Ecotoxicology and Environmental Safety 120 (2015) 243–255

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Ecotoxicology and Environmental Safety

journal homepage: www.elsevier.com/locate/ecoenv

Bioaccumulation of metals in fish species from water and sediments in

macrotidal Ennore creek, Chennai, SE coast of India: A metropolitan
city effect
M. Jayaprakash a, R. Senthil Kumar a, L. Giridharan b, S.B. Sujitha c, S.K. Sarkar d,
M.P. Jonathan c,n
a
Department of Applied Geology, University of Madras, Guindy Campus, Chennai 600 025, India
b
Department of Geology & Mining, Government of Tamil Nadu, Guindy, Chennai 600 032, India
c
Centro Interdisciplinario de Investigaciones y Estudios sobre Medio Ambiente y Desarrollo (CIIEMAD), Instituto Politécnico Nacional (IPN), Calle 30 de Junio
de 1520, Barrio la Laguna Ticomán, Del. Gustavo A. Madero, C.P. 07340 Mexico Distrito Federal, Mexico
d
Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta - 700 019, India

art ic l e i nf o a b s t r a c t

Article history: Accumulation of trace metals (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd) were investigated in water, sediment
Received 1 April 2015 (n ¼20) along with six fish of diverse feeding guilds (Sillago sihama, Liza parsia, Etroplus suratensis, Or-
Received in revised form eochromis mossambicus, Arius parkii and Gerres oyena) from the Ennore creek, northern part of Chennai
22 May 2015
metropolitan megacity, southeast coast of India. Dissolved trace metals (DTMs) in surface water samples
Accepted 26 May 2015
Available online 17 June 2015
and total trace metals (TTMs) in surface sediments (top 0–10 cm) indicate that concentration pattern of
metals was higher in the discharge point of the river/channels entering the main creek. The maximum
Keywords: mean values of DTMs exhibited the following decreasing order (expressed in mg/L): Fe (1698)4 Mn
Water (24)4Zn (14.50) 4Pb (13.89) 4Ni (6.73) 4Cu (3.53) 4Co (3.04) 4Cr (2.01) whereas the trend is
Sediments
somewhat different in sediments (mg g  1): Fe (4300) 4Mn (640)4Cr (383) 4Zn (155)4 Cu (102) 4Ni
Fish
(35)4Pb (32) 4Cd (0.51) are mainly due to the industrial complexes right on the banks of the river/
Trace metals
Bioaccumulation channels. Species-specific heterogeneous patterns of tissue metal loads were apparent and the overall
Ennore creek metal enrichment exhibited the following decreasing order (expressed in mg g  1): Cu (7.33)4Fe
SE coast of India (6.53) 4Zn (4.91) 4 Cr (1.67)4Pb (1.33)4Ni (0.44) 4 Mn (0.43) 4Co (0.36) 4 Cd (0.11). This indicates
that metals are absorbed onto the different organs, which is also endorsed by the calculated values of
bioaccumulation factor (BAFs) (avg. muscle 117, gill 126, liver 123, intestine 118) in fishes. The high
calculated biota sediment accumulation factor (BSAF) (0.437) for the species Arius parkii is considered to
be a potential bioindicator in this region. The enrichment of trace metals is also supported by the as-
sociation of metals in water, sediments and different body organs (muscle, gill, liver, intestine) of fish
samples. Comparative studies with other coastal regions indicate considerable enrichment of DTMs &
TTMs in sediments as well as in various organs of fish samples. Holistic spatial, temporal monitoring and
comprehensive regional strategies are required to prevent health risks and ensure nutritional safety
conditions.
& 2015 Elsevier Inc. All rights reserved.

1. Introduction deposition, geological weathering and run-off from adjacent

Over the last three decades, the continental and marine eco-
systems are subjected to excessive metal contamination due to the
progressive industrial growth and increase in population. Metals
sources to the aquatic regions are mostly brought in by industries,
house hold sewages as external inputs and atmospheric
n
Corresponding author. Fax: þ 52 55 57296000.
E-mail address: mpjonathan7@yahoo.com (M.P. Jonathan).
agricultural lands as natural input (Monroy et al., 2014). These
metals pose a high environmental risk due to their long time
persistence in nature and possible bioaccumulation and bio-
magnification (Uysal et al., 2009). Essential metals like manganese
(Mn), zinc (Zn), copper (Cu), iron (Fe) and nickel (Ni) play a major
role in the biological activities of marine organisms, and non-
essential metals like cadmium, lead and arsenic are the most toxic
elements. Even essential metals may be toxic for the biological
activities of organisms above certain concentrations (Merciai et al.,

