Journal of Environmental Radioactivity 102 (2011) 473e478
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Journal of Environmental Radioactivity
journal homepage: www.elsevier.com/locate/jenvrad
Radionuclides in marine mammals off the Portuguese coast
Margarida Malta, Fernando P. Carvalho*
Instituto Tecnológico e Nuclear, Departamento de Protecção Radiológica e Segurança Nuclear, E.N. 10, 2686-953 Sacavém, Portugal
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 18 June 2010
Received in revised form
21 February 2011
Accepted 7 March 2011
Available online 14 April 2011
Radionuclide analyses were performed in tissue samples including muscle, gonad, liver, mammary gland,
and bone of marine mammals stranded on the Portuguese west coast during JanuaryeJuly 2006. Tissues
were collected from seven dolphins (Delphinus delphis and Stenella coeruleoalba) and one pilot whale
(Globicephala sp.). Samples were analyzed for 210Po and 210Pb by alpha spectrometry and for 137Cs and 40K
by gamma spectrometry. Po-210 concentrations in common dolphin’s muscle (D. delphis) averaged
56 32 Bq kg 1 wet weight (w.w.), while 210Pb averaged 0.17 0.07 Bq kg 1 w.w., 137Cs averaged
0.29 0.28 Bq kg 1 w.w., and 40K 129 48 Bq kg 1 w.w. Absorbed radiation doses due to these
radionuclides for the internal organs of common dolphins were computed and attained a 1.50 mGy h 1 on
a whole body basis. 210Po was the main contributor to the weighted absorbed dose, accounting for 97% of
the dose from internally accumulated radionuclides. These computed radiation doses in dolphins are
compared to radiation doses from 210Po and other radionuclides reported for human tissues. Due to the
high 210Po activity concentration in dolphins, the internal radiation dose in these marine mammals is
about three orders of magnitude higher than in man.
Ó 2011 Elsevier Ltd. All rights reserved.
Keywords:
Marine mammals
Polonium-210
Lead-210
Potassium-40
Caesium-137
radiation dose
1. Introduction
Previously, it was assumed that when human beings are protected against the harmful effects of ionizing radiation the
remaining biological species would be protected as well (ICRP 1971,
1991). However, this line of thought has been questioned (Pentreath
and Woodhead, 2001; Bréchignac, 2003). Recent developments in
the field of radiation protection now regard the environment as
a system that must be protected on its own merits (NEA/OECD,
2002; ICRP, 2008). This viewpoint requires the risk assessment to
be performed for non-human biota when subject to ionizing radiation exposure. Several collaborative projects have been implemented with the objective of developing relevant methodologies,
namely to set up criteria and methodologies for use in the assessment of biological and ecological effects following exposure of biota
to ionizing radiation. Amongst these projects one may highlight, for
example, the European Union FASSET project (Framework for
Assessment of Environmental Impact) (Brown et al., 2003a).
In general, marine mammals are at the top of marine food chains,
and dolphins in particular are top predators consuming common
coastal fish species (Culik, 2004). Contrasting to fish and other
marine organisms, marine mammals do not absorb radionuclides
directly from sea water and most of the internally accumulated
radionuclides are ingested with the diet (Brown et al., 2005; Gwynn
* Corresponding author. Tel.: þ351 21 9946332; fax: þ351 21 9941995.
E-mail address: carvalho@itn.pt (F.P. Carvalho).
0265-931X/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jenvrad.2011.03.004
et al., 2006). Furthermore, radiosensitivity of marine mammals may
be comparable to terrestrial mammals and, thus, the knowledge on
radionuclide absorption into internal organs may be used as a proxy
for radionuclide accumulation and effects in other mammals
including man (Bréchignac, 2003). Notwithstanding, the database
on radionuclide accumulation in marine mammals is scarcer than
for other marine biota (Brown et al., 2004; Carvalho, 2010; Holm
et al., 2005).
Radionuclides currently present in the marine environment are
both naturally-occurring and of anthropogenic origin. Previous
research in assessing the accumulation of radionuclides in marine
biota, concluded that amongst the natural radionuclides the alpha
emitter polonium-210 (210Po; T1/2 ¼ 138.4 d), generally gives the
largest contribution to the internal radiation dose received by those
organisms (Carvalho, 1988; Carvalho and Oliveira, 2008; Cherry and
Heyraud, 1982) and by consumers of sea food including humans
(Aarkrog et al., 1997; Carvalho, 1995; Livingston and Povinec, 2000;
Yamamoto et al., 2009). Lead-210 (210Pb; T1/2 ¼ 22.3 y), grand parent
of 210Po, is a weak energy beta-gamma emitter but its distribution
influences the biogeochemistry of 210Po in the oceans, and it is also
largely accumulated by marine organisms and man (Carvalho, 1995;
Cherry and Shannon, 1974; Parfenov, 1974; UNSCEAR, 1982). For
these reasons, it is of great interest to investigate further those
radionuclides and radiation dose distributions in internal organs
and tissues in mammals, including marine species.
