Marine Pollution Bulletin 81 (2014) 218224

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BaselineThe New Format and Content (Mar. Pollut. Bull. 60, 12).

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 190019050

N and lon-

gitude 725573000

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 HNO3 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 32.11ab

31.2ab

1.17a

0.07a

1.84a

0.47ab

0.01a

0.01ab

Carangodiae sp. 91.5ab

52.9ab

1.7a

0.1a

5.8a

0.42ab

0.12a 0.03

ab

Arius maculetus 107.3ab

55.3ab

2.24a

0.08a

1.75a

0.49ab

0.26a 0.17

ab

Dentrophysa russelli 78.05ab

38.69ab

2.12a

0.16a

1.65a

0.08ab

0.13a 0.02

ab

Tetraden sp. 101.2ab

30.34ab

1.96a

0.09a

2.4a

0.11ab

NDa

0.01ab

Coilia dussumieri 207.2ab

54.83ab

3.87a

0.63a

5.59a

0.14ab

0.17a 0.04

ab

Therapon jarbua 70.63ab

57.72ab

2.9a

0.89a

2.54a

0.04ab

0.14a 0.03

ab

Lutjanus johni 62.31ab

25.55ab

2.08a

0.47a

1.88a

0.07ab

ND 0.01ab

Thryssa mystax 53.87ab

60.75ab

5.65a

1.06a

1.55a

0.03ab

0.16a 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 51.58ab

14.38ab

1.48a

ND 1.27a

0.08ab

0.09a

0.05ab

Arius arius 112.3ab

43.53ab

3.65a

0.18a

6.51a

0.02ab

0.14a 0.08

ab

Thryssa hamiltonii 69.26ab

53.11ab

7.27a

1a

1.98a

0.08ab

0.02a

0.1ab

Scatophagus argus 84.99ab

34.53ab

4.99a

0.1a

2.41a

0.11ab

0.13a 0.09

ab

Trypauchen sp, 40.74ab

12.77ab

1.4a

ND 1.16a

0.1ab

0.24a 0.11

ab

Trichiurus lepturus 141ab

42.34ab

6.34a

1.55a

2.11a

0.12ab

0.04a

0.07ab

Coilia dussumieri 105.8ab

38.81ab

7.75a

1.04a

2.24a

0.50ab

ND 0.08ab

Johnius macropterus 74.93ab

20.3ab

2.39a

0.55a

0.87a

0.04ab

0.11a 0.06

ab

Liza macrojepis 68.93ab

26.21ab

1.6a

0.1a

1.62a

0.02ab

0.04a

0.07ab

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

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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