http://dx.doi.org/10.1016/j.ecoenv.2015.05.042
0147-6513/& 2015 Elsevier Inc. All rights reserved.
244 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
2014). Fishes being an early warning indicator of pollution in the
aquatic systems are considered to be the most standard choice as
test organisms because they are the best understood organism in
the marine regime and its significance to man as a source of
protein (Murtala et al., 2012).
Trace metals in natural waters especially in river and in es-
tuarine region is brought in by various sources, which includes
natural or external input. The metals after entering the aquatic
medium is transformed, transported and often gets precipitated
owing to changing environment in the water arising due to the
various geochemical processes (Gaillardet et al., 2003; Yang et al.,
2014). Many studies have been conducted in various aquatic re-
gions to identify the partitioning, transformation and absorption
of elements onto different organisms (Agah et al., 2009; Ammann,
2002; Wang and Liu, 2003; Zhang et al., 2008). The studies were
made to understand the geochemical process, partitioning of trace
metals and its relation with dissolved/solid phases.
In any developed metropolitan cities different kind of wastes
are introduced into the river system, which has often led to a
significant impact on quality of the aquatic ecosystem and its
metal concentrations especially in sediments (Tessier and Camp-
bell, 1988; Buckley et al., 1995; Li et al., 2000). Metals are accu-
mulated in the sediments due to the discharge from leaded ga-
soline, chemical manufacturing industries, transportation vehicles;
corrosion of underground pipes, coal based thermal power plant
and municipal wastes. In smaller shallow creeks having low en-
ergy conditions the metals are often deposited or adsorbed onto
the finer particles in the estuarine region and it is also re-
mobilized/transferred back to the water column depending upon
the variation in the reducing oxygen deficient conditions (Martin,
2000; Chatterjee et al., 2007).
Metal bioaccumulation in fishes can be used as bioindicators
that can directly distress the fish character/ behavior or can be
transferred to the consumers in the food web structure, including
humans as they occupy a range of trophic levels and they have a
known ability to accumulate the pollutants (Burger, 2006). The
dissolved metal ions from the surrounding waters enter the body
surface of fish through the gills, whereas the particulate metal
fractions in the sediments enter via the alimentary tract. In fishes,
taking up of metals from water, the gills show higher concentra-
tion than other organs, whereas fish accumulating heavy metals
from sediments show elevated metal levels in the gut compared to
gills or other organs (Yang et al., 2007; Jones et al., 2013). The
metal accumulation in fish depends on the physico-chemical
properties of water and the ecological factors. Studies on various
fishes in different environments have addressed that the physio-
logical conditions, trophic position, age, body size, feeding beha-
vior, sex, spawning status of individual species will affect the
bioaccumulation pattern of metals in the same environment
(Farkas et al., 2003). In any aquatic environment, the higher metal
concentrations can often affect the ecological balance of the region
via bioaccumulation in different organisms, food chains and it is
also dependent on the bioavailability (Bryan and Langston, 1992;
Matthiessen and Law, 2002; Duquesne et al., 2006. Previous stu-
dies have been reported focussing on the levels of contamination
in water and sediments (Jayaprakash et al., 2008), hence the pre-
sent study has been undertaken to address an integrated account
of the metal concentration in selective fish species in the context
of both water and sediments from Ennore creek, an industrial and
human impacted water body situated in the northern part of
Chennai metropolis, India. The study is imperative since rapid
industrialization and urbanization have adversely affected the
Ennore coastal regions in SE coast of India.
2. Materials and methods
2.1. Study area
Ennore creek (13°13′54.48″N, 80°19′26.60″E) is located in the
southeast coast of metropolitan Chennai mega city, India. The total
area of the creek is  4 sq. km and is nearly 400 m wide, with an
average depth of 5–7 m. Its channels connect it in to the Pulicat
Lake to the north and to the Kortalaiyar River in the south Araniar
and Kortalaiyar are the two seasonal rivers which transverse En-
nore creek. The creek lies between the highly populous Chennai
megacity and Pulicat Lake which is the second largest brackish
water in India. This region experiences a semi-diurnal tidal activity
at the mouth of the creek experiencing interaction of fresh and
saline waters. The northern part of the creek has two well spelt
industrial developments of North Chennai Thermal Power Plant,
petrochemicals, automobiles (light & heavy), chemicals and the
Ennore Port, whereas the southern arm of the creek consists of the
industries, utilities, suburbs, and residential areas and fishing
hamlets. Buckingham Canal which trends N–S along the coast
serves as an open sewer receiving untreated domestic and in-
dustrial effluents. The chief source of metal input to the water