Anthropogenic radionuclides, such as tritium, plutonium, americium, and caesium, are present in the world ocean and mainly
474
M. Malta, F.P. Carvalho / Journal of Environmental Radioactivity 102 (2011) 473e478
originated in fallout from nuclear weapons tests, waste discharges
from spent nuclear fuel reprocessing activities, and nuclear accidents such as the Chernobyl accident. Amongst the radionuclides of
anthropogenic origin, caesium-137 (137Cs; T1/2 ¼ 30.07 y) is the
main contributor to the absorbed radiation dose both to marine
organisms and to man, especially in the muscle tissue (Livingston
and Povinec, 2000; Carvalho and Oliveira, 2008). Potassium-40
(40K; T1/2 ¼ 1.27 109 y), a long lived primordial radionuclide
present in the sea water and in all marine organisms, is fairly
abundant and accounts for about 18 Bq L 1 in sea water (Brown
et al., 2004). However, in the internal tissues of living organisms
the potassium element is maintained in constant concentration
and, thus, the absorbed radiation dose from the 40K radioactive
isotope is stable (UNSCEAR, 1982). Other radionuclides are not
subjected to metabolic regulation and their activity concentrations
in biota depend upon sea water concentrations and food chain
transfer and, thus, their contributions to radiation doses may vary.
Tissue samples from marine mammals stranded ashore at the
Portuguese coast were analysed for determining radionuclide
activity concentrations and for assessing radiation doses due to
internally accumulated radionuclides. This paper gives an account
on current radioactive concentrations in internal tissues of several
marine mammal species and compares them with concentrations
reported for marine mammals in other regions, and for man.
2. Materials and methods
Marine mammal corpses found ashore are usually communicated to maritime authorities for recording the occurrence and
removal of corpses from the beaches. Samples from marine
mammals stranded on the west coast of Portugal during the first
half of 2006 were obtained through collaboration with the Institute
for Nature Conservation (ICN, Portugal) and Câmara Municipal de
Alcobaça. As the knowledge of the time of death is important for
radioactive decay correction of the activity determined, especially
for 210Po, mammal corpses sampled were only those clearly fresh or
with minimal tissue decomposition. This effect was minimized as
much as possible through consulting with veterinary expertise
assisting the project. In the assessment of radionuclide accumulation in marine mammals it is important to take also into consideration that radionuclide concentrations may vary with the age,
sex, feeding location, and diet composition. However, the availability of samples of these protected marine mammals was limited
to the stranded specimens and not all those factors could be
addressed in this research.
After species identification and biometric data recording, tissue
samples were collected by a veterinarian into jars and transported
on ice to the laboratory. Tissues samples of eight specimens of
marine mammals, namely six common dolphins Delphinus delphis,
one striped dolphin Stenella coeruleoalba, and one pilot whale
Globicephala sp., were analyzed.
Weighted amounts of tissues were frozen, lyophilized and
homogenized. Aliquots of the homogenized powder were used
for triple determination of 210Po and 210Pb following methods
described earlier (Carvalho, 1995; Carvalho and Oliveira, 2007;
Carvalho et al., 2011). In brief, to the weighted sample aliquot
a known activity of 209Po (T1/2 ¼ 102 y) was added to be used as
internal isotopic tracer, to allow for determining the radiochemical
yield of the analytical procedure. The sample was than completely
dissolved in mineral acids (HNO3 and HCl) and H2O2. Polonium was
spontaneously deposited onto a silver disc from a 0.5 M HCl solution in the presence of 500 mg ascorbic acid. The alpha particle
emission from the disc surface was measured with an alpha spectrometer OctectePlus (Ortec EG&G) equipped with 450 mm2
surface barrier silicon detectors. After this first polonium plating
the sample solution was stored for about 6 months and then, after
the addition of a new 209Po spike, evaporated to dryness and the
residue dissolved in 0.5 M HCl solution. A second polonium deposition onto a new disc was made, allowing the determination of
210
Pb through the in growth of 210Po. The alpha particle emission
was measured for the new disc. Radionuclide activities were
computed and decay corrected using the Bateman equations and
210
Po and 210Pb activities referred to the day of the mammal
stranding on the beach. Results for the triplicate aliquots were
averaged.
Aliquots of the homogenate powder tissue samples, of approximately 10 g dry weight each, were compacted in Millipore air tight
Plexiglas Petri dishes and measured for gamma emitting radionuclides. Determinations of 137Cs and 40K were performed using the
gamma peak energies of 661.66 keV and 1460.82 keV, respectively.
Gamma spectrometry was performed in HpGe detectors for
a period of 24 h. Gamma spectra were analyzed with Genie2000Ò
software from Canberra and screened for the presence of other
artificial gamma emitters.
The Quality Assurance of analytical determinations was performed through using IAEA certified reference materials (e.g., IAEA134 cockle flesh) and participating in international intercomparison
exercises, such as those with IAEA-414 (fish muscle) and (IAEA-384
marine sediment) with good results (Pham et al., 2006; Povinec et al.,
2007). For gamma measurements the radionuclide activity concentrations reported are given with the 1 sigma (1s) confidence level
propagated uncertainty. For 210Po and 210Pb determinations, the
average activity concentrations determined are given with the one
standard deviation of the mean. All reagents used were of analytical
grade and analytical blanks were run with internal isotopic 209Po
tracer, as for the samples. The radionuclide concentrations are
expressed in Bq kg 1 wet weight. The dry:wet weight ratios (D:W)
are shown in the tables to enable unit conversion.
