AHMED ET AL (2014), FUUAST J. BIOL.

, 4(2): 195-204

CONCENTRATIONS OF HEAVY METALS (Fe, Mn, Zn, Cd, Pb, AND Cu) IN
MUSCLES, LIVER AND GILLS OF ADULT SARDINELLA
ALBELLA (VALENCIENNES, 1847) FROM GWADAR WATER OF
BALOCHISTAN, PAKISTAN
1 2 3
QURATULAN AHMED *, D. KHAN AND NAEEMA ELAHI
1
The marine reference collection and resource centre, University of Karachi, Karachi – 75270, Pakistan.
2
Department of Botany, University of Karachi, Karachi- 75270, Pakistan.
3
Department of Zoology, University of Karachi, Karachi- 75270, Pakistan.

*Corresponding author; quratulanahmed_ku@yahoo.com

Abstract

Fish samples of Sardinella albella were collected seasonally from Balochistan coast during (Pre-monsoon,
Monsoon, Post-monsoon) season in (January 2012 - December 2012). The maximum mean length (cm) and weight (g)
of the fish were (20.1 ± 0.29 cm) and (93.13 ± 1.9g) in Monsoon season and the lowest mean length (18.5 ± 0.58cm)
and weight (82 ± 3.60 g) were measured in Pre-monsoon season. Determinations of heavy metals were made by Atomic
Absorption Spectrophotometer (AA Analyst). The highest mean concentration of Fe (496.43 ± 41.79µg/g), Mn (9.42 ±
0.81µg/g), Zn (66.22 ± 7.06µg/g), Pb (2.42 ± 0.21 µg/g), and Cu (14.69 ± 2.30µg/g) were recorded in liver. The lowest
mean concentration of Fe (3.82 ± 0.91µg/g), Mn (1.41 ± 0.62µg/g), Zn (1.88 ± 0.25µg/g), Cd (0.64 ± 0.16 µg/g), Pb
(0.35 ± 0.06 µg/g), and Cu (1.69 ± 0.14µg/g) were recorded in fish muscles. Metals concentration didn’t vary
seasonally and following trends of metal concentrations were observed in various organs of S. albella.
Muscles: Fe > Zn > Mn > Cd > Pb
Liver: Fe > > Zn > Cu > Mn > Pb > Cd
Gills: Fe > Zn > Mn > Cu > Cd > Pb
Introduction

