Environmental Pollution 121 (2003) 129–136

www.elsevier.com/locate/envpol

The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn)
levels and the size of six Mediterranean fish species
Mustafa Canli*, Gülüzar Atli
Department of Biology, Faculty of Arts and Sciences, University of Çukurova, 01330 Adana, Turkey

Received 29 March 2001; accepted 15 March 2002

‘‘Capsule’’: Significant relationships between metal concentrations and fish size were negative.

Abstract
Heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) concentrations in the muscle, gill and liver of six fish species (Sparus auratus, Atherina
hepsetus, Mugil cephalus, Trigla cuculus, Sardina pilchardus and Scomberesox saurus) from the northeast Mediterranean Sea were
measured and the relationships between fish size (length and weight) and metal concentrations in the tissues were investigated by
linear regression analysis. Metal concentrations (as mg/g d.w.) were highest in the liver, except for iron in the gill of Scomberesox
saurus and lowest in the muscle of all the fish species. Highest concentrations of Cd (4.50), Cr (17.1) and Pb (41.2) were measured in
liver tissues of T. cuculus, Sardina pilchardus and A. hepsetus, respectively. The liver of M. cephalus showed strikingly high Cu
concentrations (202.8). The gill of Scomberesox saurus was the only tissue that showed highest (885.5) iron concentrations.
Results of linear regression analysis showed that, except in a few cases, significant relationships between metal concentrations and
fish size were negative. Highly significant (P< 0.001) negative relationships were found between fish length and Cr concentrations in
the liver of A. hepsetus and M. cephalus, and Cr concentrations in the gill of T. cuculus. Cr and Pb concentrations in the liver and
Cu concentrations in all the tissues of Scomberesox saurus also showed very significant (P< 0.001) negative relationships. Negative
relationships found here were discussed. # 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Heavy metal; Fish; Length; Weight; Accumulation

1. Introduction Roesijadi and Robinson, 1994; Kalay et al., 1999; Kalay

Heavy metals like copper, zinc and iron are essential
for fish metabolism while some others such as mercury,
cadmium and lead have no known role in biological
systems. For the normal metabolism of fish, the essen-
tial metals must be taken up from water, food or sedi-
ment. However, similar to the route of essential metals,
non-essential ones are also taken up by fish and accu-
mulate in their tissues. Studies from the field and
laboratory experiments showed that accumulation of
heavy metals in a tissue is mainly dependent upon water
concentrations of metals and exposure period, although
some other environmental factors such as salinity, pH,
hardness and temperature play significant roles in metal
accumulation. Ecological needs, sex, size and molt of
marine animals were also found to affect metal accu-
mulation in their tissues (Heath, 1987; Langston, 1990;
Bryan and Langston, 1992; Canli and Furness, 1993b;
* Corresponding author. Fax: +90-322-3386070.
E-mail address: mcanli@mail.cu.edu.tr (M. Canli).
0269-7491/03/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved.
PII: S0269-7491(02)00194-X
and Canli, 2000).
The sizes of marine animals have been shown to play
an important role in metal contents of tissues. However,
this evidence was consistent generally for mercury in
different groups of marine animals. For example, mussel
(Cossa and Rondeau, 1985), decapod crustacean (Canli
and Furness, 1993a,b), fish (Barak and Mason, 1990;
Monteiro and Lopes, 1990), marine mammals (Law et
al., 1991) and seabirds (Furness et al., 1986) in the
marine food-chain showed a positive relationship
between mercury levels and animal sizes. This is also an
important point for the food-chain as mercury increases
through the upper level, ending up in the diet of
humans. Nevertheless, this consistent relationship
between mercury and animal size may not be seen for
other metals because they do not have a consistent and
strong trend for a relationship with animal sizes (White
and Rainbow, 1987; Barak and Mason, 1990; Law et al.,
1991; Canli and Furness, 1993a,b; McCoy et al., 1995;
Nussey et al., 2000; Al-Yousuf et al., 2000). Therefore,
it is important to understand better the relationships
130 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136

between animal size and concentrations of both essen-
tial and non-essential metals. Fish of northeast Medi-
terranean Sea have not been examined to our
knowledge on the relationships between tissue metal
concentrations and fish size. Thus, the aim of this
study is to determine heavy metal (Cd, Cr, Cu, Fe, Pb,
Zn) levels in muscle, gill and liver tissues of six fish
species (Sparus auratus, Atherina hepsetus, Mugil
cephalus, Trigla cuculus, Sardina pilchardus, and Scom-
beresox saurus) from the northeast Mediterranean Sea
and to investigate the relationships between fish size
(length and weight) and metal concentrations in the
tissues.
Statistical analysis of data was carried out using SPSS
statistical package programs. Data used here were plot-
ted on graphs to see their distributions. Data showed
mostly normal distribution or close to normal distribu-
tion and therefore, no transformation was done for sta-
tistical analyses. The linear regression analyses were
applied to data to compare the relationships between
size and heavy metal concentrations in the tissues. The
same tissues from the fishes were also compared by one-
way ANOVA.
3. Results

