Page 1
ORIGINAL PAPER
Element levels in cultured and wild sea bass (Dicentrarchuslabrax) and gilthead sea bream (Sparus aurata)from the Adriatic Sea and potential risk assessment
Petra Zvab Rozic • Tadej Dolenec •
Branimir Bazdaric • Vatroslav Karamarko •
Goran Kniewald • Matej Dolenec
Received: 6 November 2012 / Accepted: 2 March 2013 / Published online: 16 March 2013
� Springer Science+Business Media Dordrecht 2013
Abstract In this study, the role of aquaculture
activity as a source of selected metals was analyzed.
Significant differences in element content between
cultured (Dicentrarchus labrax, Sparus aurata) and
wild fishes as well as between fish muscle and their
feed were detected. Higher concentrations of trace
elements (i.e., As, Cu, Hg, Se) in wild fish tissues in
comparison with cultured ones indicate additional
sources of metals beside fish feed as natural and/or
anthropogenic sources. Generally, mean Cd, Cu, Pb,
Se, and Zn concentrations in cultured (0.016, 1.79,
0.14, 0.87, and 34.32 lg/g, respectively) and wild
(0.011, 1.97, 0.10, 1.78, and 23,54 lg/g, respectively)
fish samples were below the permissible levels, while
mean As (2.57 lg/g in cultured, 4.77 lg/g in wild) and
Cr (5.25 lg/g in cultured, 2.92 lg/g in wild) values
exceeded those limits. Hg values were lower in
cultured (0.17 lg/g) and higher in wild (1.04 lg/g)
fish specimens. The highest elemental concentrations
were observed in almost all fish samples from Korcula
sampling site. The smallest cultured sea basses showed
As (4.01 lg/g), Cr (49.10 lg/g), Pb (0.65 lg/g), and
Zn (136 lg/g) concentrations above the recommended
limits; however, values decreased as fish size
increased. Therefore, the majority of metal concentra-
tions in commercial fishes showed no problems for
human consumption. Also calculated Se:Hg molar
ratios (all [1) and selenium health benefit values
(Se-HBVs) (all positive) showed that consumption of
all observed fishes in human nutrition is not risk.
Keywords Element content �Cultured and wild fish �Sea bass and gilthead sea bream � Risk assessment �Adriatic Sea
Introduction
Fish constitute an important healthy low-cholesterol
source of protein and other nutrients for many people
worldwide. They provide omega-3 fatty acids, which
reduce cholesterol levels and the incidence of heart
disease, stroke, and preterm delivery (Burger and
Gochfeld 2005 and references therein). Consequently,
the levels of different contaminants in fish are of
considerable interest due to the potential risk to the fish
themselves as well as to the organisms that consume
them, including people. Among several contaminants,
metals are one of the greatest threats to organisms due
to their persistence and possible bioaccumulation and
biomagnification in the food chain (Demirak et al.
2006; Fernandes et al. 2007; Uysal et al. 2009).
P. Zvab Rozic (&) � T. Dolenec � M. Dolenec
Department of Geology, Faculty of Natural Sciences
and Engineering, Askerceva 12, 1000 Ljubljana, Slovenia
e-mail: [email protected]
B. Bazdaric � V. Karamarko
Dalmar d.o.o., Jadranska cesta 4, Pakostane, Croatia
G. Kniewald
Ruder Boskovic Institute, Bijenicka 54, Zagreb, Croatia
123
Environ Geochem Health (2014) 36:19–39
DOI 10.1007/s10653-013-9516-0
Page 2
The determination of trace metals in marine
organisms as well as their potential sources (sea
water, food) is one of the most widely researched
topics in ecological and bio-monitoring studies (Dugo
et al. 2006; Ersoy et al. 2006; Dural et al. 2007;
Biladzic et al. 2011; Mieiro et al. 2011; Percın et al.
2011; Qiu et al. 2011; Copat et al. 2012). There are
many known sources of metal pollution: geologic
weathering, atmospheric deposition, and untreated
urban and industrial sewages as well as waste from
sewage treatment plants, agricultural waste sewages,
and aquaculture activities (Kalay and Canli 2000;
Demirak et al. 2006; Uysal et al. 2009; Maceda-Veiga
et al. 2012). Several studies showed that accumulation
of heavy metals in the tissue is mainly dependent upon
the water concentrations of metals, exposure period,
and other environmental factors such as salinity, pH,
hardness, and temperature. Ecological needs, size, sex,
and molt of marine animals were also found to affect
metal accumulation in their tissue (Kalay and Canli
2000; Canli and Atli 2003 and references therein).
Fish are widely used as bio-indicators of marine
pollution by metals (Evans et al. 1993). Although
several metals are essential for fish metabolism and are
important micronutrients in the human diet (Ames
1998), in higher amounts they may become toxic and
pose a serious risk for human health. This fact is highly
important, especially for people whose diet depends
mainly on sea products.
A great part of human nutrition in Mediterranean
countries, especially in coastal areas, is composed of
fish and other sea products. Due to greater demand for
new as well as large quantities of food products in the
last decades, fish breeding has experienced rapid
growth (Tovar et al. 2000). In the Mediterranean,
European sea bass (Dicentrarchus labrax) and gilt-
head sea bream (S. aurata) are two of the most
frequently farmed species produced in intensive
farming conditions. Both of these species are carni-
vores. The life-cycle from larvae (2 g) to harvest
(about 350 g) takes 14–18 months for gilthead sea
bream and 18–24 months for European sea bass
(Belias and Dassenakis 2002).
The aim of this study is (1) to assess the content of
some elements in cultured sea bass and sea bream, (2)
to compare the levels of some elements between
cultured and wild fish specimens, (3) to compare the
determined concentrations with some other studies as
well as with guidelines proposed by various authorities,
and (4) to ascertain the possible differences between
different fish sizes. For these purposes, levels of trace
metal contamination of commercial and wild sea bass,
sea bream, and some other fishes were determined. In
addition, selected elements were also measured in
commercial feed.
Study areas
The study was carried out on an aquaculture farm of
sea bass (D. labrax Linnaeus 1758) and sea bream (S.
aurata Linnaeus 1758). The observed fish farm was
located around 4 nautical miles from the mainland,
south of Vrgada Island, which is located in Murter Sea
between Zadar and Sibenik (Fig. 1). The aquaculture
area covered 10,000 m2 and at the time of sampling
extended in a predominately NW–SE direction. The
hinterland of the investigated area consisted mainly of
Cretaceous carbonates (Muzimic 1966). Fish-produc-
ing activities in the area were operated from 1998 to
2011. The farm produced about 550 tons of fish
annually, which were exported exclusively to the
Italian market. European sea bass is traditionally one
of the finfish species preferred by the Italian consumer
and represents half of the national euryhaline fish-
farming product (Poli et al. 2001). Fishes were fed by
hand with extracted pellets of different sizes and from
different producers (BioMar, Dibaq, and Skretting).
The average feed composition was 44 % protein,
19 % fat, 9 % ash, 10 % moisture, and some elements:
phosphor (1.0–1.4 %) and copper (7.5 mg/kg). Pro-
duction ran throughout the whole year, with new
generations being born between April and July.
During the winter, the amount of feed given was
obviously smaller than during the summer, when the
breeding of fishes was highest. Fishes were kept in
polyethylene–polypropylene cages with a diameter of
between 12 and 22 m, depending on the animal’s size
and age. Water depth under and around the fish cages
varied between 20 and 35 m, characterized by a
stratified water column for most of the year and
thermocline at between 15 and 20 m. The water
movement in this area is influenced by the predom-
inant direction of water current (from southeast to
northwest) and daily tides.
For the comparable wild sea fishes, three other
locations in the Adriatic Sea were chosen: Korcula
Island, Pirovac Bay, and Savudrija (northern Istra)
20 Environ Geochem Health (2014) 36:19–39
123
Page 3
(Fig. 1). Korcula Island is located in the southern part
of the Central Adriatic Sea between Split and
Dubrovnik. Samples were collected at the western
side of the island orientated toward the open sea.
Pirovac Bay is a semi-enclosed bay located in the
shore area between Zadar and Sibenik. It is one of the
most anthropogenically impacted areas in the Central
Adriatic, affected by municipal and industrial sewage
from cities as well as tourist facilities in the summer.
Savudrija town is positioned at the shore of northern
Istra. The coast is mainly affected by untreated
municipal sewages from towns.
Materials and methods
Sample collection
European sea bass (D. labrax) and gilthead sea bream
(S. aurata) were sampled in 2007 and 2009 from a
Croatian fish farm positioned near Vrgada Island in the
Central Adriatic Sea. In order to determine the element
composition between fish sizes, four various sea bass
specimens, 6–25.2 cm in length and 15–312.2 g in wet
weight, were collected. In addition, sea bass and sea
bream as well as leerfish (Lichia amia; Linnaeus
1758), mullet, and bogue (Boops boops; Linnaeus
1758) were collected around farms and three other
areas described above.
After sampling, fishes were immediately stored in a
cool box and later frozen. In the laboratory, fishes were
sectioned and freeze-dried for at least 72 h until a
constant weight was reached. Before further analyses
were carried out, dried samples were homogenized
and crushed to a fine powder by grinding in an agate
mortar. The element content in the muscle tissue of
fish samples was analyzed.
Geochemical analysis
All fishes were analyzed for chemical elements
(major, minor, and trace elements) at two certified
Canadian commercial laboratories (ACTLABS: Acti-
vation Laboratories Ltd., Ancaster and ACMELAB:
Fig. 1 Position of studied areas in the Adriatic Sea (a): Savudrija (b), detailed position of fish farm near Vrgada (c), Pirovac Bay (c)
and Korcula Island (d)
Environ Geochem Health (2014) 36:19–39 21
123
Page 4
Acme Analytical Laboratories, Vancouver) using
inductively coupled plasma mass spectrometry (ICP/
MS). Dry, ashed samples were dissolved in acid and
analyzed by High Resolution ICP/MS. Additionally, a
special microwave digestion procedure (closed vessel
digestion) was used. This method was used for total
mercury measurements after dissolving the fish tissues
in concentrated nitric acid under high pressure and
temperature using a microwave digestion system.
Samples of fish tissues were analyzed with the
strictest quality control. To check for instrument drift
and to ensure continuity and stability throughout the
multi-element analyses, every 6 fish samples blanks,
duplicates, and standard reference materials were
included. The blanks were used to measure back-
ground. The metal concentrations in the blanks were
expected very low (under detection limit) and were
subtracted from the sample values. Analytical preci-
sion of the multi-element analyses in the fish samples
was checked against the duplicates as well as standard
certified reference material (DORM-3), the in-house
laboratory reference material (NIST 1575a, NIST
1643e and SLRS-5), and our control standard (STD-
011: wild dogfish soft tissue). The results of duplicate
measurements of both fish samples and standards
indicated that the analytical precision and accuracy
were within ±10 % for the investigated elements.
Statistical analysis
Statistical analyses of data were carried out using
the statistical software program Statistica 8.0. Basic
statistics (mean, minimum, maximum, standard
deviation) of some trace elements (Ba, Be, Ga, In,
Nb, Re, Sb, Ta, Te, Th, Tl, U, V, W, and Y) were
calculated only with regard to results from 2009
because almost all values of these elements were
below the limits of detection (LOD) in 2007 due to
the different laboratory used. For other values below
the LOD, replacement with LOD/H2 was used. This
method was suggested by Verbovsek (2011) as it
gave the smallest errors among different substitution
methods of geochemical data with values below the
LOD. A Pearson correlation matrix was used to
determine the existence of any association between
the elements found in the fish muscle. Box-plot
diagrams were used to present relations with fish
feed and feeding fishes.
Results
Element content in fish muscle tissues and fish feed
Several studies have found a significant difference in
the levels of heavy metals between body parts of the
fishes (Canli and Atli 2003; Dugo et al. 2006; Burger
et al. 2007; Dural et al. 2007; Turkmen et al. 2008;
Fallah et al. 2011; Maceda-Veiga et al. 2012).
