. In general, the young are more radiosensitive than
adults (which can be attributed to cell proliferation being higher). However,
considering the wide range of organisms (plants, animals, viruses, bacteria) found
in the environment, the United Nations Scientific Committee on the Effects of
Atomic Radiation (UNSCEAR) [21] noted that the data do not allow one to
“reliably predict the potential radiation effects in the wide variety of organisms
likely to be present in a contaminated area.”
The difficulty in providing clear-cut evaluations of the effect of radioactivity
on plants and animals is that much of the available radiation effects data are based
on short-duration (e.g., seconds to hours), high-dose exposures, which are
expressed in terms of the total dose rather than a dose rate. These data, unaltered,
do little to help address the issue of radiation exposures at low dose rates and in
chronic conditions.
In a sweeping study, Rose [16] conducted an extensive, critical review of the
published literature to summarize and categorize the levels at which radiation-
induced changes were detected in organisms following both acute and chronic
exposures. Three broad categories of impact were examined: death, behavioral
or developmental, and teratogenic or genetic. This review encompassed more
than 600 citations and included data from all five kingdoms: protista, animalia,
monera, fungi, and plantae. Viruses were also examined.
The bulk of the work examined by Rose was conducted with animals and
plants and utilizing X or

γ

radiation. It is interesting to note that considering the
large dataset, only a few species were represented; the majority were mammalian.
Most also focused on acute, high-dose exposures in laboratory.
Past approaches to addressing the absence of chronic exposure data have been
to use the acute effects data to estimate which effects are expected from chronic
exposures. This approach is very conservative because, as noted earlier, a much
larger total dose can be tolerated if it is received gradually rather than all at once
[16]. Repair and compensation mechanisms that can be used at low dose rates
are overwhelmed if the dose is received rapidly. One example cited by Rose [16]
is an acute:chronic ratio of 10 or more observed for the most sensitive stages of
fish development, growth reduction in plants, and damage to somatic organs in
mammals.

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Radionuclide Concentrations in Food and the Environment

As part of the EPIC project (Environmental Protection from Ionizing Con-
taminants), a database of approximately 1600 records spanning 440 publications
on dose-effects relationships for wildlife in northern temperate climate zones was
recently published [23]. This database is built on records from Russian/FSU
experimental field studies and addresses what had previously been a large gap in
knowledge on low to moderate dose rate effects. As a consequence, much more
information is now being made available on the effects of chronic radiation in
animals. The data are still being reviewed, but some of the results are noted here.

In an article examining radiation protection criteria for northern wildlife,
Sazykina [23] proposed that five potentially measurable parameters be considered
when assessing the potential impacts of radiation exposure in the environment.
Three of these categories were similar to those identified by Rose [16]. These
five were
• Cytogenetic effects. Radiation interaction in tissue can leave indica-
tions at the cellular and subcellular level. One example of a molecular
endpoint is reciprocal chromosome aberrations [25]. The advantage of
examining this molecular marker is that the abundance of such aber-
rations can be related to cell killing, mutation and carcinogenesis, and
also reproductive successes (for germ cells). The problem is that there
are insufficient data at the present time to relate the chromosome
aberrations to individual and population-level effects.
• Radiation hormesis. Similar to the mechanism of adaptive response,
radiation hormesis is considered to be the consequence of stimulation
of the immune system from low-level irradiation. While results have
been observed, the data are inconsistent, and at this time do not appear
to be useful as a measure of assessing impacts of dose.
• Morbidity. In the context of Sazykina [23], morbidity as a parameter
referred to the appearance of illness and the general deterioration of
specific aspects of an organism such as suppression of the immune sys-
tem, changes in blood/lymph systems, and an overall decline in health.
• Reproductive effects. Reproductive organs are known to be sensitive
to radiation exposure. Sazykina [23] included damage to both the
reproductive organs of adults as well as its eggs and embryos. In its
literature review of radiation effects on biota, the International Atomic
Energy Agency (IAEA) [22] suggested that reproduction was an impor-
tant endpoint for assessing the effects of radiation on plants and ani-
mals, within the context of developing guidelines for radiation
protection. Cataloging the doses necessary to cause sterility is impor-

tant because for some organisms a dose which may cause complete
sterility may result in only minor changes within the organism [23].
And while sterilization may not directly impact the organism’s life
span, it may indirectly effect the population in which it lives [7]. While
tissues and organs within an organism vary in their radiosensitivity,

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Effects of Radioactivity on Plants and Animals