Table 1
Polonium (210Po) activity concentrations in tissues of marine mammals off the Portuguese coast (Bq kg
D:W Common
ratios dolphin #1
Sex
Body length
(cm)
Dorsal muscle
Mammary
gland
Liver
Fat tissue
Gonad
Kidney
Bone
1
1 SD, wet weight).
Common
dolphin #2
Common
dolphin #3
Common
dolphin #4
Common
dolphin #6
Common
dolphin #8
Striped
dolphin #5
Pilot
whale #7
Average for
common dolphins
Female
197
Male
168
Female
208
Male
180
Undetermined Undetermined Undetermined
n.c.
170
n.c.
177 24 (n ¼ 5)
e
e
Female
140
0.31
0.24
9.08 0.13 79.87 1.58 81.67 1.94 87.17 1.87
n.c.
29.48 0.88 n.c.
n.c
42.49 1.51
n.c
34.24 0.79
8.19 0.21
42.01 0.78
n.c.
13.69 0.27
n.c.
56 32 (n ¼ 6)
19 15 (n ¼ 2)
0.25
0.64
0.22
0.22
0.47
n.c.
n.c.
n.c.
n.c.
n.c.
74.97 1.91
22.01 0.92
9.28 0.30
104.58 2.66
n.c
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
0.70 0.06
n.c.
n.c.
n.c.
123 42 (n ¼ 3)
11 11 (n ¼ 4)
11 2 (n ¼ 4)
110 49 (n ¼ 3)
4.63 0.12 (n ¼ 1)
143.03
19.17
12.01
161.40
4.63
3.03
0.46
0.17
2.23
0.12
n.c.
2.71 0.12
13.30 0.31
n.c.
n.c.
151.33 2.98
1.41 0.11
8.92 0.24
63.02 1.32
n.c.
D:W, dry:wet weight ratio; n.c., not collected. Common dolphin, Delphinus delphis. Striped dolphin, Stenella coeruleoalba. Pilot whale, Globicephala sp.
M. Malta, F.P. Carvalho / Journal of Environmental Radioactivity 102 (2011) 473e478
6
A
X
fi Ei yi
i
Where:
_ e Dose rate (Gy h 1);
D
DCF e Dose conversion factors (mGy h 1 per Bq kg 1). Low
energy (<10 keV) beta doses are weighted by a radiation quality
factor Qb ¼ 3; alpha doses are weighted by a radiation quality factor
Qa ¼ 10.
A e Radionuclide concentration (Bq kg 1, wet weight);
Ei e Energy of “i” in gamma radiation;
yi e Ei energy photons emission rate;
4i e Absorbed fraction for Ei energy.
Units of computed absorbed radiation doses, weighed with
radiation quality factors, are given below in mGy h 1, according to
the criteria that the dose equivalent concept and conversion to
mSv h 1 developed for humans may be not applicable to biota
(Brown et al., 2003b).
3. Results and discussion
Table 1 and Table 2 show respectively the 210Po and 210Pb
activity concentrations determined in the tissues of six common
dolphins (D. delphis), one striped dolphin (S. coeruleoalba) and one
pilot whale (Globicephala sp.). Results for the six common dolphin
specimens were averaged. In the dolphins, 210Po averaged activity
concentrations were higher in the liver and kidneys, often above
100 Bq kg 1, and up to a maximum value of 161.4 2.2 Bq kg 1 in
the kidney. These concentrations were followed by those in the
dorsal muscle tissue, averaging 56 32 Bq kg 1 (n ¼ 6), and the
lowest 210Po concentration being in the bone, 4.63 0.12 Bq kg 1
(n ¼ 1) (Table 1).
In all tissues 210Pb activity concentrations were generally below
1 Bq kg 1, with the exception of the bone (Table 2). Amongst soft
tissues slightly higher 210Pb activity concentrations were measured
in the liver and kidneys, averaging respectively 0.47 0.12 Bq kg 1
(n ¼ 3) and 0.23 0.11 Bq kg 1 (n ¼ 3), and then in muscle averaging
0.17 0.07 Bq kg 1 (n ¼ 6). Pb-210 activity concentration was higher
in the bone, 3.60 0.12 Bq kg 1 (n ¼ 1), owing to the preferential
fixation of 210Pb in the calcified bone structure as documented in the
literature (Cherry et al., 1994; UNSCEAR, 1982) (Table 2). Po-210 and
210
Pb activity concentrations in the mammary gland were in the
range of concentrations measured in other internal tissues and
nearly comparable to the gonad (Tables 1e3).
