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ICES Journal of Marine Science (2011), 68(2), 333 –340. doi:10.1093/icesjms/fsq088
Radionuclides in deep-sea fish and other organisms from the
North Atlantic Ocean
Fernando P. Carvalho*, João M. Oliveira, and Margarida Malta
Departamento de Protecção Radiológica e Segurança Nuclear, Instituto Tecnológico e Nuclear, E.N. 10, 2686-953 Sacavém, Portugal
*Corresponding Author: tel: +351 219946332; fax: +351 219941995; e-mail: [email protected].
Carvalho, F. P., Oliveira, J. M., and Malta, M. 2011. Radionuclides in deep-sea fish and other organisms from the North Atlantic Ocean – ICES
Journal of Marine Science, 68: 333 – 340.
Received 21 August 2009; accepted 5 May 2010; advance access publication 30 July 2010.
The naturally occurring radionuclides potassium-40 (40K), radium-226 (226Ra), polonium-210 (210Po), and lead-210 (210Pb) were
measured in commercial fish species such as cod, halibut, redfish, and shark from several fishing grounds in the North Atlantic, as
well as the anthropogenic radionuclides caesium-137 (137Cs) and plutonium isotopes (238Pu and 239+240Pu). The concentrations of
naturally occurring radionuclides were compared with those of anthropogenic origin. The main contributors to the radiation dose
were 210Po and 40K, with anthropogenic radionuclides accounting for just a small contribution. We provide the first measurements
of naturally occurring radionuclides in abyssal organisms, including fish, molluscs, and crustaceans, from the Porcupine Abyssal Plain. In
these organisms, radionuclide concentrations and the absorbed radiation doses were dominated by 210Po and were comparable with
those determined in related coastal species, confirming that the deep-sea fauna do not live in an environment protected from ionizing
radiation. Absorbed radiation doses from naturally occurring radionuclides still exceed radiation doses caused by anthropogenic radionuclides introduced into the Northeast Atlantic.
Keywords: abyssal fauna, caesium-137, commercial fisheries, lead-210, plutonium, polonium-210, radioactivity in fish, radium-226.
Introduction
There are both anthropogenic and naturally occurring radionuclides in the environment in general and in the oceans in particular (Pentreath, 1980; Eisenbud and Gesell, 1997; Livingston
and Povinec, 2000). Radionuclides of both origins can be concentrated in the tissues of marine organisms and transferred along the
food chains, exposing the organisms to ionizing radiation that may
cause harmful biological effects on individuals, populations, and
ecosystems (UNSCEAR, 1982; Eisenbud and Gesell, 1997; Real
et al., 2004).
The introduction of anthropogenic radionuclides into the
ocean, in particular through the dumping of radioactive waste,
coastal discharges from nuclear facilities, accidents involving
nuclear-powered vessels, surface deposition of radioactive fallout
from the nuclear weapon tests, and from the Chernobyl accident,
has added radioactivity to the marine environment. The inventory
of radioactivity released into the oceans has been compiled by the
International Atomic Energy Agency (IAEA) based on the reports
produced by IAEA member states (IAEA, 1999; Livingston and
Povinec, 2000).
Between 1946 and 1982, most European countries with nuclear
power programmes dumped low- and medium-level activity
radioactive wastes into the Northeast Atlantic (NEA/OECD,
1996). In this oceanic region, a total of 4232 PBq was dumped
in several areas, from the shallow waters of the English Channel
to the Porcupine and Madeira Abyssal Plains (NEA/OECD,
1996). Most radioactive waste was dumped at the NEA
Radioactive Waste dumpsite in the Porcupine Abyssal Plain.
Radionuclides present in the waste in large amounts were
# 2010
caesium-137 (137Cs), plutonium isotopes (238Pu and 239+240Pu),
tritium (3H), radium-226 (226Ra), and carbon-14 (14C) (NEA/
OECD, 1996).
Radioactivity from sunken nuclear reactors and accidents
involving nuclear vessels, such as the accidents with the nuclear
submarines “Konsomolets” in the Norwegian Sea, the “K-159”
in the Barents Sea, and the “Kursk” in the White Sea, has been a
matter of concern, especially in Arctic Seas as a result of fission
products and long-lived radionuclides, such as 137Cs and plutonium, present in those reactors (Hamilton et al., 1994; Baxter
et al., 1995; Osvath et al., 1999; NRPA, 2009).
Anthropogenic radionuclides in coastal environments have
been monitored for decades and their concentrations compared
with the background of naturally occurring radionuclides (e.g.