217

reproductive processes and the early stages of development are seen
as the most radiosensitive due to the ongoing activities of cell division
and differentiation.
• Mortality and life shortening. The classic measure of radiation impact
has been to measure mortality. Within confined experimental settings,
determination of mortality and comparison of the life span of control
as compared to exposed animals is relatively straightforward. In the
natural environment, confounding factors may make the analysis more
complicated [7,14,23–26].
While obscuring some of the finer points, it is possible to combine the work
of Rose [16] and the summary of Sazykina [23] and an earlier summary of
Brechignac [15] to develop an overall assessment of radiation exposure on organ-
isms. These will be examined using the five-kingdom convention of Rose [16]
and incorporating the effects analyses of Sazykina [23]. Rose noted that within
individual kingdoms there was a wide range of sensitivity to radiation. Sometimes
the response appeared beneficial rather than harmful at low radiation exposures.
• Animalia. The bulk of the literature on radiosensitivity is for mammals,

and they have been observed to be the most radiosensitive, with lethal
doses, of 6 to 10 Gy for small mammals and 1.5 to 2 5 Gy for the
largest wild and domestic animals [15]. The lowest dose rate observed
to cause death was in the range of 3 to 6 Gy/yr for several species of
rodents [16].
Protraction of the lethal dose such that it is delivered over the life
span of the organism substantially decreased its impact. UNSCEAR
[27] noted that if a mouse was given the lifetime equivalent of its lethal
dose, 7 Gy, the mean reduction of the life span was estimated to be 5%
from cancer induction. In summarizing the literature on radiation effects
for animals, Brechignac [15] noted that while there was a variation
between species, if dose rates were less than 4 Gy/yr the mortality rate
of the corresponding population would not be seriously affected.
The lowest chronic exposure to produce a detectable change in
behavior or development was about 10

2

Gy/yr (detected in planarium
worms and mud snails) [16]. For acute exposures, a dose of only 10

–6

Gy could be visually detected in cockroaches.
Reproductive capacity is more sensitive to the effects of radiation
than life expectancy [2,15,16,26–29]. The lowest chronic exposure to
produce a reliable teratogenic or genetic change (reduced birth mass
and increased brain mass of laboratory rats irradiated as fetuses) was
3

×

10

–3

Gy/yr. Acute exposures of 10

–2

Gy to pregnant rats impaired
the reflexes of their offspring. The lowest lethal dose rate was 3.6 Gy/yr
and was found for several species of American rodents. The lowest dose
rate found for detectable teratogenic or genetic effects was 3

×

10

–3

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Radionuclide Concentrations in Food and the Environment

Gy/yr. This dose rate reduced the birth mass and increased the brain
mass of laboratory rats irradiated as fetuses toward the end of the

intrauterine life. The lowest single dose to cause a teratogenic effect
was 10

–2

Gy, which impaired reflexes in the offspring of irradiated
pregnant rats [15,16].
It is important to note that while mammals have comprised the bulk
of studies, work has been done on birds, reptiles, aquatic organisms,
and invertebrates. The radiosensitivity of birds is similar to those of
small mammals. Studies on reptiles, while appearing to show them as
less radiosensitive, are being reexamined because of differences in
physiology that may not have been appropriately accounted for [15].
Invertebrates, while less sensitive, still exhibit age-specific radiosensi-
tivity, with gametogenesis, egg development, and their young being
most sensitive.
In the aquatic environment, fish are the most sensitive. Doses of 10
to 25 Gy to ocean species are lethal, although embryos are substantially
more sensitive (e.g., 0.16 Gy for salmon) [15,26]. Embryo development
in fish and the process of gametogenesis appear to be the most radi-
osensitive stages of all aquatic organisms tested [22].
• Plantae. It has been noted that the plant kingdom contains the most
radiosensitive species. The lowest acute dose, 0.8 Gy, killed a small
proportion of young Douglas fir trees (

Pseudotsuga douglasii

). Yet a
different species, eastern white pine (

Pinus strobus

), required doses of
2.7 Gy [16]. In his review of the literature, Brechignac [15] observed
that literature values of lethal radiation doses are between 10 and
1000 Gy for plants. As has been reported several times, larger plants
appear more radiosensitive than small ones. The order of radiosensi-
tivity, from greatest to least, is conifers to deciduous trees, thicket
species, herbaceous plants, lichens, and mushrooms.
The review by Rose [16] indicated that dose rates on the order of
6 Gy/yr were found to kill red pine (

