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Bioaccumulation of Heavy Metals and its Effect on Organs of Edible Fishes

Located in Bhadra River, Karnataka.

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International Journal of Research in Fisheries and Aquaculture

Universal Research Publications. All rights reserved

ISSN 2277-7729
Original Article
Bioaccumulation of Heavy Metals and its Effect on Organs of Edible Fishes
Located in Bhadra River, Karnataka.
Shivakumar C.K1, Thippeswamy B*1, Tejaswikumar M.V2 and Prashanthakumara S.M 2
1
Dept. of P.G. Studies and Research in Microbiology, Kuvempu University
2
Dept. of P.G. Studies and Research in Applied Zoology, Kuvempu University
Bio-Science Complex, Jnanasahyadri, Shankaraghatta-577 451, Karnataka, India
*
Corresponding Author E-mail: thippeswamyb205@gmail.com
Received 27 May 2014; accepted 09 June 2014
Abstract
The present study aimed to assess major ecotoxic heavy metals accumulated in the organs of common edible fish species,
Etroplus maculates, Cirrhinus reba, and Ompok bimaculatus collected from region of Bhadra River before and after
received the industrial and municipal effluent. DO, COD, TDS and heavy metals content were comparatively higher at the
region of river water receiving effluent compared to river water free from effluent discharge. An inverse relationship was
observed between metals accumulated in fish species and physicochemical properties of river water. Accumulated heavy
metals in different organs varied significantly depending upon the fish species and site of collection. High metals
accumulation in fish indicate impairment of ambient stream due to discharge of industrial and municipal effluents into the
river. Total accumulated metals in the organs of Etroplus maculates was in order of Fe>Zn>Cu > Pb>Ni>Cd, followed by
Zn>Cu>Fe>Pb>Ni>Cd in Cirrhinus reba and Fe>Zn> Cu > Pb>Ni>Cd in Ompok bimaculatus. Muscle, Intestine and gills
showed greater metal accumulation site. High content of Fe, Zn and Cu was detected in fish species. In contrast, lower
concentration of Pb, Ni and Cd was recorded. The Cd and Pb concentration detected in fish species were near to
permissible limit of world health organization standard.
© 2014 Universal Research Publications. All rights reserved
Key words: Fish species; Heavy metals; Bioaccumulation; Bhadra River; Water quality.
Introduction of metals in gills reflects metal concentration in water
Fish have been considered good indicators for where the fish lives. Presence of high metal concentration
heavy metals contamination in aquatic systems. Fish are in the liver represents storage of metals from water for
widely consumed in many parts of the world by humans detoxification (Romeo et al., 1999). The accumulation of
and polluted fish may endanger human health (Zhang et al., heavy metals within the fish varies depending on route of
2007). Metals are non-biodegradable and consider as major metal uptake, type of heavy metal, and fish species (Begum
environmental pollutants causing cytotoxic, mutagenic and et al., 2009). The presence of higher amount of heavy
carcinogenic effects in animals (More et al., 2003). It is metals in any part of the body will induce changes in
important to examine the toxic effects of metals on fish biochemical metabolisms, serum biochemical changes,
since they constitute an important link in food chain and histopathological changes and other induced stresses.
their contamination by metal causes imbalances in aquatic Therefore the studies on the accumulation of heavy metals
system (Firat and Kargam, 2010). Aquatic organisms have in various organs of the fish were very much important.
ability to accumulate heavy metals from various sources Histopathological alterations in fish under the influence of
including sediments, soil erosion and runoff, air depositions heavy metals can be used as a reliable indicator of aquatic
of dust and aerosol, and discharge of waste water pollution.
(Goodwin et al., 2003). Many factors including season, Materials and Methods
physicochemical properties of water, habitat, age and Study Area
physiological conditions of fish play a significant role in The present study was undertaken on Bhadra
accumulation of metals by fish (Kargin, 1996). Gills are River in Karnataka state of southern India which receiving
directly in contact with water; therefore the concentration industrial effluents resulted from paper industry, steel

