Human and Ecological Risk Assessment: An International

Journal

ISSN: 1080-7039 (Print) 1549-7860 (Online) Journal homepage: http://www.tandfonline.com/loi/bher20

Flow of toxic metals in food-web components of

tropical mangrove ecosystem, Southern India

Ganeshkumar Arumugam, Rajaram Rajendran, Vinothkumar Shanmugam,

Rameshkumar Sethu & Mathivanan Krishnamurthi

To cite this article: Ganeshkumar Arumugam, Rajaram Rajendran, Vinothkumar Shanmugam,

Rameshkumar Sethu & Mathivanan Krishnamurthi (2018): Flow of toxic metals in food-web
components of tropical mangrove ecosystem, Southern India, Human and Ecological Risk
Assessment: An International Journal, DOI: 10.1080/10807039.2017.1412819

To link to this article: https://doi.org/10.1080/10807039.2017.1412819

Published online: 18 Jan 2018.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at

http://www.tandfonline.com/action/journalInformation?journalCode=bher20
HUMAN AND ECOLOGICAL RISK ASSESSMENT
https://doi.org/10.1080/10807039.2017.1412819

Flow of toxic metals in food-web components of tropical

mangrove ecosystem, Southern India
Ganeshkumar Arumugama, Rajaram Rajendrana, Vinothkumar Shanmugama,
Rameshkumar Sethua, and Mathivanan Krishnamurthib
a
Department of Marine Science, Bharathidasan University, Tiruchirappalli, Tamil Nadu, India; bSri Paramakalyani
Centre for Excellence in Environment Science, Manonmaniam Sundaranar University, Aalwarkurichi, Tirunelveli

ABSTRACT ARTICLE HISTORY

The concentration of heavy metals in water, sediment, and various Received 4 October 2017
food-web components like plankton, shrimp, bivalve, and fishes were Revised manuscript
collected from Muthupet mangrove ecosystem. Heavy metal accepted 30 November 2017
concentration in water samples was relatively lesser than the biological KEYWORDS
and sediment samples. Among the heavy metals studied, zinc showed heavy metals; food-web
highest concentration ranged from 1.81 to 81.5 mg/kg or mg/L, components;
whereas Cd (0–26.06 mg/kg or mg/L) was found to be lesser in all the bioconcentration factor;
samples except a few organisms viz. Anadara sp. (26.06 mg/kg), Coilia ecological risk assessment;
sp. (10.09 mg/kg), Anguila sp. (9.14 mg/kg), and Tachysurus maculates principal component analysis
(6.95 mg/kg) observed during this study. Pb and Cu were ranged from
10.29 to 14.99 mg/kg and 0.59 to 16.06 mg/kg, respectively. The
reported values of heavy metals were several folds higher than
permissible levels of international regulatory agencies like WHO, FAO,
and USEPA. The order of accumulation of heavy metals in biological
samples are as follows: Pb > Cu > Zn > Cd. All the biota showed a
higher degree of bioconcentration factor for Zn, in the range of 3.90–
34.39. Principal component analysis concluded that Muthupet was
contaminated by lithogenic as well as anthropogenic activities.
Therefore, field observation and sample analysis clearly indicated that
sampling sites were polluted with both point and nonpoint source of
pollution.

Introduction
Mangrove ecosystems are one among the very complex and dynamic ecosystems located in a
tropical and subtropical region of terrestrial, estuarine, and near shore marine environs
(Polidoro et al. 2010) and acted as a buffer zone between land and sea. It is classified as a
unique coastal ecosystem rich in productivity due to the presence of dissolved nutrients such
as nitrate, nitrite, phosphate, ammonia, and silicate and enriched by the various spectrum of
the floral and faunal communities, which facilitates several beneficiary activities including
commercial sale of forest products, protecting shoreline by acting as the barrier and support-
ing coastal fisheries (Kathiresan and Bingham 2001). Mangroves were recognized as the

CONTACT Dr. Rajaram Rajendran, Assistant Professor rajaramdms@bdu.ac.in Department of Marine Science, Bhara-
thidasan University, Tiruchirappalli 620 024, Tamil Nadu, India.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bher.
© 2018 Taylor & Francis Group, LLC
2 G. ARUMUGAM ET AL.

major reservoir for almost all the substances including various pollutants such as industrial,
agricultural, municipal, and domestic wastes. Indian Oceanic region has around
84,984.56 km2 of mangrove forest, it occupies 47% of the world’s mangroves (Kathiresan
and Rajendran 2005). Coastal zone of India, particularly mangroves directly faced various
man-made activities from fishery to fuel wood collection along with some other natural dis-
asters like subsidence, drought, hurricanes, and erosion (Singh et al. 2012). Mangrove eco-
system of Tamil Nadu (Vellar Estuary, Muthupet, Adyar, and Ennore) is under major threat
through aquaculture and agriculture effluents and accumulation of heavy metals (Upadhyay
et al. 2002).
Heavy metal pollution in an aquatic ecosystem is a growing concern since the past few
decades. Normally metals are found on the surface of the land as well as the aquatic origin
by continental and oceanic crust, respectively. Several anthropogenic activities, rapid indus-
trialization, and urbanization (Mathivanan and Rajaram, 2014a) in the coastal region are a
major concern for the elevated level of metals in the adjacent areas of the aquatic region like
the river, lake, pond, etc. (Marrugo-Negrete et al. 2017). Interestingly, heavy metals are non-
biodegradable, toxic, have potency to bioaccumulate, (Suresh et al. 2015) and are persistent
in nature. The trace level of essential metals must be needed for aquatic organisms to the reg-
ulation of various biological processes starting from energy generation to consumption
(Muralisankar et al. 2015, 2014). The level of metal pollution also increased due to expedi-
tious industrialization, enormous usages, and improper disposal of wastes. Pollution of
heavy metals in an aquatic ecosystem is growing at an alarming rate and has become an
important worldwide problem. Pollutants have caused significant undesirable effects on eco-
logical balance directly or indirectly in recent decades (Antoniadis et al. 2017; Biswas et al.
2012).
Toxic metals are the major pollutants of recent decades due to intense usage which causes
severe illness to the precious aquatic ecosystem. As an evidence in Indian aquatic ecosystem
such as Hooghly estuary (Banerjee et al. 2012), Uppanar estuary (Mathivanan and Rajaram
2014), Coleroon River estuary (Anithamary et al. 2012), Gulf of Manner (Jonathan et al.
2004) and Sundarban (Akhand et al. 2012), Pitchavaram (Ranjan et al. 2008) and Muthupet
mangroves (Rajaram et al. 2017), coastal ecosystems of Parangipettai (Sundaramanickam
et al. 2016) have been facing severe ecological imbalance due to several man-made activities.
Also, the developmental activity of coastal aquaculture, agriculture, tourism activities are the
major concern of metal concentration in mangroves ecosystem of India and the world (Bai
et al. 2015, 2011; Rajaram et al. 2017).
There are many reports available (Balakrishnan et al. 2015; Natesan et al. 2014; Priya et al.
2014; Thilagavathi et al. 2011; Ashok kumar et al. 2009; Janaki Raman et al. 2007; Rajaram
et al. 2017) on heavy metal concentration in water and sediment of Muthupet mangrove eco-
system, but no report is available on the concern of heavy metal concentration in the various
food-web components of this particular ecosystem. It is necessary to understand the metal
pollution level in various tropic level organisms to access ecosystem quality. Hence, the pres-
ent study is focused on the mangrove ecosystem of the southeast coast of India, which has
witnessed intense recreational and mechanized boating activities and seasonal idol immer-
sion activities during the past years. In this article, we compared the concentrations of four
toxic metals in different trophic levels (small plankton, zooplankton, and different class of
fishes) across the Muthupet mangroves based the analysis of atomic absorption spectros-
copy. Further, to understand the metal transfer among trophic levels of the marine food-
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 3

web, we measured metal concentration in different food-web components including primary

producers, primary consumers, and secondary consumers containing different groups of
fishes such as herbivore, carnivore, and omnivore. Finally the bioconcentration and biomag-
nification factors were calculated for different tropical levels in order to understand the tro-
phic, transfer potential of an organism. Assessment of potential ecological risk for single and
overall metals in the ecosystem was done to understand ecosystem quality and the risk level.

