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Marine Pollution Bulletin 81 (2014) 218224

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Bioaccumulation of heavy metals in commercially important marine
shes from Mumbai Harbor, India
A. Velusamy
a
, P. Satheesh Kumar
b,
, Anirudh Ram
c
, S. Chinnadurai
d


a
Department of Marine Sciences, Bharathidasan University, Tiruchirappalli 691431, Tamil Nadu, India
b
Department of Biological and Environmental Sciences, University of Messina, Messina 98166, Italy
c
Reginal Centre National Institute of Oceanography, Mumbai, India
d
Central Marine Fisheries Research Institute, Molluscan Fisheries Division, Kochi 682018, India


a r t i c l e i n f o

Keywords:
Bioaccumulation
Fish
Food safety
Pollution
Heavy metals
Seafood
a b s t r a c t

Seventeen commercially important marine sh species were caught in Mumbai Harbor using a trawl net
and evaluated using Atomic Absorption Spectroscopy and ICP-OES. It was found that certain species of
sh contained lower levels of all metals tested. J. elongatus and C. dussumieri had the highest levels of
all 8 metals tested. The heavy metal concentrations were signicantly varied within and between the
studied shes (p < 0.05). However, a signicant correlation among heavy metals was observed. This
investigation indicated that various levels of heavy metals exist in the sh species sampled, but those
concentrations are within the maximum residual levels recommended by the European Union and
FAO/WHO. Therefore, sh caught in Mumbai Harbor can be considered safe for human consumption.
2014 Elsevier Ltd. All rights reserved.



Fish are considered an important protein source for human
health. Marine pollution can increase aquatic concentrations of
toxic metals and negatively affect sh health. Pollution can be
caused by various sources, including agricultural drainage,
industrial efuent discharge, sewage discharge, accidental
chemical waste spills, and gasoline from shing boats (Handy,
1994; Mishra et al., 2007; Satheeshkumar and Kumar, 2011).
Higher concentrations of heavy metals are found in the sediment
and enter the food chain via the feeding of benthic species.
Macrobenthic invertebrates are an important nexus on the
transfer of trace metals to higher trophic levels due to their
dependent relationship on sediments and their ability to
accumulate metals (Galay Burgos and Rainbow, 2001). The metal
accumulation in sh depends on the location, distribution, habitat
preferences, trophic


Corresponding author at: Department of Biological and Environmental Sciences,
University of Messina, Messina 98166, Italy. Tel.: +39 3206253357; fax: +39
0906765526.
E-mail address: indianscientsathish@gmail.com (P. Satheesh Kumar).
level, feeding habits, age, size, duration of exposure to metals
and homeostatic regulation activity (Sankar et al., 2006).
Fish are the main aquatic product of the west coast of India.
The heavy metal pollution in Mumbai Harbor has an inuence on
the quality of the shes. Several studies have focused on the
bioaccumulation of heavy metal in shes of India and international
waters. These studies discovered that the impact of heavy metal bio-
accumulation in sh focus a gradient of pollution in one moment in
time (Topcuoglu et al., 2002; Kojadinovic et al., 2007; Deshpande
et al., 2009; Kumar et al., 2012; Kalantzi et al., 2013). Heavy metals,
such as iron (Fe), copper (Cu) and zinc (Zn), are important for sh
metabolism, while cadmium (Cd), lead (Pb), mercury (Hg) and oth-
ers have unknown functions in biological systems. Metabolic activ-
ity plays an important role in the bioaccumulation of trace metals in
marine organisms (Langston, 1990; Roesijadi and Robinson, 1994).
Mumbai lies on the west coast of India, has a deep natural harbor
and has a coastline of 140 km along its western edge. Mumbai is
also the commercial capital city of the Maharashtra state and boasts
the highest population and largest industrial center in the country,

http://dx.doi.org/10.1016/j.marpolbul.2014.01.049
0025-326X/ 2014 Elsevier Ltd. All rights reserved.
A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224 219