Pinus resinosa

), but a 50% reduc-
tion in dose rate had no observable effect on pitch pine (

Pinus rigida

).
Nonlethal effects on plants have also been observed, as well as variable
sensitivity in plant structures. Nonlethal effects observed include inhi-
bition of growth and seed production, delay in bud opening, increased
leaf dormancy, and greater susceptibility to infestation [15]. Examples
of ranges of sensitivity include seeds (very insensitive) and apical mer-
istems (most sensitive). The data of others [15,26] is in general agree-
ment with that of Rose [16], and dose rates of approximately 4 Gy/yr
will produce only minor effects on sensitive plants and have minimal
impacts on the large majority of plants in natural communities.
The literature has provided limited data on the radiosensitivity of other organ-

isms. The data provided below are summarized from Rose [16].

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Effects of Radioactivity on Plants and Animals

219

• Protista. A dose of 100 Gy was lethal to diatoms (

Nitschi closterium

). An
acute dose of 10

6

Gy temporarily slowed the rate of growth of slime mold.
• Fungi. Doses in excess of 600 Gy have failed to kill yeasts and molds
(e.g.,

Penicillium camemberti

). Species of lichens were predicted to be
unaffected by dose rates up to 1800 Gy/yr.
•Viruses. Doses in excess of 440 Gy are required to inactive viruses.
• Monera. Doses in excess of 80 Gy are survived by blue-green algae
(

Oscillatoria limosa

); bacteria (

Bacillus cereus

) survived doses of 2000
Gy. Studies on algae colonizing a reactor primary coolant estimated
dose rates of 870 Gy/yr.

7.4 ECOLOGICAL CONSEQUENCES
OF RADIATION EXPOSURE

While studies in laboratory settings can provide insights into the radiation
responses of individual organisms, it can be difficult to extrapolate these data to
a contaminated environment where entities of concern are exposed populations,
communities, or ecosystems rather than individual members of species. Unfor-
tunately studies of radiation effects at the level of populations, communities, and
ecosystems have been limited. The few that have been done were

in situ

irradiation
experiments from enclosures of natural systems to follow the dynamics of animal
populations or in areas subjected to increased levels from accidental or intentional
radioactive contamination [10,15,16]. Most of these studies lack sufficient rigor to
support strong statements as to effect [15]. One extraordinary example is found at
Chernobyl. Although severe impacts to biota occurred as a consequence of the reactor
accident, a net ecological improvement has been measured. This is attributed to the
removal of a more radiosensitive species (humans) from the environment [7,26].

In an effort to understand radiation effects on a broad scope, Polikarpov [10]
developed a conceptual model that sought to address the issue of chronic exposure,
across all levels of organization. He related specific ranges of dose rates with
resultant impacts using a model that spanned 12 orders of magnitude from less
than 10

–5

to greater than 10

6

Gy/yr. This model contained five zones of exposure
which summarized radiation effects on cells/organisms, populations, and biotic
communities [10,28]. The lowest, zone 1 (less than 1

×

10

–5

to 4

×

10

–5

Gy/yr),
was identified as the zone of biological uncertainty. The dose rate for this zone was
below the natural background rate from cosmic radiation. The second, zone 2
(4

×

10

–5

to 5

×

10

–3

Gy/yr), was labeled the natural background, or the zone of
well-being. Zone 3 (5

×

10

–2

to 5

×

10

–3
Gy/yr) was classified as a region where
masking of the physiological effects of radiation exposure occurs, as the dose
rates can overlap with those of natural background. In zone 4 (4 × 10
0
to 5 × 10
–2
Gy/yr), there are effects on individuals, but these are masked by the interactions
with the population and community. Finally, in zone 5 (4 × 10
0
to greater than
3 × 10
3
Gy/yr), the consequences are catastrophic to ecosystems because the
damage to the underlying populations and communities is severe. Polikarpov also
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© 2007 by Taylor & Francis Group, LLC
220 Radionuclide Concentrations in Food and the Environment
provided examples of environments that delivered dose rates corresponding to
these zones. The zones proposed by Polikarpov appear to be supported by the
current and past literature on radiological effects [10,15,16,23,28]. A comparison
of the model of Polikarpov [10] with data from Rose [16] and Sazykina [23] is
provided in Table 7.1.
It is relatively straightforward to identify ranges of exposure and potential
effects. The difficulty arises in trying to measure them, either in the field or in a
laboratory setting, and then interpret them with regard to an organism’s radiosen-