Table 1 shows numbers of fishes sampled, length and

2. Materials and methods weight ranges and their relationships. Table 2 shows
mean metal concentrations in the tissues of fishes and
The gilthead Sparus auratus, sand smelt A. hepsetus, their standard deviations.
grey mullet M. cephalus, red gurnard T. cuculus, sardine Highest cadmium concentrations were found in the
Sardina pilchardus and saury pike Scomberesox saurus liver of red gurnard, while lowest cadmium concentra-
used in this study were sampled by local fisherman from tions were always found in muscle tissues of the fishes.
the northeast Mediterranean Sea (Karataş, 36 320 N 35 Lead concentrations in the tissues were much higher
10 E; Turkey). The fishes were purchased from the local than the concentrations of cadmium, especially in the
fisherman in the same day of capture and brought to the liver and gill. Highest copper concentrations were in
laboratory on ice immediately and then frozen at 25  C the liver followed by the gill and the muscle. However,
until dissection. Total fish length and weight were mea- there were big differences in liver copper concentrations
sured to the nearest millimetre and gram before dissec- between M. cephalus and the other fishes. Chromium
tion and the gill, liver and muscle tissues were dissected concentrations between the fishes also varied and the
using clean equipment. Tissues of two fish (three fish in gills of Scoberesox sauratus and A. hepsetus and the liver
smaller sizes) of the same size were pooled in a petri of Sardina pilchardus showed the highest levels. Iron
dish. After the dissection, the tissues were put into an concentrations of the tissues also showed a great varia-
oven to dry set to 90  C. After the tissues reached con- tion among the fishes. For example, gill iron concentra-
stant weights in the oven they were transferred into tions between Sparus auratus and Scoberesox sauratus
digestion flasks. Perchloric acid (4 ml) and 8 ml nitric were enormously different. Zinc concentrations in the
acid (Merck) were added and then the digestion flasks tissues of fishes, however, did not vary as much as
were put on a hot plate set to 120  C (gradually the other metals.
increased). The digestion flasks were kept on the hot- Tables 3–8 show the relationships between metal
plate until all the tissues were dissolved. The digests concentrations and fish size. The relationship between
were diluted with distilled water appropriately in the metal levels and weight were also carried out and the
range of standards that were prepared from stock stan- significances of data were exactly the same except a few
dard solution of the metals (Merck). Metal concentra- cases and only these were indicated in the tables.
tions were measured using a Perkin Elmer AS 3100
flame atomic absorption spectrophotometer and metal Table 1
concentration in a tissue was presented as mg metal/g Size ranges and the relationships between weight (W) and total length
dry weight. (L) of the fishes gilthead Sparus auratus (SA), sand smelt Atherina
Accuracy of the atomic absorption spectro- hepsetus (AH), grey mullet Mugil cephalus (MC), red gurnard Trigla
cuculus (TC), sardine Sardina pilchardus (SP) and saury pike Scom-
photometer and validity of the processes were tested
beresox saurus (SS) caught from the northeast Mediterrenean Sea
with a reference material (TORT 1 lobster hepatopan-
creas, National Research Council, Canada). The values Fish n L. ranges W. ranges Equationa R value
of the reference material were 26.3  2.1 (24.9  3.0), SA 16 18.0–32.7 95.1–674.5 Y=16.58+0.026X 0.98
2.4  0.6 (3.0  1.1), 439  22 (465  32), 186  11 (173  AH 12 14.2–26.1 18.2–113.0 Y=13.16+0.109X 0.98
9.2), 10.4  2.0 (12.1  3.1) and 177 10 (184  9.2) for MC 20 15.0–36.2 25.5–411.6 Y=16.95+0.050X 0.96
Cd, Cr, Cu, Fe, Pb and Zn, respectively. The values of TC 18 13.2–21.5 19.1–92.0 Y=11.81+0.111X 0.97
SP 17 11.0–19.2 14.4–74.4 Y=11.23+0.116X 0.95
present measurements were given in parentheses. Mean
SS 21 18.3–28.1 31.8–87.8 Y=13.87+0.164X 0.95
values and standard deviations of reference material
measured in this study were within 10% the ranges. a
Y is total fish length (cm) and X is total fish weight (g).
 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136 131