Fish, as human food, are considered as a good source of protein, polyunsaturated fatty acids (particularly
omega-3 fatty acids), calcium, zinc, and iron (Chan et al., 1999; Daviglus et al., 2002}. Metal residues problems
in the fish flesh are, however, very serious owing to the high metal concentrations recorded in the water and
sediments (Wong et al., 2001). The major sources of pollution of surface waters include effluent discharges by
industries, atmospheric depositions of pollutants and occasional accidental spills of toxic chemicals (Ikem and
Egiebor, 2005) and trace metals are regarded as serious pollutants of the aquatic environment because of their
toxicity, their persistence, their difficult biodegradability and their tendency to concentrate in aquatic organisms
(Ikem and Egiebor, 2005; Schuurmann and Markert, 1998). They enter the marine environment through
atmospheric and land-based effluent sources (Islam and Tanaka, 2004). Industrial and agricultural activities also
significantly contribute to the accumulation of pollutants in the aquatics including seawater (Jordao et al., 2002).
It has been recognized for many years that the concentrations of metals found in coastal areas, whether they are
in the dissolved or particulate phases are derived from a variety of anthropogenic and natural sources (Burridge
et al., 1999). The major part of the anthropogenic metal load in the sea and sea bed sediments and organisms has
a terrestrial source from mining and intensive aquaculture and municipal wastewaters, industrial untreated
effluents, harbor activities, urban and agricultural runoff along major rivers and estuaries and bays (Tarra-
Wahlberg et al., 2001; Akif et al., 2002).
The degree of heavy metal contamination in some Karachi Seawater fishes is reported to be as Otolithes
ruber > Liza vaigiensis > Sardinella albella > Scomberomorus guttatus > Pomadasys olivaecum (Ali et al,
2013). Some of the metals found in the fish might be fundamental as they play vital role in biological system of
the fish as well as in human beings but some of them may, however, be toxic and may cause serious damage to
the human health if present in excess to the permitted limits. The common heavy metals that are found in fish
may include Cu, Fe, Zn, Ni, Mn, Hg, Pb, Cd, etc. from Pakistan waters or elsewhere (Connell, 1984, Rizvi et al.,
1988; Tariq et al., 1991, 1998; Nair et al., 1997; Zehra et al., 2003; Agusa et al., 2005, 2007; Dalman et al.,
2006; Naidu et al., 2008; Tabinda et al., 2010; Kumar et al., 2012; Shivakumar et al., 2014; El-Moselhy et al.,
2014). Ambedkar and Muniyan (2011) found Cr in maximum concentration followed by Cd > Cu > Pb > Zn in
the fishes of Vellar River, Tamil Nadu (India) for the samples caught during January to June, 2010. Heavy
metals have the tendency to differentially accumulate in various organs of marine organisms, especially fish,
which in turn may enter into the human metabolism through consumption causing serious health hazards (Puel
et al., 1987). Iron, copper, zinc and manganese are essential (physiological) metals while, mercury, lead and
cadmium are xenobiotic toxic metals (Kennish, 1992). Fish has been considered good indicators for heavy metal
contamination in aquatic systems because they occupy elevated trophic levels with different sizes and ages
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 196

(Burger et al., 2002). The levels of toxic elements in fish are related to age, sex, season and habitat (Kagi and
Schaffer, 1998).
The aim of this study was to determine heavy metal Fe, Mn, Zn, Cd, Pb, and Cu concentrations in
Sardinella albella fish muscles, liver and gills collected from Balochistan coast during (January 2012-
December 2012). It is a small pelagic fish distributed in Indo-West pacific from Red Sea, Persian Gulf, East
African coasts, Madagascar, eastwards to Indonesia and the Arabian Sea, North to Taiwan and South to Papua
New Guinea. Also in Western and Southern Taiwanese waters, and Panghu
(www.discoverlife.org/20/?search+Sardinella+albella). It is a planktivore in Sea and estuaries. It May reach 18
cm in length and have black spot on the origin of dorsal fin (Randall, 1995). Being small in size, it is graded as
trash fish but it is nutritionally rich and good if prepared fresh (Chattopadhay et al., 2004). It is eaten by humans
in coastal communities and powdered for poultry feed. Sardinella albella is reported to contain protein c 20.2 ±
0.72 % and lipid 1.9 ± 0.10% (Jayasantha and Patterson (2014). Its feeding habit and length-weight relationship
are described by K.V.Sekhran (ND) in his doctoral thesis of Madras University, India.

Materials and Methods

Fish sample of Sardinella albella (Valenciennes, 1847) were collected seasonally (Pre-monsoon, Monsoon,
Post-monsoon) from Gwadar water of Balochistan coast, Pakistan (Fig. 1 and 1B) during January to December
2012. The length (L) of the fish was measured from the tip of the mouth to the caudal fin (cm). Fish weight was
measured after drying with a piece of clean towel. Total length (TL) and body weight (W) were measured with
fresh samples to the nearest 0.1 cm and 0.01 g, respectively. Samples were collected for the analysis of heavy
metals. Fishes were dissected using steel Scissors and scalpels to remove approximately 5 g dorsal muscles,
entire liver and 2 rakers of gills. They were washed with deionized water and weighed after blotting excess
surface water. Samples were ground and calcinated at 500 oC for 3 hours until it turned to white or grey ash and
reweighed. The ashes were dissolved with 0.1 M HCl according to the method of (Gutierrez et al., 1978). The
ashes were dissolved in 10 ml (HCl) in beaker and after which the dissolved ash residue was filtered with
Whatman filter paper. One ml filtered solution was diluted with 25 ml distilled water for elemental analyses.
The standards were prepared from 1000 ppm stock solution to 2 ppm, 4 ppm, 6 ppm, etc. Elemental analysis
was made with atomic absorption spectrophotometer (Analyst 700) in the Centralized laboratories of University
of Karachi. The concentration of metals was expressed as μg per g dry weight. The data was analyzed with
SPSS version 12.
The contents of selected heavy metals in Pakistan Coast and the adjoining waters are presented in Table 1.