In the tissues analyzed, the 210Po activity concentrations were
systematically higher than those of 210Pb. High Po/Pb ratios are
concentration
(Bq kg-1 wet weight)
_ ¼ DCF A ¼ 5:04 10
D
120
210Po activity
The absorbed radiation doses originated by the radioactive
decay of 210Po, 210Pb, 40K and 137Cs, were computed, assuming that
these radionuclides are uniformly distributed in the tissue and
using radiation quality weighting factors (Golikov and Brown,
2003), through using the equation
100
#4
#3
80
#2
60
#5
40
#6
y = 1.0471x - 128.43
R² = 0.6596
20
#1
0
120
140
160
180
200
220
240
Body length (cm)
Fig. 1. Correlation between 210Po activity concentration in muscle tissue and body
length of dolphins. Sample numbers as in Table 1.
a consequence of the preferential 210Po absorption through gut
walls comparatively to 210Pb, followed by 210Po accumulation in the
internal organs of marine organisms (Carvalho and Fowler, 1993,
1994) and in man (Hunt and Allington, 1993).
Results for the pilot whale and striped dolphin were treated
separately because of the different biology and ecology of these
species. However, radionuclide concentrations were not very
different and fell in the range of values for dolphins (Tables 1 and 2).
Activity concentrations of 210Po in the muscle tissue were very
similar in dolphins #2, 3 and 4 (Table 1). However, specimens #1, 5
and 6 displayed lower concentrations which could be a consequence of the more advanced decomposition of corpses of these
two specimens. Post-mortem decomposition leads to tissue dehydration and destruction of amino acid chains in proteins, followed
by cellular destruction. Due to the substitution of sulphur compound radicals (eSH) by 210Po in amino acids (Durand et al., 1999),
decomposition may result in physical loss of 210Po atoms. This fact
supports the idea that the state of the body conservation could be
extremely important to the 210Po activity concentration determined in the organs. Nevertheless, the post-mortem elapsed time
apparently didn’t affect the 210Pb concentration. Notwithstanding
the activity differences in muscle tissue, 210Po concentrations were
similar in the liver of all specimens. 210Po concentrations in the
gonad were similar amongst specimens as well, although not all of
them did belong to the same gender (Table 1).
As amongst internal tissues the muscle contributes with the
largest fraction (64%) to the whole dolphin body weight (Dubois et al.,
1948), that tissue is also the main reservoir of 210Po radionuclide in
dolphins, contributing to 41 Bq kg 1 on a whole body weight basis. A
plot of 210Po concentration in muscle tissue against animal body
length, demonstrated that there is a positive correlation (R2 ¼ 0.66)
with a statistically significant association (ManneWhitney test,
p < 0.05) between 210Po concentration and body length, and thus
Table 2
Radioactive lead (210Pb) activity concentrations in tissues of marine mammals off the Portuguese coast (Bq kg
Dorsal muscle
Mammary gland
Liver
Fat tissue
Gonad
Kidney
Bone
475
1
1 SD, wet weight).
D:W
Ratios
Common
dolphin #1
Common
dolphin #2
Common
dolphin #3
Common
dolphin #4
Common
dolphin #6
Common
dolphin #8
Striped
dolphin #5
Pilot whale #7
Average for
common dolphins
0.31
0.24
0.25
0.64
0.22
0.22
0.47
0.12 0.01
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
0.15
0.47
0.54
0.20
0.15
0.34
3.60
0.18 0.01
n.c.
n.c.
0.26 0.02
0.34 0.02
n.c.
n.c.
0.08
n.c
0.34
0.11
0.04
0.13
n.c.
0.30
n.c
0.54
0.28
0.11
0.21
n.c.
0.16 0.02
0.13 0.01
n.c.
n.c.
n.c.
n.c.
n.c.
0.16 0.01
n.c.
n.c.
n.c.
n.c.
n.c.
n.c.
0.18 0.01
n.c.
n.c.
0.17 0.02
n.c.
n.c.
n.c.
0.17
0.30
0.47
0.20
0.16
0.23
3.60
0.02
0.06
0.03
0.02
0.01
0.01
0.12
0.01
0.04
0.02
0.01
0.01
0.04
0.04
0.04
0.01
0.08
D:W, dry:wet weight ratio; n.c., not collected. Common dolphin, Delphinus delphis. Striped dolphin, Stenella coeruleoalba. Pilot whale, Globicephala sp.
0.07
0.24
0.12
0.07
0.13
0.11
0.12
(n
(n
(n
(n
(n
(n
(n
¼
¼
¼
¼
¼
¼
¼
6)
2)
3)
4)
4)
3)
1)
476
M. Malta, F.P. Carvalho / Journal of Environmental Radioactivity 102 (2011) 473e478
Table 3
Polonium (210Po) activity concentrations (Bq kg
Cherry et al. (1994)
Folsom et al. (1974)
Carvalho et al. (2007)
Peniche
Portuguese west coast
Cape Town
South Africa
San Diego
California, USA
Azores Islands
Portugal
a
Common dolphin
Dorsal muscle
Mammary gland
Liver
Fat tissue
Gonad
Kidney
Bone
56 32 (9.08e87.2)
19 15 (8.19e29.5)
123 42 (75e151.3)
11 11 (1.4e22.0)
11 2 (8.92e13.3)
110 49 (105e161)
4.63 0.12
a
c
d
e
f
e
e
e
e
e
e
1 SD, wet weight) in tissues of marine mammals from several regions.
This study
Species
b
1
Striped dolphin
42.01 0.78
e
e
e
e
e
e
b
Pilot whale
c
13.69 0.27
e
e
0.7 0.06
e
e
e
Dolphin
d
83 2.4
e
124 4
e
4.7 0.3
136 4.6
26 0.5
#1
Dolphin
d
#2
Whale
80 1.8
e
124 2
7.23 0.7
3.9 .3
242 2.8
e
e
Dolphin
3.7 0.1
e
72 1
e
8.3 0.4
196 4
5.4 0.4
d
94.5 (78e111)
e
e
e
e
e
e
Sperm whale
f
5.0
e
e
e
e
e
e
Average and range of values shown in Table 1 (Delphinus delphis).