Methods and materials

Study area
Muthupet mangrove ecosystem (Lat. 10 250 N: Long. 79 390 E) is situated at the southern
most end of the Cauvery delta connected to Palk Strait which opens to Bay of Bengal
(Figure 1). There are some important developmental and socioeconomic activities occur-
ring in the study area such as agriculture, aquaculture, salt pan, fishing, and other recrea-
tional boating. Beside the above action, the ecosystem received plenty of untreated
municipal wastes of solid and liquid form, seasonal immersion idols, aquaculture and
agriculture drainages, dumping of solid wastages in and around the river lines of the eco-
system. Rapid industrialization and urbanization around the ecosystem have been docu-
mented. All the listed actions contain an abundance of heavy metal load and are
discharged into the lagoon. For this study, the samples were collected in 10 different sta-
tions and the geological coordinates of the sampling sites are given in Table 1. All these

Figure 1. Geographical situation of Muthupet mangrove ecosystem.

4 G. ARUMUGAM ET AL.

stations were selected based on different environmental conditions, fresh water input and
sewage, and wastage influence.

Collection and preservation of samples

All the sediment and water samples were collected seasonally post monsoon (January–March),
summer (April–June), pre-monsoon (July–September), and monsoon (October–December)
across the mangrove region for a period of one year from April 2015 to March 2016. In all
the stations, 2 cm depth of sediment samples were collected using the acid cleaned PVC pipes
and stored in zip lock covers for further analysis, 1 L of water samples were collected for metal
analysis. Collected water samples were stored at 4 C and the sediment samples were air dried
at room temperature in the laboratory.
In total, 23 species of fishes, 2 species of bivalves, and 2 species of prawn were seasonally
collected from the study area (108 individuals). Most of the samples were directly collected
through the fishermen. Samples were aseptically transported to the laboratory at the chilled
condition and brought down to 4 C until analysis. Plankton samples were collected every
time at early morning by using different sized plankton net (phytoplankton – 47 mm; zoo-
plankton – 158 mm) with the help of a mechanical boat. During the collection, most of the
larger particles were removed manually and care was taken in order to eliminate the clay
particles, however small amount of fine clay and mud particles were included. The collected
plankton samples were filtered and washed several times with distilled water and divided
into two parts, one was stored in formalin for identification and other stored in HNO3 for
metal analysis. All the biological organisms were identified with the help of standard meth-
odologies following Fishbase, Saa et al. (2000); Tomas (1997); Verlencar and Desai (2004);
Goswami (2004).

Analysis of heavy metals in water and sediment samples

The preserved water samples were filtered through millipore filtration unit (0.45 m). Then
they were transferred into 2 L separating funnel and added to 10 mL of 1% APDC solution
(Ammonium Pyrrolidine Dithio Carbamate). The chelates were extracted by adding MIBK
(Methyl Iso-Butyl Ketone) with vigorous shaking for 15 min. The aqueous phase was
removed and the organic layer was collected separately. The same procedure was repeated to
extract the organic layer. The collected organic layer was extracted with 50% HNO3 and
finally made up into 25 mL with Millipore filtered water (Jonathan et al. 2008).

Table 1. Station name and geographical coordinates of study area.

Name of the stations Latitude Longitude

S1- Azad Nagar 10 23.58.N 79 30.09.E

S2- Jambuvanodai 10 21.90N 79 30.99E
S3- Vavval Thottam 10 20.19.N 79 32.38.E
S4- Kandankurichanar 10 20.46.N 79 33.01.E
S5- Kilaithangi River 10 20.34.N 79 33.47.E
S6- Karpaganadhar Kulam 10 20.16.N 79 35.10.E
S7- Mayil Island 10 19.93N 79 33.23E
S8- Mullipallam creek 10 19.35N 79 32.44E
S9- Sea mouth 10 18.49.N 79 31.17.E
S10- Pamini River end 10 19.12.N 79 29.47.E
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 5

The heavy metal extraction in sediment samples were carried out by the modified
method of Karbassi et al. (2008). Briefly, finely grounded 1 g of sediment samples was
digested with 10 mL of acid mixture HNO3, H2SO4, and HCLO4 in the ratio of 5:2:1 at
60 C in the hot plate. A few drops of hydrochloric acid were added to allow the com-
plete digestion of sample. Finally, the dried and digested samples were made up into
25 mL with Millipore water and filtered using Whatman No.1 paper for analysis of
heavy metals.

Analysis of heavy metals in biological samples

Plankton samples were analyzed according to the methods described by Zhang et al. (2016)
with slight modification. Briefly, powdered 1g of plankton sample was digested with the mix-
ture of HNO3 and H2O2, and finally the suspension was made up into 25 ml with dH2O.
Bivalve samples were collected and transported to laboratory, all the samples were pre-
cleaned with distilled water followed by immersion overnight in tap water to eliminate sedi-
mentary particles from the digestive track (Siriporn Praditv et al. 2006). The muscle was
carefully removed by shelling the bivalves with sterile knife and they were dried at 70 C.
Similarly, fish and shrimp samples were cleaned with dH2O and muscles were separated and
dried at 70 C. All the samples were homogenized to a fine powder in a mortar and pestle
before analysis. 1 g of powdered samples was subjected to acid digestion with a mixture of
HNO3, H2SO4, and HCLO4 in the ratio of 1:2:1 and then filtered, the filtrate was made up
into 25 mL with dH2O (Ayeloja et al. 2014).
The extracted samples were analyzed with the Atomic Absorption Spectrophotometer
(AA7000-Shimadzu Corporation, Japan). The working wavelength for the heavy metals are
213.85 nm for Zn, 324.75 nm for Cu, 228.80 nm for Cd, and 217.00 nm for Pb. Quality
assurance and quality control (Table 2) testing was relied on the control of blanks and yield
for chemical procedure. For acquired quantification, triplicate samples, blanks, and stan-
dardized reference materials were used during analysis. The metal standards were prepared
by (Himedia, Mumbai) analytical grade chemicals with double distilled water in the range of
0.5–3 ppm concentration and were run to check the precision of the instrument throughout
the analysis.

Table 2. Quality control and quality assurance of instrumental methods.

Metal True ppm of standard Concentration detected (ppm) % R, r

0.50 0.59 118

Cd 1.00 1.05 105, 1.00
2.00 1.95 97.5
0.50 0.46 92
Cu 1.00 1.03 103, 0.99
2.00 1.99 99.5
0.50 0.67 134
Pb 1.00 0.99 99, 0.99
2.00 1.82 91
0.50 0.49 98
Zn 1.00 1.12 112, 0.99
2.00 1.95 97.5

%R D recovery percentage, r D linear regression.

6 G. ARUMUGAM ET AL.

Potential ecological risk assessment (PEA)

PEA is a method used to evaluate the ecological risk of heavy metal in an ecosystem with ref-
erence metal concentration in sediment samples of particular ecosystem (Giri and Singh
2017; Shen et al. 2017). Potential ecological risk assessment was calculated according to the
following formulae

C i f D C i s =C i r ;  Ei r D T i f XC i r ;  ERi D ∑ni D 1 Ei r

where Cif D contamination level of heavy metal; Cis: concentration of heavy metal on
sediment; Cir: background concentration of heavy metal during earth crust; Eir: ecologi-
cal risk potential of heavy metal; Tif: toxicity response factor of heavy metal; ERi (risk
index): ecological risk potential of environment. The factor scores on each of the heavy
metals accordingly (Hakanson 1980) were: As (10), Cd (30), Cr (2), Cu (5), Pb (5), Ni
(5), and Zn (1). Then, the criteria for potential ecological risk of heavy metals were
presented in Table 3.

Bioconcentration factor (BCF)

BCF was used to access the potential aquatic environmental hazards identification to deter-
mine adverse effect to the aquatic organism. This criterion is generally applied to various
chemicals including heavy metals. Mainly BCF was calculated between the ratio of metals
absorbed by an organism only through respiratory and dermal surfaces (Arnot and Gobas
2006), as well as the surrounding medium like water. The following formula is employed to
calculate BCF of various elements

BCF D Concentration of metal in organism 6 Concentration in surrounding medium

Biomagnification factor (BMF)

Biomagnification is a process to increase the concentration of hazards chemical in various
tropic level food-webs. It is expressed through BMF, defined as ratio of chemical concentra-
tion of an organism and its diet at steady state. The following formula is used to calculate
BMF of various elements

BMF D concentration of metal in biota = concentration in diet

Biomagnification factors of different tropical food-web components were calculated as

follows (Chen et al. 2000).

