Cadmium Accumulation in Gill, Liver, Kidney and MuscleTissues of Common Carp, Cyprinus carpio, and Nile Tilapia,Oreochromis niloticus

Burcu Yesilbudak • Cahit Erdem

Received: 12 November 2013 / Accepted: 4 February 2014

� Springer Science+Business Media New York 2014

Abstract Accumulation of cadmium in gill, liver, muscle

and kidney tissues of Cyprinus carpio and Oreochromis

niloticus were investigated in fish exposed to 0.5 ppm

cadmium over 1, 15 and 30 days under controlled labora-

tory conditions. Tissue accumulation of the metal was

measured using Atomic Absorption Spectrophotometric

techniques. Cadmium accumulation in gill, liver, kidney

and muscle, tissues of C. carpio and O. niloticus exposed to

metal for 1, 15 and 30 days increased significantly com-

pared with the control group (p \ 0.05), except muscle

tissue of O. niloticus. A general increase was observed in

Cd accumulation with increasing exposure periods. Highest

metal accumulation was observed in kidney followed by

liver, gill and muscle tissues in both species. Liver accu-

mulation of Cd was higher in C. carpio than O. niloticus,

whereas kidney accumulation of the metal was higher in O.

niloticus than C. carpio.

Keywords Accumulation � Cadmium � Cyprinus carpio �Oreochromis niloticus

Aquatic environments act as reservoirs for various land

based and atmospheric pollutants and the organisms living

in these waters are in direct contact with these pollutants.

Determining the levels of pollutants especially in pollution

indicator organisms and economically important species is

vital with regards to ecological balance and human health.

Toxicity of heavy metals to aquatic organisms depends

upon the physical and chemical characteristics of water

such as dissolved oxygen, temperature, salinity and the

presence of other metals in water. Metal toxicity is known

to increase under hypoxic conditions and increasing tem-

peratures whereas it decreases with increasing salinity and

water hardness (Witeska and Jezierska 2003).

Some heavy metals, such as copper and zinc, are nec-

essary in trace amounts for the continuation of structural

and metabolic functions, however, when their levels

exceed certain levels they accumulate mainly in metabol-

ically active organs and become toxic (Galvez et al. 1998).

Cadmium, which is known to have no biological function,

is related closely to Zn and is mined as a second product

during mining activities (May et al. 2001). Its presence

even in low concentrations causes tissue and vertebral

deformations, respiration abnormalities and death in fish

(De Smet and Blust 2001).

Gill, liver and kidney are metabolically active and

readily available organs which are analyzed for bio-moni-

toring (Ewers and Schlipkoter 1991), whereas muscle is an

important protein source for human consumption (Marco-

vecchio et al. 1991).

It was reported that Oreochromis niloticus and Cyprinus

carpio are important freshwater fish which are resistant to

highly polluted habitats and are used as bio-indicator spe-

cies in understanding environmental pollution (Abedi et al.

2012; Fırat and Kargın 2010). Garcia Santos et al. (2006),

repoted that O. niloticus and C. carpio contribute a lot in

understanding toxic mechanism of cadmium exposure in

aquatic organisms. The two economically important trop-

ical fish C. carpio and O. niloticus are selected as study

animals since they are known to have wide resistance to

metal poisoning and are widely cultured in Cukurova

region as a protein source. The purposes of this study were

to determine heavy metal levels in these fish organs such as

gill, liver, kidney and muscle and to compare accumulated

levels in tissues of these two species under the same

B. Yesilbudak (&) � C. Erdem

Department of Biology, Faculty of Science and Letters,

Cukurova University, Adana 01330, Turkey

e-mail: yesilbudak@gmail.com

123

Bull Environ Contam Toxicol

DOI 10.1007/s00128-014-1228-3

ambient conditions. Hence the present study was designed

to examine the accumulation of cadmium in four tissues of

C. carpio and O. niloticus after exposing 0.5 ppm Cd over

30 days. This concentration is well below the 96 h LC50

values of both species (Garcia Santos et al. 2006; Abedi

et al. 2012).

Materials and Methods

Study materials, O. niloticus and C. carpio were obtained

from the culture pools of the 6th Regional Directorate of

State Water Works, Adana. Experiments were carried out in

the Basic Sciences research laboratories of Mersin Univer-

sity, Faculty of Aquaculture under controlled conditions.

Fish were acclimatized to laboratory conditions for

1 month in glass aquaria, 40 9 120 9 40 cm in height.