sitivity. The radiation field generated by a source is rarely uniform — either
spatially or temporally. This makes an accurate determination of dose problem-
atic. Several individuals are working on molecular probes in an effort to address
this problem [7,25,29,30]. The utility of such tools is obvious, but their ability
to link microscale measurements to ecosystem level impacts has not yet been
demonstrated [7,25,29–31].
Also, until recently there were only a limited number of studies published in
the Western literature that examined the responses of plant and animal populations
to radiation exposure in their natural environments [15,23]. Instead, the bulk of
the research has emphasized individual over population responses. Because of
the ease and immediacy of information retrieval, mortality rather than reproduc-
tion was assessed. Similarly, acute rather than chronic doses were given. Due to
technical considerations surrounding the delivery of doses, external γ irradiation
rather than internal contamination studies were favored. All of these factors have
contributed to an incomplete understanding of the consequences of low-level
radiation exposure in natural settings [11,25,27,32].
In the last 15 years, acute and chronic radiation effects data have been
reviewed by several organizations [16,21,22,33]. Based on their reviews, the
National Council on Radiation Protection and Measurements (NCRP) [33] iden-
tified an expected safe level of exposure of approximately 4 Gy/yr (10 mGy/day)
for populations of aquatic animals. Shortly thereafter the IAEA [22] identified
an expected safe level of exposure of approximately 4 Gy/yr (10 mGy/day) for
populations of terrestrial plants and an expected safe level of exposure of approx-
imately 0.4 Gy/yr (1 mGy/day) for populations of terrestrial animals. At the time,
these levels of exposure were selected based on the understanding that the pop-
ulation would be adequately protected if the dose rate to the maximally exposed
individual did not exceed that level of exposure [22,33]. The radiological data
suggest that approximately 0.4 Gy/yr represents a threshold for effects, however, the
data are sparse for nonmammals, particularly with respect to ecosystem level effects.
It is also important to note that the previously proposed safe levels of exposure

have largely been derived from observed dose-response relationships for deter-
ministic effects. This has led to some concern that stochastic radiation effects,
which might be important in the protection of biota, are not being adequately
considered [7,34]. Information on stochastic effects in biota was considered in
the 1996 UNSCEAR report on the effects of radiation on the environment [21],
which concluded that as long as the dose was kept below the expected safe levels
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© 2007 by Taylor & Francis Group, LLC
Effects of Radioactivity on Plants and Animals 221
TABLE 7.1
A Comparison of Dose-Effects Relationships Found in the Literature
Dose Rate, Gy/yr Polikarpov [10] Rose [16] Sazykina [23]
<1 × 10
5
Uncertainty
Natural background
4
× 10
5
Well-being
4 × 10
4
3 × 10
3
Teratogenic effects
(Animalia)
4
× 10
3
No data

5 × 10
3
Physiologic
masking
1 × 10
2
Developmental
(Animalia)
2 × 10
2
Behavioral
(Animalia)
4 × 10
2
Minor cytogenetic effects,
stimulation of vertebrate
species
5 × 10
2
Ecological
masking
2 × 10
1
Threshold for minor effects
on morbidity in vertebrates
4 × 10
1
Teratogenic
(Plantae)
7 × 10

1
Threshold for reproductive
effects on vertebrates
2 × 10
0
Threshold for life shortening
of vertebrates, threshold for
invertebrates and plants
3 × 10
0
Lethality (Animalia)
4 × 10
0
Obvious effects
Life shortening of
vertebrates; damage to
conifers
6 × 10
0
Lethality (Plantae)
4 × 10
1
Acute radiation sickness of
vertebrates, death of conifers,
damage to invertebrate young
4 × 10
2
8.7 × 10
2
Lethality (Monera) Acute radiation sickness of

vertebrates, increased
mortality of invertebrate
young; damage to deciduous
plants
3 × 10
3
Lethality (Fungi)
5.3 × 10
3
Teratogenic
(Monera)
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© 2007 by Taylor & Francis Group, LLC
222 Radionuclide Concentrations in Food and the Environment
of exposure based on reproductive effects, stochastic effects should not be sig-
nificant at a population level.
The available stochastic effects data are difficult to interpret in regard to harm
to an individual organism [21,22,33,34]. The expected safe levels of exposure
were based on the dose–response relationships for reproductive effects, rather
than all effects that might be important for the viability of any given individual
organism in a population (e.g., early mortality). Thus the levels of exposure
expected to protect the viability of natural populations may not be protective for
individual members of a species. The implication was, however, that although a
few individuals could be damaged, the population would remain viable
[21,22,33].
7.5 CONCLUSION
Research on radiation effects on living systems spans more than half a century.
It is well known that a range of more than four orders of magnitude exists in
radiosensitivity among taxonomic groups, largely from differences in cellular and
molecular characteristics [2,3,10,15,16,27,35]. Consequently discussions of radi-