Sandy plain
Rocky Outcrop

NORTH ARABIAN SEA

Tidal flats

Fig. 1A. Map of Pakistan coast showing the study area. Adopted from Khan (1987). The map was
originally drawn by Pakistan Generalized Soil Map. III. Draft (1969). Soil Survey Project, Pakistan.

Fig. 1B. An individual of Sardinella albella from Pakistan Coast. Source: Hamid Badar Osmani
(hamid61612002@yahoo.com). www.fishbase.us / photos
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 197

Table 1. Contents of heavy metals in Seawater of Arabian Sea / Indian Ocean (in ppm).
Location Fe Mn Cd Pb Cr Reference
Karachi mangroves - - 0.064 ± 0.16 0.77 ± 0.16 -
(ppm) * Ismaili et al
Miani Hor (ppm) - - 0.057 0.04 - (2014)
0.531 ± 0.302 ± 0.0133 ± 0.003 0.159 ± 0.885 ±
Keti Bunder to Giddani 0.11** 0.154 (N = 11) 0.0046 0.472 Mumtaz (2002)
(ppm) **** (35.9 ± (N= 13) (N = 13) (N =12)
27.9) ***
South coast, India - - 14.55 ± 4.42 4.93 ± 0.77 14.13±1.44 Kumar et al.
(μg/L) (2013)
Indian Ocean (μg/L) 2 - 220 2 - 180 - - - Gaid (2011)
Persian Gulf (ppm)
Station I - - 0.087 ± 0.008 4.94 ± 1.33 Khoshnoud et al.
Station II 0.066 ± 0.0018 4.39 ± 0.824 - (2011)
Station III 0.086 ± 0.004 6.941±1.92
Standard unpolluted 0.0034 0.0004 0.00011 0.00003 0.0002 Turekian (1968)
Seawater (ppm)
*, mean of six sites; **, mean excluding Bin Qasim sample (312 ppm) and Giddani sample (148 ppm) - heavily
Fe-polluted sites; ***, Mean including Port Qasim and Giddani sites; ****, mean for thirteen sites calculated
from the data of Mumtaz (2002).
Results and Discussion

Thirty six Sardinella albella fish samples were collected from Gwadar, Balochistan coast during (Pre-
monsoon, Monsoon, Post-monsoon) season in (January 2012- December 2012). The fish samples studied for
metallic contents varied little in size - from 3.16 to 9.64% in length and 4.49 to 15.68% in weight season. The
maximum mean length (20.1+ 0.29cm cm) and weight (93 + 1.19g g) of fish were recorded in Monsoon season
and the lowest mean length (18.5 + 0.17cm) and weight (82 + 1.04 g) were measured in Pre-monsoon season
(Table 2). There was direct relationship between length and weight (r = 0.90, p < 0.0001) (Table 2).
The heavy metal (Fe, Mn, Zn, Cd, Pb, and Cu) concentration were measured in Muscles, Liver, and Gills of
the fish. The highest mean concentration of Fe (496.43 + 41.79 µg/g), Mn (9.42 + 0.81 µg/g), Zn (66.22 + 7.06
µg/g), Pb (2.42 ± 0.23 µg/g), and Cu (14.69 ± 2.30 µg/g) were recorded in liver in any season. The lowest mean
concentration of Fe (3.82 + 0.54µg/g), Mn (1.41 + 0.18µg/g), Zn (1.88 + 0.18 µg/g), Cd (0.64 + 0.16 µg/g), Pb
(0.35 + 0.06 µg/g), Cu (1.69 + 0.14 µg/g) were recorded in fish muscles. The maximum mean concentrations of
heavy metals were associated with liver in all seasons. Muscles showed lowest level of concentration throughout
the study (Table3, 4 and 5). The metals contents on annual basis are presented in Table 6.
Table 2. Mean length (L) and weight (W) of S. albella fish collected from Gwadar water.