resulting in large amounts of waste water generation. This sewage
water is treated and immediately discharged into the Arabian Sea.
However, many industries also discharge their efuents directly
into the ocean. These indirectly affect the health of the aquatic envi-
ronment by transmitting toxicity through the food web (Deshpande
et al., 2009). Recent water quality analyses of the Thane Creek and
Ulhas River estuaries have shown increasing evidence of heavy me-
tal contamination due to anthropogenic discharges from the sur-
rounding areas (Thane Municipal Corporation, 2006). Heavy metal
contents in the sediment exhibited spatial and temporal variability
and recorded relatively high values of Pb, Cd, Hg, and Zn (NIO,
2010). Because seafood is the most preferred food among the local
people and tourists, it is important to study the bioaccumulation of
heavy metals in different commercial shes in Mumbai Harbor. This
study focused on determining heavy metal concentrations (Fe, Zn,
Mn, Cu, Cr, Cd, Pb, Hg) in the muscle tissues of 17 marine sh spe-
cies from Mumbai Harbor on the west coast of India. In addition, we
investigated the relationships between heavy metal concentrations
and sh size (length and weight) using statistical analyses. The re-
sults obtained from this study were compared with sh caught
from international waters. Observed levels of heavy metals were
compared with certied human consumption safety guidelines rec-
ommended by the Food and Agricultural Organization (FAO) and
the World Health Organization (WHO).
Fishes used in this study have been sampled from different sites
along Colaba, Vashi and Thane Creek. Thane Creek is part of the Ulhas
River in Western India and ows into the Mumbai Harbor (see
Table 1). This study region is within latitude 19001905
0
N and lon-
gitude 72557300
0
E (Fig. 1). Thane Creek ows through the most
important industrial zones in Mumbai: bulb industries, chemical
industries and other small scale industries. Many of these industries
directly release their efuents, which contain metals and chemical
compounds, into Thane Creek. The efuent water entering the creek
causes nutrient pollution. However, the wastewater entering the
estuarine environment has severely deteriorated the water quality
in some areas. Dissolved oxygen (DO) and Biochemical Oxygen
Demand (BOD) distribution patterns indicate that the daily organic
load is being effectively dispersed (Deshpande et al., 2009).
The water quality parameters of pH, temperature, DO, BOD, total
nitrogen, petroleum hydrocarbons, reactive silicates, ammonia, ni-
trite, nitrate and phosphate have been measured using standard
procedure (APHA, 1995). Fishes were caught in JanuaryFebruary
2012 using a trawl net, which has a large opening measuring
20.7 m and 636 50-mm mesh openings throughout. The net was
trawled for about 3045 min in the direction opposite the current.
Starting and nishing positions were taken using a handheld GPS.
After trawling, the net was lifted into the boat and sh were col-
lected and packed in polyethylene bags. Fish samples were stored
in a deep freezer prior to analysis. The name of the sh species,
feeding habits, length, weight, habitat, and shery importance were
documented. Approximately 5 g of muscle was removed, washed
with deionized water to avoid contamination, and placed into glass
beakers to dry at 60 C. A wet sample was used to conduct the Hg
analysis. Triplicate samples were collected, and the complete ana-
lytical study was conducted three times to compare to standards.
A microwave accelerated digestion system (CEM-MARS 5) is
used to help digest a wide variety of materials in the laboratory,
particularly during metal analysis. This system condenses materials
of different matrices, allowing for the analysis of volatile metals,
such as Hg. During the digestion portion of the Hg analysis, 1 ml
of HNO
3
and 3 ml of HCL were added to 5 g of tissue sample, and
the volume was increased to 10 ml using Milli-Q water. Teon ves-
sels containing the samples were kept in the double walled, outer
liner of the digestion bomb, capped with a sensor head and pressure
rupture disc. Sealed vessels were then placed in the microwave car-
ousels in the same manner as for digestion. Each set of samples was
accompanied with a blank, spike and certied reference material.
Mercury was analyzed with a ow Injection Mercury System
(FIMS-400, Perkin Elmer, Inc., Shelton, USA), whereas the other
metals were analyzed using Graphite Furnace Atomic Absorption
Spectrometry (GF-AAS, PerkinElmer, Analyst 600) and an Induc-
tively Coupled Plasma Optical Emission Spectrophotometer
(ICP-OES, Optima 7300 DV, Perkin Elmer, Inc., Shelton, USA).
The results obtained from this study were analyzed using Anal-
ysis of Variance (ANOVA), Duncan multiple range test (DMRT) for
homogenous datasets of metal concentrations, and correlation
coefcient (r) to study the signicant variation between the sh
length, weight and heavy metal concentrations observed in sh tis-
sues. The physico-chemical parameters of water quality used in
this study are given in Table 2. The Limit of Detection (LOD) and
Limit of Quantication (LOQ) were obtained using the standard
deviation of the blank signal multiplied by 3 and 10, respectively.
The recovery percentages resulted in ranges from 96% to 101%
using various spiked metal concentrations (Table 3).
Heavy metal pollution is a very serious issue in many countries
and is caused by industrial waste disposal into the sea, where it
becomes toxic for many marine organisms. Concentrations of hea-
vy metals observed in the tissue samples of shes from Thane
Creek-Mumbai Harbor are presented in Table 4. The metal
accumulation in the sh in this study was compared with samples

Table 1
Fishes sampled, length and weight, feeding habits and shery importance.