ITN, 2008; RIFE-13, 2008; NRPA, 2009). To take into consideration the effect of radioactive discharges from nuclear and nonnuclear industries into coastal seas, the environmental radiation
impact and the radiological risk to humans were assessed for the
European Community (CEC, 1990; OSPAR Commission, 2002).
It was concluded that the anthropogenic radioactivity in most
fish species was moderately low and, for the human consumer,
the main dietary contributor to the internal radiation dose was
the naturally occurring 210Po (Aarkrog et al., 1997). Using a conservative scenario for the world population in the year 2000, the
average annual individual effective doses from ingestion of
marine food were estimated to be of the order of 0.03 mSv from
137
Cs and 9 mSv from 210Po (Livingston and Povinec, 2000).
Human populations, however, have different dietary habits and
seafood, the main 210Po source, may account for varying
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334
contributions to the diet. For example, the annual seafood consumption in the UK averages 10 kg year21 per capita, whereas in
Portugal it averages 60 kg year21 per capita and in Japan it accounts
for 64 kg year21 per capita. 210Po ingested with the diet gives rise to
average daily intakes of 210Po estimated at 0.04–0.37 Bq d21 in the
UK, 1.3 Bq d21 in Portugal, and 0.61 Bq d21 in Japan and, therefore, internal absorbed radiation doses vary accordingly (Watson,
1985; Carvalho, 1995; Yamamoto et al., 2009).
The release of anthropogenic radionuclides into the marine
environment has also caused changes in the exposure of marine
biota to ionizing radiation. The assessment of absorbed radiation
doses from internal and external radioactive sources of anthropogenic and naturally occurring radionuclides indicates that most of
the radiation dose is usually the result of naturally occurring radionuclides (Carvalho and Oliveira, 2008). Much less information is
available about radioactivity in the deep sea and the resulting radiation exposure of deep-sea biota to the naturally occurring radionuclides. Little is known also about the radioecological impact of
anthropogenic radioactivity introduced into the deep ocean by
waste-dumping operations. North Atlantic fisheries have increased
the captures of deep-water species off the continental shelf at
bathyal depths (i.e. from 200 to 4000 m) in recent years. Some
species now commonly found in the market, such as the grenadier
(Coryphaenoides rupestris), the slickhead (Alepocephalus spp.), the
black scabbardfish (Aphanopus carbo), and several deep-sea sharks
(e.g. Centroscymnus coelepis, Dalatias licha) were not part of the
human diet some years ago.
This paper provides an account of the main radionuclide concentrations in commercial species of demersal fish from the outer
shelves and continental slopes of the North Atlantic and in abyssal
organisms from the Northeast Atlantic. To answer questions about
the radioactive contamination of the North Atlantic and radiation
exposure of the marine biota, a comparison is made (i) between
radionuclide concentrations in species from different environments and (ii) between the contributions of radionuclides to the
absorbed radiation dose in marine biota.
Material and methods
Sampling
Samples of cod (Gadus morhua), redfish (Sebastes mentella),
Greenland halibut (Reinhardtius hippoglossoides), plaice
(Hippoglossoides platessoides), ray (Raja centa), roundnose grenadier
(C. rupestris), red hake (Urophycis chuss), kitefin shark (D. licha),
horse mackerel (Trachurus trachurus), pouting (Trisopterus luscus),
and catshark (Scyliorhinus canicula) were obtained directly from
Portuguese trawlers fishing in various North Atlantic fishing areas
(along the west coast of Portugal, in the Iceland, White, and
Barents Seas, in the Labrador Sea, and on the Newfoundland
slope) in 2003, 2004, and 2006 (Table 1). The samples were
tagged, frozen, and stored, and capture-related data were annotated
on board the ship. Most samples were a pool of several specimens of
the same species from the same catch.
One set of samples from deep water off the Madeira and Azores
archipelagos was obtained mostly through longline fishing carried
out by artisanal fishing boats. These samples included locally
abundant commercial species, such as the black scabbardfish (A.
carbo) in Madeira, and the sperm whale (Physeter catodon), once
commonly hunted in the Azores.
Another set of samples was obtained with an Agassiz bottom
trawl with an opening–closing device (discrete depth sampling)
F. P. Carvalho et al.
from the Porcupine Abyssal Plain, Northeast Atlantic. Most of
the abyssal organisms captured in this area were small in size
and number and could be analysed only by alpha spectrometry
for the naturally occurring radionuclides. Attempts were made
to determine gamma-emitting radionuclide concentrations (nondestructive analysis) but these were below the detection limits. The
amount of material in these samples generally was not sufficient to
quantify anthropogenic alpha-emitting radionuclides.