Although the liver usually showed the highest con-
centrations of metals, in our study elemental concen-
trations were determined only in muscle tissue, which
is the most important part of the fish body for human
consumption. The element contents of five fishes, as
well as basic statistics (mean, minimum, maximum,
and standard deviation), are presented in Table 1. As
the main potential source of observed elements in fish
tissue, the element contents in three fish food samples
were measured (Table 2). The size of food pellets
differs depending on the size of fishes in the farm. The
smallest feed pellets in our research were in HR1
(BioMar producer feed), which were used for feeding
the youngest fishes. The biggest feed pellets were in
HR3 (Skretting producer feed).
The concentrations of major elements (Ca, Fe, Mg,
Na, Mn) in observed cultured fishes were generally
lower than in their feed. The exception was K, which
had higher mean concentrations in cultured fishes
(19,916.7 lg/g) and 1.6-fold lower values in their feed
(12,086.7 lg/g). The highest difference between
fishes and their feed source was found for Mn, whose
mean concentration in feed (47,333.3 lg/g) exceeded
the values in fish tissues (2,966.7 lg/g) by almost 18
times. Concentrations of K in fish tissues as well as fish
feed were also obviously higher than values of K
observed in sediment below the investigated fish farm
(Zvab Rozic et al. 2012). Strong correlations were
observed between Ca, Fe, Mg, and Mn (r = 0.99–
0.70) and between Na and Mg (r = 0.74). The only
exception is again K, which is uncorrelated or even
negatively correlated with other major elements.
These results suggest at least two different sources
of the presented elements.
The mean concentrations of trace elements in
cultured fish tissues were lower than in their feed for
Ag, B, Ba, Cd, Co, Cu, In, Mo, Pb, Rb, Sb, Se, Sr, Tl,
V, and Zn, while for As, Be, Bi, Cr, Cs, Ga, Ge, Hf,
Hg, Li, Nb, Ni, Re, Sc, Sn, Ta, Te, Th, Ti, U, W, Y, and
Zr, the observed values were higher in fish tissue. The
22 Environ Geochem Health (2014) 36:19–39
123
Page 5
Ta
ble
1E
lem
ent
con
ten
tan
db
asic
stat
isti
cs(m
ean
,m
inim
um
,m
axim
um
,st
and
ard
dev
iati
on
)o
ffi
shm
usc
lem
easu
red
info
ur
cult
ure
dan
dw
ild
fish
essa
mp
led
from
afi
shfa
rm
nea
rV
rgad
aan
dth
ree
com
par
able
area
s(K
orc
ula
Isla
nd
,P
iro
vac
Bay
,an
dS
avu
dri
ja)
Sam
ple
Fis
hL
oca
tion
Wei
ght
(g)
Len
gth
(cm
)C
a(l
g/g
)F
e(l
g/g
)K
(lg/g
)M
g(l
g/g
)N
a(l
g/g
)M
n(n
g/g
)A
g(n
g/g
)A
s(n
g/g
)B
(lg/g
)
2009
R1
Sea
bas
s,w
ild
Korc
ula
Isla
nd
326.3
26.0
1,5
50
245
22,9
00
1,7
60
6,3
30
3,2
10
15
4,4
60
2,5
00
R2
Sea
bas
s,w
ild
Pir
ovac
bay
317.2
25.8
727
47.8
20,4
00
1,4
30
3,8
10
940
52,0
00
1,5
00
R3
Sea
bas
s,cu
lture
dF
FV
rgad
aX
S15.0
6.0
–8.0
14,5
00
834
19,9
00
2,4
40
9,5
80
13,0
00
31
4,0
10
8,3
00
R4
Sea
bas
s,cu
lture
dF
FV
rgad
aS
103.6
12.3
1,6
40
17.4
19,8
00
1,3
20
4,6
60
1,3
50
33,6
40
1,3
00
R5
Sea
bas
s,cu
lture
dF
FV
rgad
aM
204.8
16.4
2,0
50
12.4
21,0
00
1,3
60
3,9
20
1,2
20
32,3
00
1,3
00
R6
Sea
bas
s,cu
lture
dF
FV
rgad
aL
312.2
25.2
1,6
40
26.9
19,0
00
1,2
80
3,0
60
1,0
10
81,6
40
600
R7
Sea
bas
s,cu
lture
dF
FV
rgad
a278.6
24.8
875
15
21,3
00
1,3
50
3,2
30
770
22,1
90
900
R8
Sea
bre
am,
cult
ure
dF
FV
rgad
a288.5
24.9
1,8
40
9.4
18,5
00
1,1
00
2,1
20
450
23,8
00
700
R9
Sea
bre
am,
wil
dF
FV
rgad
a278.3
23.6
624
16.8
21,1
00
1,1
70
3,6
30
310
214,9
00
1,9
00
R10
Lee
rfish
,w
ild
FF
Vrg
ada
––
983
52.1
19,0
00
2,1
90
10,5
00
320
10
8,2
60
4,5
00
2007
R11
Bogue,
wil
dF
FV
rgad
a–
–4,3
00
20
14,0
00
2,0
40
11,1
50
2,0
00
BD
L8,3
00
4,0
00
R12
Sea
bas
s,cu
lture
dF
FV
rgad
a310.6
25.3
700
40
19,1
00
1,2
80
2,6
50
BD
L9
1,3
00
BD
L
R13
Sea
bre
am,
cult
ure
dF
FV
rgad
a316.3
24.8
1,2
00
20
22,8
00
1,1
60
2,5
80
BD
LB
DL
3,0
09
1,0
00
R14
Sea
bas
s,w
ild
Korc
ula
bra
nci
n280.7
23.9
1,7
00
20
17,2
00
1,4
50
5,2
40
1,0
00
BD
L1,3
00
2,0
00
R15
Sea
bas
s,w
ild
Korc
ula
bra
nci
n295.6
24.2
1,3
00
10
17,7
00
1,4
10
5,8
70
BD
LB
DL
1,2
00
2,0
00
R16
Sea
bre
am,
wil
dK
orc
ula
Isla
nd
301.2
23.9
1,2
00
10
20,6
00
1,5
30
3,9
70
2,0
00
BD
L4,7
00
1,0
00
R17
Lee
rfish
,w
ild
FF
Vrg
ada
––
1,7
00
10
20,2
00
1,3
80
2,2
60
BD
LB
DL
3,3
00
BD
L
R18
Sea
bas
s,cu
lture
dF
FV
rgad
aS
90.3
10.8
7,9
00
20
9,0
00
860
2,8
50
3,0
00
21,8
00
1,0
00
R19
Sea
bas
s,cu
lture
dF
FV
rgad
a312.7
25.4
2,2
00
20
19,6
00
1,6
80
8,8
30
2,0
00
21,8
00
3,0
00
R20
Sea
bre
am,
cult
ure
dF
FV
rgad
a315.5
24.4
4,4
00
10
18,7
00
1,4
00
4,3
40
1,0
00
BD
L3,9
00
2,0
00
R21
Mull
et,
wil
dS
avudri
ja(I
stra
)–
–400
20
17,8
00
1,5
60
4,5
70
1,0
00
BD
L2,8
00
2,0
00
R22
Lee
rfish
,w
ild
Sav
udri
ja(I
stra
)–
–400
20
19,9
00
1,5
50
3,9
10
1,0
00
24,4
00
1,0
00
R23
Sea
bas
s,w
ild
Sav
udri
ja(I
stra
)297.5
24.2
2,5
00
20
14,3
00
1,1
50
4,6
60
1,0
00
BD
L1,6
00
1,0
00
AS
2,4
49.0
965.9
518,8
60.8
71,4
71.7
44,9
44.3
51,7
13.4
14.7
33,7
65.6
11,9
52.7
9
Min
400
9.4
9,0
00
860
2,1
20
310
1.4
11,2
00
600
Max
14,5
00
834
22,9
00
2,4
40
11,1
50
13,0
00
31
14,9
00
8,3
00
SD
3,1
10.2
8174.1
93,0
54.7
6361.0
42,6
32.7
52,5
76.0
26.7
53,1
02.2
91,7
26.5
6
Cult
ure
d2009
AS
3,7
57.5
0152.5
219,9
16.6
71,4
75.0
04,4
28.3
32,9
66.6
78.1
72,9
30.0
02,1
83.3
3
Min
875.0
09.4
018,5
00.0
01,1
00.0
02,1
20.0
0450.0
02.0
01,6
40.0
0600.0
0
Max
14,5
00.0
0834.0
021,3
00.0
02,4
40.0
09,5
80.0
013,0
00.0
031.0
04,0
10.0
08,3
00.0
0
SD
5,2
77.6
9333.9
11,0
90.7
2482.2
32,6
64.1
54,9
25.8
411.4
11,0
03.5
93,0
10.9
2
Environ Geochem Health (2014) 36:19–39 23
123
Page 6
Ta
ble
1co
nti
nu
ed
Sam
ple
Fis
hL
oca
tion
Wei
ght
(g)
Len
gth
(cm
)B
a(n
g/g
)B
e(n
g/g
)B
i(n
g/g
)C
d(n
g/g
)C
o(n
g/g
)C
r(n
g/g
)C
s(n
g/g
)C
u(n
g/g
)G
a(n
g/g
)
2009
R1
Sea
bas
s,w
ild
Korc
ula
Isla
nd
326.3
26.0
117.3
915.5
293
18,0
00
245
2,1
20
77.2
R2
Sea
bas
s,w
ild
Pir
ovac
bay
317.2
25.8
BD
L3.1
BD
L6.6
58.6
3,5
50
198
1,2
70
12.6
R3
Sea
bas
s,cu
lture
dF
FV
rgad
aX
S15.0
6.0
–8.0
467
678.7
844
49,1
00
242
4,8
50
283
R4
Sea
bas
s,cu
lture
dF
FV
rgad
aS
103.6
12.3
BD
LB
DL
BD
L9.9
27.5
290
101
1,7
70
1.5
R5
Sea
bas
s,cu
lture
dF
FV
rgad
aM
204.8
16.4
BD
L0.2
BD
L8.3
11.6
140
104
1,8
60
0.5
R6
Sea
bas
s,cu
lture
dF
FV
rgad
aL
312.2
25.2
BD
LB
DL
BD
L11.2
23.4
850
117
2,3
30
2.2
R7
Sea
bas
s,cu
lture
dF
FV
rgad
a278.6
24.8
BD
LB
DL
BD
L4.5
12.1
260
179
1,5
00
BD
L
R8
Sea
bre
am,
cult
ure
dF
FV
rgad
a288.5
24.9
BD
LB
DL
BD
L4.1
8240
135
990
BD
L
R9
Sea
bre
am,
wil
dF
FV
rgad
a278.3
23.6
BD
LB
DL
BD
L5.2
22.8
250
125
1,3
80
0.5
R10
Lee
rfish
,w
ild
FF
Vrg
ada
––
7B
DL
14
14.8
1,0
40
210
1,6
60
1.6
2007
R11
Bogue,
wil
dF
FV
rgad
a–
–0.9
BD
LB
DL
10
10
1,2
00
31
10,0
00
BD
L
R12
Sea
bas
s,cu
lture
dF
FV
rgad
a310.6
25.3
0.7
BD
LB
DL
10
10
1,5
00
203
1,5
40
BD