Name of sh Length (cm) Weight (gm) Habitat Feeding Fishery importance

Johnius elongatus 21.5 92 Demersal Carnivorous Commercial
Polynemus tetraductylus 28 240 Pelagic Carnivorous Commercial
Carangodiae sp. 27.5 310 Pelagic Carnivorous Commercial
Arius maculetus 36.2 411.6 Demersal Carnivorous Commercial
Dentrophysa russelli 19.2 72.4 Demersal NA Minor Commercial
Tetraden sp. 26.1 113 Demersal Omnivores Medicinal value
Coilia dussumieri 14.21 13 Neretic Carnivorous Commercial
Therapon jarbua 13.2 19.1 Demersal Omnivores Commercial
Lutjanus johni 37 374 Demersal Carnivorous Commercial
Thryssa mystax 14.2 113 Pelagic Carnivorous Commercial
Therapon jarbua 11 17.955 Demersal Omnivores Commercial
Plotosus limbatcus 28.5 220 Demersal Carnivorous Minor Commercial
Arius arius 13.5 128 Demersal Carnivorous Commercial
Thryssa hamiltonii 16.1 38.33 Pelagic Carnivorous Commercial
Scatophagus argus 9.6 7.1 Demersal Omnivores Aquarium
Trypauchen sp, 11.2 8.888 Demersal Carnivorous Minor Commercial
Trichiurus lepturus 37 22.6 Bentho Pelagic Carnivorous Commercial
Coilia dussumieri 14.8 14.5 Neretic Carnivorous Commercial
Johnius macropterus 13.5 24.64 Demersal Carnivorous Commercial
Liza macrojepis 17.9 37.714 Demersal Omnivores Commercial
3 A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224

Min Max Ave Min Max Ave
Water temperature (C) 24.1 24.1 24.1 22.8 25.4 23.5
Suspended solids (mg/l) 63 65 64 39 46 43
pH 7.6 7.6 7.6 7.5 7.7 7.6
Salinity (ppt) 33.7 33.7 33.7 30.4 33.5 32.3
Dissolved oxygen (mg/l) 4.8 4.8 4.8 2.2 5.4 3.8
BOD 3.9 4 3.8 1.3 1.6 1.4
Phosphate (lmol/l) 7.4 10.3 8.8 4.9 10.7 7.5
Nitrate (lmol/l) 54 57.9 52 41.1 55.8 48.3
Nitrite (lmol/l) 7.2 8 7.6 9.9 14.1 12.3
Ammonia (lmol/l) 19.9 19.9 19.9 16.1 68.5 38.7
Total nitrogen (lmol/l) 310.6 330.2 320.8 522 533.6 527.8
Reactive Silicate (lmol/l) 30.7 33.9 32.3 26 40.2 31.9
Petroleum Hydrocarbon (lg/l) 16.1 16.4 16.2 13 26.3 19.7













































Fig. 1. Study area of Mumbai Harbor, India.


Table 2
Physico-chemical parameters of surface water from study site.
Parameters Station 1 Station 2













from different regions/oceans, as shown in Table 5. The hierarchy
of concentrations of the heavy metals analyzed in this study is as
follows, Fe > Zn > Mn > Cu > Cr > Cd > Pb > Hg.
Cadmium (Cd) metals are a non-essential toxic metal and have
no biological role. Human toxicity occurs through food chain mag-
nication. The concentration of Cd in this study varied from 0.02
to 0.57 lg g
-1
. The highest values of Cd were observed in Johnius
elongatus (0.57 lg g
-1
) and Coilia dussumieri (0.50 lg g
-1
). The low-
est values were detected in Liza macrolepis and Arius arius
(0.02 lg g
-1
). A signicant variation of Cd concentration was
observed between the tissues from different sh species (p < 0.05).
The high Cd concentration detected in J. elongatus (0.57 lg g
-1
)
could be due to their feeding habits because they feed on benthic
worms and crustaceans. The average Cd concentration (0.19 lg g
-1
)
in the marine teleost sampled is very close to the mean values re-
ported for various sh species (Stange et al., 1995 and Sivaperumal
et al., 2007). Sankar et al. (2006) detected cadmium content in
marine sh at a level of 0.1 mg kg
-1
. Pimonwan et al. (2009) re-
ported that the Cd concentration in seafood from Muang, Rayong
Province ranged from 0.009 to 0.31 mg kg
-1
. The mean value of Cd
calculated from the studied sh was smaller than that reported from
other locations, such as Llobet et al. (2003) in Catalonia, Spain
(0.037 mg kg
-1
), Llobet et al. (2003) in Thailand (0.082 mg kg
-1
),
and Kalay et al. (1999) in the Mediterranean Sea (1.07
1.43 mg kg
-1
). However, Kwon and Lee (1999) observed that the
concentration of Cd in seafood in the Masan Bay, Korea was lower
than the mean concentration observed in this study. The Food
and Drug Administration (FDA) sets a Cd concentration limit of
A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224 221

Table 3
Recovery of various heavy metals in sh muscles.