Table 2
Mean concentrations (mg metal/g d.w.) of metals and standard deviations in the tissues of the gilthead Sparus auratus (SA), sand smelt Atherina
hepsetus (AH), grey mullet Mugil cephalus (MC), red gurnard Trigla cuculus (TC), sardine Sardina pilchardus (SP) and saury pike Scomberesox
saurus (SS) caught from the northeast Mediterranean Seaa

Fish Tissue Cadmium Chromium Copper Iron Lead Zinc

SA Muscle 0.370.11 1.24 0.46 2.840.43 19.607.84 5.54 0.74 26.667.62

AH 0.370.08 2.21 1.09 4.000.56 78.4036.84 6.12 1.25 24.345.30
MC 0.660.08 1.56 0.30 4.411.67 38.7118.28 5.32 2.33 37.396.88
TC 0.790.17 2.42 0.47 2.190.83 30.6810.20 4.27 1.03 24.896.46
SP 0.550.08 2.22 0.54 4.170.58 39.608.62 5.57 1.03 34.588.64
SS 0.450.06 1.70 0.42 2.340.45 29.8216.24 2.98 0.03 16.482.83

SA Liver 0.960.24 1.66 0.33 33.3716.24 256.50108.8 8.87 2.13 76.4717.41

AH 1.170.78 3.69 2.77 54.1735.38 393.22171.4 41.24 46.27 70.1824.87
MC 1.640.91 4.58 3.45 202.80265.8 370.43252.7 12.59 5.80 110.0334.58
TC 4.502.25 8.77 4.69 26.098.14 582.37208.9 23.01 10.87 108.6432.18
SP 2.991.31 17.169.57 29.2613.19 225.4751.49 39.43 17.91 73.2219.84
SS 1.720.93 5.01 2.10 18.186.96 407.08144.9 17.54 7.89 68.9914.95

SA Gill 1.790.44 3.31 0.71 5.020.83 152.9162.33 13.31 2.87 63.109.10

AH 1.850.57 14.746.00 14.643.64 793.73411.1 12.37 4.76 85.5111.36
MC 2.080.44 4.85 1.41 13.487.34 275.6771.28 8.95 3.07 71.2114.24
TC 2.250.93 10.284.69 10.925.96 499.05339.9 12.81 4.74 89.3655.98
SP 1.560.21 7.58 1.01 8.991.49 227.4232.46 8.99 2.48 101.8511.97
SS 2.550.71 14.629.42 11.012.05 885.49514.3 16.25 4.52 80.8211.17
a
Metal concentrations among the tissues from different fishes were compared statistically using one-way ANOVA. All comparisons were statis-
tically significant at P<0.01.

Table 3
The relationships between heavy metal concentrations and total fish lengths and weights (only P values are given in paranthesis) in the tissues of the
gilthead Sparus auratusa

Tissue Data Cadmium Chromium Copper Iron Lead Zinc

Muscle DF 14 14 13 14 14 14
Equation Y=0.41+ Y=2.14+ Y=3.16+ Y=12.55+0.31X Y=5.40+0.01X Y=37.387+
(0.01)X (0.04)X (0.01)X (0.475)X
R value 0.065 0.406 0.154 0.186 0.041 0.292
P value NSb (NS) NS (NS) NS (NS) NS (NS) NS (NS) NS (NS)

Liver DF 14 14 14 14 14 14
Equation Y=1.09+ Y=2.22+ Y=2.63+1.36X Y=611.8+ Y=14.79+ Y=35.039+1.834X
(0.01)X (0.02)X (15.72)X (0.26)X
R value 0.112 0.353 0.392 0.676 0.574 0.493
P value NS (NS) NS (NS) NS (NS) ** (***) * (*) NS (NS)

Gill DF 14 14 14 14 14 14
Equation Y=1.48+0.01X Y=2.04+0.05X Y=5.00+8.47X Y=327.2+ Y=10.91+0.10X Y=70.12+
(7.71)X (0.31)X
R value 0.143 0.372 0.005 0.579 0.173 0.160
P value NS (NS) NS (NS) NS (NS) * (*) NS (NS) NS (NS)
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant, P >0.05.
* P <0.05.
** P <0.01.
*** P <0.001.