Length (cm) CV Weight (g) CV

Seasons (Mean ± SE) (Length) (Mean ± SE) (Weight)
(%) (%)
Pre-monsoon 18.5 ± 0.17 3.16 82 ± 1.04 4.49
Monsoon 20.1 ± 0.29 3.98 93 ± 1.19 4.44
Post-monsoon 19.5 ± 0.48 9.64 87 ± 3.94 15.68
;;

Annual 19.6 6.59 88.50 9.45

Linear relationship: W = -39.391 + 6.584 L ± 4.237
t = -3.66 t = 12.01
p < 0.001 p < 0.0001
r = 0.90, r2 = 0.809, Adj. r2 = 0.804, F = 144.28 ( p < 0.0001)

Comparing the concentrations of metals in various parts of the fish with that of the Seawater (Table 1) it is
clear that multi-fold bioaccumulation of metals has taken place in fish at different rates in different organs.
Following trends of metal concentrations approximated the metals concentration in various organs of S. albella:
Muscles: Fe > Zn > Mn > Cd > Pb
Liver: Fe > > Zn > Cu > Mn > Pb > Cd
Gills: Fe > Zn > Mn > Cu > Cd > Pb
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 198

More or less similar Fe-dominated heavy metal trends in different organs of Megalaspis cordyla have been
reported from Karachi coast, Pakistan (Ahmed, et al., 2014).
Muscles: Fe > Mn > Cd > Pb > Cr
Liver: Fe > > Zn > Cr ≈ Cd ≈ Pb
Gills: Fe > Mn > Cd > Pb > Cr
The overall metals concentration ((µg/g) sequence irrespective of any season or organ of S. albella was as
follows:
Fe (160.25) > > Zn (23.05) > Cu (6.562) > Mn (4.989) > Cd (1.515) > Pb (1.394)

An order of heavy metals concentrations (Fe > Zn > Cu > Mn > As > Hg > Cd) with Fe being the
predominant metal in the fishes of Northeast coast of India has also been reported by Kumar et al. (2012).
Shivakumar et al (2014) have also given Fe-dominated metallic accumulation sequences in some Indian fishes
as follows:
Etrophus maculates: Fe > Zn > Cu > Pb > Ni > Cd
Cirrhinus reba: Fe > Cu > Zn > Pb > Ni > Cd
Ompok bimaculatus: Fe > Zn > Cu > Pb > Ni > Cd

Table 3. Concentration of heavy metals in S. albella during Pre monsoon season.

Fe (µg/g) Mn (µg/g) Zn (µg/g) Cd (µg/g) Pb (µg/g) Cu (µg/g)

Organs (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE)
Muscles 6.93 + 0.51 1.64 + 0.14 2.66 + 0.36 0.70 + 0.10 0.35 + 0.06 1.69 + 0.14
Liver 496.43 + 41.79 9.42 + 0.81 50.15 + 5.92 1.64 + 0.14 2.42 + 0.21 12.85 + 1.18
Gills 37.48 + 4.52 3.08 + 0.42 16.64 + 1.39 1.48 + 0.23 1.64 + 0.14 3.25 + 0.37

Table 4. Concentration of heavy metals in S. albella during monsoon season.