International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98

90
industry and municipal. Bhadra River originates in Western statistical significance were evaluated using Duncan’s test.
Ghat range and flows initially through Bhadravathi city Histopathological study
towards east across the Deccan plateau which empties into Fresh liver tissue specimen of Ompok bimaculatus
the Bay of Bengal. Bhadrvati city is located at 75.42N was taken and fixed in 15 % buffered neutral formalin. This
Latitude and 13.50E Longitude. The city is known for was processed to obtain five micron thick paraffin sections
paper and steel industries. Width of the river is about 120 to then stained with Hematoxylin and Eosin (Bancroft et al.,
150 meter and depth is about 10 to 15 meter during flood. 1996) and examined under light microscope. A comparison
River receives 75,000m3/day waste water from factory was made between the organs of fishes collected from
effluents. effluent mixed river water and effluent free river water.
Sampling Result and Discussion
Three fish species (5 individuals of each species) Figure 1 shows the area of fish species collected
namely, Etroplus maculates, Cirrhinus reba, and Ompok form Bhadra river region before and after receiving
bimaculatus were caught from Bhadra River through local effluents from industries and municipal of Bhadaravathi
fishermen of the area on seasonal basis for one year period city.
from June 2011 to July 2012. Biometric data were recorded
for the collected fish species.
Physico-chemical analysis of water samples
The river water temperature, pH, color and odor
were recorded on the spot. Electrical conductivity, total
dissolved solids (TDS), biological oxygen demand (BOD),
chemical oxygen demand (COD), dissolved oxygen (DO),
total alkalinity, total acidity, , chloride, sulphate, calcium
and magnesium content were analyzed according to
standard methods (APHA, 2005). After the samples were
acid digested, Cu, Zn, Cd, Ni, Fe and Pb content were
analyzed using Flame Atomic Absorption
Spectrophotometer (AAS) (Thermo Electron Corporation, Figure 1. Location map of study area, Bhadravathi city,
M5 Series-UK Model). Karnataka state, Southern India.
Sample preparation for heavy metal analysis Figure 2 shows the biometric characteristics
Fish were brought to the laboratory and dissected recorded after the collection of the fish samples. The results
to separate organs (Muscles, gills, liver, brain, intestine, showed that Ompok bimaculatus had increased weight
kidney and brain) with clean stainless steel instruments on followed by Etroplus maculates and Cirrhinus reba.
the same day according to FAO methods (Dybem, 1983). Growth length in Ompok bimaculatus is highest followed
The organs from five individuals of each species were by Cirrhinus reba and Etroplus maculates.
polled to make a sample for analysis. Each tissue was put in
a separate Petri dish and dried in an ovan at 1100C for 48h
until constant weight was reached. 0.5g of each dry tissue
was weighed and put in a separate test tube. Then nitric
acid (HNO3) and perchloric acid (HClO4) in 2:1 ratio were
added to each sample and left over night at room
temperature. Samples were digested in a water bath set to
1000C water boiling temperature and the content was boiled
for about 2h until all the tissues dissolved. The digest was
allowed to cool and 5 ml of distilled water was added. The
solution transferred to 25ml volumetric flask and made up
Figure 2. Biometric data showing length (a) and weight (b)
to mark with 1% HNO3 (FAO, 1984). The digest were kept
of collected fish species.
in plastic bottles and accumulated heavy metals
concentration in mg/g dry weight were determined using Accumulation of heavy metals in a tissue is
atomic absorption spectrophotometer (Shah and Altindag, mainly dependent upon water concentrations of metals and
2005). its exposure period. High levels of heavy metals were
Actual concentration of each metal in sample was found in the intestine of fish. Although fish intestines are
calculated using the formula: seldom consumed, it usually accumulated more heavy
Actual concentration of metal in sample = ppmR X dilution metals in this study and might represent good biomonitors
factor of metals present in the surrounding environment (Zhang et
Where, ppmR = AAS reading of digest al., 2007). The obtained result is in agree with previous
Dilution factor = Volume of digest used / Weight of the observations made by Deb and Fukushima (1999) that
sample digested metals may be high concentrations in the gills, intestine and
Obtained data from the experiments were statistically digestive glands. These organs have relatively high
analyzed using SPSS 10.0 statistic software and the results potential for metal accumulation. Copper (Cu), zinc (Zn),
were expressed as mean ± Standard error. The results for iron (Fe), lead (Pb), cadmium (Cd), and nickel (Ni) content

International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98

91
Table 1. Concentrations of Cu, Zn, Cd, Ni, Fe, and Pb (mg/kg dry weight) in different organs of three fish species
collected from Bhadra River before receiving industrial effluent during the period of June 2011-July 2012.