Table 3. The general criteria for potential ecological risk of individual heavy metals and the ecosystem.
Eir Ecological risk of individual metals ERi Ecological risk of ecosystem

Eir < 30 Low risk ERi < 100 Low risk

30 < Eir < 50 Moderate risk 100 < ERi < 150 Moderate risk
50 < Eir < 100 Considerable risk 150 < ERi < 200 Considerable risk
100 < Eir < 150 Very High risk 200 < ERi < 300 Very High risk
Eir 150 Disastrous risk ERi > 300 Disastrous risk
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 7

 Producers D [mean metal concentrations of plankton in mg/kg]/[mean metal concen-

tration of sediment mg/kg]
 Primary consumer D [mean metal concentrations of primary consumer in mg/kg]/
[mean metal concentration of Producers in mg/kg]
 Secondary consumer D [mean metal concentrations of Secondary consumer in mg/kg]/
[mean metal concentration of primary consumer in mg/kg]
As mentioned above the bioconcentration factor is also calculated from ratio of metals in the
tissue and the surrounding medium instead of metal concentration in the diet of the
predator.

Statistical approaches
The Pearson Correlation (PC) was conducted to find the interrelationship of metal concen-
tration in various components. One-way ANOVA-parametric test was performed to find
significant variation between various classes of organism and different seasons at 5% signifi-
cant level. The principal component analysis (PCA) was conducted to identify the source of
pollutants in Muthupet mangrove ecosystem (Prasanna et al. 2012) and it is used to reduce
the dimensionality of data set consisting of a large number of inter-related variables. The sta-
tistical methods like PC and ANOVA were performed with Origin 8.0, PCA was performed
by PAST (Ver. 3.0) and SPSS (Ver. 16.0).

Results and discussion

The concentration of heavy metals (Cu, Cd, Pb, and Zn) in food-web components of Muthu-
pet mangrove ecosystem viz. water, sediment (Table 3), mixed phytoplankton and zooplank-
ton, shrimp, bivalve, and different class of fishes (Table 4).

Concentration of heavy metals in water

Dissolved Pb concentration in the surface water ranged between 10.29 and 11.28 mg/L with
an average of 10.92 mg/L, the highest concentration was recorded in station 7. Zn

Table 4. Mean and standard deviation of total heavy metal concentrations in water (mg/L) and sediment
(mg/kg) along with statistical significant level.
Sediment Water

Station Cu Cd Pb Zn Cu Cd Pb Zn

St-1 10.23 § 5.25 0.28 § 0.30 11.52 § 5.68 15.73 § 3.36 1.69 § 0.12 0.49 § 0.63 10.6 § 2.98 1.81 § 2.09
St-2 7.92 § 2.84 0.39 § 0.26 11.55 § 6.95 13.04 § 5.95 1.3 § 0.34 1.01 § 1.67 11.03 § 4.07 2.06 § 2.57
St-3 9.85 § 2.89 0.34 § 0.24 12.41 § 6.75 20.27 § 1.54 1.88 § 0.76 0.28 § 0.27 10.72 § 3.60 2.58 § 3.02
St-4 15.06 § 3.50 0.26 § 0.20 14.79 § 8.18 33.29 § 3.11 1.5 § 0.41 0.17 § 0.14 11.27 § 4.92 3.47 § 4.11
St-5 16.06 § 5.05 0.30 § 0.23 13.82 § 7.57 32.92 § 2.12 2.12 § 1.4 0.24 § 0.23 11.21 § 3.90 4.62 § 6.12
St-6 15.33 § 3.05 0.29 § 0.24 13.85 § 7.31 33.39 § 3.90 1.96 § 1.61 0.9 § 1.63 10.92 § 4.11 2.57 § 3.03
St-7 15.68 § 1.45 0.25 § 0.18 13.29 § 8.13 32.26 § 4.57 2.00 § 1.62 1.03 § 1.79 11.28 § 4.54 3.08 § 3.57
St-8 14.73 § 3.72 0.27 § 0.23 13.59 § 7.64 32.65 § 3.89 0.92 § 0.35 1.02 § 1.69 10.29 § 3.90 2.47 § 2.74
St-9 15.75 § 3.16 0.31 § 0.24 13.86 § 7.47 34.07 § 1.63 1.35 § 0.22 0.77 § 0.84 11.1 § 4.72 4.07 § 4.24
St-10 14.07 § 2.97 0.24 § 0.17 13.57 § 6.99 31.99 § 1.75 1.87 § 1.65 1.03 § 1.68 10.82 § 4.76 2.02 § 2.66
Mean 13.468 0.293 13.225 27.961 1.659 0.694 10.924 2.875
P value 0.016 0.997 0.999 5.34E–11 0.837 0.956 1 0.978

P values indicated the statistical significant level among the different stations.
8 G. ARUMUGAM ET AL.

concentration was ranged from 1.81 to 4.62 mg/L (average 2.87 mg/L) almost similar to all
the stations (Table 4). The concentrations of dissolved Cu ranged from 0.92 to 2.12 mg/L
(average 1.65 mg/L), Cd ranged from 0.17 to 1.03 mg/L at station 7 with an average of
0.69 mg/L. By taking an account of station 7, located in the interior of the lagoon system
there might be a chance for accumulation of all type of contaminants from various river
mouths resulting in higher concentrations of metals (Rajaram et al. 2017). In the present
study no significant different was observed for heavy metals present in different stations
(p > 0.05 for Cu, Cd, Pb, and Zn; Table 4). The water samples of lagoon contain higher con-
centrations of heavy metals which might be due to the influence of land drainage, sewage
and wastes dump, irrigation through channels and municipal wastes as also attribution of
agricultural activities during monsoon and pre-monsoon season (Rajaram et al. 2017; Thila-
gavathi et al. 2011). Primarily the main sources of heavy metals in the lagoon was agricul-
tural drain, the ecosystem contained enormous agricultural land which was mainly used for
paddy cultivation. Nitrogen, phosphorous and potassium (NPK) is the prime factor control-
ling paddy cultivation, recent reports suggested that commercially available NPK fertilizers
have the massive range of heavy metals like Cu, Pb, Cd, Cr, Zn, and Mo (Bhatti et al. 2016).
The atmospheric deposition of Pb is mainly due to anti-fouling paints, combustion of petro-
leum and diesel in boat (Veerasingam et al. 2015; Mathivanan and Rajaram 2014a,b) thermal
plant operation, fly ash along with constant fishing activities (Chatterjee et al. 2007; Stephen-
Pichaimani et al. 2008). Idols immersion is a major anthropogenic activity which suddenly
causes significant water pollution in different water bodies such as lakes, reservoirs, ponds,
rivers, canals, and seas. There are many researchers (Giripunje et al. 2014; Vyas et al. 2007;
Bajpai et al. 2002) who reported that heavy metal concentrations significantly increased after
immersion of idols in certain water bodies in India.

Concentration of heavy metals in sediment

In the present study, the concentration of heavy metals like Cu, Cd, Pb, and Zn was recorded
(Table 4) from the sediment samples. Copper with an average of 13.46 mg/kg, highest at sta-
tion 5 (16.06 mg/kg) and lowest at station 2 (7.92 mg/kg). Zn, with an average of 27.96,
recorded highest at station 9 (34.07 mg/kg) and lowest at station 2 (13.04 mg/kg). Pb with
an average of 13.22, recorded highest at station 4 (14.79 mg/kg) and lowest at station 1
(11.52 mg/kg). Cd, with an average of 0.29 mg/kg, recorded highest at station 2 (0.39 mg/kg)
and lowest at station 10 (0.24 mg/kg). The order of metal concentration in sediment of
Muthupet showed as follows: Zn > Cu > Pb > Cd. Changes in soil texture from sandy to
silt and grain size might be attributed to the metal concentration in coastal ecosystems of
Parangipettai (Sundaramanickam et al. 2016; Abrahim et al. 2007). Toxic metals in the sedi-
ments possess strong relationship with Fe, indicating strong association with Fe as oxyhydr-
oxides and they suggested the sediments of this ecosystem acted as a sink for various metals
(Janaki Raman et al. 2006). The concentrations of metals obtained in this study did not
show any significant differences between different stations for Cd (p > 0.05) and Pb (p >
0.05) but statistical significance was observed for Cu (p < 0.05) and Zn (Table 4). ANOVA
results indicated that the non-essential elemental concentration was almost same for all the
stations because of the extended release of these elements, whereas the concentrations of
essential elements were (Cu and Zn) altered throughout the study area. As sediments
become anoxic in nature, soluble metals are converted into sulphides and other insoluble
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 9

