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Marine Pollution Bulletin 119 (2017) 454–459

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Marine Pollution Bulletin

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Baseline

Toxic heavy metals in commercially important food fishes collected from


Palk Bay, Southeastern India
Abimannan Arulkumar a, Sadayan Paramasivam a,⁎, Rajendran Rajaram b
a
Department of Oceanography and Coastal Area Studies, School of Marine Sciences, Alagappa University, Thondi Campus, Thondi 623 409, Tamil Nadu, India
b
Department of Marine Science, Bharathidasan University, Tiruchirappalli 620024, Tamil Nadu, India

a r t i c l e i n f o a b s t r a c t

Article history: Toxic heavy metals are an important group of emerging chemical contaminants in seafood. Heavy metal concen-
Received 2 December 2016 trations in commercially important and most commonly eaten 10 fish species from Thondi fish landing, southeast
Received in revised form 18 March 2017 coast of India, were determined by atomic absorption spectrometry. The concentrations of heavy metals signifi-
Accepted 22 March 2017
cantly varied within and between the investigated fish species (P b 0.05). The results of this study showed best
Available online 4 April 2017
significant correlations among the toxic heavy metals in the fish samples. It was revealed that Cd, Pb, Cu, and
Keywords:
Zn metals were present in the fish samples at various levels. The residual levels of toxic heavy metals were less
Heavy metal than the permissible levels specified for human consumption by the European Union, Food and Agriculture Or-
Fish ganization and World Health Organization guidelines. Therefore, the fish species found in the Thondi fish landing
Thondi coast and their fishery products can be considered safe for human consumption and can be exported worldwide.
Contaminant © 2017 Elsevier Ltd. All rights reserved.

Fishes are considered as an important food source of macronutrients with proven hazardous nature are to be completely excluded in food
(carbohydrates, animal protein, fatty acids, vitamins, and polyunsatu- for human consumption. Heavy metals such as Cd, Cu, Pb, and Zn are
rated fatty acids) and micronutrients (copper, zinc, iron, and selenium) the most common contaminants in fish and fishery products. Consump-
for human health. Marine chemical contamination can increase the con- tion of elements such as Pb causes severe health risks such as fatigue, ir-
centrations of toxic heavy metals in aquatic systems and thereby nega- ritability, myalgia, coma, kidney, liver, and brain damage, seizures,
tively affect the fish health. Such heavy metal pollution can be caused by encephalopathy, nervous system dysfunction, and development of can-
different natural and anthropogenic sources, including agricultural cer. Cadmium toxicity caused Itai-Itai disease in Japan and can causes
drainage, industrial effluent discharge, sewage discharge, accidental bone disease, anosmia, yellow discoloration of the teeth, and loss of ol-
chemical waste spills, and gasoline from fishing boats (Mishra et al., faction abilities (Sanders et al., 2009; Sankar and Ashok Kumar, 2014).
2007; Satheeshkumar and Kumar, 2011; Velusamy et al., 2014; Various analytical methods have been developed for the determination
Mathivanan and Rajaram, 2014). The accumulation of heavy metals in of heavy metals in fishes. The most widely used techniques are atomic
marine fishes depends on the environmental condition, season, loca- absorption spectrometry (AAS), inductively coupled plasma optical
tion, distribution, habitat preference, tropic level, feeding habit, age, emission spectrometry, inductively coupled plasma-mass spectrome-
size, sex, duration of exposure to the metals, and homeostatic regulation try, X-ray fluorescence, particle-induced X-ray emission, total reflection
activity (Sankar et al., 2006). Accumulations of heavy metals were found X-ray fluorescence, neutron activation analysis, atomic fluorescence
in the water and sediment columns, and these metals enter into the spectrometry, ion chromatography, and immunoassay (Sivaperumal et
food web through the feeding of benthic and pelagic species (Galay al., 2007; Sankar and Ashok Kumar, 2014; Velusamy et al., 2014;
Burgos and Rainbow, 2001). El-Moselhy et al., 2014; Kulawik et al., 2016).
Heavy metals such as iron (Fe), copper (Cu), and zinc (Zn) are im- Marine fish and fishery products constitute an important diet of
portant for fish metabolism, while mercury (Hg), lead (Pb), cadmium human food, and it is therefore not surprising that abundant reports
(Cd), and other metals have unknown functions in their biological sys- are available on toxic heavy metal contamination in different marine
tem. Metabolic activity plays an important role in the bioaccumulation edible fish species (Mitral et al., 2000; Sankar et al., 2006; Sivaperumal
of trace metals in marine organisms (Velusamy et al., 2014). et al., 2007; Prabhu Dass Batvari et al., 2008; Uysal et al., 2008; Prabhu
Sivaperumal et al. (2007) stated that the essential metals can also pro- Dass Batvari et al., 2012; Akan et al., 2012; Kumar et al., 2012; Murthy
duce toxic effects at high residual concentrations. Only few metals et al., 2013; Heidarieh et al., 2013; Javed and Usmani, 2013; Usha and
Vikram Reddy, 2013; Elnabris et al., 2013; El-Moselhy et al., 2014;
⁎ Corresponding author. Kulawik et al., 2016; Velusamy et al., 2014). Seafood is the most pre-
E-mail address: psivams@alagappauniversity.ac.in (S. Paramasivam). ferred food worldwide, and it is important to study the bioaccumulation