L
R13
Sea
bre
am,
cult
ure
dF
FV
rgad
a316.3
24.8
0.4
BD
LB
DL
BD
L10
1,6
00
158
1,0
50
BD
L
R14
Sea
bas
s,w
ild
Korc
ula
bra
nci
n280.7
23.9
0.4
BD
LB
DL
BD
L10
1,7
00
152
820
BD
L
R15
Sea
bas
s,w
ild
Korc
ula
bra
nci
n295.6
24.2
0.2
BD
LB
DL
BD
L10
1,5
00
147
1,0
40
BD
L
R16
Sea
bre
am,
wil
dK
orc
ula
Isla
nd
301.2
23.9
0.4
BD
LB
DL
BD
L60
1,6
00
79
710
BD
L
R17
Lee
rfish
,w
ild
FF
Vrg
ada
––
0.5
BD
LB
DL
BD
L10
1,5
00
299
830
BD
L
R18
Sea
bas
s,cu
lture
dF
FV
rgad
aS
90.3
10.8
0.7
BD
LB
DL
10
20
600
39
1,0
80
BD
L
R19
Sea
bas
s,cu
lture
dF
FV
rgad
a312.7
25.4
0.4
BD
LB
DL
10
BD
L1,6
00
199
1,4
80
BD
L
R20
Sea
bre
am,
cult
ure
dF
FV
rgad
a315.5
24.4
0.5
BD
LB
DL
10
10
1,6
00
137
1,2
60
BD
L
R21
Mull
et,
wil
dS
avudri
ja(I
stra
)–
–0.2
BD
LB
DL
BD
L50
1,5
00
59
1,3
20
BD
L
R22
Lee
rfish
,w
ild
Sav
udri
ja(I
stra
)–
–0.6
BD
LB
DL
10
10
1,6
00
210
1,1
60
BD
L
R23
Sea
bas
s,w
ild
Sav
udri
ja(I
stra
)297.5
24.2
0.3
BD
LB
DL
10
10
1,6
00
185
1,3
80
BD
L
AS
1.0
18.8
2.0
911.3
267.0
84,0
35.6
5154.5
21,8
86.9
637.9
2
Min
0.2
0.0
70.7
14
7.0
7140
31
710
0.0
4
Max
767
978.7
844
49,1
00
299
10,0
00
283
SD
1.5
21.1
42.9
414.9
3179.3
910,4
53.2
968.2
61,9
54.0
889.3
4
Cult
ure
d2009
AS
1.2
611.2
51.5
919.4
5154.4
38,4
80.0
0146.3
32,2
16.6
747.8
8
Min
0.7
10.0
70.7
14.1
08.0
0140.0
0101.0
0990.0
00.0
4
Max
4.0
067.0
06.0
078.7
0844.0
049,1
00.0
0242.0
04,8
50.0
0283.0
0
SD
1.3
427.3
12.1
629.1
7337.9
019,9
01.2
554.8
71,3
63.2
6115.1
9
24 Environ Geochem Health (2014) 36:19–39
123
Page 7
Ta
ble
1co
nti
nu
ed
Sam
ple
Fis
hL
oca
tion
Wei
ght
(g)
Len
gth
(cm
)G
e(n
g/g
)H
f(n
g/g
)H
g(n
g/g
)In
(ng/g
)L
i(n
g/g
)M
o(n
g/g
)N
b(n
g/g
)N
i(l
g/g
)P
b(n
g/g
)
2009
R1
Sea
bas
s,w
ild
Korc
ula
Isla
nd
326.3
26.0
10
10
1,3
10
0.6
241
1,9
20
71.8
9.5
190
R2
Sea
bas
s,w
ild
Pir
ovac
bay
317.2
25.8
BD
LB
DL
260
BD
LB
DL
394
12.1
1.9
30
R3
Sea
bas
s,cu
lture
dF
FV
rgad
aX
S15.0
6.0
–8.0
30
34
274
1.2
1,3
60
5,7
90
246
24.6
650
R4
Sea
bas
s,cu
lture
dF
FV
rgad
aS
103.6
12.3
BD
LB
DL
122
0.1
BD
L31
0.6
0.1
10
R5
Sea
bas
s,cu
lture
dF
FV
rgad
aM
204.8
16.4
BD
LB
DL
106
0.1
BD
L18
0.8
BD
L20
R6
Sea
bas
s,cu
lture
dF
FV
rgad
aL
312.2
25.2
BD
LB
DL
136
0.1
BD
L100
20.5
BD
L
R7
Sea
bas
s,cu
lture
dF
FV
rgad
a278.6
24.8
BD
LB
DL
289
0.2
BD
L28
0.6
0.1
BD
L
R8
Sea
bre
am,
cult
ure
dF
FV
rgad
a288.5
24.9
BD
LB
DL
205
0.7
BD
L10
BD
LB
DL
20
R9
Sea
bre
am,
wil
dF
FV
rgad
a278.3
23.6
BD
LB
DL
238
0.1
BD
L27
0.6
0.1
50
R10
Lee
rfish
,w
ild
FF
Vrg
ada
––
BD
LB
DL
1,3
10
0.2
BD
L54
13.6
0.5
50
2007
R11
Bogue,
wil
dF
FV
rgad
a–
–B
DL
1137
BD
L210
20
10
BD
L290
R12
Sea
bas
s,cu
lture
dF
FV
rgad
a310.6
25.3
30
BD
L179
BD
L60
10
10
0.1
90
R13
Sea
bre
am,
cult
ure
dF
FV
rgad
a316.3
24.8
20
BD
L185
BD
L80
BD
LB
DL
BD
L30
R14
Sea
bas
s,w
ild
Korc
ula
bra
nci
n280.7
23.9
20
BD
L919
BD
L100
10
BD
LB
DL
10
R15
Sea
bas
s,w
ild
Korc
ula
bra
nci
n295.6
24.2
20
1960
BD
L60
10
BD
LB
DL
40
R16
Sea
bre
am,
wil
dK
orc
ula
Isla
nd
301.2
23.9
BD
L1
1,6
22
BD
L70
BD
LB
DL
BD
L70
R17
Lee
rfish
,w
ild
FF
Vrg
ada
––
20
BD
L3,6
94
BD
L60
BD
LB
DL
BD
L20
R18
Sea
bas
s,cu
lture
dF
FV
rgad
aS
90.3
10.8
BD
LB
DL
81
BD
L100
10
BD
LB
DL
80
R19
Sea
bas
s,cu
lture
dF
FV
rgad
a312.7
25.4
40
1200
BD
L160
10
BD
LB
DL
310
R20
Sea
bre
am,
cult
ure
dF
FV
rgad
a315.5
24.4
30
BD
L132
BD
L170
10
BD
LB
DL
80
R21
Mull
et,
wil
dS
avudri
ja(I
stra
)–
–10
BD
L420
BD
L70
BD
LB
DL
BD
L160
R22
Lee
rfish
,w
ild
Sav
udri
ja(I
stra
)–
–B
DL
11,4
14
BD
L60
10
BD
L0.1
130
R23
Sea
bas
s,w
ild
Sav
udri
ja(I
stra
)297.5
24.2
10
2192
BD
L130
40
10
BD
L180
AS
14.1
22.9
2625.4
30.3
4128.6
6370.8
834.8
51.6
7109.7
5
Min
7.0
70.7
181
0.0
73.5
47.0
70.3
50.0
77.0
7
Max
40
34
3,6
94
1.2
1,3
60
5,7
90
246
24.6
650
SD
10.0
37.0
3831.4
60.3
8277.4
21,2
47.1
977.3
65.3
7146.5
3
Cult
ure
d2009
AS
10.8
96.8
5188.6
70.4
0229.6
1996.1
741.7
34.2
4119.0
2
Min
7.0
71.4
1106.0
00.1
03.5
410.0
00.3
50.0
77.0
7
Max
30.0
034.0
0289.0
01.2
01,3
60.0
05,7
90.0
0246.0
024.6
0650.0
0
SD
9.3
613.3
079.5
80.4
6553.7
72,3
48.7
1100.0
89.9
8260.1
9
Environ Geochem Health (2014) 36:19–39 25
123
Page 8
Ta
ble
1co
nti
nu
ed
Sam
ple
Fis
hL
oca
tion
Wei
ght
(g)
Len
gth
(cm
)R
b(n
g/g
)R
e(n
g/g
)S
b(n
g/g
)S
c(n
g/g
)S
e(l
g/g
)S
n(n
g/g
)S
r(n
g/g
)T
a(n
g/g
)T
e(n
g/g
)
2009
R1
Sea
bas
s,w
ild
Korc
ula
Isla
nd
326.3
26.0
4,8
20
0.4
10.6
63
3B
DL
7,3
10
8.9
BD
L
R2
Sea
bas
s,w
ild
Pir
ovac
bay
317.2
25.8
4,2
90
BD
L1.4
90.6
BD
L3,0
40
1.5
3
R3
Sea
bas
s,cu
lture
dF
FV
rgad
aX
S15.0
6.0
–8.0
7,5
40
1.3
29.7
243
0.8
90
52,0
00
29.9
4
R4
Sea
bas
s,cu
lture
dF
FV
rgad
aS
103.6
12.3
4,9
40
BD
L2.2
BD
L0.9
BD
L4,9
80
0.2
BD
L
R5
Sea
bas
s,cu
lture
dF
FV
rgad
aM
204.8
16.4
4,7
60
BD
L1.5
BD
L0.9
BD
L7,7
50
0.2
BD
L
R6
Sea
bas
s,cu
lture
dF
FV
rgad
aL
312.2
25.2
4,4
70
BD
L2.1
BD
L0.5
BD
L6,1
30
0.4
BD
L
R7
Sea
bas
s,cu
lture
dF
FV
rgad
a278.6
24.8
3,8
30
BD
L0.8
BD
L0.9
BD
L3,4
50
0.2
BD
L
R8
Sea
bre
am,
cult
ure
dF
FV
rgad
a288.5
24.9
3,4
10
BD
L7.2
BD
L0.8
210
7,4
20
0.2
BD
L
R9
Sea
bre
am,
wil
dF
FV
rgad
a278.3
23.6
4,0
30
BD
L1.5
BD
L0.7
BD
L2,4
10
0.2
BD
L
R10
Lee
rfish
,w
ild
FF
Vrg
ada
––
3,4
80
0.2
7.1
BD
L1.8
70
8,9
00
1.1
BD
L
2007
R11
Bogue,
wil
dF
FV
rgad
a–
–2,8
00
BD
LB
DL
100
2.1
30
26,7
00
BD
LB
DL
R12
Sea
bas
s,cu
lture
dF
FV
rgad
a310.6
25.3
3,5
00
BD
LB
DL
100
1.0
BD
L2,8
00
BD
LB
DL
R13
Sea
bre
am,
cult
ure
dF
FV
rgad
a316.3
24.8
4,0
00
BD
LB
DL
300
1.1
BD
L5,1
00
BD
LB
DL
R14
Sea
bas
s,w
ild
Korc
ula
bra
nci
n280.7
23.9
2,9
00
BD
LB
DL
200
2.4
20
8,5
00
BD
LB
DL
R15
Sea
bas
s,w
ild
Korc
ula
bra
nci
n295.6
24.2
3,2
00
BD
LB
DL
200
2.3
BD
L5,8
00
BD
LB
DL
R16
Sea
bre
am,
wil
dK
orc
ula
Isla
nd
301.2
23.9
3,9
00
BD
LB
DL
300
2.1
BD
L6,4
00
BD
LB
DL
R17
Lee
rfish
,w
ild
FF
Vrg
ada
––
3,0
00
BD
LB
DL
200
2.0
110
6,4
00
BD
LB
DL
R18
Sea
bas
s,cu
lture
dF
FV
rgad
aS
90.3
10.8
2,3
00
BD
LB
DL
100
0.6
BD
L30,2
00
BD
LB
DL
R19
Sea
bas
s,cu
lture
dF
FV
rgad
a312.7
25.4
3,3
00
BD
LB
DL
200
1.1
BD
L11,4
00
BD
LB
DL
R20
Sea
bre
am,
cult
ure
dF
FV
rgad
a315.5
24.4
3,3
00
BD
LB
DL
200
1.0
20
40,2
00
BD
LB
DL
R21
Mull
et,
wil
dS
avudri
ja(I
stra
)–
–4,5
00
BD
LB
DL
200
1.5
20
3,1
00
BD
LB
DL
R22
Lee
rfish
,w
ild
Sav
udri
ja(I
stra
)–
–3,4
00
BD
LB
DL
100
2.0
80
1,8
00
BD
LB
DL
R23
Sea
bas
s,w
ild
Sav
udri
ja(I
stra
)297.5
24.2
2,6
00
BD
LB
DL
200
1.1
BD
L11,3
00
BD
LB
DL
AS
3,8
37.8
30.2
46.4
1118.2
61.3
641.1
711,4
38.7
4.2
81.2
7
Min
2,3
00
0.0
70.8
0.7
10.5
14.1
41,8
00
0.2
0.7
1
Max
7,5
40
1.3
29.7
300
3210
52,0
00
29.9
4
SD
1,0
87.1
90.3
98.8
3104.7
60.7
45.5
813,0
81.5
99.3
91.2
Cult
ure
d2009
AS
4,8
25.0
00.2
87.2
541.0
90.8
068.8
613,6
21.6
75.1
81.2
6
Min
3,4
10.0
00.0
70.8
00.7
10.5
028.2
83,4
50.0
00.2
00.7
1
Max
7,5
40.0
01.3
029.7
0243.0
00.9
0210.0
052,0
00.0
029.9
04.0
0
SD
1,4
49.6
20.5