ation effects on plants and animals must take place within the context of the
circumstances of exposure. As with humans, plants and animals can exhibit acute
and chronic responses to ionizing radiation. Effects which can be documented at
the cellular level may not transfer to observable impacts at the organism or
ecosystem level. Studies on acute exposure of individuals may provide only
limited insight into effects at the ecosystem level from chronic exposures. Current
research is under way to try and link the data produced by molecular probes to
impacts on organisms and populations. There are sufficient new data to help fill
in many of the gaps in knowledge on the effects of chronic exposures
[15,16,23,24]. While remaining in general agreement with past research, some
differences have been found that can be attributed to environmental conditions
of exposure [23].
Finally, at a very broad level, the preponderance of data suggest that the
lowest dose rate at which deterministic effects of chronic irradiation would be
expected from low-LET radiation are in the range of 0.4 to 1 Gy/yr. The lowest
dose at which effects of acute irradiation might be observed is 0.01 Gy. It is
important to note, however, that the complexity of the environment is such that
adverse impacts might not be observed at considerably higher doses and dose
rates.
REFERENCES
1 Muller, H.J., Artificial transmutation of the gene, Science, 66, 84, 1927.
2. Whicker, F.W. and Schultz, V., Radioecology: Nuclear Energy and the Environ-
ment, CRC Press, Boca Raton, FL, 1982.
DK594X_book.fm Page 222 Tuesday, June 6, 2006 9:53 AM
© 2007 by Taylor & Francis Group, LLC
Effects of Radioactivity on Plants and Animals 223
3. Hall, E.J., Radiobiology for the Radiologist, 4th edition, J.B. Lippincott, Phila-
delphia, 1994.
4. Turner, J.E., Atoms, Radiation, and Radiation Protection, 2nd edition, Wiley-
Interscience, New York, 1995.

5. Streffer, C., Bolt, H., Follesdal, D., Hall, P., Hengstler, J.G., Jakob, P., Oughton,
D., Prieß, K., Rehbinder, E., and Swaton, E., Low Dose Exposures in the Envi-
ronment, Dose-Effect Relations and Risk Evaluation, Springer, New York, 2004.
6. Florou, H., Tsytsugina, V., Polikarpov, G.G, Trabidou, G., Gorbenko, V., and
Chaloulou, C.H., Field observations of the effects of protracted low levels of
ionizing radiation on natural aquatic population by using a cytogenetic tool,
J Environ. Radioactiv., 75, 267, 2004.
7. Hinton, T.G., Bedford, J.S., Congdon, J.C., and Whicker, F.W., Effects of radiation
on the environment: a need to question old paradigms and enhance collaboration
among radiation biologists and radiation ecologists, Radiat. Res., 162, 332, 2004.
8. Jackson, D., Copplestone, D., Stone, D.M., and Smith, G.M., Terrestrial inverte-
brate population studies in the Chernobyl exclusion zone, Ukraine, Radioprotec-
tion, 40, S857, 2005.
9. Hingston, J.L., Wood, M.D., Copplestone, D., and Zinger, I., Impact of chronic
low-level ionising radiation exposure on terrestrial invertebrates, Radioprotection,
40, S145, 2005.
10. Polikarpov G.G., Conceptual model of responses of organisms, populations and
ecosystems to all possible dose rates of ionising radiation in the environment,
Radiat. Protect. Dosim., 75, 181, 1998.
11. United Nations Scientific Committee on the Effects of Atomic Radiation, Scientific
Committee on the Effects of Atomic Radiation, Report to the General Assembly,
with 10 Scientific Annexes. United Nations, New York, 2000.
12. Kocher, D.C. and Trabalka, J.R., On the application of a radiation weighting factor
for alpha particles in protection of non-human biota, Health Phys., 79, 407, 2000.
13. International Commission on Radiological Protection, RBE for Deterministic
Effects, Publication 58, Pergamon Press, Oxford, 1989.
14. International Commission on Radiation Units and Measurements, Microdosimetry,
Report 36, International Commission on Radiation Units and Measurements,
Bethesda, MD, 1993.
15. Brechignac, F., Impact of radioactivity on the environment: problems, state of