1
All results are expressed as Mean± Standard Error (SE) of Mean; n=5.
2
In an organ analysis, SE followed by the same superscripts in a column are not significantly different where as values with
different superscripts are significantly different from one another at 0.05 significance level (Duncan’s test).
3
In mean concentration, SE followed by same superscripts in a column are not significantly different where as values with
different superscripts are significantly different from one another at 0.05 significance level (Duncan’s test ).
Table 2. Concentrations of Cu, Zn, Cd, Ni, Fe and Pb (mg/kg dry weight) in different organs of three fish species
collected from Bhadra River after receiving industrial effluent during the period of June 2011-July 2012.

1
All results are expressed as Mean± Standard Error (SE) of Mean; n=5.
2
In an organ analysis, SE followed by same superscripts in a column are not significantly different where as values with
different superscripts are significantly different from one another at 0.05 significance level (Duncan’s test).
3
In mean concentration, SE followed by same superscripts in a column are not significantly different where as values with
different superscripts are significantly different from one another at 0.05 significance level (Duncan’s test).

International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98

92
get accumulated in different organs like liver, gills,

M ea n c o nc . o f m eta l s a c c um ul a ted
6 (c)
kidneys, intestine, muscles and brain tissues of the fish
species were analyzed. These fish speceies were collected 5

from bhadra river water before and after receiving the 4

industrial and maniple effluents. A significant difference

(m g)
(p<0.05) was observed between the accumulated metal 3

concentrations in each fish species. Mean concentration of 2

accumulated heavy metals in the organs of Etroplus
maculates, Cirrhinus reba and Ompok bimaculatus was 1

studied. Accumulated metals in the organs of Etroplus 0

maculates was in order of Fe>Zn>Cu > Pb>Ni>Cd, Muscle Liver Intestine Gills Brain Kidney
followed by Zn>Cu>Fe>Pb>Ni>Cd in Cirrhinus reba and
Organs of Cirrhinus reba
Fe>Zn> Cu > Pb>Ni>Cd in Ompok bimaculatus. Gills
showed greater accumulation of metal followed by
intestine, muscles, liver, brain and kidney in Etroplus

M ea n co nc. o f m eta l s a ccum ul a ted

6 (d)
maculates (Figure 3). Muscle accumulated high content of
5
metals followed by intestine, gills, liver, kidney and brain
in Cirrhinus rebba (Figure 4). Ompok bimaculatus 4
accumulated high metal content in the liver followed by

(m g)
3
intestine, gills, kidney, muscle and brain (Figure 5).
2
M ea n c o nc . o f m eta l s a c c um ul a ted

9
8
(a) 1

7 0
6 Muscle Liver Intestine Gills Brain Kidney
5
(m g)

Organs of Cirrhinus reba

4
3 Figure 4. Mean concentration of accumulated heavy metals
2 in the organs of Cirrhinus reba collected from Bhadra river
1 in the region before (c) and (d) after receiving effluents.
0
6 (e)
M ean co nc. o f m etal s accum ul ated

Muscle Liver Intestine Gills Brain Kidney

Organs of Etroplus maculates 5

4
Mean co nc. o f metals accumulated

12
(b)
(m g)

3
10
2
8
(mg)

6 1

4 0

2 Muscle Liver Intestine Gills Brain Kidney

Organs of Ompok bimaculatus

0
Muscle Liver Intestine Gills Brain Kidney

Organs o f E tro plus maculates 7 (f)