Significant negative relationships were found between
fish length (and weight) and iron levels in the gill
(P < 0.05), liver (P < 0.001), and lead level in the
liver (P < 0.05) of Sparus auratus (Table 3). The tissues
of A. hepsetus also showed negative relationships
between length and cadmium levels in the liver
(P < 0.01), chromium levels in the muscle (P < 0.05) and
in the liver (P < 0.001), copper levels in the muscle
(P < 0.05) and in the gill (P < 0.05), iron and lead levels
in the muscle (P < 0.05) and zinc levels in the liver
132 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136

Table 4
The relationships between heavy metal concentrations and fish length and weight in the tissues the sand smelt Atherina hepsetusa

Tissue Data Cadmium Choromium Copper Iron Lead Zinc

Muscle DF 10 10 10 10 10 10
Equation Y=0.37+3.21X Y=6.45+ Y=6.12+ Y=230.77+ Y=10.76+ Y=41.18+
(0.20)X (0.10)X (7.26)X (0.22)X (0.80)X
R value 0.014 0.643 0.631 0.684 0.614 0.525
P value NSb * * * * NS

Liver DF 10 10 10 10 10 10
Equation Y=5.09+ Y=18.44+ Y=141.58+ Y=850.33+ Y=75.62+ Y=186.87+
(0.19)X (0.70)X (4.17)X (21.78)X (1.64)X (5.56)X
R value 0.830 0.879 0.409 0.441 0.123 0.776
P value ** *** NS NS NS **

Gill DF 10 10 10 10 10 10
Equation Y=1.02+0.04X Y=22.02+ Y=28.74+ Y=2096.90+ Y=23.43+ Y=112.94+
(0.35)X (0.67)X (62.11)X (0.53)X (1.31)X
R value 0.247 0.201 0.641 0.524 0.385 0.399
P value NS NS * NS NS NS
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant, P >0.05.
* P <0.05.
** P <0.01.
*** P <0.001.

Table 5
The relationships between heavy metalconcentrations and fish length and weight in the tissues the grey mullet Mugil cephalusa

Tissue Data Cadmium Chromium Copper Iron Lead Zinc

Muscle DF 18 18 17 18 18 18
Equation Y=0.84+ Y=1.71+ Y=3.94+0.02X Y=32.84+0.24X Y=6.50+ Y=42.20+
(0.01)X (0.01)X (0.05)X (0.20)X
R value 0.525 0.128 0.065 0.081 0.127 0.175
P value * NSb NS NS NS NS

Liver DF 18 18 18 18 18 18
Equation Y=3.97+ Y=14.28+ Y=218.58+ Y=984.36+ Y=28.16+ Y=154.63+
(0.10)X (0.40)X (0.66)X (25.53)X (0.65)X (1.86)X
R value 0.643 0.706 0.015 0.610 0.675 0.324
P value ** *** NS ** ** NS

Gill DF 18 18 18 18 18 18
Equation Y=1.84+0.01X Y=3.88+0.04X Y=16.75+ Y=416.99+ Y=4.25+0.20X Y=32.68+1.60X
(0.14)X (5.88)X
R value 0.134 0.172 0.112 0.498 0.385 0.679
P value NS NS NS * (**) NS (*) ** *
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant, P >0.05.
* P <0.05.
** P <0.01.
*** P <0.001.

(P < 0.01) (Table 4). In M. cephalus, there was positive
relationship between zinc levels in the gill and length
(P < 0.001). Similarly, lead levels in the gill also showed
a positive relationship (P < 0.05) with weight but not
with length (P > 0.05). All the other significant relation-
ships were negative (Table 5). These were found in cad-
mium levels of the muscle (P < 0.05) and liver (P < 0.01),
in chromium levels of the liver (P < 0.001), in iron levels
of the liver (P < 0.01) and gill (P < 0.05) and in lead
levels of the liver (P < 0.01). The gill and liver tissues of
Trigla cuculus also showed negative relationships
between length and metal levels except zinc, while mus-
cle tissue did not show any significant relationship
(Table 6). The muscle and liver tissues of Sardina
 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136 133

Table 6
The relationships between heavy metal concentrations and fish length and weight in the tissues the red gurnard Trigla cuculusa

Tissue Data Cadmium Chromium Copper Iron Lead Zinc

Muscle DF 15 15 15 15 15 15
Equation Y=0.74+0.03X Y=2.97+ Y=3.72+ Y=28.34+0.16X Y=6.17+ Y=31.40+
(0.03)X (0.09)X (0.11)X (0.38)X
R value 0.047 0.163 0.260 0.038 0.264 0.141
P value NSb NS NS NS NS NS