Stenella coeruleoalba.
Globicephala sp.
Delphinus delphis.
Hyperoodon planifrons.
Physeter catodon.
with age (Fig.1). Pb-210 concentration was higher in the dolphin bone
and as the bone contributes to 3.61% of body weight, it is still the
largest 210Pb reservoir in dolphins, even larger than the 210Pb muscle
reservoir, and averaging 0.13 Bq kg 1 whole body weight basis.
K-40 activity concentration in the muscle tissue of the six
common dolphins ranged from 75 to 218 Bq kg 1, averaging
129 48 Bq kg 1 (Table 4). Cs-137 was detected in the muscle
tissue of 5 out of 8 mammal specimens. In the 6 common dolphins
137
Cs was detected in 4 specimens, and concentrations ranged from
<0.06 to 0.81 Bq kg 1 and averaged 0.29 0.28 Bq kg 1. Cs-137 and
40
K in the muscle tissue and in the liver of several marine mammals
reported in the literature are compared with results for dolphins
(D. delphis and S. coeruleoalba) and pilot whale (Globicephala sp) in
Table 4. Concentrations of 40K were very similar in these marine
mammals, but 137Cs seemed slightly higher in mammals from the
coast of United Kingdom than in those off the Portuguese coast,
which is a trend related probably to past coastal discharges of
radioactive liquid wastes in UK and currently higher 137Cs levels in
UK coastal seas than in other European seas (RIFE-14, 2009).
Po-210 activity concentrations in mammals were of the same
order of magnitude as those of 40K, but since 210Po is a pure alpha
emitter it was expectedly more relevant to the absorbed radiation
dose than 40K (beta-gamma emitter) due to the higher alpha
radiation quality factor (Qa ¼ 10, Qb ¼ 3). Furthermore, 210Pb and
137
Cs contributions to the absorbed dose were much smaller than
that of 40K because of lower concentrations of those radionuclides
in comparison with 40K. Table 5 shows the radionuclide activity
concentrations in tissues, the weighted absorbed dose computed
for each radionuclide on a whole body basis, and the sum of their
contributions to the whole body absorbed dose. Considering these
internal radiation sources, computed whole body weighted
Table 4
Average activity concentrations of
137
Cs and
40
K (Bq kg
1
1 SD, wet weight) and range of values in liver and muscle of marine mammals of the Northeast Atlantic.
Species
Tissue
Local
Delphinus delphis (This work)
Stenella coeruleoalba (This work)
Globicephala sp. (This work)
Delphinus delphis (Yoshitome et al., 2003)
Stenella longirostris (Yoshitome et al., 2003)
Stenella attenuata (Yoshitome et al., 2003)
Phocoena phocoena (Watson et al., 1999)
Phocoena phocoena (Watson et al., 1999)
Delphinus delphis (This work)
Phocoena phocoena (Watson et al., 1999)
Muscle
Muscle
Muscle
Muscle
Muscle
Muscle
Muscle
Muscle
Liver
Liver
Peniche, Portuguese
Peniche, Portuguese
Peniche, Portuguese
Pacific Ocean
Pacific Ocean
Pacific Ocean
UK coast
Ireland coast
Peniche, Portuguese
UK coast
n.d., not detected; n, number of specimens analyzed.
absorbed dose rate in common dolphins is 1.50 mGy h 1. Po-210 is
the main contributor to this dose rate, with an absorbed radiation
dose of 1.46 mGy h 1, i.e., more than 97% for the total. In contrast to
this, 137Cs in dolphin’s internal tissues gives a negligible contribution to the absorbed dose (Table 5).
These radionuclides, namely the naturally-occurring 210Pb, 210Po,
40
K, are accumulated in the tissues of human body as well. In the
adult man, the average activity concentrations of these radionuclides
are about 0.2, 0.2 and 60 Bq kg 1, respectively (UNSCEAR, 1982).
Cs-137 accumulation, although small, is more variable (average value
0.52 Bq kg 1, range 0.22e1.1 Bq kg 1). Based on these concentrations,
the average absorbed radiation dose (not weighted with the radiation quality factor) in the human muscle from internally accumulated 210Pb was computed at 4.6 10 6 mGy h 1, from 210Po at
6.2 10 4 mGy h 1, from 40K at 1.9 10 2 mGy h 1, and from 137Cs at
about 4.3 10 4 mGy h 1. Absorbed radiation doses from these
radionuclides in human tissues, if computed using the same DCF as
defined in the section Materials and methods above and such as used
for dolphins, for 210Pb, 210Po, 40K, and 137Cs would be 5.2 10 5,
6.2 10 3, 2.1 10 2 and 2.1 10 4 mGy h 1 respectively. A comparison of the above radionuclide concentrations and absorbed
radiation doses for the adult man with the adult marine mammals
(dolphins; Table 5) highlights that 210Pb, 40K and 137Cs activity
concentrations and doses may be similar, but the 210Po activity
concentration and the absorbed radiation dose are three orders of
magnitude higher in these marine mammals than in man.