Element Wave length Instrument LOD (lg/l) LOQ Sample (Wt mg/kg) Spiked concentration (lg/g) Content of metal (lg/g) % Recovery
Pb 283.3 GF-AAS 50 ppb 150 2.5 0.058 0.038 0.057 0.037 97.5
Cd 228.6 GF-AAS 1 ppb 3 2.5 0.07 0.04 0.069 0.03 99
Hg 523.7 CV-AAS 1 3 2.5 0.116 0.07 0.115 0.07 98.4
Cr 205.6 ICP-OES 2 6 2.5 0.466 0.30 0.465 0.3 99.5
Zn 213.857 ICP-OES 1 3 2.5 0.553 0.27 0.548 0.28 98
Mn 259.372 ICP-OES 0.4 1.2 2.5 0.123 0.08 0.119 0.084 97
Cu 327.393 ICP-OES 0.4 1.2 2.5 0.70 0.045 0.69 0.4 99
Fe 238.024 ICP-OES 5 15 2.5 0.606 0.35 0.603 0.36 98.6

Table 4
Concentrations metals in sh tissues (lg g
-1
dry wt) in Mumbai Harbor.

Name of sh Fe Zn Mn Cr Cu Cd Pb Hg (Wet)
Vashi (Station 1)

Johnius elongatus 240.5
ab
41.45
ab
4.47
a
0.62
a
2.15
a
0.57
ab
0.22
a
0.23
ab

Polynemus tetraductylus 32.11
ab
31.2
ab
1.17
a
0.07
a
1.84
a
0.47
ab
0.01
a
0.01
ab

Carangodiae sp. 91.5
ab
52.9
ab
1.7
a
0.1
a
5.8
a
0.42
ab
0.12
a
0.03
ab

Arius maculetus 107.3
ab
55.3
ab
2.24
a
0.08
a
1.75
a
0.49
ab
0.26
a
0.17
ab

Dentrophysa russelli 78.05
ab
38.69
ab
2.12
a
0.16
a
1.65
a
0.08
ab
0.13
a
0.02
ab

Tetraden sp. 101.2
ab
30.34
ab
1.96
a
0.09
a
2.4
a
0.11
ab
ND
a
0.01
ab

Coilia dussumieri 207.2
ab
54.83
ab
3.87
a
0.63
a
5.59
a
0.14
ab
0.17
a
0.04
ab

Therapon jarbua 70.63
ab
57.72
ab
2.9
a
0.89
a
2.54
a
0.04
ab
0.14
a
0.03
ab

Lutjanus johni 62.31
ab
25.55
ab
2.08
a
0.47
a
1.88
a
0.07
ab
ND 0.01
ab

Thryssa mystax 53.87
ab
60.75
ab
5.65
a
1.06
a
1.55
a
0.03
ab
0.16
a
0.01
ab

Colaba (Station 2)

Therapon jarbua 46.7
ab
36.15
ab
4.42
a
0.74
a
2.05
a
0.31
ab
0.24
a
0.09
ab

Plotosus limbatcus 51.58
ab
14.38
ab
1.48
a
ND 1.27
a
0.08
ab
0.09
a
0.05
ab

Arius arius 112.3
ab
43.53
ab
3.65
a
0.18
a
6.51
a
0.02
ab
0.14
a
0.08
ab

Thryssa hamiltonii 69.26
ab
53.11
ab
7.27
a
1
a
1.98
a
0.08
ab
0.02
a
0.1
ab

Scatophagus argus 84.99
ab
34.53
ab
4.99
a
0.1
a
2.41
a
0.11
ab
0.13
a
0.09
ab

Trypauchen sp, 40.74
ab
12.77
ab
1.4
a
ND 1.16
a
0.1
ab
0.24
a
0.11
ab

Trichiurus lepturus 141
ab
42.34
ab
6.34
a
1.55
a
2.11
a
0.12
ab
0.04
a
0.07
ab

Coilia dussumieri 105.8
ab
38.81
ab
7.75
a
1.04
a
2.24
a
0.50
ab
ND 0.08
ab

Johnius macropterus 74.93
ab
20.3
ab
2.39
a
0.55
a
0.87
a
0.04
ab
0.11
a
0.06
ab

Liza macrojepis 68.93
ab
26.21
ab
1.6
a
0.1
a
1.62
a
0.02
ab
0.04
a
0.07
ab

Metal concentrations among the tissues from different shes were compared statistically using one-way ANOVA. a, ab Means for groups in homogenous subsets are
displayed. All comparisons were statistically signicant at p < 0.05. ND; Not Deducted.

Table 5
Comparison of heavy metal concentrations (lg/g) in sh with values taken from the open literature.