forms because of the depletion of oxygen and rapid decomposition of organic matter (Wal-
dichuk 1985). Primarily, mangrove stem, leaf litters, industrial and associated infrastructure
developmental activities are the potential sources of organic matter in mangrove ecosystem,
where they are incorporated with solid soil particles (Cheung and Wong 2006). In Yellow
river delta, heavy metals were primarily originated by freshwater influx containing dissolved
and sedimentary metal particles (Bai et al. 2015). The study area receives various agricultural
and domestic sewage considered as a serious contaminant, reported higher concentrations of
metals like Pb and Cu due to broad spectrum of boating and other man-made activities
(Rajaram et al. 2017; Thilagavathi et al. 2011).
Abu-Hilal et al. (1987); Laxen et al. (1983) noted high concentration of Pb in an ecosys-
tem by several destined sources like boat exhaust systems, spillage of oil carriers, and other
petroleum from mechanized boats employed for fishing and tourism. However, the dissolved
form of lead can be quickly observed by negatively charged molecules present in the water
body which included organic carbon and litters, clay minerals, carbonates, oxides and
hydroxides of iron (Chakraborty et al. 2014, 2012). In coastal sediments, Pb shows the vari-
able physiochemical form that includes water soluble, exchangeable, association with
hydroxides of Fe and Mn, bounded with organic carbon and carbonates (Chakraborty et al.
2015). Higher concentration of metal in mangrove environment could be the reason that
high silt and clay contents can adsorb metals by fine grained particles (Shriadah 1999;
Ranjan et al. 2008). Thilagavathi et al. (2011); Balakrishan et al. (2015) found the accumula-
tion order of heavy metals in the sediment of Muthupet to be Zn > Pb > Cd and Zn > Cu
> Pb > Cd, respectively. The order of metal concentration in Mai Po Nature Reserve, Hong
Kong is as follows: Zn> Cu> Pb> Cd (Cheung and Wong 2006). The core collected from
the Muthupet area which is closer to aqua farms and dense mangrove forest is the most pol-
luted compared with core samples from river mouth (Natesan et al. 2014). Janaki raman
et al. (2006) offers the historical trends in metals concentration with respect to core size.
Both Cu and Pb shows greater proposition when the depth is increased whereas Cd shows
the decreased trend. An elevated levels of Cu and Pb from the core samples revealed that
both the metals were originated by extended anthropogenic activities for several decades.
Nevertheless, Southeast coast of India was rich in Charnockites and intermediate granites
having an average level of Pb (16.00 mg/kg) in coastal associated sedimentary particles
(Chattopadhyay and Sarkar 1999). Also, in Tamil Nadu region several authors reported the
concentration of lead ranged from 0.1 to 130 mg/kg based on the geographical distribution,
natural weathering process, and local anthropogenic activities.

Concentration of heavy metals in primary producers

The collected plankton samples consisted of 18 families of phytoplankton including Biddul-
phiaceae, Coscinodiscaceae, Triceratiaceae, Naviculaceae, Ceratiaceae and the most abun-
dant phytoplanktonic species are Coscinodiscus excentricus, Triceracium favus, Ceratium
tripos, and Oscilattoria sp. from which a simple food-web was constructed (Figure 2). In the
mixed sample of phytoplankton, Pb reached the highest concentration (10.31 mg/kg), fol-
lowed by Zn (9.24 mg/kg), Cu (4.21 mg/kg), and Cd (0 mg/kg) (Table 5). One-way ANOVA
revealed that mean metal concentrations in primary producers significantly differ at 5%
significant level (F D 5.02, p D 0.017). Heavy metals are being combined with planktonic
cells either by biphasic mechanism or binding on the surface of the organism with various
10 G. ARUMUGAM ET AL.

Figure 2. Diagrammatic representation of Muthupet mangrove ecosystem food web.

types of interaction like ion-exchange and electrostatic interaction (Crist et al. 1992). Metal
concentration in plankton depends on various factors such as physicochemical properties,
species composition of phytoplankton and zooplankton, season and capability of absorbance
(Radwan et al. 1990; Elmaci et al. 2007).

Primary consumer
Heavy metal concentrations of primary consumer were shown (Table 5), which includes
mixed zooplankton (Copepods, Tintinnida, Chaetognatha, and Meroplankton), two species
of Crustacean and two species of bivalve. Copepodes are the dominated group of the study
area and it consists of Acartia danae, Acartia erythriaea, Acartia spinicauda, and Acrocala-
nus gracilis. The Zn concentrations in these classes were significantly higher (68 mg/kg) in
Penaeus indicus than the concentrations of Cd (26.06 mg/kg) Anadara sp, Pb (13.15 mg/kg)
in Meretrix meretrix, and Cu (10.51) in zooplankton. Bivalves are filter-feeders, the metal
contamination of the highly productive mudflats leads to over accumulation in their whole
body tissue (Hossen et al. 2014). ANOVA results showed that significant differences were
found between the groups of organisms at 5% significant level (F D 11.35, p < 0.05). Zoo-
plankton has two ways to accumulate metals adsorption onto their body surfaces from the
external environment and also from the water passing over their gills, and assimilation of
metals from food particles ingested by the animals provides the other pathway for uptake.
They eliminated the metal via fecal matter from both solid and liquid form or by laying
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 11

Table 5. Mean and standard deviation of total heavy metal concentrations (mg/kg) in biological samples.
Group/Species N Cu Cd Pb Zn

Primary producers
Phytoplankton 4 4.21 § 2.70 ND 10.31 § 1.08 9.24 § 8.00
Primary consumers
Zooplankton 4 10.51 § 8.17 ND 10.65 § 0.97 25.92 § 17.06
Penaeus monodon 4 6.73 § 2.38 0.29 § 0.14 12.67 § 4.82 61.52 § 19.68
Penaeus indicus 4 5.93 § 4.81 0.49 § 0.65 12.78 § 5.42 68.35 § 25.51
Anadara sp. 4 6.42 § 3.48 26.06 § 10.29 12.64 § 4.82 64.52 § 37.33
Meretrix meretrix 4 8.69 § 3.56 4.21 § 7.33 13.15 § 4.97 60.58 § 15.90
Secondary consumer herbivore
Liza sp 4 0.72 § 0.19 0.23 § 0.17 13.46 § 5.71 47.91 § 17.79
Hemiramphus archipelagicus 4 0.73 § 0.12 0.27 § 0.24 12.02 § 4.12 38.87 § 27.68
Etroplus suratensis. 4 1.14 § 0.71 0.21 § 0.17 13.72 § 3.63 62.1 § 26.97
Carnivore
Tachysurus maculatus 4 0.84 § 0.33 6.95 § 12.81 14.99 § 7.23 46.66 § 10.49
Anguila sp. 4 0.59 § 0.22 9.14 § 16.23 11.76 § 3.97 40.2 § 21.09
Thryssa sp. 4 1.03 § 0.62 0.29 § 0.22 12.61 § 4.56 81.5 § 19.40
Coilia sp 4 0.84 § 0.51 10.09 § 19.35 13.04 § 5.05 67.54 § 13.29
Ilisha sp 4 0.66 § 0.19 0.23 § 0.19 13.58 § 4.48 49.18 § 23.23
Pseudorhombus sp. 4 1.41 § 0.90 ND 3.99 § 0.21 44.62 § 18.20
Cynoglossus puncticeps 4 0.61 § 0.31 0.05 § 0.01 1.72 § 0.54 44.47 § 17.06
Cynoglossus abbreviatus 4 0.52 § 0.29 0.02 § 0.01 12.95 § 5.20 31.07 § 8.20
Gerres sp. 4 0.67 § 0.45 ND 13.86 § 4.12 54.52 § 7.93
Gerres macracathus 4 0.64 § 0.39 0.14 § 0.07 20.89 § 3.62 50.56 § 10.27
Eleutheronema tetradactylum 4 0.44 § 0.22 0.19 § 0.21 13.29 § 7.23 42.29 § 8.65
Elops machnata 4 0.41 § 0.80 0.17 § 0.02 13.86 § 5.05 38.16 § 12.45
Plotosus canius 4 0.92 § 0.12 0.14 § 0.10 13.97 § 4.23 61.14 § 7.89
Brachirus sp. 4 0.71 § 0.19 0.34 § 0.29 15.33 § 9.17 81.10 § 20.23
Strongylura strongylura 4 0.52 § 0.59 0.48 § 0.13 12.61 § 2.13 72.45 § 13.29
Plectorhinchus sp. 4 0.95 § 0.66 0.26 § 0.10 19.19 § 4.42 36.47 § 15.90
Setipinna paxtoni 4 0.93 § 0.23 0.38 § 0.29 22.03 § 9.21 42.55 § 7.92
Cynoglossus sp. 4 0.84 § 0.26 0.29 § 0.02 16.70 § 5.67 47.04 § 19.68
Lutjanus sp. 4 0.63 § 39 0.34§0.20 14.54 § 1.08 50.96 § 21.09
Omnivore
Awaous banana 4 0.95 § 0.58 0.26 § 0.16 14.45 § 5.74 57.41 § 7.92

ND D Not Detectable, N D No. of specimen/samples.

eggs, the concentration of metal is directly linked with intake, storage, and out elimination
fluxes (Melchor GonzAlez-Dkila 1995).