011.2
398.9
20.1
573.4
218,8
68.4
912.1
11.3
4
26 Environ Geochem Health (2014) 36:19–39
123
Page 9
Ta
ble
1co
nti
nu
ed
Sam
ple
Fis
hL
oca
tion
Wei
ght
(g)
Len
gth
(cm
)T
h(n
g/g
)T
i(n
g/g
)T
l(n
g/g
)U
(ng/g
)V
(ng/g
)W
(ng/g
)Y
(ng/g
)Z
n(l
g/g
)Z
r(n
g/g
)
2009
R1
Sea
bas
s,w
ild
Korc
ula
Isla
nd
326.3
26.0
68
8,8
10
7.3
52
810
64
107
56
464
R2
Sea
bas
s,w
ild
Pir
ovac
bay
317.2
25.8
10
1,6
10
1.5
8130
15
16
21.9
79
R3
Sea
bas
s,cu
lture
dF
FV
rgad
aX
S15.0
6.0
–8.0
241
33,4
00
24.4
195
3,0
80
155
386
136
1,5
20
R4
Sea
bas
s,cu
lture
dF
FV
rgad
aS
103.6
12.3
BD
L100
1.4
BD
L20
BD
L1
42.4
34
R5
Sea
bas
s,cu
lture
dF
FV
rgad
aM
204.8
16.4
BD
L110
1.3
BD
L10
BD
L0.9
38.7
40
R6
Sea
bas
s,cu
lture
dF
FV
rgad
aL
312.2
25.2
BD
L220
7.3
120
BD
L2.3
23.2
15
R7
Sea
bas
s,cu
lture
dF
FV
rgad
a278.6
24.8
BD
L80
BD
LB
DL
10
60.6
28.6
16
R8
Sea
bre
am,
cult
ure
dF
FV
rgad
a288.5
24.9
BD
L70
BD
LB
DL
BD
LB
DL
0.6
12.7
13
R9
Sea
bre
am,
wil
dF
FV
rgad
a278.3
23.6
BD
L120
BD
LB
DL
10
BD
L0.7
16
7
R10
Lee
rfish
,w
ild
FF
Vrg
ada
––
BD
L7,3
10
0.7
620
12
2.3
37.3
80
2007
R11
Bogue,
wil
dF
FV
rgad
a–
–B
DL
37,0
00
BD
LB
DL
BD
LB
DL
BD
L21.9
30
R12
Sea
bas
s,cu
lture
dF
FV
rgad
a310.6
25.3
BD
L34,0
00
BD
LB
DL
BD
LB
DL
BD
L16.9
10
R13
Sea
bre
am,
cult
ure
dF
FV
rgad
a316.3
24.8
BD
L43,0
00
BD
LB
DL
BD
LB
DL
BD
L13.8
10
R14
Sea
bas
s,w
ild
Korc
ula
bra
nci
n280.7
23.9
BD
L36,0
00
BD
LB
DL
BD
LB
DL
BD
L16.1
10
R15
Sea
bas
s,w
ild
Korc
ula
bra
nci
n295.6
24.2
BD
L37,0
00
BD
LB
DL
BD
LB
DL
BD
L19.7
10
R16
Sea
bre
am,
wil
dK
orc
ula
Isla
nd
301.2
23.9
BD
L43,0
00
BD
LB
DL
BD
LB
DL
BD
L17.7
10
R17
Lee
rfish
,w
ild
FF
Vrg
ada
––
BD
L39,0
00
BD
LB
DL
BD
LB
DL
BD
L14
10
R18
Sea
bas
s,cu
lture
dF
FV
rgad
aS
90.3
10.8
BD
L30,0
00
BD
LB
DL
BD
LB
DL
BD
L27.2
10
R19
Sea
bas
s,cu
lture
dF
FV
rgad
a312.7
25.4
BD
L34,0
00
BD
LB
DL
BD
LB
DL
BD
L20.5
50
R20
Sea
bre
am,
cult
ure
dF
FV
rgad
a315.5
24.4
BD
L42,0
00
BD
LB
DL
BD
LB
DL
BD
L17.5
20
R21
Mull
et,
wil
dS
avudri
ja(I
stra
)–
–B
DL
34,0
00
BD
LB
DL
BD
LB
DL
BD
L15.3
20
R22
Lee
rfish
,w
ild
Sav
udri
ja(I
stra
)–
–B
DL
39,0
00
BD
LB
DL
BD
LB
DL
BD
L16.3
40
R23
Sea
bas
s,w
ild
Sav
udri
ja(I
stra
)297.5
24.2
BD
L31,0
00
BD
LB
DL
BD
LB
DL
BD
L30.3
20
AS
34.3
723,0
79.5
74.5
26.5
5411.7
126.9
751.7
428.7
109.4
8
Min
3.5
470
0.3
50.7
17.0
73.5
40.6
12.7
7
Max
241
43,0
00
24.4
195
3,0
80
155
386
136
1,5
20
SD
75.3
317,6
64.7
87.5
61.2
7969.8
848.6
7121.9
925.7
9321.4
3
Cult
ure
d2009
AS
43.1
15,6
63.3
35.8
533.1
4524.5
129.1
965.2
346.9
3273.0
0
Min
3.5
470.0
00.3
50.7
17.0
73.5
40.6
012.7
013.0
0
Max
241.0
033,4
00.0
024.4
0195.0
03,0
80.0
0155.0
0386.0
0136.0
01,5
20.0
0
SD
96.9
413,5
88.2
49.4
679.3
01,2
51.9
461.6
4157.1
444.9
3611.0
0
BD
Lbel
ow
det
ecti
on
lim
it
Environ Geochem Health (2014) 36:19–39 27
123
Page 10
observed mean values of trace elements in fish tissues
as well as feed were mostly evidently lower than mean
concentrations in sediment (Zvab Rozic et al. 2012).
The exceptions were Hg, Se, and Zn, whose mean
concentrations in fishes exceeded their content in
sediment by up to 12.6 times (Hg). These results
indicate different sources of element origin in fish
tissues, with the most important expected to be the fish
food as well as other surrounding substances, that is,
sea water. The majority of trace elements were
Table 2 Concentrations of elements and basic statistics (mean, minimum, maximum, standard deviation) of three different fish feeds
used for feeding sea bass and sea bream on fish farms near Vrgada
Sample (2009) Pelet size (mm) Ca (lg/g) Fe (lg/g) K (lg/g) Mg (lg/g) Na (lg/g) Mn (ng/g) Ag (ng/g) As (ng/g) B (ng/g)
HR1 h = 2.5–3, r = 1.5 24,000 210 14,300 2,630 8,800 62,000 3 3,370 13,200
HR2 h = 5–6, r = 4.5 18,200 214 12,700 2,410 10,800 39,700 14 1,950 16,000
HR3 h = 6–7, r = 5.5 11,500 199 9,260 2,030 4,050 40,300 11 1,720 8,800
AS 17,900.00 207.67 12,086.67 2,356.67 7,883.33 47,333.33 9.33 2,346.67 12,666.67
Min 11,500.00 199.00 9,260.00 2,030.00 4,050.00 39,700.00 3.00 1,720.00 8,800.00
Max 24,000.00 214.00 14,300.00 2,630.00 10,800.00 62,000.00 14.00 3,370.00 16,000.00
SD 6,255.40 7.77 2,575.37 303.53 3,467.11 12,705.25 5.69 893.66 3,629.51
Sample (2009) Pelet size (mm) Ba (lg/g) Be (ng/g) Bi (ng/g) Cd (ng/g) Co (ng/g) Cr (ng/g) Cs (ng/g) Cu (ng/g) Ga (ng/g)
HR1 h = 2.5–3, r = 1.5 5 1.4 1 601 1,770 340 52.5 11,600 16
HR2 h = 5–6, r = 4.5 5 1.7 2 395 290 690 56.8 9,280 21.3
HR3 h = 6–7, r = 5.5 4 4.7 1 349 90.7 430 112 10,600 22.5
AS 4.67 2.60 1.33 448.33 716.90 486.67 73.77 10,493.33 19.93
Min 4.00 1.40 1.00 349.00 90.70 340.00 52.50 9,280.00 16.00
Max 5.00 4.70 2.00 601.00 1,770.00 690.00 112.00 11,600.00 22.50
SD 0.58 1.82 0.58 134.20 917.44 181.75 33.18 1,163.67 3.46
Sample (2009) Pelet size (mm) Ge (ng/g) Hf (ng/g) Hg (ng/g) In (ng/g) Li (ng/g) Mo (ng/g) Nb (ng/g) Ni (lg/g) Pb (ng/g)
HR1 h = 2.5–3, r = 1.5 BDL BDL 39 0.7 199 1,150 14.6 1.6 110
HR2 h = 5–6, r = 4.5 BDL 3 126 0.5 BDL 1,620 10.5 0.7 1,020
HR3 h = 6–7, r = 5.5 BDL 4 32 0.4 BDL 965 14.8 1.4 120
AS 7.07 2.80 65.67 0.53 68.69 1,245.00 13.30 1.23 416.67
Min 7.07 1.41 32.00 0.40 3.54 965.00 10.50 0.70 110.00
Max 7.07 4.00 126.00 0.70 199.00 1,620.00 14.80 1.60 1,020.00
SD 0.00 1.30 52.37 0.15 112.85 337.68 2.43 0.47 522.53
Sample (2009) Pelet size (mm) Rb (ng/g) Re (ng/g) Sb (ng/g) Sc (ng/g) Se (lg/g) Sn (ng/g) Sr (ng/g) Ta (ng/g) Te (ng/g)
HR1 h = 2.5–3, r = 1.5 6,760 0.3 15.3 14 1.1 90 49,100 2 3
HR2 h = 5–6, r = 4.5 6,960 0.2 18.6 13 2 80 74,000 1.8 3
HR3 h = 6–7, r = 5.5 6,530 0.2 12.4 13 0.7 BDL 21,400 2.5 BDL
AS 6,750.00 0.23 15.43 13.33 1.27 66.09 48,166.67 2.10 2.24
Min 6,530.00 0.20 12.40 13.00 0.70 28.28 21,400.00 1.80 0.71
Max 6,960.00 0.30 18.60 14.00 2.00 90.00 74,000.00 2.50 3.00
SD 215.17 0.06 3.10 0.58 0.67 33.12 26,312.42 0.36 1.32
Sample (2009) Pelet size (mm) Th (ng/g) Ti (ng/g) Tl (ng/g) U (ng/g) V (ng/g) W (ng/g) Y (ng/g) Zn (lg/g) Zr (ng/g)
HR1 h = 2.5–3, r = 1.5 10 4,870 10.7 35 3,780 53 28.7 158 97
HR2 h = 5–6, r = 4.5 12 2,860 3.5 25 390 11 19.3 119 149
HR3 h = 6–7, r = 5.5 20 2,610 188 34 2,650 13 64.3 158 152
AS 14.00 3,446.67 67.40 31.33 2,273.33 25.67 37.43 145.00 132.67
Min 10.00 2,610.00 3.50 25.00 390.00 11.00 19.30 119.00 97.00
Max 20.00 4,870.00 188.00 35.00 3,780.00 53.00 64.30 158.00 152.00
SD 5.29 1,238.96 104.50 5.51 1,726.10 23.69 23.74 22.52 30.92
BDL below detection limit
28 Environ Geochem Health (2014) 36:19–39
123
Page 11
positive correlated with Ca (r = 0.99–0.67), Fe (r =
0.99–0.69), Mg (r = 0.93–0.64), and Mn (r = 0.99–
0.63). In contrast, a good positive correlation was
observed between Na and only Ag, B, Ba, Cs, Hg, and
Sb (r = 0.78–0.60) and no or even a negative
correlation of all trace elements with K was found.