M ea n co nc. o f m eta l s a ccum ul a ted

6
Figure 3. Mean concentration of accumulated heavy metals
in the organs of Etroplus maculates collected from Bhadra 5

river in the region before (a) and (b) after receiving 4

(m g)

effluents. 3
Table 1 and Table 2 shows the significant
2
differences in concentration of accumulated metals in
organs of fish species collected from bhadra river water 1

before and after receiving effluents. Even though the metal 0

content of fish species present in both ecosystems were Muscle Liver Intestine Gills Brain Kidney
nearly identical but slight higher metal content was Organs of Ompok bimaculatus
detected in the fish species located at the region of river
water receiving effluents. Greater accumulation of heavy Figure 5. Mean concentration of accumulated heavy metals
metals in fish species is indicating impairment of in the organs of Ompok bimaculatus collected from bhadra
ambient stream water due to discharge of industrial and river in the region before (e) and (f) after receiving
municipal effluents into the studied river streams. Highest effluents.
International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98
93
Figure 6. Mean concentration of accumulated heavy metals in the fish species collected from Bhadra river before (a) and
(b) after receiving effluents.
damage. Ompok bimaculatus showed high amount of heavy
concentration of Fe and Zn was detected in Etroplus metals accumulation in the liver. High amount of heavy
maculates and Ompok bimaculatus. Whereas Cirrhinus metal accumulation in fish liver is due to detoxification of
reba showed presence of highest Zn and Cu content. In heavy metals. Thus the liver in its role as a storage and
contrast, lower concentration of Cd and Pb. was observed detoxification of high level accumulated heavy metals
in all the fish species (Figure 6). (Maaboodi et al., 2011). Differences in concentration of
The results indicate the differences in sensitivity metals in different parts of an organism could be attributed
to metals among the three fish species. The high to the tendency of metals to bind to various molecular
concentration of copper, zinc and iron in tissues of fish groups found within the cells of organisms as well as the
species could be related to the essential of these metals in degree of exposure to metal as influenced by its metabolic
the cellular metabolic process. Thus these metal characteristics and position in the food chain. This may
concentrations in fish organs were much higher than those explain why the gills in all the fish species have more
of non essentials metal such as cadmium and lead. High concentration of the metals than the muscles (Nwani et al.,
content of zinc was detected in fish species because zinc 2010). Ompok bimaculatus and Cirrhinus rebba contained
metal is necessary for respiratory and enzymatic activities high metal content in kidney when compared to muscle and
of fishes. But at high concentration it can affect circulatory brain. This shows that considerable amount of heavy
and heart system of fish body. Even though low metals were accumulated in kidney tissues. Kidney is the
concentration of cadmium and lead were detected but long gateway for heavy metals detoxification in body. Except
term accumulation of these metals can cause damage to Cirrhinus rebba, the other two fish species of Ompok
nerve, blood and respiratory systems (Filipovic and Raspor, bimaculatus and Etroplus maculates have lower metal
2003). Different organisms have different metabolic rates content in muscle compared to liver, intestine, gill and
and different food requirements. The requirement of kidney tissue in Ompok bimaculatus. This indicates that the
essential metals such as copper, zinc and iron for the heavy metals were uniformly spread over the body of
growth of organisms depends on its physiological muscles. Hence, the observed heavy metal content in the
conditions. The different organs absorb metals depending fish muscle was relatively low when compared to other
upon its requirement for metabolic functions. The organs like gills and intestine (Vinodhini and Narayanan,
difference in heavy metal accumulation in different organs 2008). Fish liver and kidney exhibited higher tendency of
is due to the differences in physiological and biochemical metal accumulation when compared to muscle. This
functions. Thus the results indicate that the gills and shows that the fish muscle meets the requirements for safe
intestine of Etroplus maculates and Ompok bimaculatus consumption (Andreji et al., 2006; Javed and Saeed, 2010).
have high iron content while the least were recorded in the Even though the brain and kidney of fish species have
gills and intestine of Cirrhinus reba respectively. Total accumulated heavy metals but their content was less when
accumulation of copper and zinc metals are high in compared to other organs (Agrahari and Gopal, 2007). The
Cirrhinus reba when compared to Etroplus maculates and resistance for metal toxicity in fish species is attributed by
Ompok bimaculatus. Organism with high food intake also the presence of metallothionein and is coded by
tends to accumulate more metals (Ademoroti, 1996; Metallothionein (MT) genes. Resistance to heavy metal