Area Samples Fe Mn Cu Cr Hg Pb Cd Zn References
Mediterranean Sea Dry wt 59.673.4 3.405.88 1.281.6 1.071.43 16.131.4 Kalay et al. (1999)
Masan B ay, Korea Dry wt

0.180.25 0.020.05 6.3312.9 Kwon and Lee (1999)
Middle Black Sea Dry wt 9.5232.4 1.060.76 1.282.93

0.090.48 9.522.9 Tuzen (2002)
Black Sea Dry wt 3060 0.69 0.56 1.014.54 <0.060.84 <0.020.24 25.744.2 Topcuoglu et al. (2002)
Iskenderun Bay, Turkey Dry wt 0.93.6 0.661.98 1.031.79 8.992.18 Yilmaz (2003)
Karp Farvel, Greenland Wet wt 0.20.3 0.180.21 0.0030.012 0.00990.019 2.33.6 Stange et al. (1995)
Barents sea Wet wt 0.60.6 0.07 <0.1 <0.01 5.67.8 Plotitsyna and Kireeva (1996)
Mumbai, India Wet wt 0.31 0.78 0.015 0.08 0.02 8.36 Mishra et al. (2007)
Parangipettai, India Dry wt 24.150.3 0.311.2 0.120.31 0.650.92 0.180.54 14.133.5 Raja et al. (2009)
Calicut, India Wet wt 0.5 2.8 0.6 0.13 0.1 6 Sankar et al. (2006)
Mumbai, India Wet wt 0.6 0.6 1.78 0.03 0.019 Deshpande et al. (2009)
Mozambigue Channel Wet wt 5.33 0.06 0.15 0.38 0.03 0.25 9.92 Kojadinovic et al. (2007)
East coast of India Wet wt 80.1 2.9 5.7 1.6 0.41 21.9 Kumar et al. (2012)
Kolkata Wet wt 58.66 4.24 7.54 0.41 0.31 47.8 Kumar et al. (2011)
Mumbai Harbor, India Dry wt 97.04 3.47 2.46 0.47 0.06 0.12 0.19 38.54 This present study

0.010.21 lg g
-1
in sh. The results from this study varied from 0.02
to 0.57 lg g
-1
. A maximum Cd content of 0.050.1 mg kg
-1
was set
by the European Union (2008). Values of all sh species sampled
were smaller than the acceptable limit suggested by the European
Union (EU), except J. elongatus (0.57 lg g
-1
) and C. dussumieri
(0.50 lg g
-1
). The average value of Cd concentration reported for
marine sh in this study did not exceed the permissible level of
the National Health and Medical Council, Australia (2 lg g
-1
).
Lead is a toxic element that has no biological role and causes car-
cinogenic effects in marine biota and humans. The concentration of
Pb measured in this present study varied from 0.01 to 0.26 lg g
-1
.
Maximum Pb values were present in A. maculetus (0.26 lg g
-1
)
and Therapon jarbua (0.24 lg g
-1
). The lowest concentration was
detected in Polynemus tetradactylcus (0.01 lg g
-1
). Pb concentra-
tions were below the detection level in Lutjanus johni, Tetraden sp.
and C. dussumieri. However, the average Pb concentration value
(0.12 lg g
-1
) observed in the studied species was similar to values
reported by Burger and Gochfeld (2005) and lesser than reported
by Sankar et al. (2006) in Kochi waters, India. Sankar et al. (2006) re-
ported that lead was not detected in the commercially important
sh species they studied, except for J. dussumerri (0.13 mg kg
-1
).
Sivaperumal et al. (2007) recorded Pb concentrations in 25% of
nsh, shellsh and other shery products from the Indian coast.
However, the FDA sets a permissible Cd range of 0.0010.003 mg kg
-1
.
5 A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224