Among potentially the most dangerous metals,
mean concentrations of Cd, Cr, Cu, Pb, Se, and Zn
were higher in fish feed comparing to the fishes that
show possible source of these metals in feed and
bioaccumulation in fish tissues. Contrary, for As and
Hg, values were higher in fish tissues. For detailed
determination and understanding of sources and
transport mechanisms of metals, concentrations in
different segments and their chemical compounds.
Relations of metal concentrations were presented in
Fig. 2.
Comparisons of concentrations of As, Cd, Cr, Cu,
Hg, Pb, Se, and Zn between cultured and wild
fishes and with other areas
The most dangerous metals are considered to be
mercury (Hg), lead (Pb), and cadmium (Cd), while
some other essential elements, such as copper (Cu),
nickel (Ni), chromium (Cr), and zinc (Zn), can also
cause toxic effects at excessively elevated values (Cid
et al. 2001 and references therein). In this chapter,
concentrations of eight potentially toxic metals (As,
Cd, Cr, Cu, Hg, Pb, Se, and Zn) measured in cultured
and wild fish muscle are presented and discussed in
detail and compared with findings from other areas
(Table 3).
Several studies have examined the metal content of
different marine fishes (Alam et al. 2002; Canli and
Atli 2003; Burger and Gochfeld 2005; Turkmen et al.
2005; Turkmen et al. 2008; Yılmaz et al. 2007; Fallah
et al. 2011; Kucuksezgin et al. 2011; Percın et al. 2011;
Qiu et al. 2011); however, few investigations have
focused on the metal content in sea bass and sea bream
(Cid et al. 2001; Celik et al. 2004; Celik and
Oehlenschlager 2005; Dugo et al. 2006; Ersoy et al.
2006; Dural et al. 2007; Mieiro et al. 2011). Previous
studies showed that different fish species contained
different metal levels in their tissues (Canli and Atli
2003; Usero et al. 2003; Henry et al. 2004). This may
be related with the differences in ecological needs,
variations in feeding habits, swimming behavior, and
metabolic activities among different fish species,
dissimilarities in type and level of pollution of the
aquatic environment, and distinct growth rates of
species (Canli and Atli 2003; Papagiannis et al. 2004;
Demirak et al. 2006; Ricart et al. 2010). Considering
these facts, it is rather difficult to compare metal
concentrations, even for the same tissue, between
different species.
According to the data presented in Table 1, zinc has
the highest mean concentration (28.78 lg/g), followed
by arsenic (8.28 lg/g), chromium (3.88 lg/g), copper
(1.85 lg/g), selenium (1.36 lg/g), mercury (0.81
lg/g), lead (0.11 lg/g), and cadmium (0.01 lg/g).
Generally, mean concentrations of As, Cu, Hg, and Se
were higher in wild fishes, while Cd, Cr, Pb, and Zn
values were higher in cultured fishes. The average
concentrations of Cd, Cu, Pb, Se, and Zn were higher
in feed than in fishes, while As, Cr, and Hg concen-
trations were higher in fishes (Tables 1, 2). Similarly,
negative relations between feed and fishes were also
observed by Dugo et al. (2006) and Qiu et al. (2011).
These results suggest no obvious biomagnifications of
presented trace metals in farmed sea basses.
Arsenic is a metalloid that is considered toxic to
organisms (plants, animals, and humans). Mean con-
centrations of As in cultured fishes (2.67 lg/g) were
1.8 times lower than in wild fishes (4.77 lg/g). Similar
than in our study, Fallah et al. (2011) showed higher
As values in wild specimens compared to the cultured
one, while Alam et al. (2002) observed opposite trend.
Regarding the comparisons between observed cul-
tured and wild fish specimens and locations and also
due to the lower arsenic content in the fish feed used
(2.35 lg/g), other natural and anthropogenic sources
of these metals are suggested. The higher arsenic
content of wild specimens in our research was mainly
the result of wild sea bream concentrations (9.80 lg/g)
that were 2.7 times higher than cultured one, while
mean As values of wild sea basses were 2.11 lg/g and
those of cultured sea basses were even slightly higher
(2.34 lg/g). The highest concentrations among wild
fishes were measured in sea bream fish (9.80 lg/g),
following bogue (8.30 lg/g), leerfish (5.32 lg/g),
mullet (2.80 lg/g), and sea bass (2.34 lg/g).
Concentrations of As in cultured sea bass tissues
found in our research were higher than those from a
sea bass farm in Adana, Turkey (Ersoy et al. 2006).
The mean arsenic level found in red mullet in the
Adriatic Sea was higher than our observed value
(Biladzic et al. 2011).
Environ Geochem Health (2014) 36:19–39 29
123
Page 12
Fig. 2 Box-plot diagrams
of metal concentrations
between fish feed and
cultured fishes
30 Environ Geochem Health (2014) 36:19–39
123
Page 13
Cadmium is one of the non-essential and dangerous
metals for the environment and living species includ-
ing humans. In our research, the values of Cd were the
lowest among the most toxic metals presented in this
chapter. Cd concentrations were relatively high in
cultured fishes (0.016 lg/g) when compared with the
wild ones (0.011 lg/g), which is the opposite of what
were found in Japan (Alam et al. 2002) and Iran (Fallah
et al. 2011). The highest Cd concentration in sea bass
muscle was measured in cultured fishes (0.018 lg/g),
followed by wild specimens from Savudrija (0.010 lg/
g), Korcula (0.009 lg/g), and Pirovac Bay (0.006 lg/
g). Among wild fish specimens, the highest Cd values
were found in sea bass (0.011 lg/g), following bogue
(0.010 lg/g), mullet (0.007 lg/g), leerfish (0.007 lg/
g), and sea bream (0.005 lg/g).
The possible main source of cadmium for the caged
fishes was fish feed, due to its higher concentrations in
the latter (0.448 lg/g). The same ratio between pellets
and fishes was also observed in Sicily (Dugo et al.
2006). When compared with other studies, our Cd
values for cultured and wild sea bass and sea bream
were higher than those found by Celik et al. (2004) in
the eastern Mediterranean and lower than in sea bass
and sea bream samples from Turkey (Ersoy et al.
2006; Dural et al. 2007), Sicily (Dugo et al. 2006), and
Table 3 Concentrations of As, Cd, Cr, Cu, Hg, Pb, Se, and Zn (mg/kg = lg/g) observed in our research and other comparable areas
around the world
Location As Cd Cr Cu Hg Pb Se Zn
Our research; range (mean) 1.20–14.90
(3.77)
0.004–0.079
(0.011)
0.14–49.10
(4.04)
0.71–10
(1.89)
0.081–3.69
(0.63)
\0.01–0.65
(0.11)
0.5–3.0
(1.36)
12.7–136.0
(28.78)
Cultured—mean 2.672 0.016 5.252 1.792 0.174 0.143 0.870 34.320
Wild—mean 4.768 0.009 2.920 1.974 1.040 0.102 1.800 23.540
Food—mean 2.347 0.448 0.487 10.493 0.066 0.417 1.270 145.000
Sicily (Dugo et al. 2006);
sea bass
0.01–0.13 0.88–2.80 0.08–0.35 0.19–0.51 2.63–4.08
Pellets 0.190 2.730 0.340 0.580 3.310
Turkey (Dural et al. 2007);
sea bass
0.03–0.08 0.26–0.42 0.40–1.58 8.99–75.38
Sea bream 0.08–0.12 0.55–0.82 0.64–2.44 8.82–76.98
Turkey (Ersoy et al. 2006);
sea bass-cultured
0.372 nd 0.112 0.278
Portugal (Cid et al. 2001);
sea bass
6.190 0.785 0.038 11.240
Portugal (Mieiro et al. 2011);
sea bass
0.04–0.46
Mediterranean (Celik et al.
2004; Celik and
Oehlenschlager 2005);
sea bass
0.005 0.38 0.125 4.86
Sea bream 0.0003–0.0012 0.17–0.30 0.006–0.013 4.81–5.56
Adriatic Sea (Kljakovic
Gaspic et al. 2002) red
mullet
0.008–0.029 0.057–0.158
Adriatic Sea (Bilandzic et al.
2011) red mullet
0.01–70.9 0.001–0.85 0.001–57.6 0.001–2.07 0.001–0.27
Adriatic Sea (Sepe et al. 2003)
red mullet
0.001–0.003 0.008–0.026 0.009–0.003
Japan (Alam et al. 2002); wild 0.095 0.009 0.067 0.249 0.031 0.300 5.433
Cultured 0.179 0.007 0.076 0.332 0.032 0.226 5.449
Iran (Fallah et al. 2011); wild 1.119 0.13 0.63 8.398 0.292 1.201 2.324 46.742
Cultured 0.934 0.097 0.565 21.813 0.314 1.108 2.046 20.973
South Cina (Qiu et al. 2011);
cultured
0.1–10.9 0.02–0.12 0.034–0.550 0.10–2.60 0.01–1.04 0.04–3.80 3.40–26.90
nd not detected
Environ Geochem Health (2014) 36:19–39 31
123
Page 14
Portugal (Cid et al. 2001). Measured Cd values in
mullet were lower than in some locations of the
Adriatic Sea investigated by Kljakovic Gaspic et al.
(2002) and Biladzic et al. (2011), but higher than
samples observed by Sepe et al. (2003).
Chromium is an essential metal but at high levels it
can cause adverse effects in organisms. Generally,
mean Cr concentrations in cultured fishes (5.25 lg/g)
were higher than in wild ones (2.92 lg/g). The same
relation was also observed in Japan (Alam et al. 2002),
while in Iran (Fallah et al. 2011), it was reversed. The
Cr content of fish feed (0.49 lg/g) was obviously lower
than the mean values in cultured fish tissues, due to the
extremely high Cr concentrations of the smallest
sea bass samples. Without the latter values, the Cr
concentrations in fish feed exceeded those in fish
tissues (0.36 lg/g). Among the sampled sea basses, the
highest Cr concentrations were observed in specimens
from Korcula sampling site (7.07 lg/g), followed by
cultured specimens from Vrgada (6.79 lg/g), Pirovac
Bay (3.55 lg/g), and Savudrija (1.6 lg/g). Equally, Cr
values in sea bream muscles were higher in samples
from Korcula (1.60 lg/g) than in cultured specimens
(1.15 lg/g). Among wild sampled fishes, the highest
Cr concentrations were measured in sea bass (5.27
lg/g), following mullet (1.50 lg/g), leerfish (1.38 lg/g),
bogue (1.20 lg/g), and sea bass (0.93 lg/g).
Concentrations of Cr in cultured sea bass tissues from
farm near Vrgada were higher than in those from a sea
bass farm in Adana, Turkey (Ersoy et al. 2006). Cd
concentrations of mullet from Savudrija were higher than
values observed by Sepe et al. (2003) in Adriatic Sea.
Copper is an essential element for organisms’
growth and development. Mean Cu concentrations in
cultured fish tissues (1.79 lg/g) were relatively lower
than in wild fishes (1.97 lg/g), while the opposite was
the case in Japan (Alam et al. 2002) and Iran (Fallah
et al. 2011). Among wild fishes, obviously higher
concentrations were observed in bogue (10.00 lg/g),
lower in sea bass (1.33 lg/g), mullet (1.32 lg/g) and
leerfish (1.22 lg/g), and the lowest in sea bream
(1.05 lg/g). The highest Cu values of sea bass tissues
were observed in cultured samples (2.05 lg/g)
followed by samples from Savudrija (1.38 lg/g),
Korcula (1.33 lg/g), and Pirovac Bay (1.27 lg/g).
Comparison of Cu content in feeding fishes
(1.79 lg/g) and feed (10.49 lg/g) shows obviously
higher Cu concentration in latter, which indicates the
possible source of this metal in fish feed. Higher Cu
values in pellets regarding the feeding fishes were also
observed by Dugo et al. (2006). Mean Cu levels in sea
bass in the present study were higher than mean values
from the Mediterranean (Celik and Oehlenschlager
2005), the Sicilian coast (Dugo et al. 2006), Ria de
Aveiro (Cid et al. 2001), and Tuzla lagoon in Turkey
(Dural et al. 2007). Similarly, Cu concentrations of sea
bream were higher than in Turkey (Dural et al. 2007)
and from Mediterranean (Celik and Oehlenschlager
2005). Measured Cu concentrations in mullet from
Savudrija sampling location were also mostly higher
than concentrations from the Adriatic Sea observed by
Biladzic et al. (2011).