In the laboratory, fish samples were thawed, dissected, freezedried, and prepared for analysis. Because the commercial species
provided more abundant sample material, it was possible to
analyse the fish muscle (fish fillet) by gamma as well as by alpha
spectrometry.
Analysis
Samples of muscle tissue [10 g dry weight (dw)] were analysed for
gamma-emitting radionuclides, such as radiocaesium (137Cs and
134
Cs), cobalt-60 (60Co), potassium-40 (40K), and iodine-131
131
( I). Gamma spectrometry was performed on freeze-dried biological material compacted in Millipore air-tight Plexiglas Petri
dishes, with HpGe large-volume detectors (Canberra), using
24-h counts. Gamma spectra were analysed with Genie 2000 software from Canberra.
Analyses of plutonium isotopes (239+240Pu and 238Pu),
uranium isotopes (238U, 235U, and 234U), 226Ra, 210Po, and 210Pb
were performed by radiochemical separation and alpha spectrometry using established and quality-controlled methods
(Carvalho, 1995; Oliveira and Carvalho, 2006; Carvalho and
Oliveira, 2007). In brief, the activities of known isotopic tracers
(242Pu, 232U, 224Ra, 209Po, and stable Pb) were added to accurately
weighed amounts of biological sample to determine the radiochemical yield of the analytical procedure. After the complete dissolution of the sample in HNO3 and HCl and the separation of the
radioelements using a sequential radiochemical extraction procedure, these were electroplated on silver or stainless-steel discs
and the radioactivity measured with 600 mm2 ion-implanted silicium detectors in an alpha spectrometer (OCTETEPlus, Ortec
EG&G; Carvalho and Oliveira, 2007, 2009). Analytical quality
assurance was ensured through repeated analyses of certified
reference materials and participation in international comparison
exercises organized by the IAEA (e.g. Pham et al., 2006; Povinec
et al., 2007).
Results and discussion
Commercial species from North Atlantic seas
In general, the concentrations of uranium isotopes were lower
than those of 226Ra, 210Pb, and 210Po (Table 2). Among the naturally occurring alpha emitters, 210Po displayed concentrations
ranging from 29 to 5522 mBq kg21 wet weight (ww) and was
present in fish muscle in concentrations higher than other radionuclides. Among naturally occurring gamma-emitting radionuclides, radioactive potassium (40K) displayed the highest
concentrations, ranging roughly from 100 to 150 Bq kg21 (ww).
Among fish species, deep-sea species, such as the roundnose
grenadier (C. rupestris) and the red hake (U. chuss), displayed
radionuclide concentrations similar to those of other demersal
fish from the continental shelf, such as cod (G. morhua).
Elasmobranchs (cartilaginous fish), namely the kitefin shark
(D. licha) and the catshark (S. canicula), generally displayed
335
Radionuclides in deep-sea fish from the North Atlantic
Table 1. Fish species collected for analysis from trawlers fishing in the North Atlantic Ocean.
Fish species
2003
Redfish (Sebastes mentella)
Cod (Gadus morhua)
Cod (Gadus morhua)
Cod (Gadus morhua)
Greenland halibut (Reinhardtius hippoglossoides)
Plaice (Hippoglossoides platessoides)
2004
Greenland halibut (Reinhardtius hippoglossoides)
Cod (Gadus morhua)
Plaice (Hippoglossoides platessoides)
Ray (Raja centa)
Roundnose grenadier (Coryphaenoides rupestris)
Red hake (Urophycis chuss)
Kitefin shark (Dalatias licha)
Redfish (Sebastes mentella)
Redfish (Sebastes mentella)
2006
Horse mackerel (Trachurus trachurus)
Pouting (Trisopterus luscus)
Catshark (Scyliorhinus canicula)
n
Average weight (kg)
Latitude (N)
Longitude (W)
Depth (m)
Region
1
3
1
1
2
3
3.0
–
3.0
3.0
2.5
1.0
–
–
–
–
–
–
–
–
–
–
–
–
500
500
500
500
500
500
Iceland sea
White sea
Labrador Sea
Barents sea
Labrador Sea
Labrador Sea
3
2
4
2
3
4
2
4
7
0.813
1.215
0.714
1.733
0.894
0.512
1.330
0.554
0.699
48806′
48806′
48806′
48806′
48808′
48808.5′
48808.5′
48806′
62805′
48806′
48806′
48806′
47827′
47835′
47840′
47840′
48806′
30826′
800
800
800
750
850
900
900
800
850
Newfoundland
Newfoundland
Newfoundland
Newfoundland
Newfoundland
Newfoundland
Newfoundland
Newfoundland
Iceland sea
14
12
5
0.149
0.173
0.446
39811′
39811′
39811′
09853′
09853′
09853′
250
250
250
Portuguese coast
Portuguese coast
Portuguese coast
concentrations of 210Po and other radionuclides lower than those
in teleost (bony) fish.