Secondary consumer
Fish samples were collected from entire Muthupet mangrove ecosystem, a total of 23 species
(each has minimum four numbers) of fishes which included three different classes such as
Herbivore, Carnivore, and Omnivore. Exposure of metal to fish happened by two ways, pri-
marily absorption via gills or transported by biological membrane, likewise intake by food or
any other sedimentary organic matter (Newarman 1998; Burger et al. 2002). The results of
the heavy metals in different fish species are also presented in Table 4.

Herbivore
Generally, high concentration of Zn was found in all fish tissues. Maximum concentration of
Zn was observed in Etroplus suratensis (62.1 § 26.97 mg/kg) and minimum level was
observed in Tenualosa sp. (37.73 § 10.10 mg/kg). Cu, Cd, and Pb ranged from 0.36 to 1.14,
12 G. ARUMUGAM ET AL.

0.19 to 0.27, and 12.02 to 13.72 mg/kg, respectively. One-way ANOVA result showed signifi-
cant differences between the concentration of metals in the tissues (F D 59.71, p < 0.000).
The concentration of metal showed the following order Zn > Pb > Cu > Cd.

Carnivore fish
Cu, Cd, Pb, and Zn levels were found to be higher than the permissible level of biological
samples (Table 5). Concentration of Zn seems higher than other metals present in Thryssa
sp (81.50 mg/kg), followed by Pb (Setipinna paxtoni; 22.03 mg/kg), Cd (Coilia sp; 10.09 mg/
kg), and Cu (Etroplus suratensis; 1.14 mg/kg). The metal contents ranges in different classes
of fishes are as follows: Cu 0.41–1.42, Cd 0.01–10.09, Pb 1.72–22.03, and Zn 31.07–
81.50 mg/kg. Significant differences found between concentration of metals in the tissues
were shown (F D 176.68, p < 0.000) at 5% significant level. The above results showed higher
concentration of metals in the fish tissue due to the feeding habit of these classes compared
with any other external sources.

Omnivore fish
Awaous banana is an only omnivore fish found in this study area. The metals (Cu, Cd,
Pb, and Zn) concentration in the tissue ranged as 0.95–57 mg/kg, and the order of
metals is as follows: Zn > Pb > Cu > Cd. The mean concentration of Cd and Pb in
Awaous banana tissue (0.26 mg/kg; 14.45 mg/kg) was above the critical limit values of
the Food and Agriculture Organization (FAO). Higher concentration of Pb is typically
coupled with both lithogenic and anthropogenic activities. As lithogenic source, average
concentration of Pb in different type of soil was around 0.2–115 by various processes
like sea salt spray, natural fires, vegetation, pollen, and spores (Richardson et al. 2001;
Nriagu 1989) and as anthropogenic activities like fuel additives, dumping of plastic
waste, and boatyard activities (Pacyna and Pacyna 2001). The ANOVA results indicated
that concentration of metals in omnivore fish significantly varied at 5% between the
groups (F D 120.50, p < 0.000).
The concentration of Zn in the biological samples showed relatively higher than any
other metals found in the tissue. Zn and Cu are essential elements which play an
important role in fish physiology to maintain the activity of enzymes or metallo pro-
teins (Kalay and Canli 2000) Cu is an essential nutrient to regulate the body metabo-
lism at trace level, even lower concentration leads to various metabolic and
developmental abnormalities. Although higher level may cause lethal effects on respira-
tion, osmoregulation, behavior, metabolic and growth alteration, and sometimes leads
to death (Burger et al. 2002). Lead is a neurotoxin that causes rapid behavioral mal-
function, decreases the growth, metabolism, and survival rate, alteration of social
behavior in some mammals (Eisler 1988).The main source of Zn in the study area is
galvanizing and paint manufacturing discharge, roofing wastages. Cu is mainly obtained
by antifouling paint containing trawlers and boats, algaecides used in various aqua cul-
ture and agricultural practices.
Raja et al. (2009) found that different fishes collected from Parangipettai mangrove
ecosystem consisted of Cu (0.12–0.31), Zn (14.1–33.5), Cd (0.18–0.54) mg/kg of dry
weight in muscle and the results were lower than the present study. All the metals in
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 13

Muthupet ecosystem exhibits several fold higher than other studies in the various
aquatic ecosystem in the world viz. Mediterranean Sea (Kalay and Canli 1999), Black
Sea (Topcuoglu et al. 2002), Mumbai, India (Mishra et al. 2007), and Kolkata, India
(Kumar et al. 2011).
PEA is used to determine the ecological risk level of heavy metals in the surface sediments
of Muthupet mangrove ecosystem. The results of PEA as shown in Figures 3a, b, are based
on the analysis that the order of PEA for individual heavy metal is Cd > Pb > Cu > Zn.
Similar results were observed by Shen et al. (2017) at smelters in Feng County, China due to
smelter activities causing elevated level of heavy metals. Risk level of Cd is much higher than
other metals followed by Pb and it confirmed that the ecosystem has struggled with enor-
mous anthropogenic activities. Even though, the experimental values show comparably
lesser concentration of Cd but the risk to the aquatic environment is much higher than the
experimental values. ERi values are between 80 and 125 that show the ecosystem has a mod-
erate risk by heavy metals.

Bioconcentration factor
The organism which has BCF value >1 is considered as potent bioaccumulator of
heavy metals, but when the BCF values exceeded 100 or more, that was harmful to the
organism. Highest BCF for Cd was found in bivalve (Anadara sp. 37.77), followed by
Carnivore fish (Coilia sp. 14.62). BCF of Zn showed the higher degree of variations
including all classes of animals listed (Figure 4) the maximum in Carnivore fish
(Thryssa sp. 34.39) and minimum in phytoplankton 3.90. Zooplankton the primary
consumer has the ability to accumulate the metal by following the order Cu > Zn >
Pb > Cd. Copepods are the dominant zooplanktons in Muthupet and it plays an
important role in marine food-web. Because of the versatile level of accumulation
behavior they can be acted as bio-indicators in Lagoon of Venice (Bianchi et al. 2003).

Figure 3a. Distribution of potential ecological risk of individual metals.

14 G. ARUMUGAM ET AL.

Figure 3b. Distribution of potential ecological risk of overall metals to the ecosystem.

Bioconcentration of heavy metals in fishes is regulated by several exogenous and endog-

enous factors like feeding behavior, ambient temperature, water hardness, pH, salinity,
age, sex, and metal interactions, etc. (Moiseenko and Kudryavtseva 2001; Hakanson
1980).

Figure 4. Detailed bioconcentration factor (BCF) for various organisms.

 HUMAN AND ECOLOGICAL RISK ASSESSMENT 15

Table 6. Biomagnification Factor (BMF) for various classes of organisms.