Fe (µg/g) Mn (µg/g) Zn (µg/g) Cd (µg/g) Pb (µg/g) Cu (µg/g)

Organs (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE)
Muscles 3.82+ 0.54 2.15+ 0.19 1.88+ 0.25 1.22+ 0.17 0.47+ 0.07 1.79+ 0.22
Liver 305.17+ 34.19 8.63+ 0.70 66.22+ 7.06 2.15+ 0.19 2.42+ 0.23 11.2+ 2.39
Gills 39.96+ 4.68 3.08+ 0.86 13.88+ 1.93 2.28+ 0.25 1.34+ 0.10 2.77+ 0.24

Table 5. Concentration of heavy metals in S. albella during post monsoon season.

Fe (µg/g) Mn (µg/g) Zn (µg/g) Cd (µg/g) Pb (µg/g) Cu (µg/g)

Organs (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE)
Muscles 7.76 + 0.91 1.41 + 0.18 2.36 + 0.25 0.64 + 0.16 0.38 + 0.06 2.08 + 0.23
Liver 476.85 + 48.53 8.57 + 0.73 45.64 + 4.48 1.65 + 0.18 1.61 + 0.13 14.69 + 2.30
Gills 45.21 + 5.03 2.24 + 0.23 12.94 + 1.48 1.59 + 0.16 2.15 + 0.19 2.30 + 0.34

Table 6. Mean concentration of heavy metals in various organs of S. albella (data of all seasons pooled).

Organs Fe (µg/g) Mn (µg/g) Zn (µg/g) Cd (µg/g) Pb (µg/g) Cu (µg/g)

(Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE) (Mean ± SE)
Muscles 6.16 ± 0.47 a * 1.77 ± 0.10 a 2.50 ± 0.171 a 0.812 ± 0.103 a 0.479 ± 0.048 a 1.975 ± 0.119 a
Liver 433.11± 25.31 b 9.77 ± 0.42 b 51.78 ± 3.51 b 1.84 ± 0.100 b 2.077 ± 0.132 b 14.738 ± 1.154 b
Gills 41.48\ ± 2.78 c 3.42 ± 0.57 c 14.86 ± 0.86 c 1.90 ± 0.316 b 1.624 ± 0.099 c 2.971 ± 0.193 c

*, Figures provided with similar letter in a column are not significantly different.
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 199

100
PRE-MONSOON
90

LIVER / MUSCLE RATIO

MONSOON
80
POST-MONSOON
70
60
50
40
30
20
10
0
Fe Mn Zn Cd Pb Cu
METALS

Fig.2. Comparison of seasonal values of liver: muscle ratio of heavy metals in S. albella.

Table 7. ANOVA for heavy metals data in various organs of fish S. albella captured from Gwadar water.

Source SS df MS F p
Seasons 5143.23 2 2571.62 2.114 0.1217 (NS)
organs 2134742.09 5 426948.42 350.91 0.00001
Metals 904471.57 2 452235.79 371.69 0.00001
Seasons x Metals 35433.73 10 3543.37 2.912 0.0014
Seasons x Organs 10066.21 4 2516.55 2.0683 0.0835 (NS)
Metals x Organs 3190816.46 10 319081 26.225 0.00001
Seasons x organs x metals 62618.76 20 3130.94 2.573 0.0002
Error 722717.57 594 1216.70 - -
Total 7066009.64 647 - - -

Metals Organs Seasons

Rank Metals Mean Rank Organs Mean Rank Seasons Mean
1 Fe 160.253a 1 Liver 85.553 a 1 Post-Monsoon 35.868 a
2 Zn 23.05 b 2 Gills 11.044 b 2 Monsoon 33.864 a
3 Cu 6.562 c 3 Muscles 2.284 c 3 Pre-Monsoon 29.147 a
4 Mn 4.989 c
5 Cd 1.514 c LSD0.05: 6.592
6 Pb 1.954 c LSD0.05: 6.592
LSD0.05: 9.322