The artificial radionuclides 137Cs (gamma emitter) and plutonium isotopes (several alpha-emitting isotopes) were the only
radionuclides of anthropogenic origin detected. Other anthropogenic gamma-emitting radionuclides, such as 60Co, 134Cs, and
131
I, were not detected in any sample. 137Cs concentrations were
generally ,0.5 Bq kg21 (ww), whereas the sum of plutonium
isotopes was always ,1 mBq kg21 (ww), i.e. three orders of magnitude lower than 137Cs activity concentrations. The concentrations of these radionuclides in deep-sea fish were in the range
of concentrations measured in common coastal fish species,
such as the horse mackerel (T. trachurus), pouting (T. luscus),
and catshark (S. canicula) from the Portuguese slopes (Table 2).
They were also in the range of values reported before for other
marine fish (Carvalho, 1995; Carvalho and Oliveira, 2008;
RIFE-13, 2008; NRPA, 2009).
In terms of the absorbed radiation dose, and taking into
account the concentrations measured, the naturally occurring
radionuclides, especially 40K, 226Ra, and 210Po, are the ones that
provide higher contributions to the radiation doses to the fish as
well as to the human consumers of seafood.
The concentrations of radionuclides in fish muscle varied
among species even when they were caught in the same fishing
area, suggesting differential bioaccumulation of radionuclides
(Table 2). Furthermore, in several species, including cod, plaice,
and redfish concentrations of 210Po and 210Pb varied substantially
in internal organs (Table 3). The lowest concentrations of these
radionuclides were generally measured in the muscle and bone,
whereas the highest concentrations were more consistently
measured in the liver. It is interesting to note the elevated 210Po
concentrations in fish liver and gonad, which are consumed in
many countries (Table 3).
radionuclides, 210Po was always higher than the other nuclides of
the uranium series, namely 226Ra and 210Pb. However, when systematically analysed in fish captured at several depths in the
ocean, 210Po and 210Pb in the muscle tissue did not show a specific
relationship with water depth.
As reported above for other species (Table 3), 210Po and 210Pb
concentrations in muscle tissue were generally lower than in
internal organs, such as the liver and gonad, and displayed Po/Pb
ratios above unity (Tables 3 and 4). In general, in the muscle
tissue, 210Po concentrations were 10 –100 times higher than
those of 226Ra, which in turn was about ten times higher than
238
U (Table 2).
In fish muscle, 226Ra concentrations were around 0.1 –
0.6 Bq kg21 (ww). 137Cs was detected in the muscle tissue of
several fish species but always in concentrations 3 orders of magnitude lower than those of the naturally occurring 226Ra.
Plutonium isotopes had also been quantified in several species
from this area and concentrations were systematically under
1 mBq kg21 (ww), so generally 3 – 4 orders of magnitude lower
than those of the naturally occurring 210Po (Carvalho and
Oliveira, 2008).
Overall, concentrations of the anthropogenic radionuclides
137
Cs and plutonium in fish muscle in the seas of Madeira and
the Azores were of the same order of magnitude as in the fish
from other areas of the North Atlantic reported above. This was
not entirely surprising taking into account that the main source
of these radionuclides has been the widespread fallout deposition.
In fish samples from several depths of the Northeast Atlantic, no
major differences were observed in radionuclide concentrations
according to depth. However, no fish samples were available
from the seafloor at the radioactive waste dumpsite for the analysis
of anthropogenic radionuclides.