current knowledge and approaches for identification of radioprotection criteria,
Radioprotection, 36, 511, 2001.
16. Rose, K.S.B., Lower limits of radiosensitivity in organisms, excluding man,
J. Environ. Radioactiv., 15, 113, 1992.
17. Little, J.B., Radiation-induced genomic instability, J. Radiat. Biol., 74, 663, 1998.
18. Little, J.B., Radiation carcinogenesis, Carcinogenesis, 21, 397, 2000.
19. Lorimore, S.A., Coates, P.J., and Wright, E.G., Radiation-induced genomic insta-
bility and bystander effects: inter-related nontargeted effects of exposure to ion-
izing radiation, Oncogene, 22, 7058, 2003.
20. Feinendegen, L.E., Evidence for beneficial low level radiation effects and radiation
hormesis, UKRC 2004 debate, Br. J. Radiol., 78, 3, 2005.
21. United Nations Scientific Committee on the Effects of Atomic Radiation, Effects
of Radiation on the Environment, Report to the General Assembly, United Nations,
New York, 1996.
DK594X_book.fm Page 223 Tuesday, June 6, 2006 9:53 AM
© 2007 by Taylor & Francis Group, LLC
224 Radionuclide Concentrations in Food and the Environment
22. International Atomic Energy Agency, Effects of Ionizing Radiation on Plants and
Animals at Levels Implied by Current Radiation Protection Standards, Technical
Report Series no. 332, International Atomic Energy Agency, Vienna, 1992.
23. Sazykina, T.G., A system of dose-effects relationships for the northern wildlife:
radiation protection criteria, Radioprotection, 40, S889, 2005.
24. Copplestone, D., Howard, B.J., and Brechignac, F., The ecological relevance of
current approaches for environmental protection from exposure to ionising radi-
ation, J. Environ. Radioactiv., 74, 31, 2004.
25. Hinton, T.G, Coughlin, D.P., Yi, Y., and Marsh, L.C., Low dose rate irradiation
facility: initial study on chronic exposures to medaka, J. Environ. Radioactiv., 74,
43, 2004.
26. Baker, R.J., The Chernobyl nuclear disaster and subsequent creation of a wildlife
preserve, Environ. Toxicol. Chem., 19, 1231, 2000.

27. United Nations Scientific Committee on the Effects of Atomic Radiation, Ionizing
Radiation: Sources and Biological Effects, Report to the General Assembly with
annexes, United Nations, New York, 1982.
28. Kuz’menko, M.I. and Polikarpov, G.G., Radioecology of natural waters at the turn
of the millennia, Hydrobiol. J., 38, 13, 2002,
29. Ulsh, B.A., Miller, S.M., Mallory, F.F., Mitchel, R.E.J., Morrison, D.P., and Bore-
ham, D.R., Cytogenetic dose-response and adaptive response in cells of ungulate
species exposed to ionizing radiation, J. Environ. Radioactiv., 74, 73, 2004.
30. Wickliffe, J.K., Chesser, R.K., Rodgers, B.E., and Baker, R.J., Assessing the
genotoxicity of chronic environmental irradiation by using mitochondrial DNA
heteroplasmy in the bank vole (Clethrionomys glareolus) at Chernobyl, Ukraine,
Environ. Toxicol. Chem., 21,1249, 2002.
31. Suter, G.W. II, Efroymson, R.A., Sample, B.E., and Jones, D.S., Ecological Risk
Assessment for Contaminated Sites, Lewis, Boca Raton, FL, 2000.
32. Smith, J.T., The case against protecting the environment from ionising radiation,
Radioprotection, 40, S967, 2005.
33. National Council on Radiation Protection and Measurements, Effects of Ionizing
Radiation on Aquatic Organisms, Report no. 109, National Council on Radiation
Protection and Measurements, Bethesda, MD, 1991.
34. International Commission on Radiological Protection, A Framework for Assessing
the Impact of Ionizing Radiation on Non-Human Species, Publication 91, Perga-
mon Press, Oxford, 2003.
35. Woodwell, G.M., Effects of ionizing radiation on terrestrial ecosystems, Science,
138, 572, 1962.
DK594X_book.fm Page 224 Tuesday, June 6, 2006 9:53 AM
© 2007 by Taylor & Francis Group, LLC