http://dx.doi.org/10.1016/j.marpolbul.2017.03.045
0025-326X/© 2017 Elsevier Ltd. All rights reserved.
A. Arulkumar et al. / Marine Pollution Bulletin 119 (2017) 454–459 455

of heavy metals in commercially and economically important fish and They were collected from fishermen and packed into HiMedia polyeth-
fishery products. Toxic heavy metal residues can be hazardous to ylene bags (HiMedia Mumbai, India). Fish samples were stored in a
human health, and it often becomes mandatory to screen the chem- deep freezer (−20 °C) prior to analysis.
ical contaminants in fish and fishery products from the aquatic en- The concentration levels of Cd, Pb, Cu, and Zn were analyzed accord-
vironment to understand their potential health effects. Therefore, ing to the European Standards. One gram of homogenized fish sample
this study aimed to determine the levels of toxic heavy metal resi- was added to a mixed reagent of nitric acid, perchloric acid, and sulfuric
dues (Cd, Pb, Cu, and Zn) in the muscle tissues of 10 marine fish acid at a ratio of 5:2:1. Mineralization was performed on a hot plate at
species. 50 °C for 30 min. After the end of digestion, 10 ml of 2 N HCl was
Fish samples used in this study were collected from Thondi, Palk Bay, added; digested solutions were filtered and made up to 25 ml with dou-
Southeast Coast of India (latitude: 9° 44′ N and longitude: 79° 00′ E) ble distilled water and stored at room temperature for further analysis
(Fig. 1). The water quality parameters like pH, atmospheric tempera- (FAO/SIDA, 1983). Cd, Cu, Pb, and Zn were determined by AAS
ture, surface water temperature, dissolved oxygen, salinity, and levels (Shimadzu 7000, Japan) at the wavelengths of 228.80, 324.75, 217.00,
of phosphate, nitrate, nitrite, total nitrogen, and ammonia were mea- and 213.85 nm, respectively. Heavy metal standards were prepared
sured using the standard procedures (APHA, 1998; AWWA, 1998; and run to check the precision of the instrument throughout the analy-
WEF, 1998). Fishes were caught during April–May 2016 using trawl sis. The quality assurance and quality control protocol set by the U.S. En-
net. The net was trawled approximately 30–50 min in the direction op- vironmental Protection Agency for metal analysis was used. The quality
posite to the water current. After trawling, the fishnet was lifted on to assurance testing relied on the blank controls and the yield of the chem-
the boat and finfish, shrimps, crabs, and cuttle fish were segregated. ical procedure.

Fig. 1. Study Area of Thondi, Palk Bay, Southeast coast of India.