body is from the discharge of chemicals, leachates, paints, fertili-
zers and other waste products which are directly drained into the
creek region from the surrounding industries (Jayaprakash et al.,
2008). The study area is also surrounded by three industrial belts
namely the Manali, Ennore–Tiruvottiyur and Ambattur–Padi
complexes.
The region also consists of mangroves in the creek arm leading
to Pulicat Lake. Despite the human impacted pollution factors, the
greatest pressure is the closure of the creek mouth due to sand
accretion resulting deficient tidal flow. Economically, the area is
used for shell fishing as large number of oysters is present in the
region. The city's growth rate was 7.77% during 2001–2011 and the
urban population account nearly 8,653,521 according to 2011
census.
2.2. Sample collections and analysis
The collection of water and sediment samples in the study area
is plotted in Fig. 1.
2.2.1. Water
Surface water samples were collected from 20 sites scattered
throughout the study region using Aqua trap water sampler. 2 ml
of conc. HNO3 was added to each sample (1 L) in the field itself
(after filtration) for further analysis. Liquid–liquid extraction
technique of Mentasti et al. (1989) was adopted in the present
study to know the concentration level of dissolved trace metals
(Fe, Mn, Cr, Cu, Co, Ni, Pb, Zn). A 100 ml unfiltered sample was
taken in a separating funnel, which was subsequently mixed with
2 ml of 2% ammonium pyrrolidine dithiocarbamate (APDC). Con-
sequently, they were extracted using 10 ml of iso-butyl methyl
ketone (IBMK) after severe agitation. The extracted aqueous phase
was back extracted using conc. HNO3 and high purity water. The
traces of organic solvents in the solvents in the solutes were
evaporated on a low temperature hot plate and the final solution
was determined using Atomic Absorption Spectrometry (AAS). The
precision of the instrument was checked through the chemical
standards (Merck, Germany) with control blanks yielding a
quantitative value of 100 74.1%. Certified reference material
(SLRS-4) of River water was used to cross-check the precision of
our analytical method and measurement, which was around
711.8% to that of certified values.
Atomic Absorption Spectroscopy (AAS Perkin Elmer AA 700) was
used to measure the concentration level of metals in water
 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
Fig. 1. Study area map and sampling locations in the macro-tidal estuary Ennore creek, Chennai, SE coast of India.
sediments and in fish samples. Suitable chemical standard and
Standard Reference Material (SRMs) were used in all the three
components during the analysis. The recovery levels and the
concentration level were within the acceptable limits.
2.2.2. Sediment
Sediment samples were procured from 20 sites all over the
creek using Van Veen grab sampler. The samples were dried (at
40 °C) and powdered in an agate mortar for the digestion proce-
dures. About 1 g of dried sediment sample was digested with an
acid mixture containing HClO4 þHF þHCl and the residue was
dissolved with concentrated HCl and finally diluted to 25 ml
(Loring and Rantala, 1992). The sample solution was analyzed in
flame AAS to estimate the metal concentrations (Fe, Mn, Cr, Cu, Ni,
Pb and Zn). Likewise, MESS-1a known Standard Reference Material
(SRM) was run after every fifth sample to check the precision of
our analysis and the recovery percentage with reference to the
certified values were between 91.38 and 98.80 7 1.93%.
2.2.3. Fish
Fish samples from the study region were collected from local
fishermen fishing in the creek region alone. Nearly 10 individual
fishes of each species of similar size were collected for greater
representation. The fish species considered for the present study
belong to diverse feeding guilds as follows: Sillago sihama (Silla-
gindae; omnivorous), Liza parsia (Mugilidae; herbivorous), Etroplus
suratensis (Cichlidae; herbivorous),Oreochromis mossambicus (Ci-
chlidae; omnivorous), Arius parkii (Ariidae; herbivorous) and Gerres
oyena (Gerreidae; herbivorous). The samples procured from the
creek were later transferred to laboratory and refrigerated until
further analysis. The organs of the fish were dissected using a
stainless ted scalpel. About 5 ml of HNO3 and H2SO4 were added to
each dissected organ in a digestion tube and was allowed to react.
245
The samples were then digested using a hot block digestion ap-
paratus at a temperature of 60 °C for 30 min. After the sample
cooled down, 10 ml of HNO3 was added and again heated for 120–
150 °C temperature until the solution turned dark in color. 1 ml of
H2O2 was then added to obtain a clear solution for filtration pro-
cess. The filtered samples were analyzed using AAS to estimate the
metal (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn, Cd) concentrations (Agemian
et al., 1980). For precising the analytical results, certified reference
material (CRM-TMF Lot 1204706) for trace metals in fish were
used. The CRMs were injected after every fifth sample to check the
accuracy of the analysis and the experimental procedure. The
overall results of the entire analysis were within 86.52 and
102.17 71.42%.
2.3. Data analyses
2.3.1. Enrichment factor in sediments (EFs)
Generally EF calculation is used to identify the nature of en-