Class Cu Cd Pb Zn

Producers 2.55 0 0.94 3.89

Primary consumers 1.81 0 1.19 6.07
Secondary consumer
Herbivour 0.17 0.00 1.27 5.04
Carnivour 0.16 0.43 1.08 0.99
Omnivour 0.95 1.22 1.08 1.14

Biomagnification factor
The results of BMF for different classes of organisms in Muthupet mangrove ecosystem
are in Table 6. Awaous banana is positioned in the higher trophic level of this ecosys-
tem. The BMF values between 0 (Cd) and 6.07 (Zn), order of BMF in all the organisms
is as follows: Primary consumer > Herbivore fish > Primary producers > Omnivore
fishes > Carnivore fishes. Comparison of all the BMF values showed that Primary con-
sumer reaches the higher level of metal magnification. But there is no evidence for
magnification at any tropical level of metals (Table 6), interestingly Cd showed the
gradual increasing trend in the tropical level. Based on the metal concentration, the
strong positive correlation was found between Primary Consumers and Producers, Her-
bivore and Primary Consumers, Omnivore and Primary Consumers at statistically sig-
nificant level. Correlation results clearly indicated that BMF values of higher trophic
organisms depend on the values of primary consumers, but originally most of the met-
als consumed via prey of primary consumers instead of water and sediment. Zooplank-
ton, Crustaceans, and different species of bivalves have the ability to accumulate
different kind and level of metals (Villar et al. 1999; Jeng et al. 2000).Studies from Pearl
River estuary by Yanyi Zeng et al. (2013) found that mollusc-crab community and ben-
thic community organisms showed higher BMF value for Cu and Pb which denoted
that Cu has more tendency to biomagnifications than any other metal and some of the
environmental parameters regulate bioavailability of metals in the benthic community.

Principal component analysis

The results of PCA for heavy metal contents in various species are presented in Table 7.
Based on the correlation co-efficiency, four different PCs (Principal Components) were
generated, namely PC1, PC2, PC3 and PC4. PC1 and PC2 possess the Eigen value >1,
so these alone were taken for further consideration and they have cumulative variance

Table 7. Matrix rotation for all principal components (PC1, PC2, PC3, and PC4).
Metals PC1 PC2 PC3 PC4

Cu ¡0.52209 0.47061 0.50738 0.49852

Cd 0.10084 0.78684 ¡0.028469 ¡0.6082
Pb 0.56366 ¡0.12871 0.80834 ¡0.11089
Zn 0.63209 0.37795 ¡0.29722 0.60768
Eigen value 1.277 1.202 0.866 0.653
% of variance 31.92 30.06 21.66 16.34
Cumulative 31.93% 61.99% 83.65% 100.00%
16 G. ARUMUGAM ET AL.

Figure 5. Biplot of different metals in aquatic organisms defined by PC1 and PC2.

of 61.99% (Rajaram et al. 2017; Mathivanan and Rajaram 2014). PC1 has the strong
correlation with Zn followed by Pb, the results summarized higher concentration of Pb
in the ecosystem because of extended anthropogenic activities instead of the lithogenic
source (Figure 5). It includes automobile emissions, paint preparations, fertilizers and
pesticides, lead-acid batteries, or other industrial products and Zn is associated with
specific agronomic practices. Although, background values of Zn in an ecosystem is
higher than the experimental value suggested that elevated level of Zn is not related to
the anthropogenic activity. The obtained results showed the PC1 is strongly influenced
by both anthropogenic and lithogenic activities. As a result of PC2, Cd has higher load-
ing points with the variance of 30% and metal in the ecosystem may be related to man-
made activities such as dumping of municipal wastages, direct influence of plating and
galvanizing product wastages, and mechanical tools (Dinesh et al. 2014; Ramesh et al.
2008). Cadmium in salt water is lesser toxic to aquatic organisms compared with
fresher water, because the ions like chloride and others may combine with Cd and
make them as lesser availability (Bradl 2005; Wright and Welbourn 2002).

Table 8. Comparison of permissible level of heavy metals in various components of international agencies
(mg/L water; mg/kg sediment, and biological samples) for various components with the present study.
Component International agencies Cu Cd Pb Zn Reference

Water Aquatic life 0.007 0.002 0.01 0.086 Nazeer et al. (2014)
USEPA aquatic life protection 0.004 0.005 0.014 3.6 Nazeer et al. (2014)
WHO 2 0.003 0.01 3 Nazeer et al. (2014)

Present study 0.92–2.12 0.17–1.03 10.29–11.28 1.81–4.62

Sediment CEQG 2001 18.7 0.7 30.2 124 CEQG (2001)

Present study 7.92–16.06 0.24–0.39 11.52–14.79 13.04–34.07

Fish FAO (1983) 30 0.05 0.5 30 FAO (1983)
WHO (1989) 30 1 2 100 WHO (1989)
Present study 0.35–1.42 0.01–10.09 1.72–22.03 31.07–81.50

USEPA D United States Environmental Protection Agency; WHO D World Health Organization; FAO D Food and Agriculture
Organization; CEQG D Canadian Environmental Quality Guidelines.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 17

The essential metals Cu and Zn were higher in water and it reaches above the permissible
limits for USEPA aquatic life protection and WHO, whereas in sediment it was under the
permissible limits of Canadian Environmental Quality Guidelines (CEQG) and in the bio-
logical organism like fish and prawn it was under the limit for human consumption accord-
ing to FAO and WHO (Table 8). While, the non-essential metal Pb and Cd showed several
fold higher than the recommended level of USEPA aquatic life protection and WHO in
water, it is likely that these metals exceeded the concentration in fish and prawn recom-
mended by FAO and WHO for human consumption. Surprisingly, both the metals in sedi-
ment showed under the controlled limit of CEQG recommended limit.

Conclusion
The present study concluded that most of the sediment and biological samples from Muthu-
pet have a relatively higher concentration of heavy metals compared with water and
exceeded the permissible level of international regulatory agencies. Results indicated that Pb
was highly accumulated in the ecosystem in terms of concentration compared with other
metals. Also, influences of metal load through various anthropogenic activities were noted.
Field observation described that Muthupet lagoon receives the massive amount of untreated
aqua culture wastage, a large number of boating activities, and seasonal immersion of idols
as also dumping of municipal wastage around the river line. Hakanson’s PEA recommended
that the ecosystem has moderate risk due to the elevated levels of heavy metals remarkably,
Cd has high risk toward the ecosystem quality. BCF calculation suggested that organisms
from the ecosystem have much more capability to accumulate various toxic and non-toxic
elements from the surrounding medium. This study provided an excellent baseline for eco-
system monitoring and health assessment. Continuous monitoring and regulatory actions
are needed to protect the environment from the various contaminants.

Acknowledgment
All the authors are thankful to the authorities of Bharathidasan University for providing the necessary
facilities to conduct this study.

Funding
The authors are thankful to the Ministry of Earth Science, Government of India (Ref. No.: MoES/36/
OOIS/Extra./9/2013) for providing financial assistance.

References
Abrahim GMS, Parker RJ, and Nichol SL. 2007. Distribution and assessment of sediment toxicity in
Tamaki Estuary, Auckland, New Zealand. Environ Geol 52:1315–23.
Abu Hilal AH. 1987. Distribution of trace elements in near shore surface sediments from the Jordan
Gulf of Agaba (Red Sea). Mar Pollut Bull 18:190–3.
Akhand A, Chanda A, Dutta S, et al. 2012. Comparative study of heavy metals in selected mangroves
of Sundarban ecosystem. Indian J Environ Bio 33:1045–9.
18 G. ARUMUGAM ET AL.

Anithamary I, Ramkumar T, and Venkatramanan S. 2012. Distribution and accumulation of metals in