456 A. Arulkumar et al. / Marine Pollution Bulletin 119 (2017) 454–459

The results obtained from this study were analyzed using the analy- Table 2
sis of variance (ANOVA), and the differences among the heavy metal Physicochemical parameters of the Thondi coast.

(Cd, Pb, Cu and Zn) concentration levels were considered significant at No Physicochemical parameters Values
the 5% level at 95% confidence interval (P b 0.05). Correlation coefficient 1 Atmospheric water temperature (°C) 36
(r2) analysis was used to determine the significant relationship between 2 Surface water temperature (°C) 32
the fish weight, length, and heavy metal residues. For all the cases, the 3 pH 7.6
analyses were performed using the SPSS Statistical package 14 for 4 Dissolved oxygen (DO) mg/l 7.3
5 Salinity (%) 36
Windows (SPSS Inc., USA).
6 Phosphate (μmol/l) 5.6
Pollution by heavy metals is a very serious problem in many coun- 7 Nitrate (μmol/l) 5.3
tries and is caused by the disposal of industrial effluents into the sea 8 Nitrite (μmol/l) 4.3
water, where it becomes toxic for many marine animals and flowering 9 Total nitrogen (μmol/l) 10.2
halophytic plants (Velusamy et al., 2014). Table 1 shows the character- 10 Ammonia (μmol/l) 7.6

istics of the 10 fish species used in the present study. The physicochem-
ical parameters of the Thondi coast are given in Table 2. The heavy metal
residues observed in the muscle samples of the fish species from the Table 3
Thondi coast are provided in Table 3. Standard regulatory limits of Concentration of heavy metals in the fish samples (ppm) from Thondi coast.

heavy metals (Table 4) and its accumulation in the fish species of this Sl. no Scientific name of the fish Cd Pb Cu Zn
region was compared with different regions in the world (Table 5). 1 Chirocentrus dorab 0.04a 0.1a 1.14a 29.75a
Cd is a nonessential toxic metal and has no biological activity in 2 Rastrelliger kanagurta 0.04b 0.1b 1.30b 29.34b
humans. Human exposure to Cd poisoning occurs through food chain 3 Carangoides caeruleopinatus 0.05a 0.4a 1.16a 26.69a
magnification (Velusamy et al., 2014). In the present study, the concen- 4 Stolephorus indicus 0.02b 0.2b 0.90b 21.48b
5 Upeneus vittatus 0.04a 0.1a 1.11a 18.80a
tration of Cd in the muscle tissues of the fish species ranged from 0.02 to
6 Chanos chanos 0.10b 0.1b 8.68b 39.99b
0.28 ppm. The highest Cd concentration of 0.28 ppm was recorded in 7 Peneaus indicus 0.14a 0.3a 4.60a 39.03a
Portunus pelagicus. This could be because of their feeding habits. A pos- 8 Portunus pelagicus 0.28b 0.9b 8.35b 55.14b
itive significance of P b 0.05 of Cd residues was noted between the mus- 9 Sepia brevimana 0.11a 0.11a 5.88a 52.06a
cle tissues from different fish species (Table 6). Velusamy et al. (2014) 10 Sepia aculeate 0.07b 0.12b 6.42b 42.83b