Biota from the Porcupine Abyssal Plain
Fisheries from Atlantic islands
Radioactivity in samples from the seas around Madeira and the
Azores are shown in Table 4. Among naturally occurring
Samples from the Abyssal Plain contained 210Po and 210Pb in concentrations (Table 5) that were comparable with those measured in
similar coastal water species (Carvalho, 1995). For example, the
336
Table 2. Concentration for Pu, U, RA, Pb, and Po radionuclides are mBq kg21, and those for
Species
2003 Capture
Red fish (Sebastes mentella)
Cod (Gadus morhua)
Cod (Gadus morhua)
Cod (Gadus morhua)
Greenland halibut (Reinhardtius
hippoglossoides)
Plaice (Hippoglossoides
platessoides)
2004 Capture
Greenland halibut (Reinhardtius
hippoglossoides)
Cod (Gadus morhua)
Plaice (Hippoglossoides
platessoides)
Red fish (Sebastes mentella)
Ray (Raja centa)
Roundnose grenadier
(Coryphaenoides rupestris)
Red hake (Urophycis chuss)
Kite fin shark (Dalatias licha)
Red fish (Sebastes mentella)
2006 Capture
Horse mackerel (Trachurus
trachurus)
Pouting (Trisopterus luscus)
Cat shark (Scyliorhinus canicula)
Dry:wet weight ratio
2391240
Pu
238
Pu
137
Cs and 40K are Bq kg21
238
U
235
U
234
U
226
Ra
0.26
0.19
0.18
0.19
0.19
0.25 + 0.12
0.59 + 0.14
0.61 + 0.18
0.67 + 0.16
0.31 + 0.10
,0.08
,0.08
,0.08
0.19 + 0.08
,0.08
2.6 + 0.3
2.0 + 0.3
2.8 + 0.9
6.0 + 0.9
3.5 + 04
0.14 + 0.17
0.12 + 0.12
0.6 + 0.6
0.4 + 0.4
0.13 + 0.13
3.7 + 0.4
2.6 + 0.4
3.6 + 0.9
5.8 + 0.9
4.6 + 0.5
–
24.4 + 2.5
15.6 + 1.6
19.2 + 1.5
26.3 + 1.9
0.24
0.32 + 0.08
0.13 + 0.05
3.5 + 0.7
0.13 + 0.13
8.1 + 0.1
34.9 + 3.1
210
Pb
–
49.6 + 2.4
24.9 + 2.0
17.1 + 2.0
50.3 + 2.1
–
210
Po
137
Cs
40
K
113.0 + 6.3
23.0 + 1.6
64.7 + 4.4
487 + 18
130.8 + 9.1
0.14 + 0.02
0.18 + 0.03
0.26 + 0.03
0.17 + 0.03
0.15 + 0.03
118 + 3
140 + 4
138 + 4
122 + 3
101 + 3
182.3 + 8.7
0.21 + 0.03
119 + 3
0.30
,0.02
–
12.7 + 0.5
0.52 + 0.08
16.4 + 0.6
103 + 9
12 + 2
410 + 57
0.19
0.19
,0.02
,0.02
–
–
30.2 + 1.2
16.4 + 0.6
1.5 + 0.2
0.38 + 0.07
39.9 + 1.6
4.3 + 0.2
73 + 10
876 + 109
40 + 3
–
628 + 59
–
0.35 + 0.05
–
125 + 4
–
0.22
0.20
0.15
,0.02
,0.02
,0.02
–
–
–
8.1 + 0.3
6.1 + 0.2
24.1 + 1.0
0.17 + 0.03
0.54 + 0.08
1.6 + 0.2
8.5 + 0.3
3.4 + 0.1
30.9 + 1.2
510 + 66
89 + 1.3
324 + 36
204 + 19
138 + 10
136 + 9
478 + 24
5522 + 262
233 + 11
0.21 + 0.05
–
0.10 + 0.03
152 + 4
–
95 + 3
0.07
0.10
0.20
,0.02
,0.02
,0.02
–
–
–
210 + 9
26.1 + 1.2
12.0 + 0.5
7.8 + 1.4
0.87 + 0.18
0.10 + 0.01
193 + 9
34.6 + 1.6
9.0 + 0.4
702 + 74
387 + 47
445 + 50
65 + 5
14 + 1
200 + 20
4489 + 218
29 + 3
480 + 20
0.24
–
–
–
–
–
–
200 + 10
2360 + 50
0.21
0.24
–
–
–
–
–
–
–
–
–
–
–
–
130 + 10
150 + 10
2870 + 60
820 + 20
–
n.d.
–
n.d.
0.17 + 0.06
n.d.
n.d.
–
32 + 1
–
116 + 4
149 + 6
148 + 5
105 + 4
nd, not detected.
F. P. Carvalho et al.
337
Radionuclides in deep-sea fish from the North Atlantic
deep-sea rattail (Nematonurus armatus) displayed 210Po concentrations similar to those commonly measured in fish from other
environments. The deep-sea crustaceans and fish displayed a
radionuclide distribution among organs similar to that seen in
Table 3. Concentrations of radionuclides in internal organs of
commercial fish species from the Newfoundland slope, Canada, in
Bq kg21 (ww) (mean + s.d.) in 2004.