Ghedira et al., 2010). toxicity in fish is related to their ability to over express MT
In Etroplus maculates the concentration of metals genes after exposure to metal ions (Andrews, 2000).
in gills was significantly higher (p<0.05) when compared Induction of metallothioneins in the fish liver indicates as
with other organs. The gills tissue play an important role in the main form of storage and detoxification of metals ions.
ion regulation, gas exchange, acid balance, nitrogenous The higest MT level and metal concentrations were
wastes and excretion which signifies the key role it play at measured in liver (De Smet et al., 2001).
the interface with the environment (Karthikeyan et al., Table 3 shows the physico-chemical
2007). Hence gill is an important site for the entry of heavy characteristics of river water before and after receiving
metals and in high concentrations provokes lesion and gills effluents. The toxicity of heavy metals in aquatic habitat is
International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98
94
 Table 3. Physico-chemical parameters of river water before and after receiving the
industrial effluent.
Parameter unit - mgL-1, except pH, temperature and conductivity, Mean ± Standard Error
WHO (2006) - World Health Organization
IS (1998) - Indian Standard for effluent discharge to inland surface water
also dependent on phyisco-chemical status of water. The
river water receiving effluent had showed considerable
amount of calcium, magnesium, sulfate, BOD and COD
level when compared to river water away form effluent
discharge (Ebtesam, 2008). The wastewater from paper
industry, steel industry and municipal are discharge in to
the water bodies. It results in the entry of alkali and
chlorine compounds into the water. Lignin and its
derivatives in paper waste are difficult to degrade because
of the linkages within the molecule, especially the biphenyl
type carbon to carbon linkages (Singh et al., 2008). Dark
brown color of the effluent increases water temperature and
decrease photosynthesis, both of these lead to decreased
concentration of dissolved oxygen. The color of paper
effluent is most difficult to remove and it also indicates an
increased BOD and COD level. Metallic effluents can have
ecological impacts on water bodies leading to increased
nutrient load especially if they are essential metals. These
metals in effluents may increase the fertility of sediment
and water column. The increase fertility leads to
eutrophication intern cause oxygen deficiency, algal bloom
formation and death of aquatic life. Heavy metals content
of paper and steel effluent was found to be high due its
increased application as catalyst, pigments, wood
preservatives and corrosion inhibitors (Goel, 1996). Heavy
metals beyond permissible limit cause direct toxicity to all
living organisms. The major modifying physico-chemical
factors of metal toxicity are hardness and pH of water.
Water born metals exhibit higher metal toxicity to aquatic
organisms in soft water of low pH and low dissolved
carbon. This is because the cations like Mg and Ca compete
with heavy metal cations for binding sites within the
organisms.
International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98
95
Table 4 shows some positive correlation between
physico-chemical parameters of river water. Biological
oxygen demand was high significantly correlated with total
hardness, copper and cadmium. Water temperature was
most significantly correlated with calcium. pH was most
significantly correlated with copper. Chemical oxygen
demand was most significantly correlated with nickel and
chloride. Among the heavy metals lead showed strong
positive correlation with iron and copper. Factors
including pH, hardness, aeration and temperature have
pronounced effects on LC50 values. The fish has high risk
for industrial effluent containing heavy metals. Adults were
more tolerant than their young. Among adults, female was
more sensitive than male (Shjile et al., 2006). Different
metal accumulation sensitivity in the fish species can be
caused by different breed conditions, feed quality and
environmental quality (water source, geological sediments
etc.). The measured heavy metals concentrations of
cadmium and lead in fish species near to permissible limit
indicate potential health risks for human consumption. The
results of the study indicate that amount of heavy metals
accumulated depends on fish species and its habitat or
sampling area. Therefore, care should be taken in terms of
frequent physicochemical analysis of river water and to
measure accumulated metals in the organs of edible fish
species collected from the region of water receiving
effluent. Fishes used for human diet from the studied
locations should be avoided in presence of high heavy
metal concentrations. Fish absorb dissolved metals in water
and serves as a reliable indicator of metal pollution in an
aquatic ecosystem. It is important to examine the toxic
effect of metals on fish since they constitute an important
link in food chain and their contamination by metal causes
Table 4. Spearman’s correlation matrix among the physico-chemical properties of river water collected during the period
June 2011-July 2012.