reported that the highest Cd concentration of 0.57 ppm in Johnius Heavy metal residues in the muscle tissues of different fish samples were compared statis-
elongatus. Prabhu Dass Batvari et al. (2012) reported high concentra- tically using one-way ANOVA. a and b are statistically significant at P b 0.05.
tions of Cd from Scylla serrata (0.136 ppm), Penaeus semisulcatus
(0.150 ppm), and Penaeus indicus (0.182 ppm) in the North Chennai
coastal region, India. Sankar et al. (2006) reported lower Cd concentra- Table 4
tion (0.1 ppm) in marine fish. However, the above mentioned concen- Standard regulatory limits (ppm/mg/kg) of heavy metals in fish samples as reported in the
literature.
trations of Cd in the studied fish species were lower than those
reported in other geographical locations, including the Red Sea in Organization/country Heavy metals References
Egypt (0.12 ppm) (El-Moselhy et al., 2014); Cracow, Poland Cd Pb Cu Zn
(0.002 ppm) (Kulawik et al., 2016); Cochin, Kerala, India (0.03 ppm)
FAO 0.005 0.5 30 30 FAO (1983)
(Sivaperumal et al., 2007); and Southern Nigeria (0.10 ppm) FAO/WHO 0.5 0.5 30 100 FAO/WHO (1989)
(Oyakhilome et al., 2013). In addition, Vasanthi et al. (2014) reported European commission 0.5 0.3 – 30 EC (2008; 2014)
a lower level of Cd concentration (0.1 ppm) in Pulicat Lake, FSSAI 0.3 0.3 – – FSSAI (2015)
Chennai, India, which was lower than that observed in the present FDA for crustaceans 3 1.5 – – FDA (2001)
Codex Stan 2 0.3 – – Codex Stan (193–1995)
study (Table 2). The FAO/WHO set the residual limit of Cd as 0.5 ppm Turkey guideline 0.1 1 20 50 Dural et al. (2007)
for fish, and the FDA set the maximum permissible limit as 3.0 ppm for England 0.2 2 20 50 MAFF (2000)
crustaceans and cephalopods. In our study, the Cd concentrations varied
from 0.02 to 0.28 ppm. The European commission (EC) (2008) and (EU)
(2014) set the maximum allowable limit of Cd concentration as 0.5 ppm Pb is considered as carcinogenic to human (IARC group 1 and MAK
in fish samples. In the present study, all the fish samples showed low commission category 1). Humans can be exposed to Pb through chronic
level of Cd as regulated by the EU (2014). The report of Joint FAO/ inhalation (EU, 2014; Sankar and Ashok Kumar, 2014). The concentra-
WHO Expert Committee on Food Additives (JECFA) has recommended tion of Pb in the present study varied from 0.1 to 0.9 ppm. Higher con-
a provisional tolerable weekly intake (PTWI) of 0.007 ppm/kg body centration (0.9 ppm) of Pb residues were observed in P. pelagicus and
weight for Cd (Sankar and Ashok Kumar, 2014). The average Cd concen- lower concentration (0.1 ppm) of Pb were noted in C. dorab, R.
tration in the present study did not exceed the maximum allowable level kanagurta, U. vittatus, and C. chanos. However, the average Pb concentra-
(2.0 ppm) set by the Codex Standard (193–1995). tion in the present study was 0.23 ppm. Higher value was reported by

Table 1
Fish and shell fish samples, length and weight, feeding habits, and values of importance to fishery.

Scientific name of the fish No. of samples analyzed Weight (g) Length (cm) Habitat Feeding habits

Chirocentrus dorab 5 200 35.3 Pelagic Carnivorous


Rastrelliger kanagurta 6 175 25 Pelagic Carnivorous
Carangoides caeruleopinatus 5 230 25.4 Pelagic Carnivorous
Stolephorus indicus 5 2.55 12.6 Demersal Carnivorous
Upeneus vittatus 5 18.2 13 Demersal Carnivorous
Chanos chanos 6 43 26.2 Pelagic Carnivorous/Omnivores
Penaeus indicus 7 43.5 13.1 Demersal Carnivorous
Portunus pelagicus 8 67.5 18.2 Pelagic Carnivorous
Sepia brevimana 7 350 23.6 Demersal Carnivorous
Sepia aculeate 6 180 16.5 Demersal Carnivorous
A. Arulkumar et al. / Marine Pollution Bulletin 119 (2017) 454–459 457

Table 5
Comparison of toxic heavy metal levels (ppm) in fish samples as reported in the literature.