210
210
Organ
Po
Pb
Po/Pb
Liver
6.59 + 0.28
0.08 + 0.01
81.31
Gonad 1.87 + 0.15
0.14 + 0.02
13.50
Bone
0.41 + 0.02
0.61 + 0.06
0.67
Muscle 0.628 + 0.059 0.040 + 0.003 15.70
Plaice
Liver
7.73 + 0.38
0.21 + 0.01
37.44
(Hippoglossoides
Gonad 0.39 + 0.02
0.03 + 0.00
14.70
platessoides)
Bone
1.53 + 0.06
1.58 + 0.08
0.97
Redfish
Liver
24.66 + 1.04
4.35 + 0.20
5.66
(Sebastes mentella) Gonad 5.34 + 0.16
0.70 + 0.05
7.63
Bone
5.68 + 0.23
6.55 + 0.29
0.87
Muscle 0.478 + 0.024 0.204 + 0.019
2.34
Species
Cod (Gadus morhua)
surface-water species, with higher 210Po concentrations associated
with digestive organs (Table 5).
As observed in the upper pelagic domain and in coastal waters,
in the deep ocean, crustaceans were the biota group displaying
higher 210Po concentrations. These concentrations were not exceptional, however, in comparison to coastal crustaceans (Cherry and
Heyraud, 1982; Heyraud et al., 1988; Carvalho, 1995).
So far, all the experimental evidence accumulated indicates that
210
Po intake by marine organisms mainly takes place via food
ingestion and it is not absorbed directly from seawater in significant amounts (Carvalho and Fowler, 1993, 1994). Furthermore,
it has been demonstrated that, in cells, polonium binds easily to
amino acids and proteins, which facilitates 210Po absorption
through a predator’s gut and accumulation in the internal
organs (Durand et al., 1999).
In the ocean foodwebs, 210Po transfer from prey to predator is
likely to depend on the feeding habits of the predator (Cherry
et al., 1989). Assuming that the main diet items of a predator
species are known, the 210Po food chain transfer factor [TF ¼
(Bq kg21 in predator tissues) × (Bq kg21 in prey tissues)21] can
be estimated using the concentrations measured in the various
Table 4. Concentrations of artificial radionuclides (137Cs; mBq kg21 ww) and natural radionuclides (40K, 210Po, and 210Pb; Bq kg21 ww)
(mean + s.d.) in large predators and deep-sea organisms of the seas of Madeira and Azores Atlantic islands.
Species
Tuna (Thunnus obesus), Madeira,
D ¼ surface, n ¼ 1, W ¼ 31 kg
Oilfish (Ruvettus pretiosus), Madeira,
D ¼ 100 m, n ¼ 1, W ¼ 12 kg
Black scabbardfish (Aphanopus carbo),
Madeira, D ¼ 1000 m, n ¼ 5, Wm ¼ 1.5 kg
Baird’s slickhead (Alepocephalus bairdii),
Madeira, D ¼ 2000 m, n ¼ 3, Wm ¼ 0.3 kg
Deep-sea eel (Synaphobranchus kaupi),
Madeira, D ¼ 2000 m, n ¼ 2, Wm ¼ 0.2 kg
Deep-sea shark (Centroscymnus coelepis),
Madeira, D ¼ 1500 m, n ¼ 2, Wm ¼ 10 kg
Squid (Loligo forbesi), Azores, D ¼ 10 m,
n ¼ 1, W ¼ 2 kg
Sperm whale (Physeter catodon), Azores,
D ¼ surface, n ¼ 1, W ¼ 40 t
Tissues
Muscle
Liver
Gonad
Bone
Muscle
Liver
Gonad
Bone
Muscle
Liver
Gonad
Bone
Muscle
Liver
Gonad
Bone
Muscle
Liver
Gonad
Bone
Muscle
Liver
Gonad
Bone
Mantle
Liver
Gonad
Pyloric
caeca
Branchial
hearts
Whole body
Muscle
Dry:wet
weight ratio
0.33
0.40