richment in any particular element above uncontaminated back-
ground values. In addition, EF method normalizes the concentra-
tion value of the particular metal with reference to Fe or Al (e.g.
Windom et al., 1989; Ravichandran et al., 1995). Since, Fe is often
present above the natural concentration; Fe was used as the re-
ference value in the present study (Niencheski et al., 1994; Sharma
et al., 1999; Abrahim and Parker, 2008). EF is calculated using the
following formula: EF ¼Mx  Feb/Mb  Fex, where Mx and Fex are
the sediment sample concentrations of trace metal and Fe, while
Mb and Feb are the concentrations in a suitable background [Upper
continental Crust (UCC) values in the present study] as reference
material (Wedepohl et al., 1989).
2.3.2. Bio-accumulation factor (BAF)
Bio-accumulation factor is defined as the ratio of the concentration
246 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
of metal in an organism to that of the concentration of metal in water
during steady state or equilibrium (Opperhuizen, 1991). The uptake of
metals could differ in each organism as they follow a passive diffusion
mechanism analogous to that of oxygen uptake (Van der Oost et al.,
2003). The BAF is calculated using the formula: BAF¼Concentration of
metal in the organism/Concentration of metal in water.
2.3.3. Biota sediment accumulation factor (BSAF)
BSAF are calculated to assess the net bioaccumulation of che-
micals by an organism as a result of uptake from environmental
sources and processes (Burkhard et al., 2005). Efficiency of metal
accumulation in the fish species was evaluated to determine BSAF
using the formula (Thomann et al., 1995): BSAF¼ Concentration of
metal in the organism/Concentration of metal in sediments. As-
sessment of BSAF is a vital factor since the concentration of metals
in such biota is used not only for the ecological risk assessment but
are highly required for the characterization of the biota under
study as well as its consequent human health assessments.
Fig. 2. a–h Dissolved trace metals (DTMs: Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn) from Ennore creek, Chennai, SE coast of India.
2.3.4. Statistical analysis
Correlation analyses data were generated separately for all the
three components (water, sediment, fishes). The correlations of
different elements were calculated using different p values (0.5;
0.1; 0.001) for water, sediments and for different organs in fish
samples. The whole set of statistical analysis was done using Sta-
tistica (version 10).
3. Results
3.1. Dissolved trace metals (DTMs)
Concentration pattern of DTMs (Fe, Mn, Cr, Cu, Ni, Co, Pb, Zn) is
presented in Fig. 2a–h. The concentration pattern of the DTMs in-
dicates an average (expressed in mg/L) of 1698 for Fe, 23.75 for Mn,
2.0 for Cr, 3.5 for Cu, 6.7 for Ni, 3.05 for Co, 13.9 for Pb and 14.5 for Zn
respectively. Based on the average of DTMs the following decreasing
 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
sequential order is observed Fe4Mn4Zn4Pb4Ni4Cu4Co4Cr.
Higher values of DTMs Fe 570–4771; Mn 14.55–51.50; Cu 3.40–5.35;
Ni 6.50–10.40; Co 2.20–7.60; Pb 9.10–26.60; Zn 15.40–36.50] are
observed in the discharging points (Site nos. 1, 2, 9, 11, 18, 20) of
smaller river mouths/channels close to the Pulicat lake. The higher
values of DTMs could be attributed to the activity of Fe dissolution
from reduced oxygen (anoxic) sediments present in the region
(Jayaprakash et al., 2008). In these types of short, small scale oxygen
deficiency zones in estuarine region the behavior of Fe and Mn will
not be similar, where Fe is often found in dissolved form, but Mn
remains in solid phase (Yeats and Strain, 1990; Tappin et al., 1995;
Sokolowski, et al., 2001). The higher values of Cu, Ni, Co, Pb and Zn in
the discharge points of smaller channels also indicate that they are
due to the newly arrived fluvial particles. In addition, the solid Fe
dissolution and oxygen deficiency accompanied by stagnated water
conditions also promote the increase in dissolved concentration
(Chiffoleau et al., 1994; Szefer et al., 1995; Glasby and Szefer, 1998).
Fig. 3. a–h Total trace metals (TTMs: Fe, Mn, Cr, Cu, Ni, Pb, Zn, Cd) in sediments from Ennore creek, Chennai, SE coast of India.
247
3.2. Total trace metals in sediments (TTMs)
Distribution pattern of trace metals (Fe, Mn, Cr, Cu, Ni, Pb, Zn,
Cd) is presented in Fig. 3a–h. The concentration pattern in the
sediments indicates an overall average value of 4.30% for Fe,
640 mg g  1 for Mn, 383 mg g  1 for Cr, 102 mg g  1 for Cu, 35 mg g  1
for Ni, 32 mg g  1 for Pb, 155 mg g  1 for Zn and 0.51 mg g  1 for Cd
respectively. Higher values were observed for most of the metals
Fe (5.40%), Mn (1009 mg g  1), Cr (637 mg g  1), Cu (207 mg g  1)
from station 12 and Fe (5.18%), Mn (812 mg g  1), Cr (429 mg g  1),
Cu (195 mg g  1), Ni (52 mg g  1), Zn (205 mg g  1), Cd (0.80 mg g  1)
in station 5 is observed.
The higher values of TTMs in the surface sediments (in the
discharge point from channels) is primarily attributed to the ex-
ternal source mainly due to manufacturing, chemical, rubber,
paint, tannery and metal based industries located (industrial
complexes) in the region and in the upstream side. In addition,
coagulation, precipitation process which often happens during the
248 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255