This value is lower than the results obtained in this study (FDA,
2003). The EUs acceptable limit for Pb concentration is 0.5
1.0 lg g
-1
. The Pb concentrations of several sh species were
found to be lower than the acceptable limit suggested by the Euro-
pean Union (EU, 2001; EU, 2008). The sh species in this study with
high concentrations of Pb require further research, including an
analysis of the number of tissue samples and maximum sample size.
Mercury (Hg) is a highly toxic metal, which causes severe pollu-
tion via industrial waste discharges. Fish acquire Hg through feed-
ing, which can be determined by sh size, diet, ecological
parameters, and water quality parameters. Mercury was detected
in all sh samples from this study. The concentrations varied from
0.01 to 0.23 lg g
-1
. The maximum concentration of Hg was ob-
served in J. elongatus (0.23 lg g
-1
) and the minimum concentration
was detected in Thryssa mystax (0.01 lg g
-1
) followed by L. johni, P.
tetraductylus and Tetraden sp. The average value of Hg observed in
this study was 0.06 lg g
-1
. Sankar et al. (2006) reported concentra-
tions of Hg in the range of 0.30.5 mg kg
-1
in 5% of marine sh.
Sivaperumal et al. (2007) found that Hg could not be detected in
88% of the Indian marine sh tissue samples they analyzed. The
absorbance of Hg in Mumbai Harbor sh was not high compared
to other international waters (Burger et al., 2005). This study ob-
served lower levels than Kumar et al. (2011) (0.41 lg g
-1
). Simi-
larly, Bordajandi et al. (2004) observed Hg concentrations in sea
sh from Spain, ranging from 0.069 to 0.549 mg k g
-1
. Cirillo
et al. (2010) stated that Hg concentrations varied from 0.08 to
0.339 mg k g
-1
in wild seafood. This value is very close to the Hg
levels detected in the species analyzed in this study. The FDA sets
a permissible range of 0.0040.16 mg k g
-1
for several sh species
(FDA, 2003). The EUs acceptable limit for Hg concentration is
0.5 mg kg
-1
, with the exception of certain larger predatory sh
species, which have a limit of 1.0 mg kg
-1
(EU, 2008). In this study,
none of the sh samples had Hg concentrations higher than the EU
limits. The variations in Hg concentrations in the sh species sam-
pled is due to their feeding habits, habitat preference, distribution
and seasonal variation. Additionally, Hg concentrations in prey and
bio-concentration capacities of each species are important.
Copper (Cu) was recorded in all of the tissue samples from this
study. The concentration of Cu in sh muscle samples varied be-
tween 0.87 and 6.51 lg g
-1
. The highest concentration of Cu was
detected in A. arius (6.51 lg g
-1
), and the lowest value was de-
tected in J. macropterus (0.87 lg g
-1
). The mean Cu content for
marine teleost sh species in this study was 2.46 lg g
-1
. A similar
mean value (2.8 mg kg
-1
) was reported by Sankar et al. (2006) in
different sh species from the west coast of India. The observed
values of Cu in sh tissues were higher than those observed by Raja
et al. (2009) in sh collected from Parangipettai water, India (0.12
0.31 lg g
-1
), and Stange et al. (1995) in Karp Farvel, Greenland
(0.200.3 lg g
-1
) but lower than Kalay et al. (1999) reported in
the Mediterranean Sea (3.405.88 lg g
-1
). The mean Cu concentra-
tions observed in commercially important marine sh species in
this study did not exceed the acceptable limit (1.53.0 mg kg
-1
)
suggested by the National Research Council, China and maximum
Cu content (30 mg/kg) set by FAO/WHO (1989). It is well known
that Cu and Manganese are important elements in sh, play a vital
role in enzymatic processes and are essential for the synthesis of
hemoglobin. However, very high intake will cause adverse health
problems (Demirezen and Uruc, 2006; Satheeshkumar et al., 2011).
The concentration of Chromium (Cr) in sh tissues sampled var-
ied from 0.08 to 1.55 lg g
-1
. The maximum value of Cr was present
in Trichiurus lepturus (1.55 lg g
-1
) followed by C. dussumieri
(1.0 lg g
-1
), and the minimum values of Cr were detected in P. tet-
raductylus (0.07 lg g
-1
), A. maculetus (0.08 lg g
-1
) and Tetraden sp
(0.09 lg g
-1
). Cr was below detection level in Plotosus limbatcus
and Trypauchen sp. The average Cr concentration from samples in
this study was 0.47 lg g
-1
. The Cr values from this study are sim-