Three way ANOVA of the metal data for factors such as seasons, metal types and the organ types indicated
no influence of seasons over metal concentration (F = 2.1, p < 0.1217, NS). However, metal concentration was
significantly influenced by metal types (F = 371.69, p < 0.0001) and the organ types (F = 350.91, p < 0.0001).
There was significant interaction amongst the factors except that there was no significant interaction of seasons
with the organ types (Table 7). The predominant metal in S. albella was Fe followed by Zn i.e. Fe >> Zn > Cu
> Mn > Cd > Pb. The metal content of liver was much higher than that in gills or the muscles. The metal
concentration in the fish didn’t vary in the three seasons. The concentration of metals in fish organs are
determined primarily by the level of pollution in their environment, in water and food (Farkas et al., 2003). The
concentration in muscles and gills reflect the concentrations of metals in the water (Fathi et al., 2013). The
maximum mean concentrations of heavy metals were found in liver in all seasons. Liver has also been reported
to be the target organ for Cu, Zn and Fe accumulation by El-Moselhy et al., (2014). Pb and Mn were found in
higher concentration in the gills by El-Moselhy et al. (2014). Highly increased concentrations of metals in
general and iron in particular in liver may represent storage of sequestrated products in this organ (Hamilton and
Mehrle, 1986). Iron is physiologically (reversibly) stored in liver as ferritin and hemosiderin (Ahmad, J, <
www.fda.gov.ph/...annex% 20J%20....>). Ferritin has the capacity of about 4500 iron (III) ions per protein
molecule. This is the major form of iron storage (< http://library.med.utah.edu/ NetBiochem/hi.htm>). The
metallic accumulation may depend on seasonal variations also (Deram et al., 2006).
The liver / muscles ratio of metals varied seasonally and were always higher than one – maximally around
63.64 - 90.15 in case of Fe, 4.83-6.06 for Mn, 3.22-5.22 for Pb and 2.33 - 2.61 in case of Cd. The ratios for Fe,
Zn was comparatively higher in monsoon season (Fig. 2). In other metals the liver / muscles ratio was relatively
much lower and less variant amongst the seasons. Multi-fold accumulation (up to 100 times) of heavy metal in
liver is well known (Agusa et al., 2007). Accumulation of Fe in liver by 10-12 folds over muscles is also
reported by Ahmed et al (2014) in Megalaspis cordyla from Karachi waters. The magnitude of such a ratio
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 200

should obviously depend upon not only the metallic concentration in the Seawater but also on the intrinsic
metabolic characteristics related to metallic bioaccumulation in various organs of a species.
The concentrations of various metals in Sardinella spp. from various Coasts of India and Pakistan are
outlined in Table 8. Fe in muscles of Sardinella longiceps was much higher than that recorded in S. albella in

Table 8. Comparison of heavy metals contents in Sardinella spp. reported from Indo-Pak sub-continent.