0.35
0.35
0.36
0.38
0.18
0.55
0.20
0.26
0.21
0.53
0.12
0.21
0.09
0.28
0.20
0.28
0.32
0.30
0.35
0.87
0.34
0.36
–
–
–
–
137
226
Ra
0.6 + 0.2
–
–
–
0.10 + 0.05
–
–
–
0.20 + 0.05
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
210
Po
3.0 + 0.1
268 + 9
63 + 1
8.0 + 0.3
0.72 + 0.02
36.1 + 1.6
7.9 + 0.5
4.7 + 0.3
0.33 + 0.02
8.7 + 0.5
15.4 + 0.5
6.2 + 0.4
2.6 + 0.2
90 + 14
109 + 8
66 + 3
0.47 + 0.02
4.45 + 0.67
2.49 + 0.10
5.31 + 0.31
0.29 + 0.03
0.28 + 0.02
0.20 + 0.01
9.10 + 0.93
1.61 + 0.04
47 + 2
15 + 0.4
64 + 2
Pb
0.46 + 0.02
4.90 + 0.2
1.91 + 0.1
1.60 + 0.05
0.012 + 0.007
0.80 + 0.06
0.13 + 0.01
0.68 + 0.03
0.12 + 0.01
5.14 + 0.25
3.8 + 0.1
2.40 + 0.05
0.45 + 0.02
34 + 1
14.3 + 0.2
15 + 1
0.014 + 0.001
3.50 + 0.16
0.19 + 0.01
0.42 + 0.02
0.04 + 0.01
0.11 + 0.01
0.013 + 0.001
1.83 + 0.54
0.41 + 0.01
118 + 4
1.27 + 0.04
1.88 + 0.06
–
–
–
153 + 4
2.65 + 0.07
58
–
0.27
–
0.9 + 0.2
–
0.5 + 0.2
2
5.0 + 0.2
0.5
0.45 + 0.16
4
11
n, number of specimens analysed; W, whole body wet weight; Wm, average body weight; D, depth of capture.
210
Po/Pb
ratio
6.6
54
33
5.0
60
45
62
7
2.5
1.6
4.0
2.6
5.9
2.6
7.6
4.4
34
1.2
13
12.5
7
2.5
15
5
3.9
0.4
12
34
Cs
0.4 + 0.2
–
–
–
0.2 + 0.1
–
–
–
0.34 + 0.05
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
–
338
F. P. Carvalho et al.
Table 5. Concentrations of 210Po and 210Pb (Bq kg21 ww; mean + s.d.) in benthic fauna of the Porcupine Abyssal Plain, 45808′ N 17812′ W,
4500-m depth in the Northeast Atlantic.
Species
Ascidian
Chitonanthus abyssorum, n ¼ 4
Sipunculidae
Pelagosphera (larvae), n ¼ 4
Golfingia flagrifera, n ¼ 1
Polychaetes, n ¼ 3, W ¼ 1.5 –2.5 g
Gut
Remainder
Ophiuridae
Ophiomusium lymani, n ¼ 3
Asteridae
Astropecten sp., n ¼ 3, W ¼ 0.6 g
Astropecten sp., n ¼ 1, W ¼ 13 g
Mollusc (soft tissues)
Silicula fragilis, n ¼ 1
Isopods, n ¼ 2, W ¼ 0.53 –1.0 g
Whole body
Gut
Exoskeleton
Amphipods
Eurythenes gryllus, n ¼ 3
Mysids
Gnathophausia ingens, n ¼ 1, W ¼ 10.7 g
Decapods
Eryonidae, n ¼ 3, W ¼ 2.5–5.6 g
Cephalopods
Vampyroteuthis infernalis, n ¼ 1, W ¼ 6.8 g
Fish
Nematonurus (c.) armatus
W ¼ 2 + 0.5 kg
Muscle, n ¼ 9
Liver, n ¼ 9
Skin, n ¼ 4
Bone, n ¼ 4
Parabrotula sp., n ¼ 1, W ¼ 0.5 kg
Muscle
Dry:wet weight ratio
210
Po (Bq kg21)
210
Pb (Bq kg21)
Po/Pb ratio
0.15
38 + 2
38 + 2
1
0.11
0.08
13 + 1
44 + 2
1.17 + 0.07
7.3 + 0.2
11
6
0.22
0.18
27 + 2
52 + 2
11 + 0.5
13 + 0.5
2.5
4
0.47
15.2 + 0.7
6.4 + 0.2
2.4
0.38
0.23
50 + 3
171 + 13
7.6 + 0.4
25 + 2
6.4
6.7
0.16
124 + 8
123 + 4
1
0.23
0.41
0.68
27 + 1
94 + 3
194 + 5
1.91 + 0.09
11.4 + 0.3
8.4 + 0.2
14
8.2
23
0.20
32 + 10
28 + 11
1.1
0.19
18 + 2
6.3 + 0.3
2.8
0.21
22 + 2
1.2 + 0.1
0.07
39 + 3
6.9 + 0.3
5.6
0.17
–
–
–
0.31 + 0.28
3.58 + 2.29
1.94 + 0.73
3.25 + 1.96
0.60 + 0.55
2.50 + 1.64
0.68 + 0.33
0.85 + 0.24
0.5
1.4
2.8
3.8
0.15
6.8 + 0.2
0.24 + 0.01
18
29
n, number of specimens analysed; W, average body wet weight.