Liver DF 15 15 15 15 15 15
Equation Y=15.35+ Y=25.52+ Y=56.02+ Y=1545.85+ Y=75.83+ Y=195.64+
(0.63)X (0.97)X (1.77)X (55.79)X (3.08)X (5.13)X
R value 0.703 0.514 0.527 0.691 0.708 0.385
P value ** * * ** ** NS

Gill DF 15 15 15 15 15 15
Equation Y=6.61+ Y=34.35+ Y=34.35+ Y=2035.41+ Y=35.07+ Y=252.80+
(0.25)X (1.39)X (1.36)X (89.15)X (1.29)X (9.43)X
R value 0.690 0.792 0.571 0.667 0.704 0.423
P value ** *** * ** ** NS
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant, P >0.05.
* P <0.05.
** P <0.01.
*** P <0.001.

Table 7
The relationships between heavy metal concentrations and fish length and weight in the tissues the sardine Sardina pilchardusa

Tissue Data Cadmium Chromium Copper Iron Lead Zinc

Muscle DF 15 15 15 15 15 15
Equation Y=0.73+ Y=3.45+ Y=3.59+0.03X Y=26.05+0.82X Y=3.66+0.12X Y=42.56+
(0.01)X (0.08)X (0.48)X
R value 0.306 0.320 0.141 0.219 0.259 0.128
P value NSb NS NS NS NS NS

Liver DF 12 12 12 12 12 12
Equation Y=4.07+ Y=39.02+ Y=24.32+0.29X Y=22.90+12.00X Y=46.87+ Y=32.78+2.40X
(0.06)X (1.29)X (0.44)X
R value 0.108 0.299 0.049 0.575 0.054 0.267
P value NS NS NS * NS NS

Gill DF 15 15 15 15 15 15
Equation Y=1.84+ Y=8.15+ Y=16.09+ Y=297.68+ Y=21.50+ Y=113.62+
(0.02)X (0.03)X (0.43)X (4.25)X (0.76)X (0.71)X
R value 0.189 0.078 0.663 0.301 0.700 0.137
P value NS NS ** NS ** (*) NS
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant.
* P <0.05.
** P <0.01.

pilchardus did not show any significant relationship
(P > 0.05) between metal levels and size, except iron in
the liver, whereas in the gill there were significant nega-
tive relationships between length and copper (P < 0.01)
and lead levels (P < 0.01) (Table 7). The tissues of
Scomberesox saurus showed significant negative rela-
tionships between length and copper and iron levels in
the muscle (P < 0.01), cadmium (P < 0.01), chromium
(P < 0.001), copper (P < 0.001), lead (P < 0.001) and
zinc (P < 0.05) levels in the liver and copper (P < 0.001),
lead (P < 0.01) and zinc (P < 0.05) levels in the gill.
4. Discussion
Mean concentrations of both essential and non-
essential metals in the gill, liver and muscle of each fish
species showed great variations. Statistical comparisons
134 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136

Table 8
The relationships between heavy metal concentrations and fish length and weight in the tissues saury pike Scomberesox saurusa

Tissue Data Cadmium Chromium Copper Iron Lead Zinc

Muscle DF 19 19 19 19 19 19
Equation Y=0.48+ Y=2.71+ Y=4.84+ Y=111.72+ Y=2.99+ Y=23.71+
(0.01)X (0.04)X (0.10)X (3.34)X (6.57)X (0.30)X
R value 0.070 0.313 0.725 0.658 0.079 0.334
P value NSb NS *** ** NS NS

Liver DF 19 19 19 19 19 19
Equation Y=6.43+ Y=16.43+ Y=57.70+ Y=829.34+ Y=65.86+ Y=123.02+
(0.19)X (0.47)X (1.61)X (17.21)X (1.97)X (2.20)X
R value 0.660 0.710 0.742 0.380 0.799 0.472
P value ** *** *** NS *** *

Gill DF 19 19 19 19 19 19
Equation Y=3.99+ Y=8.39+0.25X Y=22.69+ Y=86.25+32.56X Y=35.94+ Y=120.41+
(0.06)X (0.48)X (0.80)X (1.61)X
R value 0.266 0.086 0.743 0.203 0.569 0.463
P value NS NS *** NS ** *
a
In the equations, Y is metal concentration (mg/g d.w.) and X is total fish length (cm). Asterisks indicate significant results.
b
NS, not significant, P >0.05.
* P <0.05.
** P <0.01.
*** P <0.001.