Reference &
Species Organ Fe Mn Zn Cd Pb Cu
Locality
Sardinella. Muscles 148.5±32.0 ND 20.52 ± 1.8 - - 1.54±0.10 Nair et al.
Longiceps Al. canal 2255.40 ± 609 6.14±1.1 63.42 ± 11 6.94±0.41 (1997)
μg/g DW ± Gills 428.39 ± 68 16.39 ±2.4 110.8 ± 12.0 2.72 ±0.1 India
SD Cochin, IndiaMersing Malaysia)
Sardinella. Muscles 0.24 0.25 1.4 Anand and
Longiceps Gills - - - 0.33 0.33 1.62 Kumaraswamy
(ppm) Kidneys 0.30 0.32 0.30 (2013), India
Sardinella Tabinda et al.
sindensis Muscles 0.104 ± - 1.215 ± 0.031 ± 0.200 ± 0.007 ± (2010)
μg/g DW ± 0.001 0.136 0.003 0.002 0. 001 Keti Bunder,
SD Pakistan
Sardinella
albella Muscles 32.2 3.2 19.30 - - - Jayasantha &
(India) Patterson (2014)
μg/g DW ± Tuticorin, India
SD
Sardinella
fimbriata Muscles 2.21 2.59 14.94 - - 0.59 Sing bal et al.
Goa (India) (1982), India
ppm
S, albella Muscles 6.16 ± 2.79 1.77 ±0.60 2.5 ±1.02 0.81 ±0.62 0.48 ±0.29 1.97 ±0.70
μg/g DW ± Liver 433.1 ±151.8 9.77 ±2.53 51.78 ±21.08 1.835 ±0.60 2.08 ±0.79 14.74 ±4.9 Present study
SD Gills 41.48 ±16.7 3.42 ±2.14 14.86 ±5.16 1.897 ±1.79 1.62 ±0.60 2.97 ±1.58
the present study. It was heavily accumulated in alimentary canal in S. longiceps (Nair et al., 1997). As
compared to the present studies, Fe in muscles was higher in S. longiceps (Nair et al., 1997) and S. albella from
Tuticorin, India (Jayasantha and Patterson, 2014). Mn and Zn were also higher in concentration in gills of S.
longiceps. Cu was somewhat higher in liver of S. albella (present study) than that in S. longiceps (Nair et al.,
1997) and S. fimbriata (Sing bal et al., 1982). Pb was substantially higher in S. albella of Karachi water than
that in S. sindensis of Keti Bunder (Tabinda et al., 2010) that may presumably be attributed to higher level of
pollution of Karachi Seawater (cf. Table 1).
Muscles which are the edible part of the fish showed the lowest level of metals concentration in S. albella
throughout this study. El-Moselhy et al. (2014) have also reported muscles of the fish to possess the lowest
concentration of metals. Quite varying concentrations of various heavy metals in fishes as a function of the
species or the pollution of their environment have been reported by various authors. The metallic concentration
amongst fishes of Cochin (India) varied from species to species. Cu, Zn, Fe and Mn showed increased
concentration in gills and alimentary canal as compared to the muscles. The difference in heavy metal
concentrations in various species were attributed to their varying feeding habit (Nair et al., 1997). According to
the studies of Nair et al. (1997) Fe was dominant element which was 362.32 ± 70 in muscles, 347.82 ± 88.4 in
gills and maximally 833.33 ± 178 μg /g dry weight in alimentary canal in M. cordyla of Cochin. ShivaKumar et
al. (2014) also showed relatively higher accumulation of metals in intestine and gills. Tuzen (2003) reported Pb
levels in the fish of Black Sea in the range of 0.22-0.85 mg/kg and Uluozlu et al. (2007) reported lead in the fish
edible tissue in the range of 0.33 – 0.93 mg/kg. Dicentrarchus labrax, a fish of Güllük Bay (Aegean Sea,
Turkey) was found to contain Pb (< 0.0042 – 0.4 mg/kg) and Cd (0.01-0.04 mg/kg) - to be within permissible
limit (Dalman et al., 2006). Zehra et al. (2003) reported Cd (0.04-0.15 μg / g) and Pb (0.25-0.5 μg / g) in
Acanthopagurus berda from Balochistan coast.
Some heavy metals are health damaging elements. Pb is known to induce reduced cognitive development
and intellectual retardation in children and increase blood pressure and cardiovascular disease in adults
(Commission of the European; 2002). It may cause learning disabilities, impaired protein and hemoglobin
synthesis and shorten the lifespan of red blood cells which leads to severe anemia (hypochromic microcytic
anemia) in children (Sultana and Rao, 1998). The most common toxic effects of cadmium in human are renal
failure, accumulation in the bone resulting in calcium loss and malfunctioning of peripheral and central nervous
system (Schroeder, 1965; Castro-Gonzalez and Méndez-Armenta 2008). Cd proves to be a risk factor for lung
disease, kidney dysfunction, skeletal damage and reproductive deficiency (Nordberg, 2003). Gutenmann et al.
(1988) indicated that a frequently used food safety limit for Cd in food is 2 ppm. In 1993, Food and Agriculture
Organization (FAO) reduced the limit for Cd is 0.5 ppm. WHO (1990, 1993) indicated that Cd permissible limit
AHMED ET AL (2014), FUUAST J. BIOL., 4(2): 195-204 201