species. The computed average transfer factors for the food chain
from the Porcupine Abyssal Plain based on our measurements are
indicated on Figure 1, with the arrows depicting the main routes of
energy (carbon) flow. Conversely, 210Po concentrations in the
tissues of a fish may give an indication about its diet.
Concentration factors [CF ¼ (Bq kg21 in whole-body
organism) × (Bq l21 in seawater)21] of 210Po are also indicated
in Figure 1 and were computed using an average 210Po concentration in filtered seawater of 1 mBq l21. The CF values for organisms living in the same habitat vary by orders of magnitude and
demonstrate that 210Po bioaccumulation is not from simple radionuclide absorption from seawater, underscoring the role of foodchain transfer, as suggested above.
It has been shown that in all oceanic ecological domains there
are organisms with particularly high concentrations of 210Po, and
these organisms or some of their organs may receive high radiation doses from internally accumulated 210Po (Cherry and
Heyraud, 1982; Carvalho, 1995; Godoy et al., 2008). Absorbed
radiation doses have been estimated for organisms such as the
pelagic planktivorous sardine and the pelagic top predator blue
marlin (Carvalho and Oliveira, 2008). Results from that work
showed that the radiation dose received from internally
accumulated radionuclides is higher than the dose from external
radionuclides in seawater and seafloor sediments. For example,
the radiation dose from internal radionuclides in the blue
marlin (Makaira nigricans) was computed at 2.6 ×
1022 mGy h21, whereas from external radioactive sources in seawater it was 1.2 × 1022 mGy h21. Among the internal radionuclides, 40K and 210Po were the main contributors to the
dose. Radiation doses caused by internally accumulated artificial
radionuclides add a very small contribution, ,1%, to the dose
from naturally occurring radionuclides (Carvalho and Oliveira,
2008).
For the human consumers of fish, the presence of anthropogenic radionuclides in fish and their absorption through the diet
certainly adds a radiation dose to consumers. However, concentrations of plutonium isotopes, nearly all pure alpha emitters
and with radiation energy close to that of 210Po (5.3 MeV), will
not add more than 0.01% to the dose delivered by 210Po to consumers (Carvalho and Oliveira, 2008). In an early assessment of
210
Po and 210Pb contributions to the radiation dose received by
human consumers through the ingestion of food and water and
air inhalation, Carvalho (1995) had concluded that ingestion is
the main exposure pathway for humans, and that the dose from
339
Radionuclides in deep-sea fish from the North Atlantic
Figure 1. Outline of the abyssal food chain at the Porcupine abyssal seabed and transfer of energy (arrows). TF ¼ 210Po transfer factor; CF ¼
210
Po concentration factor.
marine products would be higher in the Portuguese population
than in nations with a low consumption of seafood.
Conclusions
Our results showed that activity concentrations of naturally occurring radionuclides, especially those of 210Po and 40K, were much
higher than those of anthropogenic radionuclides. Among these,
137
Cs and plutonium were often present, but their concentrations
were low and make only a small contribution to the total radiation
dose to biota and, thus, to human consumers of seafood. Current
levels of artificial radionuclides determined in fish from traditional
fishing grounds in the North Atlantic do not significantly change
the radioactivity and radiation doses to consumers, as previously
assessed.
The concentrations of naturally occurring radionuclides in
organisms from the Porcupine Abyssal Plain in the Northeast
Atlantic were measured for the first time. These organisms contained radionuclides, especially 210Po, in concentrations roughly
similar to those found in coastal organisms of the same taxa.
210
Po concentrations seem to be dependent upon a food chain
transfer of this radionuclide, so it seems that the 210Po concentration levels were more related to the trophic level of the organisms than the ocean depth at which they live.
More data are needed on artificial radionuclides in abyssal biota
from radioactive waste dumpsites to fully assess their impact on
deep-sea fauna. The internal radiation doses received by marine
biota seemed to be driven mainly by 210Po, and 40K and it
appears unlikely that the deep-sea biota are exposed to a radiation
dose regime different from that affecting animals in coastal or
pelagic environments.
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