Mean weight and total length of O. niloticus and C. carpio

were 21.49 ± 0.98 g, 16.40 ± 1.02 cm and 18.72 ±

0.73 g, 15.66 ± 1.24 cm respectively at the end of this

period. Two series of experiments were carried out taking

the two species studied into account. Two glass aquaria, of

the same size were used in each series. 120 L of 0.5 ppm Cd

solution was added in the first two aquaria of each series and

the same amount of Cd free tap water was added in the

second and used as controls. Cadmium chloride (CdCl2-

H2O) salt of the metal was used in preparing the experi-

mental solutions. Tri-sodium citrate (C6H5Na3O7�5H2O)

was added to the stock solutions to prevent precipitation.

Experiments were run in triplicate, two fish were used in

each replicate, and 18 fish were placed in each aquarium

taking the 1, 15 and 30 days of exposure periods into

account. Aquaria were aerated by a central aeration system

and fish were fed at 2 % of the total biomass with com-

mercial fish feed (Camlı Feed Ind. Trade Co. Ltd., Izmir,

TURKEY, Pınar: Palette No: 2). Experimental solutions

were replaced once every 2 days from freshly prepared

stock solutions using dechlorinated water to prevent chan-

ges in concentration due to adsorption and evaporation.

Metal levels in the tap water were below the detection limits

of Cd (0.001 mg/L). Mean Cd level experimental water at

different durations were determined as 0.42 ± 0.08 mg/L.

Some physical and chemical parameters of the experimental

aquaria are given in Table 1.

Six fish were removed from each aquarium at the end of

the experimental periods for metal analysis. Gill, liver,

kidney and muscle tissues of the two fish in each replicate

were dissected and their tissues were combined. The tissues

were then brought to a stable dry weight in a drying oven

set at 150�C for 48 h. Tissues were transferred into

experimental tubes after measuring their dry weight (Sar-

torius CP-224S) and nitric acid (Merck, 65 %, S.W.: 1.40)

and per chloric acid (Merck, 60 %, S.W.: 1.53) mixture

(2:1 v:v) was added. Tissues were then wet burned on a

hotplate set at 105�C until a clear solution was obtained

(Muramoto 1983). Tissues homogenates were then trans-

ferred into polyethylene tubes and their volumes were

made up to 5 mL with distilled water. Tissue Cd levels

were measured using Atomic Absorption Techniques

(GBC 999). Statistical analysis of data was carried out

using Analysis of Variance and Student Newman Keul’s

Procedure (SNK) (Sokal and Rohlf 1995) on a SPSS 15.0

software (IBM Corp., Armonk, NY, USA).

Results

No mortality was observed in either C. carpio or O. niloticus

exposed to 0.5 ppm Cd during the 30 days of the experi-

mental period. Some behavioral abnormalities were

observed such as rejecting food, moving towards the surface,

increase in operculum movement and coordination distur-

bance in swimming activities at the beginning of metal

exposure which turned to normal at prolonged contact with

the metal.

Gill, liver, kidney and muscle levels of C. carpio and O.

niloticus exposed to 0.5 ppm Cd over 1, 15 and 30 days are

given in Tables 2 and 3 respectively.

Cadmium levels in gill, liver, kidney and muscle tissues

of C. carpio exposed to 0.5 ppm Cd increased significantly

at all exposure periods tested compared with the control

fish (p \ 0.05) (Table 2). Cadmium accumulation

increased with increasing exposure periods at all tissues

except the muscle tissue. This increase in gill, kidney and

liver tissues on day 30 was about 2, 3 and 6 times com-

pared with the first day respectively. Cadmium accumula-

tion was highest in kidney tissue of C. carpio followed by

the liver, gill and muscle tissues at all exposure periods.

Significant increase in Cd accumulation in the tissues of

O. niloticus was also observed with prolonged exposure

periods (p \ 0.05) except the muscle tissue (Table 3). Gill

cadmium levels showed a ninefold increase on day 30

compared with day 1. Highest accumulation of Cd was also

in kidney tissue followed by liver, gill and muscle tissues

Table 1 Some physical and chemical parameters of the experimental

water

Illumination 12 h with fluorescent lamps (daylight 65/80 W)

Temperature 21.2 ± 1�C (YSI 550A temperature meter)

Total hardness 268.7 ± 4.8 mg CaCO3/L (EDTA titration

method)

Total alkalinity 319 ± 0.5 mg CaCO3/L (acidimetry method)

Dissolved

oxygen

6.46 ± 0.6 mg/L (YSI 550A oxygen meter)

pH 6.91 ± 1 (WTW pH 330i meter)

Bull Environ Contam Toxicol

123

as in C. carpio at the exposure periods tested. Cadmium

levels in gill and liver tissues of both species increased with

exposure periods reaching to its maximum level on day 15

in C. carpio and on day 30 in O. niloticus. Liver and kidney

accumulation also was time dependent in both species, C.

carpio accumulating higher levels of Cd in its liver and O.

niloticus in its kidney tissues at prolonged exposures.