ilar to those reported by Kwon and Lee (1999) (0.180.25 lg g
-1
)
in Masan Bay, Korea, and lower than those measured by Sankar
et al. (2006) (0.47 lg g
-1
) in Calicut, India, Raja et al. (2009)
(0.650.92 lg g
-1
) in Parangipettai water, India and Yilmaz, 2003
(1.031.79 lg g
-1
) in Iskenderun Bay, Turkey. The concentration
of Cr in sh tissues in this study was comparable to concentrations
reported in other studies. The range of absorption values observed
was lower than the Cr contents (0.120.92 mg/kg wet weight) re-
ported in sh tissue samples from New Zealand (Winchester,
1988; Vlieg et al., 1991), Australia (0.440.63 mg/kg dry wt), and
California (0.273.0 mg/kg dry wt) waters (Moeller et al., 2003).
The maximum allowable Cr content level in sh is 1213 mg/kg,
as set by the USFDA (1993). The permissible level of heavy metals
set by the European Union is 0.5 mg/kg wet weight (EU 2008). Cr
concentration in the sh species studied met permissible level cri-
teria for human consumption. Cr is an important trace element and
plays a critical role in glucose metabolism (Mertz, 1969). Cr de-
ciency can result in impaired development and disturbances in
glucose, lipid, and protein metabolism (Calabrese et al., 1985).
Iron (Fe) was observed in all samples and was the most abundant
trace element in tissue samples from this study. The maximum Fe
concentration was observed in J. elongatus (240.50 lg g
-1
), and the
lowest Fe concentration was observed in P. tetraductylus
(32.11 lg g
-1
). The mean Fe concentration of tissue samples
analyzed in this study was 97.4 lg g
-1
. High values of Fe in the sam-
ples indicates that the environment is stressed. This study observed
values higher than permissible limits set by the FAO and the WHO.
The Fe values are similar to those reported by Kalay et al. (1999)
(59.673.4 lg g
-1
) in the Mediterranean Sea, except J. elongatus
(240.5 lg g
-1
), C. dussumieri (207.2 lg g
-1
), and A. arius
(112.3 lg g
-1
). The iron concentrations in sh samples from this
study were higher than those from studies conducted in interna-
tional waters (Yilmaz, 2003; Tuzen, 2002; Kojadinovic et al., 2007).
The high Fe concentration observed in J. elongatus is due to their
feeding habits and habitat preference. Fe concentrations increased
due to a decrease in grain size and an increased input of organic mat-
ter and anthropogenic metals from industrial pollution. Domestic
sewage waste and hospital waste were discharged directly into
the river (Satheeshkumar and Kumar, 2011). Similar detection was
reported by Zhang et al. (2007) in Yangtze Estuary, China.
Zinc was found to be the second most abundant metal in the
sh species sampled in this study. The absorption of Zn varied
signicantly between tissue samples from different sh species
(p < 0.05). The highest concentration of Zn was detected in
T. mystax (60.75 lg g
-1
) followed by T. jarbua (57.72 lg g
-1
) and
A. maculetus (55.3 lg g
-1
). The lowest values of Zn were observed
in Trypauchen sp (12.7 lg g
-1
) and P. limbatcus (14.38 lg g
-1
).
The mean value for tissue samples examined in this study was
38.54 lg g
-1
. Similar mean values were reported by Raja et al.
(2009) (14.133.5 lg g
-1
) in Parangipettai waters, India, and Kalay
et al. (1999) (14.133.5 lg g
-1
) in sh species caught from the
Mediterranean Sea. Sankar et al. (2006) reported Zn concentrations
of 6 mg kg
-1
in marine sh caught in Kochi waters. The mean Zn
concentration from sh samples in this study was lower than other
studies in international waters, including Kojadinovic et al. (2007)
in Mozambique Channel (41.7 mg kg
-1
), Topcuoglu et al. (2002) in
the Black Sea (44.2 mg kg
-1
) and Kumar et al. (2011) in the Kolkata
wetlands (48 lg g
-1
). However, Kwon and Lee (1999) in Masan
Bay, Korea recorded values ranging from 6.33 to 12.9 lg g
-1
, which
is lower than the values observed in this study. The acceptable
limit of Zn in most sh is 5 mg/kg or 25 mg/kg for certain types
of seafood, as suggested by the New Zealand Food Standards Code
(FSANZ, 2004). The European Unions permissible level of Zn for
human consumption is 30 mg/kg wet weight (EU 2008). Zinc is
one of the most important trace elements for the human body be-
cause it is a key component of cells, and enzymes depend upon it
A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224 223