is 2.0 ppm for seafood and 0.70 ppm for water. Opinions differ regard the residual level of heavy metals in the
water and their relation to the residuals level in fish flesh. Kock and Hofer (1998) reported that even low
concentrations of heavy metal in the water may result in high concentrations in fish flesh. However, others such
as Wong et al. (2001) reported that despite high metal levels in the Seawater and sediments, concentrations of
Cd and Pb in fish flesh did not exceed permissible levels. WHO (1990, 1993) indicated that Cu permissible limit
is 20 ppm for fish and 2.00 ppm for water. Cu occurs in foods in many chemical forms and has an important role
in the physiological activities of living bodies. Abou-Arab et al. (1996) reported Cu residues in sardines and
mackerel of 0.086 and 0.077 ppm, respectively. Cu is considered as public health hazard if an abnormal high
level of Cu is ingested. Cu may cause Mediterranean anemia, hemochromatosis, liver cirrhosis and Wilson’s
disease (Underwood, 1977). Abou-Arab et al. (1996) reported mean Pb residue in whole sardines and mackerel
of 11.1 and 12.6 ppm, respectively. Hodson et al. (1984) indicated that the Canadian Pb limit of 10 ppm was
discontinued, but that the British limit remains at 2 ppm for fish. Abou-Arab et al. (1996) indicated that the
FAO limit (1983) is 2.0 ppm. WHO (1990, 1993) indicated that Pb permissible limit is 2.0 ppm for seafood, and
0.50 ppm for water. Industrial and agricultural discharges are the sources of Pb pollution in Iran. Pb is identified
as a serious public health problem particularly for children. The adverse toxic effect caused by Pb on human was
recognized (Subramanian, 1988). Neurological defects, renal tubular dysfunction, anemia are the most
characterized of Pb poisoning (Forstner and Wittmann, 1983). Zinc is known to be involved in most metabolic
pathways in humans and zinc deficiency can lead to loss of appetite, growth retardation, skin changes and
immunological abnormalities. Zinc is widespread among living organisms, due to its biological significance.
The maximum zinc level permitted for fish is 50 mg/kg according to Food Codex (Maff et. al., 1993). The
recommended daily intakes of zinc are 15 mg for adult males and 12 mg for adult females. Zinc causes slow
growth in children, reduced fertility, dry mouth, headache and nausea (Schroeder, 1965). The United States
environmental protection agency and the European Commission (US-EPA and EC) have not considered any
standards or limits for the zinc concentrations (Alimentarius, joint FAO / WHO; 1994, Ashraf et. al., 2006).
It is clear from the above discussion that the metals such as Cd, Pb, Cu and Mn in edible part of S. albella were
within permissible limits.
Per capita fish consumption per year in Pakistan is the lowest in the World (c 2 kg per capita per year or
5.48g per capita per day (Government of Pakistan, Agric. Statistics, MINFAL, Islamabad (seen in Waseem,
2007) which is much lower than that of global estimate of 17 kg per capita per year and very much lower than
that in southeast Asia (170 g per capita per day in Malaysia (Agusa et al., 2007). Toxicity due to heavy metals
by eating S. albella is, therefore, quite unlikely in general terms, in Pakistan but there remains great likelihood
of heavy metal toxicity in Pakistan’s populations due to heavy pollution of all kinds in the country. There is a
great need to investigate heavy metals load in all kinds of fishes or Sea food consumed locally or exported
elsewhere.

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(Accepted for publication …… November, 2014)