Mercury is one of the major global environmental
problems due to several adverse effects on the envi-
ronment and organisms, especially top predators
including fishes and humans. Numerous studies have
exclusively investigated mercury contamination in
fishes and its potential risk to their consumers, humans
(Liang et al. 2011; Mieiro et al. 2011; Burger and
Gochfeld 2011; Liu et al. 2012; Onsanit et al. 2012). In
our study, Hg concentrations in wild sampled fishes
(1.04 lg/g) were obviously higher than those in
cultured ones (0.17 lg/g). Fallah et al. (2011) observed
higher Hg concentration in cultured fishes, while in our
study, Hg values were higher in wild specimens.
Among the measured Hg values in sea basses, the
highest concentrations were observed in specimens
from Korcula sampling site (1.06 lg/g), followed by
specimens from Savudrija (0.19 lg/g), Pirovac Bay
(0.26 lg/g), and cultured fishes from Vrgada aquacul-
ture (0.17 lg/g). Similarly, higher values in sea bream
were measured in Korcula (1.62 lg/g) compared with
Vrgada fish farm (0.17 lg/g). Fish samples showed the
highest Hg concentrations in leerfish (2.14 lg/g),
following sea bream (0.93 lg/g), sea bass (0.73 lg/
g), mullet (0.42 lg/g), and bogue (0.14 lg/g).
Mercury levels in forage fish (0.19 lg/g) were
higher than those in feed pellets (0.07 lg/g), which
suggests that fish feed was possibly not the main
source of mercury for the caged fishes. The same
relation was observed in China (Liang et al. 2011;
Onsanit et al. 2012). The concentrations of Hg
obtained in sea bass muscle in the present study were
higher than those of the reference site and obviously
lower than those from contaminated locations in Ria
de Aveiro, Portugal (Mieiro et al. 2011). Mean Hg
values in red mullet species in the Adriatic Sea were
lower than in our samples (Biladzic et al. 2011).
32 Environ Geochem Health (2014) 36:19–39
123
Page 15
Lead is known as one of the major toxic dangerous
metals due to its natural presence even in small
amounts in all environmental segments. In our study,
Pb concentrations were relatively higher in cultured
specimens (0.14 lg/g) than in wild ones (0.10 lg/g).
Among wild sea bass, the highest Pb values were
measured in Savudrija (0.18 lg/g); lower ones were
found at the Korcula sampling location (0.008 lg/g)
and the lowest in Pirovac Bay (0.03 lg/g). Pb values
in sea bream were higher in samples from Korcula
sampling location (0.07 lg/g), lower in wild fishes
sampled around farm (0.05 lg/g) and the lowest in
cultured fishes (0.04 lg/g). Among fish specimens, the
highest Pb concentrations were observed in bogue
(0.29 lg/g), following mullet (0.16 lg/g), sea bass
(0.09 lg/g), leerfish (0.07 lg/g), and sea bream
(0.06 lg/g).
The Pb content of fish feed (0.42 lg/g) was higher
than that of forage fishes (0.18 lg/g), which was a
similar relation to that found in Sicily (Dugo et al.
2006). In comparison with other sampling areas, Pb
concentrations in sea bass muscle in our study were
similar to concentrations in the eastern Mediterranean
(Celik et al. 2004), higher than those in specimens
from Ria de Aveiro, Portugal (Cid et al. 2001), and
obviously lower than mean values from the Sicilian
coast (Dugo et al. 2006), Adana in Turkey (Ersoy et al.
2006), and Tuzla lagoon in Turkey (Dural et al. 2007).
Also, the concentrations in sea bream muscle were
lower than those from a comparable area in Turkey
(Dural et al. 2007) and higher than those found in the
Mediterranean (Celik et al. 2004). Measured Pb
concentrations in mullet from Savudrija were lower
than in specimens observed by Biladzic et al. (2011)
and Sepe et al. (2003) and higher than in samples
observed by Kljakovic Gaspic et al. (2002) in Adriatic
Sea.
Selenium can be toxic at high levels, even though it is
an essential micronutrient. Concentrations of Se were
higher in wild fishes (1.78 lg/g) compared to the
cultured one (0.87 lg/g). The same relations between
cultured and wild fishes were found in Japan (Alam et al.
2002) and Iran (Fallah et al. 2011). The concentration of
Se in sea bass tissues was in the following order: Korcula
(2.57 lg/g), Savudrija (1.10 lg/g), cultured specimens
from Vrgada (0.84 lg/g), and Pirovac Bay (0.60 lg/g).
Also in sea bream samples, the highest Se concentra-
tions were observed in samples from Korcula sampling
location (2.10 lg/g). Among wild sampled fishes, the
highest Se concentrations were measured in bogue
(2.10 lg/g), following leerfish (1.50 lg/g), sea bass (1.88
lg/g), mullet (1.50 lg/g), and sea bream (1.40 lg/g).
The Se content in fish feed (1.27 lg/g) was higher
than in cultured fishes, similar to values found in Sicily
(Dugo et al. 2006). All the Se concentrations of sea
basses in our study were higher than those observed on
the Sicilian coast (Dugo et al. 2006).
Zinc is an essential element for organisms (plants,
animals, and humans) but in high concentrations it can
be toxic. The total mean concentrations in cultured
fishes (34.32 lg/g) were 1.4 times higher than in wild
fishes (23.54 lg/g). The opposite relation was observed
in Iran (Fallah et al. 2011), while Alam et al. (2002)
presented comparable Zn values in cultured and wild
fishes. The obviously high Zn content in fish feed
(145 lg/g) may be the main source of this metal.
Among all sampled sea basses, the observed mean Zn
concentrations were highest in cultured specimens
(41.69 lg/g), lower in specimens from Korcula and
Savudrija sampling sites (30.60 and 30.30 lg/g,
respectively), and lowest in those from Pirovac Bay
(21.60 lg/g). In contrast, the Zn concentrations in sea
bream muscles were higher in wild specimens, which
suggest there are also other natural or anthropogenic
sources of zinc. Among sampled wild specimens, the
highest Zn concentrations were measured in sea bass
(28.80 lg/g), following leerfish (22.53 lg/g), bogue
(21.90 lg/g), sea bream (16.85 lg/g), and mullet
(15.30 lg/g).
Our results for sea bass tissues were obviously
higher than those found for fishes from the eastern
Mediterranean (Celik and Oehlenschlager 2005), the
Tyrrhenian and Sicilian Sea (Dugo et al. 2006), and
Ria de Aveiro, Portugal (Cid et al. 2001). The reason
may be that fish feed from Vrgada fish farm had an
evidently higher Zn concentration (our research,
145 lg/g) than that from the Sicilian coast (3.31
lg/g). The mean Zn levels of sea bass from Tuzla
Lagoon, Turkey, were higher (Dural et al. 2007) than
in our study in winter and spring but lower in autumn.
However, Zn values in sea bream were higher in spring
and autumn and lower in winter.
Between presented potentially toxic elements,
Pearson correlation coefficients were calculated and
presented in Table 4. High positive correlations were
observed between Cd, Cr, Cu, Pb, and Zn (r =
1.00–0.86) that may present anthropogenic source of
these elements (fish farming). As and Hg were high
Environ Geochem Health (2014) 36:19–39 33
123
Page 16
positive correlated (r = 0.98), while with other
elements correlations were weak. Because Hg was
highly correlated with majority of major elements, its
source is probably geogenic. Se was low correlated
with practically all trace and also major elements,
exception is only Hg with medium correlation
(r = 0.43).
Selenium:mercury molar ratios and Se-HBV
Selenium (Se) was found to be significant element in
the prevention of mercury (Hg) toxicity. Interactions
between these two elements and their molar ratios in
seafood are essential factors in evaluating risk asso-
ciated with dietary Hg exposure (Kaneko and Ralston
2007). Numerous studies have shown that Se coun-
teracts the adverse impacts of Hg exposure (Ganther
et al. 1972; Kaneko and Ralston 2007; Ralston et al.
2007; Ralston 2008; Ralston et al. 2008; Burger and
Gochfeld 2011). The main effect that reduces Hg
toxicity is high binding affinity between Se and Hg
that protects direct sequestration of Hg by Se (Kaneko
and Ralston 2007). There were known also some other
Hg interactions with Se that protect Hg toxicity
(Ralston 2008). The Se:Hg molar ratios are widely
used as essential criteria of risk for Hg exposure. When
the molar ratio is above 1, Se content exceeds Hg but
when the Se:Hg ratio is\1, molar excess of Hg over
Se is presented.
To simplify assessment of Se-specific nutritional
benefits in relation to potential Hg exposure risk
associated with seafood, the Se health benefit value
(Se-HBV) was proposed by Kaneko and Ralston
(2007). This value is calculated using the following
formula: Se-HBV = (Se/Hg molar ratio x total Se)
- (Hg/Se molar ratio x total Hg). The negative Se-
HBV indicates the health risk, while positive value
shows the expected health benefits.
In our research, Se:Hg molar ratios of different
cultured and wild fish species were defined as well as
Se-HBV was calculated. The results were presented in
Table 5. Calculated mean Se:Hg molar ratios showed
values between 2.30 and 28.94, which was a molar
excess of Se over Hg. No excess of Hg over Se was
observed. The higher mean molar ratio was found in
wild bogue tissue (38.94), following cultured sea
bream (14.16), cultured sea bass (12.31), wild mullet
(9.07), wild sea bass (6.56), wild sea bream (3.82), and
wild leerfish (2.30). Presented molar ratios were also in
accordance with total Hg concentrations observed in
fish species, where the highest mean values were
measured in leerfish samples and the lowest in bogue.
Calculated selenium health benefit values showed on
the whole positive values (from 51.57 to 1,035.63).
Regarding these values, observed fish species followed
the following order: wild bogue (1,035.63) [ cultured
sea bream (173.91) [ wild mullet (172.13) [ wild sea
bass (155.60) [ cultured sea bass (130.86) [ wild sea
bream (66.59) [ wild leerfish (51.57).
Calculated molar ratios and Se-HBV values
showed that Se in all sampled fish samples had
positive influences of Hg toxicity and consequently
consumption of these fish in human nutrition is not
risk.
Comparisons with standards and guidelines
There are several references for acceptable levels of
metals in marine and freshwater fish. Concentrations
Table 4 Pearson correlation coefficient for metals (As, Cd, Cr, Cu, Hg, Pb, Se, Zn) in fish tissues
Element As Cd Cr Cu Hg Pb Se Zn
As 1.000
Cd 0.175 1.000
Cr -0.152 0.911 1.000
Cu -0.291 0.858 0.915 1.000
Hg 0.956 0.159 -0.100 -0.269 1.000
Pb -0.085 0.939 0.990 0.910 -0.051 1.000
Se 0.180 -0.016 0.143 -0.044 0.428 0.100 1.000
Zn -0.108 0.919 0.953 0.934 -0.056 0.957 0.140 1.000
Bold numbers are significant in p [ 0.05
34 Environ Geochem Health (2014) 36:19–39
123
Page 17
of eight elements (As, Cd, Cr, Cu, Hg, Pb, Se, and Zn)
in cultured and wild fishes were compared with the
recommended dietary allowance and guidelines pro-
posed by various authorities: the Ministry of Agricul-
ture, Fisheries and Food (MAFF 1995, 2000), the
United Nations Food and Agriculture Organization
(FAO), which published the ‘‘Compilation of Legal
limits for Hazardous Substances and Fish and Fishery
Products’’ (Nauen 1983), the European Commission
(EC 2001), Croatian legislation (Ordinance 2008),
Spanish legislation (BOE 1991), and Turkish legisla-
tion (TKB 2002), as shown in Table 6.
Generally, the mean concentrations of As and Cr
obtained in cultured and wild fish specimens were
higher than those established by the regulations
presented in Table 5. Mean values of other presented
trace metals (Cd, Cu, Hg, Pb, Se, and Zn) were below
the permissible levels, with the exception of Hg in
wild fish samples, which exceeded them.
