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


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


A

SPECTS
OF

I

ONIZINGR

ADIATION

I

NTERACTIONS

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

α

and

β


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


*
→

H

2

O

+

+ e
or
H

2

O

*
→

H + OH.

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


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


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


).
• 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

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

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


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-

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


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 (


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
(


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


×

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-

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

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

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.
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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-
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22. International Atomic Energy Agency, Effects of Ionizing Radiation on Plants and
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