Sample Study area Toxic metals References

Cd Pb Cu Zn

Fish Mediterranean Sea 1.07 – 3.40 16.1 Kalay et al. (1999)


Fish West Bengal, India – 98.5 1.0 11.5 Mitral et al. (2000)
Fish Sundarban Wetlands, India 18.3 – – 965.3 Sarkar et al. (2002)
Fish Kolleru Lake, India 0.11 1.84 – 41.0 Sekar et al. (2003)
Fish Calicut, India 0.1 – 1.50 16.20 Sankar et al. (2006)
Fish Mumbai, India 0.02 0.08 0.31 8.36 Mitral et al. (2000)
Fish and shell fish products Cochin, India 0.03 0.07 1.44 44 Sivaperumal et al. (2007)
Fish Western Mediterranean – – 1.03 12.28 Uysal et al. (2008)
Fish Pulicat Lake, India 0.02 0.6 – 0.08 Prabhu Dass Batvari et al. (2008)
Fish Parangipettai Coast, India 0.18 – 0.12 14.1 Raja et al. (2009)
Fish Kolkata, India 0.33 – 3.9 19.8 Kumar et al. (2011)
Fish Gaza 0.09 0.17 0.90 20.53 Elnabris et al. (2013)
Fish Southern Nigeria 0.10 0.63 1.35 1.30 Oyakhilome et al. (2013)
Fish Benin City, Nigeria – 0.29 0.68 14.05 Daniel et al. (2013)
Fish Red Sea, Egypt 0.12 0.88 0.24 2.42 El-Moselhy et al. (2014)
Fish Mumbai Harbor, India 0.19 0.12 2.46 38.54 Velusamy et al. (2014)
Fish Cracow, Poland 0.002 0.012 – – Kulawik et al. (2016)
Shrimp Southern Red Coast, Saudi Arabia 0.2 0.3 5 24 EI Gendy et al. (2015)
Crab Parangipettai Coast, India – – 61.5 72.5 Lyla and Khan Ajmal (2011)
Crab and shrimp Pulicat Lake, India 0.18 3.28 0.76 0.32 Prabhu Dass Batvari et al. (2012)
Crab Pulicat Lake, India 0.1 0.2 – 2.0 Vasanthi et al. (2014)
Fish and shell fish Thondi, Southeastern India 0.02–0.28 0.1–0.12 0.90–8.68 18.80–55.14 Present study