Taking into account the available knowledge on 210Po transfer in
marine food chains it seems likely that the diet of marine mammals
accounts for the observed 210Po activity concentrations and the
relative enrichment of 210Po in comparison to 210Pb (Carvalho, 1995,
2010; Carvalho and Fowler, 1994; Hunt and Allington, 1993).
coast
coast
coast
coast
Year
n
137
40
2005e2006
2005e2006
2005e2006
1977e1983
1977e1983
1977e1983
1988e1995
1989e1993
2005e2006
1988e1995
6
1
1
8
7
37
30
25
3
30
0.29 0.28 (<0.06e0.81)
<0.06
<0.06
0.39
0.44
0.52
6.9 (n.d.e66.6)
7.0 (<0.5e45.0)
<0.06
2.7 (n.d.e30.5)
129 48 (75e218)
31.7 18.3
140 13
132
188
130
89 (69e116)
93 (54.0e125.9)
78 22 (61.4e103)
85 (41e116)
Cs
K
M. Malta, F.P. Carvalho / Journal of Environmental Radioactivity 102 (2011) 473e478
Table 5
Activity concentrations of radionuclides and their contributions to the whole body
weighted internal absorbed dose rate (mGy h 1) and total whole body weighted
absorbed dose rate in dolphins off the Portuguese coast.
Tissues
Body weight Average activity concentrations
(%)
(arithmetic mean 1SD, n¼6)
(Bq kg 1)
210
Muscle and remaining 74.0
tissues
Liver
1.92
Fat tissue
17.4
Gonad
2.33
Kidney
0.70
Bone
3.61
Whole body
100
Internal absorbed radiation dose rate
(mGy h 1) per nuclide
Internal absorbed radiation dose rate
(mGy h 1) - total
Po
40
K
210
Pb
137
5632
12948 0.170.07 -
12342
1111
112
11049
4.630.12
47
1.46
7822
176
10253
8311
9266
106
0.036
0.470.12
0.200.07
0.160.13
0.230.11
3.600.12
0.31
8.110 5
Cs
0.29
910
5
1.50
Dolphins, which feed upon small pelagic fish show higher 210Po
activity concentrations in muscle tissue than Sperm whales, which
mainly feed upon cephalopods that have been shown to contain
lower activity concentrations of 210Po (Carvalho, 2010).
The whole body absorbed dose in dolphins estimated in this study
at 1.50 mGy h 1, is far below the threshold dose level of 100 mGy h 1
above which significant biological effects of radiation have been
observed in mammals (Real et al., 2004). However, important
knowledge gaps do exist concerning the effects of alpha radiation in
mammals and the radiosensitivity of different mammal species.
4. Conclusions
Measurement of the more common artificial and natural radionuclides in the tissues of marine mammals confirmed that 210Po and
40
K are the radionuclides with higher activity concentrations.
Concentrations of 210Po (pure alpha emitter) approached those of
40
K (beta and gamma emitter), and both were much higher than
210
Pb and 137Cs concentrations. In the dolphins, the contribution of
210
Po to the total weighted absorbed radiation dose in tissues from
the internally deposited main radioactive elements exceeded 97%.
The internal radiation dose received by marine mammals is
much higher than the dose received by human tissues, and this is
due to the higher 210Po activity accumulated in marine mammal
tissues. The source of these high and unsupported 210Po activity
concentrations in marine mammals is likely due to the ingestion of
210
Po with their food. Po-210 activity concentrations are higher in
seafood in comparison with terrestrial foods (Carvalho, 1995), and,
thus, expectedly much higher in marine mammals’ diet than in
terrestrial mammals’ diet, including man. The differences noticed
also in the 210Po activity concentrations between marine mammal
species, such as the dolphin and the sperm whale, are most likely
due to differences in their diet and food chain structure as well.
Acknowledgements
Thanks are due to Mrs S.Quaresma and Mrs. C.António, staff
members of the Camara Municipal de Alcobaça, for their assistance
with the sampling.
References
Aarkrog, A., Baxter, M., Bologa, S., Bettencourt, A., Bojanowski, R., Charmasson, A.S.,
Cunha, P.I., Delfanti, R., Duran, E., Holm, E., Jeffree, R., Livingston, H.,
Mahapanyawong, D.S., Nies, H., Osvath, I., Pingyu, Li, Povinec, P., Sanchez, A.,
477
Smith, J.N., Swift, D., 1997. A comparison of doses from 137Cs and 210Po in marine
food: a major international study. J. Environ. Radioact. 34, 69e90.
Bréchignac, F., 2003. Protection of the environment: how to position radioprotection in an ecological risk assessment perspective. Sci. Total Environ. 307, 35e54.
Brown, J., Strand, P., Hosseini, A., Børretzen, P., 2003a. Handbook for Assessment of
the Exposure of Biota to Ionising Radiation from Radionuclides in the Environment. Deliverable Report for the EC Project FASSET Contract No. FIGECT-2000-00102. Norwegian Radiation Protection Authority, Østerås, p. 101.