mixing of fresh water and salt water in the estuarine regions, Breslin and Sanudo-Wilhelmy, 1999; Leoni and Sartori, 1997).
where it could be the lower pH and dissolved oxygen that occurs Concentration pattern of Pb in sediments especially Pb varied from
due to the low flow condition in the creek region (Horowitz, 1991; 26 to 41 mg g  1 and it also indicates higher values near the

Fig. 4. a–f Concentration of trace metals in six different species and four organs (muscle, gill, liver, intestine) from Ennore creek, Chennai, SE coast of India.
 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
discharge points, which is mainly due to the coal based thermal
power plant situated right on the bank of the creek and the at-
mospheric deposit (Bargagli et al., 1997; Li et al., 2000). Higher
values of Cd is observed in both the sides of the river bank espe-
cially in stations 8–10 (0.72–0.75 mg g  1) and 14–17 (0.58–
0.62 mg g  1). The main anthropogenic source is the municipal
sludge as the creek receives from adjacent metropolitan city
through various canals as well as from the huge industrial com-
plexes very close to the study area.
The higher concentration of trace metals (TTMs) in sediments
would have originated from DTMs since that the metal distribu-
tion is high in the discharge points of smaller rivers and channels,
which brings in the external input (Bradl, 2005). Moreover, in the
low flow conditions as in the case of present study, most of the
metals are precipitated or absorbed onto the finer sediments in
the estuarine region with organic particles and due to the sul-
phidic nature of sediments (Zwolsman et al., 1997; Jiann et al.,
2005).
3.3. Trace metals in fishes
The concentration pattern of metals in muscle, gill, liver, intestine
in the six different species is presented in Fig.4.a–f., viz., Sillago si-
hama (Fig. 4a), Liza parsia (Fig. 4b), Etroplus suratensis (Fig. 4c), Or-
eochromis mossambicus (Fig. 4d), Arius parkii (Fig. 4e) and Gerres
oyena (Fig. 4f). In spite of living in the same ecological conditions, the
six different fish species demonstrated variations in accumulation of
metals which might be attributed to their feeding habits, trophic
levels and the contamination gradients of these sources. The hier-
archy of mean concentration of trace metals analyzed is as follows:
Arius parkii (32.048 mg g  1)4Liza parsia (26.765 mg g  1)4Sillago
sihama (20.81 mg g  1)4Gerres oyena (20.529 mg g  1)4Oreochromis
mossambicus (19.735 mg g  1)4Etroplus suratensis (18.739 mg g  1).
The dissimilarities in the metal levels could be attributed to the ha-
bitat and feeding behavior of each individual species. Majority of the
species thrive in shallow depths feeding on small algae, diatoms,
detritus and organic matter. The species with the highest metal
concentration, Arius parkii thrives in the continental coast entering
estuaries and normally feeds on smaller fishes and shrimps. This
species has the highest possibility to intake contaminants from the
land as well the untreated effluents from the industries. The orders of
the concentration of the metals analyzed in this region are as follows:
Cu4Fe4Zn4Cr4Pb4Ni4Mn4Co4Cd.
The highest concentration of Fe (4.34 mg g  1) was observed in
the gill of Liza parsia, whereas lowest Fe concentration of
0.571 mg g  1 was observed in the intestine of Gerres oyena. The
high average value of total Fe concentration (6.53 mg g  1) reveals
that the region experiences an increased input of organic matter,
anthropogenic metals from industries and domestic sewage dis-
posal (Satheesh-Kumar and Kumar, 2011). Higher levels of Fe were
observed in the intestine (12.18 mg g  1) of all the species, which is
clearly due to the fact of increased feeding rate and metabolic
activity during fish spawning (Filipović-Marijić and Raspor, 2014).
However, in the case of liver (11.084 mg g  1), Fe tends to accu-
mulate in the hepatic tissues owing to the physiological role of the
organ for maintaining the blood cells (Gorur et al., 2012). Nearly all
the species depicted high concentration of Mn in their gills (all
values in mg g  1 0.12, 0.27, 0.12, 0.11, 0.18, 0.14) as these organs are
the chief route for metal ion exchange from water because of their
large surface areas that assist rapid diffusion of toxic elements
(Dhaneesh et al., 2012). Overall concentration pattern of Mn in-
dicates higher values of Mn in the gills of Liza parsia species
(0.267 mg g  1) and the lowest concentration in the muscles
(0.069 mg g  1) of Arius parkii.
Fishes being resistant to chromium content are affected par-
tially when there is increase in concentration due to the external
249
inputs (Krishna et al., 2014). This low toxic, essential trace element
aids in the glucose metabolism. In the present study, the highest
concentration of Cr (0.596 mg g  1) was observed in the gills of Liza
parsia. There were only narrow variations in the Cr levels for all
the species. Cu is an essential metal in the activity of proteins/
enzymes during fish spawning and higher feeding activity (Fili-
pović-Marijić et al., 2014). In the liver, the species Gerres oyena
showed marked potential in accumulating Cu (2.408 mg g  1) due
to specific binding proteins (Papagiannis et al., 2004), while Or-
eochromis mossambicus recorded the lowest concentration of Cu
(1.308 mg g  1) in the intestine. Copper in the dissolved form is
highly toxic to the aquatic organisms than associated with the
particulates and the dissolved ions taken up by the gills are found
to fall within an average concentration of 1.721 mg g  1. Cu being
an important element for the synthesis of hemoglobin can also
lead to toxicity when the intake is high (Velusamy et al., 2014). The
concentration of Ni in the ecosystem is due to the effluents from
metallurgical, chemical and food processing industries, in the case
of Ennore creek the highest concentration of Ni (0.193 mg g  1) was
observed in the gills of Gerres oyena which is inferred as the intake
from the surrounding waters. The concentration of Ni was found
to be high (0.193 mg g  1) in the intestine of G.oyena, species in-
habiting sandy bottom in shallow depths and feeding on small
algae (Eisler, 1998) and is attributed to the high affinity of Ni to
biota particularly with the phytoplanktons. In the case of Co, all
the species showed high concentrations in the gills, which are
mainly due to intake of dissolved ions from the surrounding wa-
ters. The average concentration of Co in the fish species was
0.355 mg g  1 and the lowest concentration of 0.026 mg g  1 was
observed in the liver of Arius parkii and the highest concentration
of Co (0.152 mg g  1) was observed in Gerres oyena. Cobalt, an es-
sential metal for the nitrogen assimilation, erythrocyte maturation
and the diet of fish, could be toxic even present in lesser quantities
(Yaqub and Javed, 2012).
In case of Pb, one third of the species tend to accumulate in the
muscle with a total concentration of 2.05 mg g  1. However, highest
concentration (0.50 mg g  1) of Pb was observed in the gills of
Gerres oyena. In general, Pb is highly toxic element to the fishes
which would also damage all organs if the levels are excessive. In
this study, the average concentration of Pb (1.33 mg g  1) is above
the permissible limit (0.50 mg g  1) set by FAO (1983). Our results
clearly indicate that the region is contaminated to a wider extent
with respect to Pb. Cadmium, which is a non-essential element
with no biological role, is said to be toxic even at low levels. In
general, Cd is assimilated from food more rapidly in fresh water
habitats. Higher levels of Cd are observed in the intestine
(0.03 mg g  1), as Cd has the ability to replace the essential metals.
The maximum concentration (0.143 mg g  1) of Cd was recorded in
Oreochromis mossanbicus which inhabits the water bodies even at
reduced water levels. Higher values of Pb and Cd in muscle and
liver are attributed to the indiscriminate disposal of unused lead
based motor batteries and the coal combustion in thermal power
plant. Other possible sources of Pb and Cd are atmospheric de-
position of aerosols and the industrial effluents in the creek and
upstream region (Marcus et al., 2013).
In most fish species Zn is taken up through the food and in this
study maximum concentration is observed in the intestine
(5.53 mg g  1), gills (3.26 mg g  1) and in the liver (1.97 mg g  1) of
Arius parkii as the species inhabits the continental coast in direct
contact with the effluents. Evidently, there is rapid assimilation of
Zn for its role as an essential element (Dallinger et al., 1987).
The organs demonstrated variation in the accumulation of
metals and they are ordered as: intestine4 gill 4liver4muscle,
which is probably due to their physiological roles in fish meta-
bolism. The elevated metal concentration in gill might be attrib-
uted to (i) presence of mucous layer covering the organ which
250 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255