revealed that metal concentrations were significantly
different in each tissue from different fish species. Pre-
vious data from the same study area also showed that
different fish species contained strikingly different metal
levels in their tissues (Kalay et al., 1999). This may be
related to the differences in ecological needs, swimming
behaviors and the metabolic activities among different
fish species. The differences in metal concentrations of
the tissues might be as a result of their capacity to
induce metal-binding proteins such as metallothioneins.
The present data showed that metal concentrations in
the liver and gill were highest in all the fishes. It is well
known that large amount of metallothionein induction
occurs in liver tissue of fishes. The adsorption of metals
on to gill surface could also be an important influence in
total metal levels of the gill (Heath, 1987; Canli and
Furness, 1993a,b; Roesijadi and Robinson, 1994).
Concentrations of heavy metals in tissues of fishes
from different regions also showed great variations.
Metal concentrations of the tissues in the present
study were higher than in fish caught from oceans or
seas that were not highly contaminated (Medina et al.,
1986; Serra et al., 1993; Doganoc, 1995; Quazi et al.,
1995). However, studies from Turkish waters also
showed high concentrations in tissues of fishes (Uysal
and Tuncer, 1982; Gey, 1985; Kalay et al., 1999). The
liver of M. cephalus showed enormously high (203 mg/g)
copper concentrations. This value is much higher when
compared to copper concentrations in the liver of the
other five fish species. High copper concentrations of M.
cephalus were also found in previous studies (Medina et
al., 1986; Kalay et al., 1999) and this was related to its
swimming activity. Kalay et al. (1999) indicated that
tissue metal concentrations of M. cephalus did not differ
significantly among different stations in the Mediterra-
nean Sea. They also related this to its active swimming
behavior. Another interesting result was the high lead
concentrations in the liver, especially of A. hepsetus (41
mg/g) and Sardina pilchardus (39 mg/g). This may be
related to their feeding behavior. Sardina pilchardus are
filter-feeding fish that filter particles in surface waters
with their gill rakers and active in swimming, while A.
hepsetus are carnivorous fish that will feed particularly
on mollusk and crustaceans which are known to accu-
mulate high levels of heavy metals in their body (Heath,
1987; Roesijadi and Robinson, 1994).
This study mainly aimed to investigate relationships
between heavy metal concentrations in a tissue and fish
length and weight. Results showed that there were
negative relationships between fish sizes and metal levels
in most cases. The data showed that the positive rela-
tionships were found only between zinc and lead levels
in the gill of M. cephalus and size. The results of com-
parisons between metal concentrations and the two size
parameters showed the same trend in all fish species
except a few cases (Tables 3–8).
The negative relationships between heavy metal levels
in the tissues and fish sizes were generally supported in
the literature. Nussey et al. (2000) showed that accu-
mulation of metals (Cr, Mn, Ni, and Pb) decreased with
an increase in the length of fish Labeo umbratus. Metal
(Zn, Cu and Mn) accumulation in tissues of fish
(Lethrinidae) captured from the Arabian Gulf was
affected by the sex (Al-Yousuf et al., 2000). They found
 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136
that the average metal concentrations in tissues of
female fish were higher than those in male fish, indicat-
ing the differences in metabolic activities of the two
sexes. Widianarko et al. (2000) investigated the rela-
tionship between metal (Pb, Zn, Cu) concentration and
fish (Poecilia reticulata) size and found that there was a
significant decline in lead concentrations with the
increase in size, whereas concentrations of copper and
zinc did not depend on body weight. They indicated
that body concentrations of copper and zinc are regu-
lated and maintained at a certain concentration. Liang
et al. (1999) studied metal (Zn, Cu, Cd, Cr, Pb, Ni)
concentrations in various polycultured fish species and
found that metals in fish viscera were negatively corre-
lated (except Zn in viscera of common carp). It has been
suggested that metal metabolism in fish played an
important role in metal accumulation in fish viscera.