If we focused on the cultured specimens, the
majority of As concentrations were found to be higher
than the permissible level, while concentrations of
most other trace elements were lower. The only
exception was found in the smallest sea basses, which
also had Cr, Pb, and Zn levels above the recommended
limits. In commercially interesting fishes, metal con-
centrations mostly not exceeded the permissible
levels, the only exception was As, that can be due to
higher values potentially toxic for humans. However,
due to total As concentrations presented in this paper,
for detailed estimations separate chemical forms of As
should be known.
In wild fishes, concentrations of Cd, Cu, and Pb
were on the whole lower than recommended values,
while values of other metals (As, Cr, Hg, Se, and Zn)
often exceeded the permissible levels. Obviously
elevated values of As, Cr, Hg, Se, and Zn were
measured in almost all wild fishes collected at Korcula
sampling site, which represented the most southerly
location in the Adriatic Sea of our research. Higher
concentrations of As, Cr, Hg, and Se were also
observed in practically all wild leerfish samples.
Table 6 Standards of trace elements in fish recommended by
the Ministry of Agriculture, Fisheries and Food (MAFF 1995,
2000), the United Nations Food and Agriculture Organization
(FAO; Nauen 1983), the European Commission (EC 2001),
Croatian legislation (CRL; Ordinance 2008), Spanish legisla-
tion (BOE 1991), and Turkish legislation (TKB 2002). Values
are express in lg/g = mg/kg ww
Authority As Cd Cr Cu Hg Pb Se Zn
MAFF (1995, 2000) 0.2 20 0.3 2 50
FAO (Nauen 1983) 1.4 0.3 1 20 0.5 2 2 50
EC (2001) 2 0.05–0.3 0.5–1.0 0.3
Croatian (Ordinance 2008) 2 0.05–0.3 0.5–1.0 0.3
Spanish (BOE 1991) 0.1 20 1 2
Turkish (TKB 2002) 0.1 20 1 50
Table 5 Mass and molar concentrations, molar ratios of Se and Hg and calculated Se-HBV in cultured and wild fish species from
Adriatic Sea
Fish type Hg content
(lg Hg/g)
lmol Hg/kg Se content
(lg Se/g)
lmol Se/kg Molar ratios
(Se/Hg)
Hg/Se Free Se
(Se-Hg)
Se-HBV
Sea bass (cultured) 0.17 0.86 0.84 10.638 12.31 0.08 9.77 130.86
Sea bass (wild) 0.73 3.63 1.88 23.810 6.56 0.15 20.18 155.60
Sea bream (cultured) 0.17 0.87 0.97 12.285 14.16 0.07 11.42 173.91
Sea bream (wild) 0.93 4.64 1.40 17.730 3.82 0.26 13.09 66.59
Leerfish (wild) 2.14 10.67 1.93 24.485 2.30 0.44 13.82 51.57
Bogue (wild) 0.14 0.68 2.10 26.596 38.94 0.03 25.91 1,035.63
Mullet (wild) 0.42 2.09 1.50 18.997 9.07 0.11 16.90 172.13
Environ Geochem Health (2014) 36:19–39 35
123
Page 18
Relations between fish size and metal
concentrations
A further aim of the study was to investigate the
relationship between heavy metal concentrations in
fish tissues and their length and weight. Several studies
show that sizes of marine animals play an important
role in metal contents in their tissues. Analyses mostly
indicated a significant negative relationship between
metal concentrations and fish size (Al-Yousuf et al.
2000; Nussey et al. 2000; Widianarko et al. 2000;
Canli and Atli 2003; Henry et al. 2004). However,
different groups of marine animals showed a positive
relationship between mercury level and animal size
(Canli and Atli 2003). In our investigation, concen-
trations of elements in four different sizes of cultured
sea bass specimens were measured. In this chapter,
only concentrations of eight trace metals (As, Cd, Cr,
Cu, Hg, Pb, Se, and Zn) have been presented in detail
(Table 7). Our results showed that generally there was
a negative relationship between fish size and metal
level. The highest metal concentrations were observed
in the smallest/younger sea basses (R13; 15 g weight
and 6–8 cm length). The content of all metals
decreases with increases in the weight and length of
sea bass. Therefore, the lowest concentrations of As,
Se, and Zn were found in the biggest/older sea bass
(R16; 312.2 g weight and 25.2 cm length). The lowest
values of Cd, Cr, Cu, Hg, and Pb were measured in the
sea bass medium size (R15; 204.8 g weight and
16.4 cm length), while the concentrations in the
biggest sea bass were again slightly elevated.
Previous studies ascertained that one of the most
important factors that play an important role in heavy
metal accumulation in marine animals is the metabolic
activity (Heath 1987; Langston 1990; Roesijadi and
Robinson 1994). The metabolic activity of young
individuals is normally higher than that of older
specimens. Therefore, metal accumulation was shown
to be higher in younger individuals than in older ones
(Nussey et al. 2000; Widianarko et al. 2000; Canli and
Atli 2003). It was also indicated that metal accumu-
lation could reach a steady state after a certain age
(Douben 1989). The negative relationship in our study
between metal content and fish size can therefore be
explained by the difference in metabolic activity
between younger and older fishes. Slightly elevated
values of some elements in the oldest fishes are
ascribed to a steady-state stage of our species.
Nevertheless, they can be explained by higher metal
concentrations of potential sources, for example,
water.
Conclusions
In the present study, elemental analyses of cultured sea
bass D. labrax and sea bream S. aurata from a fish
farm near Vrgada Island in Central Adriatic were
carried out with the aim of assessing the role of
aquaculture activity in element content in fishes. The
results were compared with the element content in fish
food and wild fish specimens from other locations in
Adriatic Sea as well as with guidelines proposed by
various authorities. Additionally, relations between
fish size and metal concentrations were established.
The concentrations of major elements (Ca, Fe, Mg,
Na, and Mn) in the investigated cultured fish samples
were generally lower than in their feed, the exception
is K. The average concentrations of Cd, Cr, Cu, Pb, Se,
and Zn in feed were higher than in feeding fishes,
while As and Hg concentrations were higher in fishes.
Generally, mean concentrations of Cd, Cr, Pb, and
Zn were higher in cultured fish samples, while
Table 7 Concentrations of eight trace metals (As, Cd, Cr, Cu, Hg, Pb, Se, and Zn) in four different sizes of cultured sea bass muscle
Sample Location Weight
(g)
Length
(cm)
As
(ng/g)
Cd
(ng/g)
Cr
(ng/g)
Cu
(ng/g)
Hg
(ng/g)
Pb
(ng/g)
Se
(lg/g)
Zn
(lg/g)
R3 (sea bass,
cultured)
FF Vrgada XS 15.0 6.0–8.0 4,010 78.7 49,100 4,850 274 650 0.8 136
R4 (sea bass,
cultured)
FF Vrgada S 103.6 12.3 3,640 9.9 290 1,770 122 10 0.9 42.4
R5 (sea bass,
cultured)
FF Vrgada M 204.8 16.4 2,300 8.3 140 1,860 106 20 0.9 38.7
R6 (sea bass,
cultured)
FF Vrgada L 312.2 25.2 1,640 11.2 850 2,330 136 \10 0.5 23.2
36 Environ Geochem Health (2014) 36:19–39
123
Page 19
concentrations of As, Cu, Hg, and Se were higher in
wild fish. The highest concentrations were measured
in wild sampled specimens in almost all fishes
collected at Korcula Island. The results suggest that
besides the most expected source, fish feed, there are
likely to be other potential natural and/or anthropo-
genic sources of elements, such as sea water or
sediment, etc.
Selenium:mercury molar ratios (on the whole
above 1) and positive Se-HBVs (selenium health
benefit values) indicated that Se positively affects Hg
toxicity. Therefore, the Hg exposure due to fish
consumption showed no risk for human health.
Mean Cd, Cu, Hg, Pb, Se, and Zn values of cultured
fish samples were below the permissible levels with
the exceptions of As and Cr, whose levels were higher.
Values of As and Cr were high mainly due to the
juvenile non-commercial sea basses, which also
showed elevated concentrations of some other metals
(Pb and Zn). Mean values of Cd, Cu, Pb, Se, and Zn in
wild specimens were lower than the recommended
levels, while mean values of As, Cr, and Hg exceeded
the recommended limits.
The results of cultured sea basses showed a
generally negative relationship between fish size and
metal level; that is, metal levels decreased with
increases in the weight and length of fishes.
Therefore, in our large, that is, commercial,
cultured fish samples only arsenic was found to be
slightly above the recommended legal limits and
consequently potentially toxic for human consump-
tion. Moreover, arsenic concentrations in cultured
fishes were lower than in wild ones. Other metals
present no problems for the consumption of muscle of
these fish.
Acknowledgments The research was financially supported by
the Ministry of Higher Education, Science and Technology,
Republic of Slovenia (Bilateral projects between Croatia and
Slovenia 2001–2009), the Slovenian Research Agency (ARRS),
and Geoexp, d.o.o., Trzic, Slovenia. Thanks are also due to my
husband Bostjan Rozic for his technical and moral support.
References
Alam, M. G. M., Tanaka, A., Allinson, G., Laurenson, L. J. B.,
Stagnitti, F., & Show, E. T. (2002). A comparison of trace
element concentrations in cultured and wild carp (Cyprinus
carpio) of Lake Kasumigaura, Japan. Ecotoxicology and
Environmental Safety, 53, 348–354.
Al-Yousuf, M. H., El-Shahawi, M. S., & Al-Ghais, S. M. (2000).
Trace metals in liver, skin and muscle of Lethrinus lentjan
fish species in relation to body length and sex. Sciences of
Total Environment, 256, 87–94.
Ames, B. M. (1998). Micronutrients prevent cancer and delay
ageing. Toxicology Letters, 102, 5–18.
Belias, C., & Dassenakis, M. (2002). Environmental problems in
the development of marine fish-farming in the Mediterra-
nean Sea. Ocean Challenge, 12(1), 11–16.
Biladzic, N., Ðokic, M., & Sedak, M. (2011). Metal content
determination in four fish species from the Adriatic Sea.
Food Chemistry, 124, 1005–1010.
BOE (Boletın Oficial del Estado or Official Gazette). (1991).
Normas microbiologicas, lımites de contenido en metales
pesados y metodos analıticos para la determinacion de
metales pesados para los productos de la pesca y de la
agricultura (Microbiological standards, limits on heavy
metal content, and analytical methods for determining the
heavy metal content of fishery and agricultural products).
In BOE (Eds.) (p. 5937–5941). August 2 Order. Madrid,
Spain.
Burger, J., & Gochfeld, M. (2005). Heavy metals in commercial
fish in New Jersey. Environmental Research, 99, 403–412.
Burger, J., & Gochfeld, M. (2011). Mercury and selenium levels
in 19 species of saltwater fish from New Jersey as a func-
tion of species, size, and season. Science of the Total
Environment, 409, 1418–1429.
Burger, J., Gochfeld, M., Jeitner, C., Burke, S., & Stamm, T.
(2007). Metal levels in flated sole (Hoppoglossoides
elassodon) and great sculpin (Myoxocephalus polyacan-
thocephalus) from Adak Island, Alaska: Potential risk to
predators and fishermen. Environmnetal Research, 103,
62–69.
Canli, M., & Atli, G. (2003). The relationship between heavy
metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six
Mediterranean fish species. Environmental Pollution, 121,
129–136.
Celik, U., Cakli, S., & Oehlenschlager, J. (2004). Determination
of the lead and cadmium burden in some northeastern
Atlantic and Mediterranean fish species by DPSAV.
European Food Research and Technology, 218, 298–305.
Celik, U., & Oehlenschlager, J. (2005). Zinc and cooper content
in marine fish samples collected from the eastern Medi-
terranean Sea. European Food Research and Technology,
220, 37–41.
Cid, B. P., Boia, C., Pombo, L., & Rebelo, E. (2001). Deter-
mination of trace metals I fish species of the Ria de Aveiro
(Portugal) by electrothermal atomic absorption spectrom-
etry. Food Chemistry, 75, 93–100.
Copat, C., Bella, F., Castaing, M., Fallico, R., Sciacca, S., &
Ferrante, M. (2012). Heavy metals concentrations in fish
from Sicily (Mediterranean Sea) and evaluation of possible
health risks to consumers. Bulletin of Environmental
Contamination and Toxicology, 80, 78–83.