Table 1
Correlation matrix of water, sediment and trace metals from Ennore creek, Chennai, SE coast of India.

Fe Mn Cr Cu Ni Co Pb Zn Cd

Water (n¼ 20) (p o 0.05*, 0.01 þ , 0.001‡)* þ ‡

Fe 1.00 0.94* þ ‡ – – – – – – –
Mn 1.00 – – – – – – –
Cr 1.00 – – – – – –
Cu 1.00 – – – – –
Ni 1.00 0.71* þ ‡ – – –
Co 1.00 0.75* þ ‡ 0.60 þ –
Pb 1.00 0.67 þ –
Zn 1.00 –
Cd –

Sediment (n ¼20) (p o0.05*, 0.01 þ , 0.001‡)

Fe 1.00 0.68* þ ‡ 0.51* – 0.76* þ ‡ – 0.60* þ 0.50* –
Mn 1.00 0.79* þ ‡ 0.83* þ ‡ 0.59* þ – 0.54* 0.60* þ –
Cr 1.00 0.67* þ 0.62* þ – – 0.54* –
Cu 1.00 0.50* – – 0.56* –
Ni 1.00 – 0.52* 0.55* –
Co – – –
Pb 1.00 0.66* þ –
Zn 1.00 –
Cd 1.00

Fish muscle (n ¼6) (p o 0.05)

Fe 1.00 0.71 0.54 0.62 0.69  0.50 0.79 – –
Mn 1.00 – 0.70 – – 0.57 – –
Cr 1.00 – 0.97  0.64 –  0.66 –
Cu 1.00 – – – 0.64 –
Ni 1.00  0.71 0.50  0.61 0.50
Co 1.00  0.50 0.81  0.66
Pb 1.00 – –
Zn 1.00  0.83
Cd 1.00

Fish gill (n¼ 6) (p o 0.05)

Fe 1.00 0.93 0.65 0.50 –  0.51 – – –
Mn 1.00 0.70 0.50 – – – – –
Cr 1.00 0.49 – – – – –
Cu 1.00 – –  0.50 0.69 –
Ni 1.00 0.70 0.57 – 0.50
Co 1.00 0.67 – 0.80
Pb 1.00 – 0.96
Zn 1.00 –
Cd 1.00

Fish liver (n¼ 6) (po 0.05)

Fe 1.00 0.50 –  0.66 – –  0.50 –  0.53
Mn 1.00 –  0.86 – – –  0.55 –
Cr 1.00 – – – 0.52 – –
Cu 1.00 – – – – –
Ni 1.00 –  0.75 – –
Co 1.00  0.53  0.73 –
Pb 1.00 – 0.72
Zn 1.00  0.50
Cd 1.00

Fish intestine (n¼ 6) (p o 0.05)

Fe 1.00 0.87 – –  0.63 – – 0.50 –
Mn 1.00 – –  0.64 – – 0.50 –
Cr 1.00 –  0.50 – 0.62 0.89 –
Cu 1.00 – 0.60 0.50 0.77 –
Ni 1.00 0.50 –  0.51 –
Co 1.00 – –  0.50
Pb 1.00 0.70 0.71
Zn 1.00 –
Cd 1.00