Similarly, cadmium levels in stone loach (Noemacheilus
barbatulus) were found to be reached to a steady state in
fish of 2 years old or more, but not younger fish,
whereas there was no relationship with fish size and lead
concentrations (Douben, 1989).
It is well known that one of the most important fac-
tors that play a significant role in heavy metal accumu-
lation in marine animals is the metabolic activity
(Heath, 1987; Langston, 1990; Roesijadi and Robinson,
1994). It is also known that the metabolic activity of a
young individual is normally higher than that of an
older individual. Thus, metal accumulation was shown
to be higher in younger individuals than the older ones
(Elder and Collins, 1991; Douben, 1989; Canli and
Furness, 1993b; Nussey et al., 2000; Widianarko et al.,
2000). One explanation for the negative relationships
between metal concentrations and size found in this
study may be the difference in metabolic activity
between younger and older fish. The net accumulation
of heavy metals in an organism is a result of the differ-
ence between uptake and depuration and this is the
most important factor in metal accumulation. There-
fore, results of this study may also lead us to say that
heavy metal concentrations in the northeast Mediterra-
nean Sea are in such levels that the fishes may control
their tissue levels with the growth. Douben (1989) also
indicated that metal accumulation could reach a steady
state after a certain age. However, the dilution of tissue
metal concentrations due to growth and/or lowered
metabolic activity in older individuals may not be seen if
metal concentrations in water are higher than the capa-
city of these factors. In this case, continues accumula-
tion of metals may occur and positive relationships may
be seen between animal size and metal concentrations in
tissues.
High concentration of metals in water can retard fish
development causing possible alterations in fish size
(Heath, 1987; Weis and Weis, 1989; Friedmann et al.,
1996). Heath (1987) indicated that fish development can
135
be affected by the presence of heavy metals in water and
especially the early life stages such as hatching time,
larval development and juvenile growth as they are
more sensitive than the mature stages. Although both
essential and non-essential metals may retard fish
development, some metals like mercury seems to be
more effective than the others. For example, Friedmann
et al. (1996) showed that even low levels of dietary
mercury inhibited growth of juvenile walleye Stizostedion
vitreum. Weis and Weis (1989) also indicated that both
essential and non-essential metals could alter embryonic
development of fish embryos causing retardation of nor-
mal development, disability of organs or mortality.
Studies on fish development are generally carried out in
laboratory conditions with excess levels of metal expo-
sures. However, fish growth and its relationship with
metal concentration in the aquatic environment should
also be monitored occasionally in the field to better
understand the effects of metals on fish development and
the current situation of population dynamics.
Acknowledgements
This study was supported (FEF.2000.22) by the
Research Fund of Çukurova University (Turkey).
References
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. Sci. Total. Environ. 256,
87–94.
Barak, N.A., Mason, C.F., 1990. Mercury, cadmium and lead in eels
and roach: the effects of size, season and locality on metal con-
centrations in flesh and liver. Sci. Total Environ. 92, 249–256.
Bryan, G., Langston, W.J., 1992. Bioavailability, accumulation and
effects of heavy metals in sediments with special reference to United
Kingdom estuaries: a review. Environmental Pollution 76, 89–131.
Canli, M., Furness, R.W., 1993a. Heavy metals in tissues of the Nor-
way lobster Nephrops norvegicus: effects of sex, size and season.
Chem. Ecol. 8, 19–32.
Canli, M., Furness, R.W., 1993b. Toxicity of heavy metals dissolved in
sea water and influences of sex and size on metal accumulation and
tissue distribution in the Norway lobster Nephrops norvegicus. Mar.
Environ. Res. 36, 217–236.
Cossa, D., Rondeau, J.G., 1985. Seasonal, geographical and size-
induced variability in mercury content of Mytilus edulis in an
environment: a re-assessment of mercury pollution level in the estu-
ary and gulf of St. Lawrence. Mar. Biol. 88, 43–49.
Douben, P.E., 1989. Lead and cadmium in stone loach (Noemacheilus