Fe Zn Mn Cr Cu Cd Pb Hg Length Weight
Fe 1

Zn 0.33 1

Mn 0.527
*
0.552
*
1

Cr 0.3 0.553
*
0.81
*
1

Cu
Cd
0.611
**

0.459
*

0.49
*

0.18
0.03
0.09
-0.09 1
0.05

1

Pb 0.22 0.34 -0.13 0 0.08 0.04 1

Hg 0.53 0.04 0.25 0.03 -0.11 0.48 0.34 1

Length -0.678
*
0.385
*
-0.27 -0.07 -0.63
*
-0.58
**
-0.12 -0.05 1

Weight -0.645
*
0.679
*
-0.46 -0.42 -0.64
*
-0.57
**
0.47
*
-0.06 0.65
*
1


as a cofactor. However, excessive Zn and Cu intake is detrimental
to human health and can cause poisoning, nausea, acute stomach
pains, diarrhea and fever (Chi et al., 2007).
Manganese is a low toxicity metal with a signicant biological
role that accumulates in aquatic organisms. The maximum concen-
tration of Mn detected in this study was in C. dussumieri
(7.75 lg g
-1
) followed by T. hamiltonii (7.27 lg g
-1
) and T. lepturus
(6.34 lg g
-1
). The lowest concentration was observed in P. tetra-
ductylus (1.17 lg g
-1
). The average MA concentration (3.47 lg g
-1
)
from tissue samples in this study is similar to mean values re-
ported by Raja et al. (2009) (1.2 lg g
-1
) and Kumar et al. (2011)
(2.9 lg g
-1
) in different sh species caught from Indian waters.
Sankar et al. (2006) reported a Mn concentration of 0.5 mg kg
-1
in marine sh caught in Kochi waters. Yilmaz et al. (2007) recorded
Mn concentrations in Leuciscus cephalus ranging from 0.11 to
24.23 lg g
-1
and in Lepomis gibbosus ranging from 1.07 to
12.43 lg g
-1
in Saricay stream, Turkey. The permissible level of
Mn is 2.57 mg of total daily intake, as suggested by NAS-NRC
(1977). The mean Mn concentration from tissue samples in this
study was lower than other studies conducted in international
waters (Mendil et al., 2005; Yilmaz et al., 2007). Mn is an essential
trace metal for plants and animals. Mn deciencies can cause se-
vere skeletal and reproductive abnormalities in mammals.
The body sizes of marine organisms play an important role in
the accumulation of trace metals in tissues. Understanding the
relationship between animal size (length and weight) and the
absorption of both essential and non-essential trace elements is
crucial. Table 6 shows the relationship between trace metal con-
centrations and sh length and weight. A signicant negative cor-
relation was observed between sh (length and weight) and Fe
(p < 0.05), Cu (p < 0.05), and Cd (p < 0.01) concentrations recorded
in the tissue samples. Nussey et al. (2000) reported that the accu-
mulation of trace metals (Cr, Mn, Ni, and Pb) declined with increas-
ing length in Labeo umbratus. A signicant positive correlation was
observed between zinc and sh weight (p < 0.01). Pb content in the
tissue samples showed a positive correlation (p < 0.05) with sh
weight but not with length (p > 0.05). Widianarko et al. (2000)
examined the relationship between Pb, Zn, and Cu metal concen-
trations and Poecilia reticulata length and weight. They reported a
signicant decline in Pb concentrations as sh length increased,
whereas Cu and Zn concentrations were not dependent on sh
weight. The Pb and Hg contents in sh muscles showed no corre-
lation with sh length. The statistical analysis used in this study
proved that metal concentrations varied signicantly for different
sh species. A signicant positive correlation was observed in
tissue samples for the trace metal pairs of Fe and Mn (p < 0.05),
Fe and Cd (p < 0.05), and Fe and Cu (p < 0.01). In addition, a signif-
icant variation between Zn and Mn (p < 0.05), Zn and Cr (p < 0.05),
Zn and Cu (p < 0.05), Cr and Zn (p < 0.05), and Mn and Cr (p < 0.01)
were found in all analyses. Hg showed a poor correlation with all
ve trace elements, perhaps because the major source of Hg is coal
combustion. A report from the Mumbai coast indicated that several
marine sh contained various trace metals in their tissue samples
(Deshpande et al., 2009).
Based on the present study, the accumulation of trace metals
was highest in demersal shes, followed by neritic and pelagic
shes. The demersal species J. elongates and neritic species C. duss-
umieri from Mumbai waters showed maximum concentrations of
trace metal accumulation. Fe and Zn concentrations were higher
than allowable levels in these species. Other important toxic metal
concentrations (Pb, Cr, Cd, and Hg) were safe for human consump-
tion. Romeo et al. (1999) reported that concentrations of Cd, Cu
and Zn in edible pelagic sh species were less than those in demer-
sal shes. Similarly, this study observed that Pb, Cr, Cd, and Hg con-
centrations were lowest in tissue samples from Carangodiae sp, T.
mystax, and Liza macrojepis (benthic omnivores). The concentra-
tions of other trace elements in sh tissue samples from this study
were lower than the permissible levels recommended by the WHO
and the FAO (WHO, 1989; FAO, 1983).
It is important to note the effects of sewage waste water and
industrial run-off on marine sh populations and the bioaccumula-
tion of trace elements in their body tissues. Previous studies
showed that different contents of trace metals in various sh spe-
cies may vary based on habitats and ecological needs, metabolic
capability and feeding habits (Amundsen et al., 1997; Ayse, 2003;
Chi et al., 2007; Singh et al., 2007). The accumulation rate of trace
metals in marine sh species varies depending on the elements ex-
tracted, concentration, accumulation time from sources, and the
rate of scale formation (Patin, 1984). The efciency of trace ele-
ment uptake from contaminated water and food varies based on
ecological needs, body metabolic capability, and the environmental
parameters of salinity and temperature (Pagenkopf, 1983; Sat-
heeshkumar and Kumar, 2011).
The results of the present study represent valuable heavy metal
concentration data in sh from Mumbai Harbor and international
markets. The edible shes analyzed in this study contain metal con-
centrations of toxic trace elements Hg, Cd and Cr below the levels
recommended for human consumption. However, Fe concentra-
tions are higher in Mumbai Harbor waters due to industrial waste
overloading and sewage dumping from the city of Mumbai, as
was found in the Arabian Sea. Heavy metal concentrations in
the sh samples analyzed in this study are well within the
recommended level set by many authorities (EU, FAO/WHO), ex-
cept in a few instances. Accordingly, the sh caught from the Mum-
bai coast can be considered generally safe for human consumption.


Acknowledgements

The authors thank the Director, CSIR-National Institute of
Oceanography, Goa, India and the Scientist-in-Charge, Regional
Centre, National Institute of Oceanography, Mumbai, India for
facilities and encouragement. We gratefully acknowledge all our

Table 6
Correlation between heavy metals and sh length and weight.






-0.04




*
Correlated at 5% signicance level.
**
Correlated at 1% signicance level.
7 A. Velusamy et al. / Marine Pollution Bulletin 81 (2014) 218224

colleagues in CSIR-NIO, Mumbai who helped during sampling and
instrumental analysis.


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