Brown, J., Gomez-Ros, J.M., Jones, S.R., Prölh, G., Taranenko, V., Thorring, H., Vives I
Battle, J., Woodhead, D., 2003b. Dosimetric Models and Data for Assessing
Radiation Exposures to Biota. Deliverable Report for the EC Project FASSET
Contract No. FIGE-CT-2000-00102. Norwegian Radiation Protection Authority,
Østerås, p. 196.
Brown, J.E., Børretzen, P., Hosseini, A., 2005. Biological transfer of radionuclides in
marine environments e identifying and filling knowledge gaps for environmental impact assessments. Radioprotection. Suppl. 1 (40), S533eS539.
Brown, J.E., Jones, S.R., Saxén, R., Thørring, H., Batlle, J.V., 2004. Radiation doses to
aquatic organisms from natural radionuclides. J. Radiol. Prot. 24, A63eA77.
Carvalho, F.P., 1988. Polonium-210 in marine organisms: a wide range of natural
radiation dose domains. Radiat. Prot. Dosim. 24, 113e117.
Carvalho, F.P., Fowler, S.W., 1993. An experimental study on the bioaccumulation
and turnover of polonium-210 and lead-210 in marine shrimp. Mar. Ecol. Prog.
Ser. 102, 125e133.
Carvalho, F.P., Fowler, S.W., 1994. A double tracer technique to determine the
relative importance of water and food as sources of polonium-210 to marine
prawns and fish. Mar. Ecol. Prog. Ser. 103, 251e264.
Carvalho, F.P., 1995. 210Po and 210Pb intake by the Portuguese population: the
contribution of seafood in the dietary intake of 210Po and 210Pb. Health Phys.
69 (4), 469e480.
Carvalho, F.P., Oliveira, J.M., 2008. Radioactivity in marine organisms from Northeast Atlantic Ocean. In: Paschoa, A.S., Steinhaeusler, F. (Eds.), The Natural
Radiation Environment (NRE VIII). AIP Conference Proceedings. American
Institute of Physics, Melville, New York, USA, pp. 387e392.
Carvalho, F.P., 2010. Polonium (210Po) and lead (210Pb) in marine organisms and
their transfer in marine food chains. J. Environ. Radioact.. http://dx.doi.org/10.
1016/j.jenvrad.2010.10.011.
Carvalho, F.P., Oliveira, J.M., 2007. Alpha emitters from uranium mining in the
environment. J. Radioanal. Nucl. Chem. 274, 167e174.
Carvalho, F.P., Oliveira, J.M., Alberto, G., 2011. Factors affecting 210Po and 210Pb
concentration in mussels and implications for bio monitoring programmes.
J. Environ. Radioact. 102, 128e137.
Cherry, R.D., Shannon, L.V., 1974. The alpha radioactivity of marine organisms. Atom.
Energ. Rev. 12 (1), 3e45.
Cherry, R.D., Heyraud, M., 1982. Evidence of high natural radiation doses in certain
mid-water oceanic organisms. Science 218, 54e56.
Cherry, D.R., Heyraud, M., Rindfuss, R., 1994. Polonium -210 in Teleost Fish and in
Marine Mammals: Interfamily Differences and Possible Association between
Polunium -210 and Red Muscle Content. J. Environ. Radioactivity 24,
273e291.
Culik, B.M., 2004. Review of Small Cetaceans e Distribution, Behaviour, Migration
and Threats, Marine Mammals Action Plan / Regional Seas Reports and Studies
No. 177. UNEP/CMS Secretariat, Bonn, Germany.
Dubois, K.P., Geiling, E.M.K., Mcbride, A.F., Thomson, J.F., 1948. Studies on the
intermediary carbohydrate metabolism of aquatic animals. J. Gen. Physiol.
31 (4), 347e359.
Durand, J.P., Carvalho, F.P., Goudard, F., Pieri, J., Fowler, S.W., Cotret, O., 1999. 210Po
binding to metallothioneins and ferritin in the liver of teleost marine fish. Mar.
Ecol. Prog. Ser. 177, 189e196.
Folsom, T.R., Wong, K.M., Hodege, V.F., 1974. Some extreme accumulations of
natural polonium radioactivity observed in marine organisms. In: The Natural
Radiation Environment II. Houston, Texas. Texas University Press, Houston,
pp. 863e882.
Golikov, V., Brown, J.E., 2003. Internal and External Doses Models e A Deliverable
Report for EPIC (Environmental Protection from Ionizing Contaminants in the
Artic) Contract EU: ICA2eCTe2000e10032.
Gwynn, J.P., Brown, J.E., Kovacs, K.M., Lydersen, C., 2006. The derivation of radionuclide transfer parameters for and doseerates to adult ringed seal (Phoeca
hispida) in an Artic environment. J. Environ. Radioact. 90, 197e209.
Holm, E., Leisvik, M., Ranebo, Y., Wallberg, P., Wallberg, L., Odsjӧ, T., Mortensen, P,
2005. Radioactivity in seals from the Swedish coast. In: Bréchignac, F.,
Howard, B.J. (Eds.), Scientific Trends Radiological Protection of the Environment. ECORAD 2004. IRSN, France, pp. 85e95.