facilitates rapid accumulation of metals (ii) high volume of water storage part (liver) accumulates the metals (Sidoumou et al.,
filtered than other organs and (iii) close contact with the sur- 2005). The lower accumulation of metals in the muscles is due to
rounding water giving rise to greater and faster accumulation the low fat affinity to adsorb or combine with the heavy metals
(Pringle et al., 1968). The order of organs also suggests that the and the low metabolic activity (Uluturhan and Kucuksezgin, 2007).
 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
In the case of higher value in intestine, metals enter as a compo-
nent of sediment fractions and they represent an important source
of contamination in fish. Among the two main path ways, water
and food the latter always results in a high risk of contamination.
3.4. Correlation matrices
Correlation matrix results for the DTMs in water, TTMs in se-
diments and TMs in different organs of fish (muscle, gill, liver, and
intestine) is presented in Table 1.
Statistically significant relationship between Fe and Mn
(r2 ¼0.94) indicates that during low flow conditions in low depth
regions often Fe/Mn flocculation takes place, which also results in
higher values due to mixing (Turner et al., 1991; James et al., 1993;
Klimkhammer and Bender, 1981). The positive relationship be-
tween Co vs Ni (r2 ¼ 0.71), Pb vs Co (r2 ¼ 0.75), Zn vs Co (r2 ¼0.60),
Pb (r2 ¼0.67) indicates high similarities in the distribution and
their behavior in the creek region mainly due to external inputs.
Association of Fe vs Mn (r2 ¼ 0.68), Cr (r2 ¼0.51), Ni (r2 ¼0.76),
Pb (r2 ¼0.60), Zn (r2 ¼ 0.50) and Mn vs Cr (r2 ¼0.79), Cu (r2 ¼0.83),
Ni (r2 ¼0.59), Pb (r2 ¼0.54), Zn (r2 ¼0.60) in sediments infers that
Fe/Mn acts as metal scavengers in the study area. The association
of the metals also clearly indicates that it is naturally present as
part of the weathering process and also from external source (Wen
and He, 1985; Li et al., 2000). However, the association of Cr vs Cu
(r2 ¼0.67), Ni (r2 ¼ 0.62), Zn (r2 ¼0.54); Cu vs Ni (r2 ¼0.50), Zn
(r2 ¼0.56); Ni vs Pb (r2 ¼0.52), Zn (r2 ¼ 0.55); Pb vs Zn (r2 ¼ 0.66)
suggest that the region experiences considerable amount of ex-
ternal input from coal burning, untreated industrial sewage dis-
posal, direct municipal disposal into the river system (Alloway,
1990; Leoni and Sartori, 1997; Wong et al., 2007). The association
of metals in sediments also indicates that it is a direct reflection of
the anoxic state of the creek region, where Fe/Mn oxides often
adsorb other metals and it is also the result of the external dis-
charges at various points of the river and channels.
Correlation of Fe and Mn with different organs of fish samples
distinctly refers the elemental behavior and its presence in each
organ. Fe is mainly correlated with Mn [r2 ¼ 0.71, 0.93, 0.50, 0.87
(in all organs)], Cr [r2 ¼0.54, 0.65 (in muscle & gill)], Cu [r2 ¼0.62,
0.50 (in muscle & gill)], Ni [r2 ¼0.69 in muscle alone] and Mn with
Cr [r2 ¼0.70 in gill], Cu [r2 ¼0.70, 0.50 (in muscle & gill)], Pb
[r2 ¼0.57 (in muscle)] respectively. The positive correlations of Fe,
Mn with other elements also establish that these two elements are
natural metal scavengers, which adsorb other trace metals along
with them. Positive correlation of Pb vs Ni (r2 ¼0.57), Co (r2 ¼0.67)
in gill; Cr (r2 ¼0.52, 0.62) in liver and intestine; Cu (r2 ¼0.50) in
intestine suggest the presence of higher concentration of surface
water. This is very well supported by the positive correlations of Pb
vs Co and Ni vs Co indicating its availability in water and sediments
in the region, which, in turn, is absorbed directly by the organisms.
Previous studies have also endorsed the present observation that
the heavy metal concentrations in fish are largely affected by the
concentration in water they lived (Lin, 2009; Dsikowitzky et al.,
2013, PuYang et al., 2015). Significant positive correlation of Zn vs
Cu (r2 ¼0.64, 0.69) in muscle, gill; Co (r2 ¼0.81) in gill; Cr
(r2 ¼0.89), Cu (r2 ¼0.77), Pb (r2 ¼0.70) in intestine is also observed.
Likewise, positive relationship is observed in Cd vs Ni (r2 ¼ 0.50) in
muscle, gill; Co (r2 ¼0.80) in gill; Pb (r2 ¼ 0.96, 0.72, 0.71) in gill,
liver and intestine in the fish samples collected from the region.
The similarity in trace metal associations in the gill indicates that it
is the principal tissue for concentrating these metals and also due
to its contact directly with the pollutants in the aquatic medium.
The large surface area of the gill is also a possible reason for the
accumulation of trace metals (Wu et al., 1986; Al-Yakoob et al.,
1994). The changes or possible variations in the association of
metals also depend on the feeding habits and growth period of
251
individual species. The positive relationship also indicates that the
input of dissolved and bioavailable metals is more compared to the
flow condition, which in turn accumulates (or) increases in the
organisms and in sediments in time.
4. Trace metal enrichment/accumulations
4.1. Enrichment factor (EFs)
EFs were interpreted based on Birch, 2003, where EFo1 in-
dicates no enrichment, o3 is minor, 3–5 is moderate, 5–10 is
moderately severe, 10–25 is severe, 25–50 is very severe and4 50
is extremely severe. Based on the calculations the following se-
quential order is seen Mn (10.22) 4 Cd (4.48) 4Cr (3.73) 4Co
(3.32) 4Zn (1.85) 4Pb (1.59) 4Ni 0.65. The element-wise dis-
tribution pattern indicates a variation for Mn and it is termed as
severe; Cd, Cr, Cu is enriched moderately, whereas Zn, Pb and Ni
indicates low enrichment except in some stations especially in the
entry point of river waters. This suggests a direct external input
mainly through industrial, atmospheric deposits and municipal
wastes (González and Brügmann, 1991; Acevedo-Figueroa et al.,
2006). The higher EF values for Mn, Cd, Cr, Cu and Zn are also
attributed to the remobilization and reduced condition in the
aquatic region and its extensive use in metal based industries
(Förstner and Wittmann, 1983; Soto-Jiménez et al., 2003)
4.2. Bioaccumulation factor in fishes (BAFs)
The bioaccumulation factor of metals (Fe, Mn, Cr, Cu, Ni, Co, Pb,
Zn) for individual species is calculated and presented in Fig. 5a–h.
Based on the calculated BAF values, the metals are ranked as fol-
lows: Cu 4Cr4 Zn4 Co 4Pb 4Ni 4Mn 4Fe. It is evident that the
highest bioaccumulation factors (BAFs) of Ni, Pb, Mn, Co, Cr and Fe
were observed in the gills, whereas Cu and Zn were observed in
the liver and intestine respectively. Copper was found to be highly
accumulated in the fish species of the present study and it is at-
tributed to the high amounts of industrial and domestic wastes
from the surrounding regions. Copper (2155) and Cr (1195) with
BAF41000, signifies slow accumulation and their potentiality for
chronic effects and accretion in the food chain of organisms (De-
Forest et al., 2007; Kwok et al., 2014).
4.3. Biota sediment accumulation factor (BSAF)
BSAF is a parameter which describes the accumulation of se-
diment in associated organic compounds or metals into the tissues
of ecological receptors (Alam et al., 2012). Based on the BSAF
calculated average values for the present study, the metals are
ordered as Cd (0.202) 4Cu (0.072) 4Pb (0.042) 4Zn (0.032) 4Ni
(0.013) 4Cr (0.004) 4Mn (0.001) 4Fe (0.0015) respectively. The
higher values of Cd (0.202) signifies faster rate of accumulation in
the species. The mean concentrations of all the metals in fish
species were lower than that of the sediments. According to Dal-
linger (1993), the fish species can be classified based on the BSAF
values which include the macroconcentrator (BSAF 42), micro-
concentrator (1 oBSAFo2) and deconcentrator (BSAF o 1) and
this is revealed that the studied species are deconcentrators
(Dallinger, 1993). According to the BSAF values, the species could
be ordered as Arius parkii 4Oreochromis mossambicus 4Gerres
oyena 4Etroplus suratensis4 Liza parsia 4Sillago sihama. Thus the
species Arius parkii with the highest (0.437) BSAF would be con-
sidered as a potential bio-indicator in the region for the assess-
ment of environmental pollution status. The BAFs and BSAFs tend
to vary depending on the food web structure, the trophic level and
life history of organism (Burkhard, 2003).
252 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255

Fig. 5. a–h Bioaccumulation of trace metals in fish samples from Ennore creek, Chennai, SE coast of India.