Demirak, A., Yilmaz, F., LeventTuna, A., & Ozdemir, N.
(2006). Heavy metals in water, sediment and tissues of
Leuciscus cephalus from a stream in southwestern Turkey.
Chemosphere, 63, 1451–1458.
Douben, P. E. (1989). Lead and cadmium in stone loach (Noe-
macheilus barbatulus L.) from three rivers in Derbyshire.
Ecotoxicology and Environmental Safety, 18, 35–58.
Environ Geochem Health (2014) 36:19–39 37
123
Page 20
Dugo, G., La Pera, L., Bruzzese, A., Pellicano, T. M., & Lo
Turco, V. (2006). Concentration of Cd (II), Cu (II), Pb (II),
Se (IV) and Zn (II) in cultured sea bass (Dicentrarchus
labrax) tissues from Tyrrhenian Sea and Sicilian Sea by
derivative stripping potentiometry. Food Control, 17,
146–152.
Dural, M., Goksu, M. Z. L., & Ozak, A. A. (2007). Investigation
of heavy metals in economically important fish species
captured from Tuzla lagoon. Food Chemistry, 102,
415–421.
EC. (2001). Commission Regulation (EC) No 466/2001of 8
March 2001 setting maximum levels for certain contami-
nants in foodstuffs. Official Journal of the European
Communities, L77, 1–25.
Ersoy, B., Yanar, Y., Kucukgulmez, A., & Celik, M. (2006).
Effects of four cooking methods on the heavy metal con-
centrations of sea bass fillets (Dicentrarchus labrax Linne,
1785). Food Chemistry, 99, 748–751.
Evans, D. W., Dodoo, D. K., & Hanson, P. J. (1993). Trace
element concentrations in fish livers. Implications of
variations with fish size in pollution monitoring. Marine
Pollution Bulletin, 26(6), 329–334.
Fallah, A. A., Saei-Dehkordi, S. S., Nematollahi, A., & Jafari, T.
(2011). Comparative study of heavy metal and trace ele-
ment accumulation in edible tissues of farmed and wild
rainbow trout (Oncorhynchus mykiss) using ICP-OES
technique. Microchemical Journal, 98, 275–279.
Fernandes, C., Fontaınhas-Fernandes, A., Peixoto, F., & Sal-
gado, M. A. (2007). Bioaccu- mulation of heavy metals in
Liza saliens from the Esmoriz-Paramos coastal lagoon,
Portugal. Ecotoxicology and Environmental Safety, 66,
426–431.
Ganther, H. E., Goudie, C., Sunde, M. L., Kopecky, M. J.,
Wagner, P., Oh, S.-H., et al. (1972). Relation to decreased
toxicity of methylmercury added to diets containing tuna.
Science, 72, 1122–1124.
Heath, A. G. (1987). Water pollution and fish physiology.
Florida: CRC press.
Henry, F., Amara, R., Courcot, L., Lacouture, D., & Bertho,
M.-L. (2004). Heavy metals in four fish species from the
French coast of the Eastern English Channel and Southern
Bight of the North Sea. Environmental International, 30,
675–683.
Kalay, M., & Canli, M. (2000). Elimination of essential (Cu, Zn)
and non-essential (Cd, Pb) metals from tissues of a fresh-
water fish Tilapia zilli. Turk Zooloji Dergisi, 24, 429.
Kaneko, J. J., & Ralston, N. V. C. (2007). Selenium and mercury
in pelagic fish in the central north Pacific near Hawaii.
Biological Trace Metal Research, 119, 242–254.
Kljakovic Gaspic, Z., Zvonaric, T., Vrgoc, N., Odzak, N., &
Baric, A. (2002). Cadmium and lead in selected tissues of
two commercially important fish species from the Adriatic
Sea. Water Research, 36, 5023–5028.
Kucuksezgin, F., Kontas, A., & Uluturhan, E. (2011). Evalua-
tions of heavy metal pollution in sediment and Mullus
barbatus from Izmir Bay (Eastern Aegean) during
1997–2009. Marine Pollution Bulletin, 62, 1562–1571.
Langston, W. J. (1990). Toxic effects of metals and the inci-
dence of marine ecosystems. In R. W. Furness & P.
S. Rainbow (Eds.), Heavy metals in the marine environ-
ment. New York: CRC Press.
Liang, P., Shao, D.-D., Wu, S.-C., Shi, J.-B., Sun, X.-L., Wu, F.-
Y., et al. (2011). The influence of mariculture in the mer-
cury distribution in sediments and fish around Hong Kong
and adjacent mainland China waters. Chemosphere, 82,
1038–1043.
Liu, B., Yan, H., Wang, C., Li, Q., Guedron, S., Spangenberg,
J. E., et al. (2012). Insight into low fish mercury bioaccu-
mulation in a mercury-contaminated reservoir, Guizhou,
China. Environmental Pollution, 160, 109–117.
Maceda-Veiga, A., Monroy, M., & de Sostoa, A. (2012). Metal
bioaccumulation in the Mediterranean barbel (Barbus
meridionalis) in a Mediterranean River receiving effluents
from urban and industrial wastewater treatment plants.
Ecotoxicology and Environmental Safety, 76, 93–101.
MAFF (Ministry of Agriculture, Fisheries and Food). (1995).
Monitoring and surveillance of non-radioactive contami-
nants in the aquatic environment and activities regulating
the disposal of wastes at sea, 1993. Aquatic Environment
Monitoring Report, No. 44. Directorate of Fisheries
Research, Lowestoft, UK.
MAFF (Ministry of Agriculture, Fisheries and Food). (2000).
Monitoring and surveillance of non-radioactive contami-
nants of wastes at Sea, 1997. Aquatic Environment Mon-
itoring Report No. 52. Center for Environment Fisheries
and Aquaculture Science. Lowestoft, UK.
Mieiro, C. L., Pacheco, M., Duarte, A. C., & Pereira, M. E.
(2011). Fish consumption and risk of contamination by
mercury—Considerations on the definition of edible parts
based on the case study of European sea bass. Marine
Pollution Bulletin, 62, 2850–2853.
Muzimic, P. (1966). Osnovna geoloska karta SFRJ 1: 100.000.
Tumac za list Sibenik K 33-8. Zvezni geoloski zavod Be-
ograd, Beograd.
Nauen, C. E. (1983). Compilation of legal limits for hazardous
substances in fish and fishery products. Rome: United
Nations Food and Agriculture Organization.
Nussey, G., Van Vuren, J. H. J., & du Preez, H. H. (2000).
Bioaccumulation of chromium, manganese, nickel and lead
in the tissues of the moggel, Labeo umbratus (Cyprinidae),
from Witbank dam, Mpumalanga. Water Sa, 26, 269–284.
Onsanit, S., Chen, M., Ke, C., & Wang, W.-X. (2012). Mercury
and stable isotope signatures in caged marine fish and fish
feeds. Journal of Hazardous Materials, 203–204, 13–21.
Ordinance, (2008). Ordinance setting maximum levels for cer-
tain contaminants in foodstuffs. Official Gazette, 154,
4198.
Papagiannis, I., Kagalou, I., Leonardos, J., Petridis, D., & Kal-
fakakou, V. (2004). Cooper and zinc in four freshwater fish
species from Lake Pamvotis (Greece). EnvironmentalInternational, 30, 357–362.
Percın, F., Sogut, O., Altınelataman, C., & Soylak, M. (2011).
Some trace elements in front and rear dorsal ordinary
muscles of wild and farmed Bluefin tuna (Thunnus fhynnus
L.1758) in Turkish part of the eastern Mediterranean Sea.
Food and Chemical Toxicology, 49, 1006–1010.
Poli, M. B., Parisi, G., Zambracavallo, G., Mecotti, L., Lupi, P.,
Gualtieri, M., et al. (2001). Quality outline of European sea
bass reared in Italy: Shelf life, edible yield, nutritional and
dietetic traits. Aquaculture, 202, 303–315.
Qiu, Y.-W., Lin, D., Liu, J.-Q., & Zeng, E. Y. (2011). Bioac-
cumulation of trace metals in farmed fish from South China
38 Environ Geochem Health (2014) 36:19–39
123
Page 21
and potential risk assessment. Ecotoxicology and Envi-
ronmental Safety, 74, 284–293.
Ralston, N. V. C. (2008). Selenium health benefit values as
seafood safety criteria. EcoHealth, 5, 442–455.
Ralston, N. V. C., Balckwell, J. L., & Raymond, L. J. (2007).
Importance of molar ratios in selenium-dependent protec-
tion against methylmercury toxicity. Biological Trace
Metal Research, 119, 255–268.
Ralston, N. V. C., Ralston, C. R., Balckwell, J. L., & Raymond,
L. J. (2008). Dietary and tissue selenium in relation to
methylmercury toxicity. Neuro Toxicology, 29, 802–811.
Ricart, M., Guasch, H., Barcelo, D., Brix, R., Conceicao, M. H.,
Geiszinger, A., et al. (2010). Primary and complex stressors
in polluted mediterranean rivers: Pesticide effects on bio-
logical communities. Journal of Hydrology, 383, 52–61.
Roesijadi, G., & Robinson, W. E. (1994). Metal regulation in
aquatic animals: Mechanism of uptake, accumulation and
release. In D. C. Malins & G. K. Ostrander (Eds.), Aquatic
toxicology (molecular, biochemical and cellular perspec-
tives). London: Lewis Publishers.
Sepe, A., Ciaralli, L., Ciprotti, M., Giordano, R., Funari, E., &
Costantini, S. (2003). Determination of cadmium, chro-
mium, lead and vanadium in six fish species from the Adri-
atic Sea. Food Additives & Contaminants, 20(6), 543–552.
TKB. (2002). Fisheries laws and regulations. Ministry of
Agriculture and Rural Affairs, Conservation and Control
General Management. Ankara, Turkey.
Tovar, A., Moreno, C., Manuel-Vez, M. P., & Garcıa-Vergas,
M. (2000). Environmental impacts of intensive aquaculture
in marine waters. Water Research, 34, 334–342.
Turkmen, A., Turkmen, M., Tepe, Y., & Akyurt, I. (2005).
Heavy metals in three commercially valuable fish species
from Iskenderun Bay, Northern East Mediterranean sea,
Turkey. Food Chemistry, 91, 167–172.
Turkmen, M., Turkmen, A., Tepe, Y., Ates, A., & Gokkus, K.
(2008). Determination of metal contaminations in sea
foods from Marmara, Aegean and Mediterranean seas:
Twelve fish species. Food Chemistry, 108, 794–800.
Usero, J., Izquierdo, C., Morillo, J., & Gracia, I. (2003). Heavy
metals in fish (Solea vulgaris, Anguilla Anguilla and Liza
aurata) from salt marshes on the southern Atlantic coast of
Spain. Environmental International, 29, 949–956.
Uysal, K., Kose, E., Bulbul, M., Donmez, M., Erdogan, Y.,
Koyun, M., et al. (2009). The comparison of heavy metal
accumulation ratios of some fish species in Enne Dame
Lake (Kutahya/Turkey). Environmental Monitoring and
Assessment, 157, 355–362.
Verbovsek, T. (2011). A comparison of parameters below the
limit of detection in geochemical analyses by substitution
methods. Materials and Geoenvironment, 58(4), 393–404.
Widianarko, B., Van Gestel, C. A. M., Verweij, R. A., & Van
Straalen, N. M. (2000). Associations between trace metals
in sediment, water, and guppy, Poecilia reticulata (Peters),
from urban streams of Samarang, Indonesia. Ecotoxicology
and Environmental Safety, 46, 101–107.
Yılmaz, F., Ozdemir, N., Demirak, A., & Tuna, A. L. (2007).
Heavy metal levels in two fish species Leuciscus cephalus
and Lepomis gibbosus. Food Chemistry, 100, 830–835.
Zvab Rozic, P., Dolenec, T., Bazdaric, B., Karamarko, V., &
Dolenec, M. (2012). Major, minor and trace element con-
tent derived from aquacultural activity of marine sediments
(Central Adriatic, Croatia). Environmental Science and
Pollution Research, 19, 2708–2712.
Environ Geochem Health (2014) 36:19–39 39
123