the surface sediments of Coleroon River Estuary, East Coast of India. Bull Environ Contam Toxicol
88:413–17.
Antoniadis V, Shaheen SM, Boersch J, et al. 2017. Bioavailability and risk assessment of potentially
toxic elements in garden edible vegetables and soils around a highly contaminated former mining
area in Germany. J Environ Manage 186:192–200.
Arnot JA, and Gobas F. 2006. A review of bioconcentration factor (BCF) and bioaccumulation factor
(BAF) assessments for organic chemicals in fish. Environ Rev 14:257–97.
Ashok Kumar S, Rajaram G, Manivasagan P, et al. 2011. Studies on hydrographical parameters,
nutrients and microbial populations of Mullipallam creek in Muthupettai mangroves (southeast
coast of India). Res J Microbiol 6:71–86.
Ayeloja AA, George FOA, Shorinmade AY, et al. 2014. Heavy metal concentration in selected fish spe-
cies from Eleyele reservoir Ibadan, Oyo State, Southwestern Nigeria. AJEST 8:422–7.
Bai J, Xiao R, Cui B, et al. 2011. Assessment of heavy metal pollution in wetland soils from the young
and old reclaimed regions in the Pearl River Estuary, South China. Environ Pollut 159(3):817–24.
Bai J, Zhao Q, Lu Q, et al. 2015. Effects of freshwater input on trace element pollution in salt marsh
soils of a typical coastal estuary, China. J Hydrol 520:186–92.
Bajpai A, Pani S, Jain RK, et al. 2002. Heavy metal contamination through idol immersion in a tropical
lake. Ecol Environ Conserv 8:157–9.
Balakrishnan T, Sundaramanickam A, Shekha S, et al. 2015. Distribution and seasonal variation of
heavy metals in sediments of Muthupet lagoon, southeast coast of India. J Ecol Eng 16:49–60.
Banerjee K, Senthilkumar B, Purvaja R, et al. 2012 Sedimentation and trace metal distribution in
selected locations of Sundarbans mangroves and Hooghly estuary, northeast coast of India. Envi-
ron Geochem Health 34:27–42.
Bastami KD, Bagheri H, and Kheirabadi V. 2014. Distribution and ecological risk assessment of heavy
metals in surface sediments along southeast coast of the Caspian Sea. Mar Pollut Bull 81:262–7.
Batley GE, and Brockbank CI. 1990. Impact of Ocean Disposal of Dredged Sediments from the RTA
Glebe Island Bridge Site-A Coastal Sediment Survey. CSIRO Report. Center for Advanced Analyti-
cal Chemistry–Division of Coal and Energy Technology, Report FT/IR 050.
Bhatti SS, Sambyal V, and Nagpal AK. 2016. Heavy metals bioaccumulation in Berseem (Trifolium
alexandrinum) cultivated in areas under intensive agriculture, Punjab, India. Springer Plus 5:173.
Bianchi F, Acri F, Bernardi Aubry A, et al. 2003. Can plankton communities be considered as bio-indi-
cators of water quality in the lagoon of Venice? Mar Pollut Bull 46:964–71.
Bradl H. 2005. Heavy Metals in the Environment: Origin, Interaction and Remediation. Elsevier/Aca-
demic Press, London.
Burger J, Gaines KF, Boring CS, et al. 2002. Metal levels in fish from the Savannah River: Potential
hazards to fish and other receptors. Environ Res 89:85–97.
CEQG. 2001. Canadian Environmental Quality Guidelines Canadian Council of Ministers of the Envi-
ronment, 1999, updated 2001.
Chakraborty P, Babu PVR, and Sarma VV. 2012. A study of lead and cadmium speciation in some
estuarine and coastal sediments. Chem Geol 294:217–25.
Chakraborty P, Sarkar A, Vudamala K, et al. 2014. Organic matter—a key factor in controlling mer-
cury distribution in estuarine sediment. Mar Chem 173:302–9.
Chakraborty S, Chakraborty P, and Nagender Nath B. 2015. Lead distribution in coastal and estuarine
sediments around India. Mar Poll Bull 97:36–46.
Chatterjee M, Silva Filho EV, Sarkar SK, et al. 2007. Distribution and possible source of trace elements
in the sediment cores of a tropical macrotidal estuary and their ecotoxicological significance. Envi-
ron Int 33:346–56.
Cheung KC, and Wong MH. 2006. Risk assessment of heavy metal contamination in shrimp farming
in Mai Po Nature Reserve, Hong Kong. Environ Geochem Hlth 28:27–36.
Crist RH, Oberholser K, McGarrity J, et al. 1992. Interaction of metals and protons with algae. 3.
Marine algae, with emphasis on lead and aluminium. Environ Sci Tech 26:496–502.
Dhinesh P, Rajaram R, Mathivanan K, et al. 2014. Heavy metal concentration in water and sediment
samples of highly polluted Cuddalore coast, Southeastern India. IJCR 6:8692–700.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 19

Eisler R. 1988.Lead Hazards to Fish, Wildlife, and Invertebrates: A Synoptic Review. U. S. Fish and
Wildlife Service Rep. 85 (1.14), Washington, DC, pp 134.
Elmac A, Teksoy A, Olcay Topac F, et al. 2007. Assessment of heavy metals in Lake Uluabat, Turkey.
Afr. J. Biotech 6:2236–44.
FAO (Food and Agriculture Organization). 1983. Compilation of Legal Limits for Hazardous Substan-
ces in Fish and Fishery Products. FAO Fishery Circular No. 464. Food and Agriculture Organiza-
tion, pp 5–100.
Giripunje MD, Fulke AB, and Meshram PU. 2014. Effect of idol immersion on water quality and Tila-
pia fish in Futala, Gandhisagar and Ambazari lakes of Nagpur, India. Springer Plus 3:669.
Goswami SC. 2004. Zooplankton Methodology, Collection & Identification – A Field Manual.
National Institute of Oceanography, Dona Paula, Goa, pp 26.
Hakanson L. 1980. An ecological risk index for aquatic pollution control on a sedimentological
approach. Water Res 14:975–1001.
Hossen FM, Hamdan S, and Rahman RM. 2014. Cadmium and lead in blood cockle (Anadara gran-
osa) from Asajaya, Sarawak Malaysia. Sci World J Article ID: 924360. doi:10.1155/2014/924360
Janaki Raman D, Jonathan MP, Srinivasalu S, et al. 2007. Trace metal enrichments in core sediments
in Muthupet mangroves, SE coast of India: Application of acid leachable technique. Environ Pollut
145:245–57.
Jeng MS, Jeng WL, Hung TC, et al. 2000. Mussel Watch: A review of Cu and other metals in various
marine organisms in Taiwan, 1991–1998. Environ Pollut 110:207–15.
Jonathan MP, Ram-Mohan V, and Srinivasalu S. 2004. Geochemical variations of major and trace
elements in recent sediments, off the Gulf of Mannar, Southeast Coast of India. Environ Geol
45:466–80.
Jonathan MP, Srinivasalu S, Thangadurai N, et al. 2008. Contamination of Uppanar River and coastal
waters off Cuddalore, Southeast Coast of India. Environ Geol 53:1391–404.
Kalay M, and Canli M. 1999. Heavy metal concentrations in fish tissues from the northeast Mediterra-
nean Sea. Bull Environ Contam Toxicol 63:673–81.
Kalay M, and Canli M. 2000. Elimination of essential (Cu, Zn) and non-essential (Cd, Pb) metals from
tissues of a freshwater fish Tilapia Zilli. Turk J Zool 24:429–36.
Karbassi AR, Monavari SM, Nabi Bidhendi GHR, et al. 2008. Metal pollution assessment of sediment
and water in the Shur River. Environ Monit and Assess 147:107–16.
Kathiresan K, and Bingham BL. 2001. Biology of mangrove ecosystems. Adv Mar Bio 40:81–251.
Kathiresan K, and Rajendran N. 2005. Mangrove ecosystems of the Indian Ocean region. Indian J Mar
Sci 34:104–13.
Kumar B, Rita S, and Mukherjee D. 2011. Geochemical distribution of heavy metals in sediments from
sewage fed fish ponds from Kolkata wetlands, India. Chem Spec Bioavailab 23:24–32.
Laxen DPH. 1983. The chemistry of metal pollution in water. In: R. M. Horrison (Ed.1), Pollution
Causes Effects and Control. The Royal Society of Chemistry, London, pp 104.
Mathivanan K, and Rajaram R. 2014a. Anthropogenic influences on toxic metals in water and sedi-
ment samples collected from industrially polluted Cuddalore coast, Southeast coast of India. Envi-
ron Earth Sci 72:997–1010.
Mathivanan K, and Rajaram R. 2014b. Tolerance and biosorption of cadmium (II) ion by highly cad-
mium resistant bacteria isolated from industrially polluted estuarine environment. Indian J Geo-
Mar Sci 43:580–8.
Marrugo-Negrete J, Pinedo-Hernandez J, and Dıez S. 2017. Assessment of heavy metal pollution, spa-
tial distribution and origin in agricultural soils along the Sinu River Basin, Colombia. Environ Res
154:380–8.
Melchor GonzAlez-Dkila. 1995. The role of phytoplankton cells on the control of heavy metal concen-
tration in seawater. Mar Chem 48:215–36.
Mishra S, Bhalke S, Saradhi IV, et al. 2007. Trace metals and organ metals in selected marine species
and preliminary risk assessment to human beings in Thane Creek area, Mumbai. Chemosphere
69:972–8.
20 G. ARUMUGAM ET AL.