barbatulus L.) from three rivers in Derbyshire. Ecotox. Environ.
Safe. 18, 35–58.
Doganoc, D.Z., 1995. Heavy metals concentrations in freshwater
and marine fishes in period 1982–1993. Zbornik Biotehniske
Fakultete Univerze v Ljubljani (Slovania). Kmetijstvo (Zoo-
tehnika) 66, 89–97.
Elder, J.F., Collins, J.J., 1991. Freshwater molluscs as indicators of
bioavailability and toxicity of metals in surface systems. Rev.
Environ. Contam. Toxicol. 122, 37–79.
136 M. Canli, G. Atli / Environmental Pollution 121 (2003) 129–136
Friedmann, A.S., Watzin, M.C., Brinck-Johnsen, T., Leiter, J.C.,
1996. Low levels of dietary methylmercury inhibit growth and
gonadal development in juvenile walleye (Stizostedion vitreum).
Aquat. Toxicol. 35, 265–278.
Furness, R.W., Muirhead, S.J., Woodburn, M., 1986. Using bird
feathers to measure mercury in the environment: relationships
between mercury content and moult. Mar. Pollut. Bull. 17 (1), 27–30.
Gey, H., 1985. Izmir korfezinden avlanan levrek (Dicentrarchus
labrax L.) ve dil baliklarinin (Solea vulgaris Quensel) doku ve
organlarindaki bazi iz elementlerin (Cu, Mn, Fe, Pb, Co, Cr, Cd)
birikim duzeyleri. V. Ulusal Spektroskopi Simpozyumu, 23–25
Eylul, Sivas, Turkey 188–199.
Heath, A.G., 1987. Water Pollution and Fish Physiology. CRC press,
Florida, USA.
Kalay, M., Ay, Ö., Canli, M., 1999. Heavy metal concentrations in
fish tissues from the Northeast Mediterrenean Sea. Bull. Environ.
Contam. Toxicol. 63, 673–681.
Kalay, M., Canli, M., 2000. Elimination of essential (Cu, Zn) and non-
essential (Cd, Pb) metals from tissues of a freshwater fish Tilapia
zillii following an uptake protocol. Tr. J. Zoology. 24, 429–436.
Langston, W.J., 1990. Toxic effects of metals and the incidence of
marine ecosystems. In: Furness, R.W., Rainbow, P.S. (Eds.), Heavy
Metals in the Marine Environment. CRC Press, New York.
Law, R.J., Fileman, C.F., Hopkins, A.D., Baker, J.R., Harwood, J.,
Jackson, D.B., Kennedy, S., Martin, A.R., Morris, R.J., 1991.
Concentrations of trace metals in the livers of marine mammals
(seals, porpoises and dolphins) from waters around the British Isles.
Mar. Pollut. Bull. 22, 183–191.
Liang, Y., Cheung, R.Y.H., Wong, M.H., 1999. Reclamation of was-
tewater for polyculture of freshwater fish: bioaccumulation of trace
metals in fish. Water Research 33, 2690–2700.
McCoy, C.P., Hara, T.M., Bennett, L.W., Boyle, C.R., Lynn, B.C.,
1995. Liver and kidney concentrations of zinc, copper and cadmium
in channel catfish (Ictalurus punctatus): variation due to size, season
and health status. Vet. Hum. Toxicol. 37 (1), 11–15.
Medina, J., Hernandez, F., Pastor, A., Beferfull, J.B., Barbera, J.C.,
1986. Determination of mercury, cadmium, chromium and lead in
marine organisms by flameless atomic absorption spectro-
photometry. Mar. Pollut. Bull. 17, 41–44.
Monterio, L.R., Lopes, H.D., 1990. Mercury content of swordfish,
Xiphias fladius, in relation to length, weight, age and sex. Mar. Pol-
lut. Bull. 21, 293–296.
Nussey, G., Van Vuren, J.H.J., du Preez, H.H., 2000. Bioaccumula-
tion of chromium, manganese, nickel and lead in the tissues of the
moggel, Labeo umbratus (Cyprinidae), from Witbank dam, Mpu-
malanga. Water Sa. 26, 269–284.
Quazi, S., Banu, C.P., Rahman, M.M., Sayeed, S. (1995). Mineral
content of fresh water and marine fish species. Proceedings of the
third Asia-Pasific Food Analysis Network Conference on Food
Analysis. P.2 (IRRI call no. TX511 C65).
Roesijadi, G., Robinson, W.E., 1994. Metal regulation in aquatic
animals: mechanism of uptake, accumulation and release. In:
Malins, D.C., Ostrander, G.K. (Eds.), Aquatic Toxicology
(Molecular, Biochemical and Cellular Perspectives. Lewis Pub-
lishers, London.
Serra, R., Carpene, E., Torresani, G., Andreucci, A., Grandini, S.,
1993. Concentrations of Zn, Cu, Fe, and Cd in Liza ramada and
Leuciscus cephalus. Archivio Veterinario Italiano 44, 166–174.
Uysal, H., Tuncer, S., 1982. Levels of heavy metals in some commer-
cial food species in the Bay of Izmir. VI Journees Etud Pollutions
Cannes, CIESM 323.
Weis, J.S., Weis, P., 1989. Effects of environmental pollutants on early
fish development. Rev. Aquat. Sci. 1, 45–73.
White, S.L., Rainbow, P.S., 1987. Heavy metal concentrations and
size effects in the mesopelagic decapod crustacean Systellaspis
debilis. Mar. Ecol. Prog. Ser. 37, 147–151.
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
Semarang, Indonesia. Ecotox. Environ. Safe. 46, 101–107.