Accumulation of Cd in muscle tissue of C. carpio was

higher than that of O. niloticus at the exposure periods

tested. There were a 9, 26.5, 15.42, 10 and 18, 13.66, 9.3,

twofold increase in metal accumulation in gill, liver, kid-

ney, and muscle tissues of C. carpio and O. niloticus,

respectively, compared to control on day 30 (p \ 0.05).

Discussion

Effects of heavy metals on mortality in aquatic organisms

depend not only on biological characteristics of the species

in question, but also on physical and chemical character-

istics of the water. Mortality rate increases rapidly over a

certain concentration and exposure periods. Ten percent

mortality was observed in Oncorhynchus mykiss juveniles

exposed to 3.0 ppm Cd for 30 days (Hollis et al. 2001),

whereas no mortality was observed in O. niloticus juveniles

exposed to 0.35, 0.75, 1.5, and 3.0 ppm of Cd in water for

60 days (Almeida et al. 2002). This was also true for C.

carpio and O. niloticus exposed to 0.5 ppm Cd for 30 days

in the present study. The reason for the survival of fish

under the effect of a toxicant might be due to tolerance of

the species for a particular toxicant at the concentrations

and exposure periods tested. Formation of metal esters by

metal binding proteins such as glutathione and metallo-

thionein synthesized from detoxification centers, namely

liver and kidney, might play a role in preventing transport

of toxicants to other tissues.

The immediate reaction of fish to environmental dis-

turbances is to change their behavior. Food rejection,

moving toward the surface of water, low swimming per-

formance, increase in operculum movements and mucus

secretion and erection of fin rays were observed in C.

carpio and Poecelia reticulata under the effect of copper

(Khunyakari et al. 2001). Similar behavioral changes were

also observed in the present study which turned to normal

at prolonged exposures. Bringing the metabolic activity to

its minimum level and using its energy to adapt changing

environmental conditions rather than for behavior might be

the reason for these behavioral changes in fish under the

effect of metals. Tissue accumulation and toxic effects of

metals in fish largely depend upon the physical and

chemical characteristics of water. It was shown that Zn and

Cd toxicity is affected by water hardness, temperature, pH

and dissolved oxygen (Nussey et al. 1998). USEPA (2002)

has suggested the maximum tolerable short-term and con-

tinuous concentrations of Cd at 2 and 0.25 lg/L in surface

freshwater bodies in the United States. These environ-

mental factors were kept constant to minimize their effect

on accumulation and toxicity in the present study.

Table 2 Gill, liver, kidney and muscle accumulation of C. carpio exposed to 0.5 ppm Cd over 1, 15 and 30 days (lg Cd/g D.W.)

Exposure period (days) Tissue

Gill Liver Kidney Muscle

X� Sx * X� Sx * X� Sx * X� Sx *

Control 0.01 ± 0 as 0.02 ± 0.01 as 0.07 ± 0.02 at 0.003 ± 0 as

1 0.05 ± 0.01 bs 0.08 ± 0.01 bt 0.31 ± 0.04 bx 0.04 ± 0.01 bs

15 0.21 ± 0.03 ct 0.23 ± 0.06 ct 0.45 ± 0.05 cx 0.03 ± 0.01 bs

30 0.09 ± 0.01 dt 0.51 ± 0.04 dx 1.08 ± 0.09 dy 0.03 ± 0.01 bs

* = SNK; letters a, b, c, d and s, t, x, y show differences among exposure periods and among tissues respectively. Data shown with different

letters are significant at the p \ 0.05 level

X� Sx = Mean ± SE

Table 3 Gill, liver, kidney and

muscle accumulation of O.

niloticus exposed to 0.5 ppm Cd

over 1, 15 and 30 days (lg Cd/g

D.W.)

Abbreviations were used as in

Table 2

Exposure

period (days)

Tissue

Gill Liver Kidney Muscle

X� Sx * X� Sx * X� Sx * X� Sx *

Control 0.01 ± 0.01 as 0.03 ± 0.01 at 0.30 ± 0.14 ax 0.01 ± 0.001 as

1 0.02 ± 0.001 as 0.11 ± 0.08 bt 0.41 ± 0.16 bx 0.02 ± 0.004 bs

15 0.07 ± 0.02 bt 0.16 ± 0.021 cx 0.98 ± 0.19 cy 0.01 ± 0.001 as

30 0.18 ± 0.02 ct 0.41 ± 0.15 dx 2.79 ± 0.26 dy 0.02 ± 0.004 bs

Bull Environ Contam Toxicol

123

Studying heavy metal accumulation helps not only to

determine structural and functional disorders in metal

sensitive aquatic organisms but also to evaluate the envi-

ronmental effects of metal pollution and to understand their

routes of uptake, biotransformation and excretion (Wickl-

und et al. 1988). Heavy metals accumulate mainly in

metabolically active tissues such as gill, liver, kidney and

spleen under the effect of low concentrations for prolonged

periods (Hogstrand and Haux 1990). The levels of Cd and

Cu were found to be higher in liver followed by gill, and

muscle tissues in O. niloticus (Cogun et al. 2003). Expo-

sure to heavy metals increase mucus secretion in fish to

prevent gill uptake, hence high levels of metals found in

this tissue might be due to mucus bonded metals.