Prabhu Dass Batvari et al. (2008), who reported 0.6 ppm Pb in Pulicat Cu concentration to be 5.59 ppm in a different marine fish species from
Lake. Sivaperumal et al. (2007) and Kulawik et al. (2016) also reported Mumbai harbour, India. Sankar et al. (2006) reported that Cu concentra-
lower Pb concentrations in Cochin, India (0.07 ppm), and in Cracow, Po- tions in the marine fishes of Calicut, India, ranged between 1.50 and
land (0.012 ppm), respectively. Sankar et al. (2006) reported the heavy 4.50 ppm, and EI Gendy et al. (2015) reported an average Cu concentra-
metal concentrations in Saurida tumbil, Megalaspis cordyla, Sphyraena tion of 5 ppm in shrimps from the Southern Red coast of Saudi Arabia.
jello, Chiloscyllium spp., Johnieops dussumieri, Perna viridis, Pamphia Sivaperumal et al. (2007) reported a comparatively much lower Cu con-
malabaricus, and Sepia sp. Sankar et al. (2006) reported higher Pb con- centration of 1.44 ppm in marine fish from Cochin, India, than the
centration (1.84 ppm) in fish collected from Kolleru Lake in India. 8.68 ppm reported in the present study. Kumar et al. (2011) reported
Prabhu Dass Batvari et al. (2012) reported that the highest concentra- that the lowest Cu concentration of 3.9 ppm in West Bengal, India.
tion of Pb (3.28 ppm) from Pulicat Lake. The JECFA has recommended El-Moselhy et al. (2014) and Uysal et al. (2008) reported low Cu concen-
a PTWI of 0.025 ppm/kg body weight for Pb (Sankar and Ashok trations of 0.24 and 1.03 ppm in the Red Sea in Egypt and the Western
Kumar, 2014). The FAO/WHO (1989) set the maximum permissible Mediterranean Sea, respectively. The Cu residual limits detected in the
limit of Pb as 0.5 ppm for fish species, and the FDA (2001) set 1.5 ppm present study were within the acceptable level of 30 ppm suggested
for crustaceans and cephalopods. In the present study, all the samples by the FAO/WHO (1989). Higher levels of Cu in the liver can cause
except P. pelagicus had lower Pb concentrations than the guideline Wilson's disease, inborn error of metabolism, and hepatolenticular de-
values (FAO/WHO, 1989; FDA, 2001), as shown in Table 3. Turkey and generation; in addition, excessive levels of copper and/or deficiency of
England guideline values for maximum Pb concentrations are 1– zinc is the primary reason for “histapenia” (low blood histamine),
2 ppm. Our results suggest that the Pb concentrations in the tested sam- which is a type of schizophrenia (Passwater and Cranton, 1983).
ples were lower than the guideline values of Turkey and England (Dural Demirezen and Uruc (2006) reported that Zn is an essential element
et al., 2007 and MAFF, 2000). for human health, and it helps in disintegrating the macromolecules in
Demirezen and Uruc (2006) reported that Cu is an essential nutrient the food we eat and assists in healing wounds. Because Zn is a key com-
for human health. Cu helps to produce blood cells, triggers the release of ponent of cells, enzymes, and cofactors, it is one of the most important
iron to form haemoglobin, and strengthening bones; however, con- trace and microelements for the human body. Zinc was found to be
sumption of high amount of Cu might cause health risks. The FAO the most abundant metal in the fish samples of the present study, and
(1983) regulated the maximum permissible limit for Cu as 30 ppm. In a P b 0.05 positive significance of Zn residues was noted between the
the present study, Cu was found in all the tested fish samples, and the muscle tissues of different fish species. The highest concentration of
concentrations varied from 0.90 to 8.68 ppm. The highest concentration Zn was observed in P. pelagicus (55.14 ppm) followed by S. brevimana
of Cu was observed in C. chanos, and the lowest value was found in S. (52.06 ppm) and S. aculeate (42.83 ppm). The lowest level of Zn resi-
indicus. The average Cu concentration in the fish samples of the present dues was observed in U. vittatus (18.80 ppm) and S. indicus
study was 3.95 ppm. However, Velusamy et al. (2014) reported the high (21.48 ppm). The average value of Zn concentration in the muscle tis-
sues of the fish samples examined in the present study was
35.51 ppm. Higher values were observed by Sivaperumal et al. (2007)
Table 6
Correlation coefficients between heavy metals and fish length and weight. (44 ppm) in marine fish samples and Sekar et al. (2003) (41 ppm) in
marine fish species caught from Kolleru Lake. Uysal et al. (2008) and
Cd Pb Cu Zn Weight Length
El-Moselhy et al. (2014) reported the lowest Zn concentrations of
Cd 1 12.28 and 2.42 ppm in the fish samples from the Mediterranean Sea
Pb 0.853⁎⁎ 1
and the Red Sea, respectively. Mitral et al. (2000) and Kumar et al.
Cu 0.549 0.353 1
Zn 0.723⁎ 0.451 0.865⁎⁎ 1 (2011) reported the lowest values of Zn concentration (11.5 and
Weight −0.041 −0.187 −0.026 0.332⁎ 1 19.8 ppm) in the fish samples from West Bengal. Similarly, Prabhu
Length −0.328 −0.192 −0.064 0.068 0.572 1 Dass Batvari et al. (2012) and Vasanthi et al. (2014) reported the lowest
⁎ Correlation was significant at P b 0.05. concentrations of Zn residues (0.33 and 2.0 ppm) in Pulicat Lake. Sekar
⁎⁎ Correlation was significant at P b 0.01. et al. (2003) reported the highest level of Zn (965.3 ppm) in the fish
458 A. Arulkumar et al. / Marine Pollution Bulletin 119 (2017) 454–459

samples from Sundarban Wetlands, India, which was comparatively APHA (American Public Health Association), 1998. Standard Methods for the Examination
of Water and Wastewater. 20th ed. (Washington DC).
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