Moiseenko TI, and Kudryavtseva LP. 2001. Trace metal accumulation and fish pathologies in areas
affected by mining and metallurgical enterprises in the Kola Region, Russia. Environ Pollu
114:285–97.
Muralisankar T, Saravana Bhavan P, Srinivasan V, et al. 2015. Effects of dietary copper on the growth
physiology and biochemistry of the freshwater prawn Macrobrachium rosenbergii post larvae. Int J
Pure App Biosci 3:509–18.
Muralisankar T, Bhavan PS, Radhakrishnan S, et al. 2014. Dietary supplementation of zinc nanopar-
ticles and its influence on biology, physiology and immune responses of the freshwater prawn,
Macrobrachium rosenbergii. Biol Trace Elem Res 160:56–66.
Natesan UM, Kumar Madan, and Deepthi K. 2014. Mangrove sediments a sink for heavy metals? An
assessment of Muthupet mangroves of Tamil Nadu, southeast coast of India. Environ Earth Sci
72:1255–70.
Nazeer S, Hashmi MZ, and Malik RN. 2014. Heavy metals distribution, risk assessment and
water quality characterization by water quality index of the River Soan, Pakistan. Ecol Indic
43:262–70.
Newarman MC. 1998. Fundamentals of Ecotoxicology, pp 25–39. Ann Arbor Press, Chelsea, USA.
Nriagu JO. 1989. A global assessment of natural sources of atmospheric trace metals. Nature
338:47–8.
Pacyna JM, and Pacyna EG. 2001. An assessment of global and regional emissions of trace metals to
the atmosphere from anthropogenic sources worldwide. Environ Rev 9:269–98.
Polidoro BA, Carpenter KE, Collins L, et al. 2010. The loss of species: Mangrove extinction risk and
geographic areas of global concern. PLoS ONE 5:e10095. doi:10.1371/journal.pone.0010095
Prasanna MV, Praveena SM, Chidambaram S, et al. 2012. Evaluation of water quality pollution indices
for heavy metal contamination monitoring: A case study from Curtin Lake, Miri City, East Malay-
sia. Environ Earth Sci 67:1987–2001.
Priya KL, Jegathambal P, and James EJ. 2014. Trace metal distribution in a shallow estuary. Toxicol
Environ Chem 96:579–93.
Radwan S, Kowalik W, and Kowalczyk C. 1990. Occurrence of heavy metals in water, phytoplankton
and zooplankton of mesotrophic lake in eastern Poland. Sci Total Environ 96:115–20.
Raja P, Veerasingam S, Suresh G, et al. 2009. Heavy metals concentration in four commercially valu-
able marine edible fish species from Parangipettai Coast, South East Coast of India. Int J Anim Vet
Adv 1:10–14.
Rajaram R, Ganeshkumar A, Vinothkumar S, et al. 2017. Multivariate statistical and GIS-based
approaches for toxic metals in tropical mangrove ecosystem, southeast coast of India. Environ
Monit Assess 189(6):288.
Rajaram R, Sumitha Banu J, and Mathivanan K. 2013. Biosorption of Cu (II) ions by indigenous copper-
resistant bacteria isolated from polluted coastal environment. Environ Toxicol Chem 95:590–604.
Ramesh R, Nammalwar P, and Gowri VS. 2008. Database on Coastal Information of Tamilnadu,
Chennai, India: Institute for Ocean Management, Anna University, Chennai. Report submitted to
Environmental Information System (ENVIS), Department of Environment, Government of Tamil-
nadu, pp. 133.
Ranjan RK, Ramanathan AL, Singh G, et al. 2008. Assessment of metal enrichments in tsunamigenic
sediments of Pichavaram mangroves southeast coast of India. Environ Monit Assess 147:389–11.
doi:10.1007/s10661-007-0128-y
Richardson MG, Garrett R, Mitchell I, et al. 2001. Critical review on natural global and regional emis-
sions of six trace metals to the atmosphere. Prepared for the International Lead Zinc Research
Organisation, the International Copper Association, and the Nickel Producers Environmental
Research Association..
Saa P, Palomares ML, and Pauly D. 2000. The FOOD ITEMS table, p. 182–188. In: R. Froese and D.
Pauly (eds), FishBase 2000: Concepts, Design and Data Sources. ICLARM, Los Ba~ nos, Laguna,
Philippines, pp. 134.
Shriadah MMA. 1999. Heavy metals in mangrove sediments of the United Arab Emirates Shoreline
(Arabian Gulf). Water Air Soil Pollut 116:523–34.
 HUMAN AND ECOLOGICAL RISK ASSESSMENT 21

Shen F, Liao R, Ali A, et al. 2017. Spatial distribution and risk assessment of heavy metals in soil near a
Pb/Zn smelter in Feng County, China. Ecotoxicol Environ Saf 139:254–62.
Singh AK, Abubakar A, Dinesh Kumar, et al. 2012. Status, Biodiversity and Distribution of Mangroves
in India: An Overview. Uttar Pradesh Biodiversity Board, India.
Siriporn P, Noor Azhar Mohamed S, Prawit T, et al. 2016. Accumulation of trace metals in Anadara
granosa and Anadara inaequivalvis from Pattani Bay and the Setiu Wetlands. Bull Environ Contam
Toxico 96: 472–7.
Soma G, and Singh AK. 2017. Ecological and human health risk assessment of agricultural soils based
on heavy metals in mining areas of Singhbhum copper belt, India. Hum Ecol Risk Assess 23:1008–
27.
Stephen Pichaimani V, Jonathan MP, Srinivasalu S et al., 2008. Enrichment of trace metals in surface
sediments from the northern part of Point Calimere, South east coast of India. Environ Geol 55:
1811–19.
Suresh G, Ramasamy V, Sundarrajan M, et al. 2015. Spatial and vertical distributions of heavy metals
and their potential toxicity levels in various beach sediments from high-background-radiation
area, Kerala, India. Mar Poll Bull 91:389–400.
Thilagavathi B, Raja K, Bandana Das K, et al. 2011. Heavy metal distribution in sediments of Muthu-
pettai Mangroves, South East Coast of India. J Ocean U China 10:385–90.
Tomas CR. 1997. Identifying Marine Phytoplankton, p 858. Academic Press, Harcourt Brace and
Company, Toronto.
Topcuoglu S, Kirbasoglu C, and Gungor N. 2002. Heavy metals in organisms and sediments from
Turkish Coast of the Black Sea, 1997–1998. Environ Int 27:521–6.
Upadhyay YP, Rajan R, and Singh JS. 2002. Human-mangrove conflicts: The way out. Cur Sci
83:1328–35.
Vallee BL, and Falchuk KH. 1993. The biochemical basis of zinc physiology. Physiol Rev 73:79–118.
Veerasingam S, Vethamony P, Mani Murali R et al., 2015. Depositional record of trace metals and
degree of contamination in core sediments from the Mandovi estuarine mangrove ecosystem, west
coast of India. Mar Poll Bull 91:362–7.
Verlencar XN, and Desai S. 2004. Phytoplankton Identification Manual. National Institute of Ocean-
ography, Dona Paula, Goa.
Villar C, Stripeikis J, DHuicque L, et al. 1999. Cd, Cu and Zn concentrations in sediments and the
invasive bivalves Limmoperna fortunei and Corbicula fluminea at the Rıo de la Plata basin, Argen-
tina. Hydrobiologia 416:41–9.
Vyas A, Bajpai A, Verma N, et al. 2007. Heavy metal contamination cause of idol immersion activities
in urban lake Bhopal, India. J Appl Sci Environ Manage 11:37–9.
Waldichuk M. 1985. Biological availability of metals to marine organisms. Mar Poll Bull 16:7–11.
WHO (World Health Organization). 1989. Heavy Metals – Environmental Aspects of Environment
and Health Criteria. No.85. WHO, Geneva, Switzerland.
Wright David A, and Pamela W. 2002. Environmental Toxicology. Cambridge University Press, Cam-
bridge, UK.
Yanyi Z, Xiaoping H, Binhe G, et al. 2013. Analyzing biomagnification of heavy metals in food web
from the Pearl River estuary, south China by stable carbon and nitrogen isotopes. Fresen Environ
Bull 22(6):1652–58.
Zhang Y, Lu X, Wang N, et al. 2016. Heavy metals in aquatic organisms of different trophic levels and
their potential human health risk in Bohai Bay, China. Environ Sci Poll Res 23(17):17801–10.
doi:10.1007/s11356-016-6948-y