Note: * = Correlation is highly significant at p < 0.01 level, * = Correlation is significant at p < 0.05 level,
W.T = Water temperature, E.C = Electrical conductivity, T.D.S = Total Dissolved Solids, DO= Dissolved Oxygen BOD= Biochemical Oxygen Demand,
COD= Chemical Oxygen Demand, T.H=Total Hardness, Cl- Chlorine, Ca2+= Calcium,
Mg2+= Magnesium, Cl-= Chloride, SO4-= Sulphate, Cu2+= Copper, Cr6+= Chromium, Ni2+= Nickel, Zn2+= Zinc, Pb2+= Lead, Cd2+= Cadmium. All units are
in mgL-1, except except pH, temperature (0°C) and conductivity (μmhos /cm)

Figure 7. The photographs showing histopathological view of Ompok bimaculatus liver collected from river water without
effluents (a) and liver collected from river water with effluent containing heavy metals (b).

Figure 8. The photographs showing normal histopathological view of Ompok bimaculatus kidney (a) and histological
altered kidney cells due to heavy metals toxicity (b).
International Journal of Research in Fisheries and Aquaculture 2014; 4(2): 90-98
96
imbalances in the aquatic system.
Histopathological examination
Figure 7 shows morphological altered hepatic cells
of liver in Ompok bimaculatus collected from effluent
mixed river water. Whereas the normal structure of hepatic
cells of liver was observed in Ompok bimaculatus collected
from river water without mixed with effluent. Liver showed
degeneration of the hepatocytes and intravascular
haemolysis in blood vessels. Congestion of central vein,
hemorrhages, nuclear pyknosis was observed in the
majority of hepatic cells. Metal-binding proteins were
accumulated in the nuclei of hepatocytes. The
concentration of cadmium, lead and copper were highest in
liver and lowest in kidney tissue of Oreochromis niloticus
from Egyptian fish farms. Several histopathological
changes were noted in muscles, liver, gills, kidney and
intestine tissue attributable to heavy metals exposure
(Kaoud and El-Dahshan, 2010). Histological examination
of the kidney revealed vacuolar degeneration in the tubular
epithelium of Oreochromis niloticus collected from effluent
mixed river water (Figure 8). Kidney is concerned with
detoxification and excretion of pollutants. The changes in
the size and structure of the epithelial cells and the narrow
lumen of the renal tubule inhibits kidney functioning.
Kidneys are deeply involved in organism defense against
the pollutant and are seriously damaged soon after
fingerlings exposure to copper (Gupta and Srivastava,
2006).
Conclusion
These fishes are the main fishery resources and
mainly consumed by many people in the study area. Hence
it is ascertain to know the suitability and safety for the local
people regarding their edible fishes. This study was
undertaken to view toxicological importance of these edible
fishes to know its variations in heavy metals contamination.
Iron was the most common metal recorded in all fishes
followed by zinc, copper, lead, nickel and cadmium. Even
though cadmium and lead were the least abundant metal
recorded but their content is near to standard permissible
limit. Hence care should be taken for avoid to reach the
metal concentrations above the permissible limits. The
heavy metals contamination not only affects the fish but
also other aquatic life gets affected. Hence a proper
detoxification of heavy metals in effluent and municipal
waste is necessary before discharge into the water body.
Acknowledgement
We would like to thank the Department of
Microbiology, Kuvempu University for providing
laboratory facilities to carry out this research work.
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