4.4. Comparison studies
A comparative account is presented for all the three compo-
nents (water, sediment and fishes) in Table 2.
The distribution pattern and average concentration of DTMs in
water indicate an increase of 25% for Fe and a five-fold increase of
Pb than the stipulated Environmental Protection Agency (EPA)
values. The higher values for Fe in dissolved phase is due to the
remobilization of Fe in low condition in the creek region and Pb
due to the activity of coal based power plant in the region. In se-
diments, Fe (4300 mg g  1), Cr (383 mg g  1) and Pb (32 mg g  1) is
above the stipulated guidelines, Mn is above UCC and LEL values,
Cu of 102 mg g  1 (except PEC, SEL, ERM), Ni value of 35 (35 mg g  1)
is above TEC, LEL and ERL. Zn value of 155 mg g  1 is above UCC,
TEC, LEL, ERL and Cd of 0.51 mg g  1 is above UCC, alone respec-
tively. The above concentration pattern clearly demonstrates that
apart from natural source, considerable amount is available as
bioavailable form, from the external input (anthropogenic source)
which will be automatically absorbed into the organisms present
in the region.
The comparison table for fish samples indicates ten to fifteen
fold increases for Fe, Mn is found in Liza parsia and almost close to
reference values in other samples. Cr concentration indicates two
to six fold increase than the reference values. Cu values in the fish
 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255 253

Table 2
Comparison of concentration pattern of water, sediment and fish data set with that of other toxicological values.

Fe Mn Cr Cu Ni Co Pb Zn Cd References

Water (mg/L)
Present study 1698 23.66 2.01 3.53 6.73 3.04 13.89 14.50 –
EPA1 1000c – 74a – 52a – 2.5b 120a 0.25d EPA (1995a, 1980b, 2014c, 2001d)

Sediment (mg g  1)
Present study 4300 640 383 102 35 – 32 155 0.51
UCC2 3490 52 85 25 44 17 17 71 0.098 Taylor and Mclennan (1985)
TEC3 – – 43.4 31.6 22.7 – 35.8 121 0.99 MacDonald et al. (2000)
PEC4 – – 111 149 48.6 – 128 459 4.98 MacDonald et al. (2000)
LEL5 2000 460 26 16 16 – 31 120 – USEPA (2001)
SEL6 4000 1100 110 110 75 – 250 820 – USEPA (2001)
ERL7 – – 81 34 20.9 – 46.7 150 1.2 Long et al. (1995)
ERM8 – – 370 270 51.6 – 218 410 9.6 Long et al. (1995)

Fish (mg g  1)
Present study
Sillago Sihama 6.69 0.4 1.09 6.99 0.41 0.39 0.97 3.81 0.06
Liza Parsia 11.318 0.575 1.944 7.052 0.468 0.348 1.116 3.86 0.084
Etroplus Suratensis 4.351 0.424 1.499 6.915 0.391 0.316 1.45 3.289 0.104
Oreochromis Mossambicus 5.268 0.355 1.716 6.843 0.417 0.303 1.542 3.148 0.143
Arius Parkii 7.818 0.45 2.037 8.051 0.385 0.324 1.516 11.353 0.114
Gerres Oyena 3.706 0.386 1.746 8.113 0.595 0.449 1.387 4.021 0.126

Permissible limits in fishes

FAO (1983)9 – – – 30 – – 0.5 30 0.5
WHO (1985)10 – 0.5 0.15 3 0.6 – 2 10–75 –
EU (2001)11 0.5 – 1 1 1.5 – – – –
FEPA (2003)12 – 0.5 0.15 1.3 0.5 – 2 75 –
EU (2008) – – 0.5 0.5–1 – – – 30 0.05–0.1

1
Environmental Protection agencya-d.
2
Continental crustal values.
3
Threshold effect concentration.
4
Probable effect concentration.
5
Lowest effect level.
6
Severe effect level.
7
Effects range low.
8
Effects range medium.
9
Food and Agriculture Organization of the United Nations.
10
World Health Organization.
11
European Union.
12
Federal Environmental Protection Agency.

samples from the study area indicate two to five fold increase.
Gerres oyena exhibits higher levels of Ni than the estimated
threshold values set forth by EU and FEPA. Lead concentration
(0.97–1.54 mg g  1) indicates two to three fold increase than the
stipulated FAO values. Zn concentration pattern indicates that it is
within the limit, whereas for Cd concentration it is high only when
compared to the permissible values set by EU. The above increase
in metal intake in fish samples is alarming as it will directly enter
into the human food chain and will affect the human health.
rent organs which is evidenced from enrichment factor (EFs),
bioaccumulation factor (BAF), biota-sediment accumulation factor
(BSAF) values. The accumulation of potentially toxic elements
especially Pb and Cr in the fish tissues (especially in G. oyena)
requires immediate attention for better conservation of this pro-
ductive wetland. The authors strongly recommend for holistic
spatial and temporal monitoring and comprehensive regional
strategies to prevent health risks through dietary intake of fish and
to ensure nutritional safety conditions.

5. Conclusion Acknowledgments

This study fills a gap by providing integrated baseline data of
the enhanced bioavailability of metals in fishes in the context of
abiotic matrices (DTMs in water, TTMs in sediments) from the
Ennore creek region adjacent to the megacity Chennai, SE coast of
India. The negative impact of intensive anthropogenic activities
from the megacity are well-evidenced with the metal enrichment
in the water and sediment samples in the entry points of rivers
(Kortalaiyar and Kosistalaiar) and channels in the creek. Likewise,
the concentration pattern of trace metals in the six different fish
species also specifies the rate of metal accumulation in its diffe-
SBS thanks CONACyT for the research fellowship. MPJ thank the
Sistema Nacional de Investigadores (SNI), CONACyT, México and
EDI, COFAA of IPN, México. This article is the 81st contribution
from Earth System Science Group (ESSG), Chennai, India.
Appendix A. Supporting information
Supplementary data associated with this article can be found in
the online version at http://dx.doi.org/10.1016/j.ecoenv.2015.05.
254 M. Jayaprakash et al. / Ecotoxicology and Environmental Safety 120 (2015) 243–255
042. These data include Google maps of the most important areas
described in this article.
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