Highest Cu accumulation was in liver and highest Cd

accumulation was in kidney tissue in O. niloticus exposed

to Cu, Cd and their mixture (Saglamtimur et al. 2004).

Liver accumulation was highest and muscle accumulation

was lowest in Scylorhinus canicula exposed to sublethal

concentrations of Zn (Sanpera et al. 1983).

Cadmium levels in Clarias gariepinus during 30 days of

exposure were higher in kidney tissue followed by liver,

gill and muscle tissues. During the 15, 30 and 45 days of

depuration periods, however, no change was observed in

spleen and liver levels, there was a decrease in the levels of

metal in gill and muscle tissues and an increase in kidney

tissue (Erdem et al. 2005). C. carpio exposed to low con-

centrations of Cd accumulated high levels of this metal in

its gill tissue (Karaytug et al. 2007), while Anguilla

anguilla exposed to Cd through its digestion track accu-

mulated the metal in kidney tissue (Haesloop and Schrimer

1985). Kidney accumulation of Cd was 2 and 100 times

higher than liver and muscle accumulation respectively in

C. carpio exposed to metal over long periods (De Smet and

Blust 2001). Liver, gill and muscle accumulation of Cd was

higher compared with Zn in Tilapia nilotica exposed to

zinc and sublethal concentrations of Cd over a long period

(Kargın and Cogun 1999). Salmo trutta exposed to Cu and

Cd accumulated higher levels of Cu in its liver and Cd in

kidney tissues (Olsvik et al. 2001). Highest Cd accumula-

tion was also in kidney tissues of C. carpio and O. niloticus

exposed to 0.5 ppm Cd, followed by liver, gill and muscle

tissues. Cadmium is known to have no biological function,

and it is carried to kidney with water and other metabolic

wastes for excretion. During this process its reabsorption

and binding to metal binding proteins, such as metallo-

thioneins, can explain high levels of cadmium found in

kidney compared with other tissues.

Accumulation of cadmium in the whole body of rainbow

trout (Salmo gairdneri) exposed to 0.1, 1.0, 10 ppm Cd over

29 days increased to 4.2, 8.7, and 47.0 ppm Cd respec-

tively, on (Sorensen 1991). Some fish can accumulate

cadmium to levels much higher than the level in the ambient

water (Sorensen 1991). Laboratory studies showed that

aqueous exposure level is important in determining the level

of cadmium accumulated by tissues of fish. Exposure of C.

carpio to 0.560 ppm Cd [Cd (NO3)2] killed all fish in 8 days

(Iger et al. 1994) whereas in our study 0.5 ppm of cadmium

(CdCl2�H2O) for 1 month caused no mortality in this spe-

cies. Spinal deformities in mature minnows (Phoxinus

phoxinus) exposed to aqueous cadmium as low as 7.5 ppb

for 70 days was reported by Bengston et al. (1975). Addi-

tionally, Morgan and Kuhn (1974) observed an increased

opercular rhythm of largemouth bass (Micropterus salmo-

ides) from 35 oscillations per min to a maximum of 90

oscillations per min after exposure to 0.1–1.0 ppm aqueous

cadmium. Significant differences in sensitivity to cadmium

amongst fish species have been reported by WHO (1992).

Therefore, it is important to understand the effects of cad-

mium in different species. Cadmium accumulation differs

from species to species and depends on exposure period

(Velma et al. 2009). Liver, gill, kidney, spleen and muscle

levels of Cu, Zn, Cd and Pb levels were higher in Mullus

barbatus compared with Sparus aurata sampled from

Iskenderun Bay, which might be due to differences in

feeding habits of the two species (Kargın 1996). Accumu-

lation of Cd was higher in kidney compared with the other

tissues both in O. niloticus and C. carpio. It is well known

that heavy metals are rarely distributed uniformly within the

tissues of fish and are accumulated by particular target

organs. It was supposed that a specific role of metal

metabolism has been developed for each tissue (Cinier et al.

1999). Liver and kidney appear to be the most important

organs in cadmium sequestration (Allen1995).

In conclusion, the result of the present study showed that

after exposure to 0.5 ppm Cd for 30 days, tissue concen-

trations of the metal increased significantly in both species.

However, gill and kidney accumulation was higher in O.

niloticus whereas liver and muscle accumulation was

higher in C. carpio after 30 days of exposure. This can be

explained by the differences in osmoregulation and

detoxification mechanisms of the two species studied.

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