Hunt, G., Allington, D., 1993. Absorption of environmental polonium-210 by the
human gut. J. Radiol. Prot. 13, 119e126.
ICRP, 1971. Recommendations of the ICRP. Ann. ICRP 1 (3) ICRP Publication 26.
ICRP, 1991. 1990 Recommendations of the International Commission on Radiological
Protection. Ann. ICRP 21, 1e3. ICRP Publication 60.
ICRP, 2008. Environmental protection e the concept and use of reference animals
and plants. Ann. ICRP 38, 4e6. ICRP Publication 108.
Livingston, H.D., Povinec, P.P., 2000. Anthropogenic marine radioactivity. Ocean
Coast Manage. 43, 689e712.
NEA/OECD, 2002. Radiological Protection of the Environment: the path forward to a new
policy? In: Workshop Proceedings, Taormina, Sicily, Italy 12e14 February 2002.
Nuclear Energy Agency/Organization for Economic Cooperation and Development,
Paris, p. 35.
478
M. Malta, F.P. Carvalho / Journal of Environmental Radioactivity 102 (2011) 473e478
Parfenov, Y., 1974. Polonium-210 in the environment and in the human organism.
Atom. Energ. Rev. 12, 75e143.
Pentreath, R.J., Woodhead, D.S., 2001. A systems for protecting the environment
from ionizing radiation: selecting reference fauna and flora, and possible dose
models and environmental geometrics that could be applied to them. Sci. Total
Environ. 277, 33e43.
Pham, M.K., Sanchez-Cabeza, J.A., Povinec, P.P., Arnold, D., Benmansour, M.,
Bojanowski, R., Carvalho, F.P., Kim, C.K., Esposito, M., Gastaud, J., Ham, G.J.,
Hegde, A.G., Holm, E., Jaskierowicz, D., Kanisch, G., Llaurado, M., La Rosa, J.,
Lee, S.H., Gascó, C., Liong Wee Kwong, L., Le Petit, G., Maruo, Y., Nielsen, S.P.,
Oh, J.S., Oregioni, B., Palomares, J., Pettersson, H.B.L., Rulik, P., Ryan, T.,
Sandor, T., Satake, H., Schikowski, J., Skwarzec, B., Smedley, P.A., Vajda, N.,
Wyse, E., 2006. Certified reference material for radionuclides in fish flesh
sample IAEA-414 (mixed fish from the Irish Sea and North Sea). Appl. Radiat.
Isot. 64, 1253e1259.
Povinec, P.P., Pham, M.K., Sanchez-Cabeza, J.A., Barci-Funel, G., Bojanowski, R.,
Boshkova, I., Burnett, W.C., Carvalho, F., Chapeyron, B., Cunha, I.L., Dahlgaard, H.,
Galabov, N., Fifield, L.K., Gastaud, J., Geering, J.J., Gomez, I.F., Green, N.,
Hamilton, T., Ibanez, F.L., IbnMajah, M., John, M., Kanisch, G., Kenna, T.C.,
Kloster, M., Korun, M., Liong Wee Kwong, L., La Rosa, J., Lee, S.H., Levy-Palomo, I.,
Malatova, M., Maruo, Y., Mitchell, P., Murciano, I.V., Nelson, R., Oh, J.S., Oregioni, B.,
Le Petit, G., Pettersson, H.B.L., Reineking, A., Smedley, P.A., vander Struijs, I.D.B.,
Voors, P.I., Yoshimizu, K., Wyse, E., 2007. Reference material for radionuclides in
sediment, IAEA-384 (Fangataufa Lagoon sediment). J. Radioanal. Nucl. Chem. 273,
383e393.
Real, A., Sundell-Bergman, S., Knowles, J.F., Woodhead, D.S., Zingler, I., 2004. Effects
of ionising radiation exposure on plants, fish and animals: relevant data for
environmental radiation protection. J. Radiol. Prot. 24, A123eA138.
RIFE, 2009. Radioactivity in Food in the Environment, 2008 (RIFE-14). Cefas,
Lowestoft, pp. 242.
United Nations, 1982. Ionizing radiation: sources and biological effects. United
Nations Scientific Committee on the Effects of Atomic Radiation, 1982 Report to
the General Assembly, with annexes. United Nations, New York.
Watson, W.S., Summer, D.J., Baker, J.R., Kennedy, S., Reid, R., Robinson, I., 1999.
Radionuclides in seals and porpoises in the coastal waters around the UK. Sci.
Total Environ. 234, 1e13.
Yamamoto, M., Sakaguchi, A., Tomita, J., Imanka, T., Siraishi, K., 2009. Measurements
of 210Po and 210Pb in total diet samples: estimate of dietary intakes of 210Po and
210
Pb for Japanese. J. Radioanal. Nucl. Chem. 279, 93e103.
Yoshitome, R., Kunito, T., Ikemoto, T., Tanabe, S., Zenke, H., Yamauchi, M.,
Miyazaki, N., 2003. Global distribution of radionuclides (137Cs and 40K) in
marine mammals. Environ. Sci. Technol. 37 (20), 4597e4602.