Heavy Metals Concentration in Water, Muscles and Gills of Oreochromis niloticus Collected from the Sewage-Treated Water and the White Nile  

Elagba Haj Ali Mohamed1 , Abdel-Rahman Osman2
1. Natural History Museum, University of Khartoum, Sudan
2. Faculty of Animal Production, University of Khartoum, Sudan
Author    Correspondence author
International Journal of Aquaculture, 2014, Vol. 4, No. 6   doi: 10.5376/ija.2014.04.0006
Received: 15 Dec., 2013    Accepted: 25 Jan., 2014    Published: 01 Mar., 2014
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This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Mohamed and Osman, 2014, Heavy Metals Concentration in Water, Muscles and Gills of Oreochromis niloticus Collected from the Sewage-Treated Water and the White Nile, International Journal of Aquaculture, Vol.4, No.06: 36-42 (doi: 10.5376/ija.2014.04.0006)


The concentrations of heavy metals (Cd, Cr, Ni, Pb, Cu, Zn, Fe, and Sr) were detected by ICP-OES in muscle tissues and gills of Nile Tilapia (O. niloticus) collected from the effluent of sewage treatment plant, and the released sewage-treated water into the White; and in water samples collected from four station along the sewage treatment plant. The highest concentration of the heavy metal in tissues and gills of was recorded for Sr, followed by Fe, Zn, Cu and Pb, where Sr and Fe recorded higher concentrations in the muscle compared to fish gills. The same trend was found in the other heavy metals. The range of Fe was (10.6 – 11.6 µg/g) in water from sampling stations, with no significant difference between the four stations, while, the level was (2.2 - 3.2 µg/g) in muscle and fish gills. The level of Sr in water was (6.32 – 7.86 µg/g) with increased concentration in station 4, the discharge point of the treated waste-water into the WN; and (2.1 -3.4 µg/g) in muscle and fish gills. The concentration of lead was (0.11 – 0.2 µg/g) in water with the highest level in station 3, the discharge point of industrial effluents and (0.2 – 0.3 µg/g). The level of Zn was (0.5 - 0.9 µg/g) in muscle and fish gills, and (<0.0001 µg/g), but long-term disposal of wastewater into the Nile resulted in high level of Zn and Cu in the tissues and gills of the fish. In conclusion, the levels heavy metals observed in the fish and water samples can be considered as a serious matter of concern as it may be consumed and be harmful to human health in the study area. More safe and economic methods for the elimination of heavy metals from contaminated waters are needed and continuous assessment of the level of pollution of the Nile waters and fish with heavy metals is also necessary. 

Heavy metals; Nile Tilapia; Sewage-water; White Nile

1 Introduction
Heavy metals are potentially harmful to most organisms at some level of exposure and adsorption. Heavy metals may enter the aquatic systems from different natural and human activities sources, including industrial or domestic wastewater, application of pesticides and inorganic fertilizers, leaching from landfills, shipping and harbor activities and atmospheric deposits and geological weathering of the earth crust (Yilmaz, 2003; Marcovecchio, 2004; Nadafi and Saeed, 2006; Yilmaz, 2009). Heavy metal ions do not degrade into harmless end products and will be toxic to many life forms (Adham et al., 1999; Gupta et al., 2001; Kadirvelu et al., 2001; Olaifa et al., 2004; Ajayan et al., 2011; Paulami and Banerjee, 2012). Due to their toxicity and accumulation in biota, determination the levels of heavy metals in commercial fish species have received considerable attention in different countries (Kalfakakon and Akrida-Demertai, 2000; Papagiannis et al., 2004; Mohamed and Gad, 2008; Klavins et al., 2009; Ozturk et al.,  2009; Olowu et al., 2010; Ambedkar and Muniyan, 2011; Wariaghli et al., 2013). There has been an increasing interest in the utilization of fishes as bio-indicators of the integrity of aquatic environ- mental systems in recent years (Rashed, 2001a; Ogbeibu and Ezeunara, 2002; Tawari and Ekaye, 2007). Fish lie at the top of the aquatic food chain and may concentrate large amounts of some metals from the water. Fish take heavy metals from the surrounding water through their gills which are the primary route for the uptake of water borne pollutants and accumulate them in their tissues (Allen and Wilson, 1991). The fish diet is another source of these pollutants in the tissues. WHO (1996) reported that copper toxicity in fish is taken up directly from the water via gills and stored in the liver. Therefore, they are the most indicative factor for the estimation of pollution and risk potential of human consumption (Authman, 2008; Ekeanyanwu et al., 2011).
Several studies have indicated enhanced levels of both non-essential and essential heavy metal load in muscle and liver tissues of fishes (Ogbeibu and Ezeunara, 2002; Ekpo et al., 2008) The concentration of heavy metal were found to be higher in the liver, kidneys and gills than in the gonad and muscle tissues some fish species (Mohamed, 2005; Sabo et al., 2008) and the concentrations in the tissue of freshwater fish vary considerably among different studies.
With the increased urbanization and industrialization in Khartoum, there has been a rapid increase in the municipal waste water (sewage water and industrial effluents), which in turn has intensified the environmental pollution. Huge amount of heavy metals is released in the Nile waters from the sewage treatment plant and industrial wastewater, where there may have been metal deposits. Effluents discharged into Nile may affect aquatic organism and fish, either directly or indirectly. Tilapia nilotica (O. niloticus) is one of the aquatic organisms affected by heavy metals, so in many caseswas used as metal biological marker in toxicological studies (Mohamed et al., 1990; Prusty, 1994; Rashed, 2001b). This fish is exposed to continuous wastewater and industrial effluents discharged into the White Nile. Therefore, the present work aimed to detect the pollutants levels of the heavy metals: Cadmium (Cd), Chromium (Cr), Nickel (Ni), Lead (Pb), Copper (Cu), Zinc (Zn), Iron (Fe) and Strontium (Sr) and their accumulation in the muscle tissues and gills of the commercially important Nile fish (Oreochromis niloticus) as well as in sewage- treated water from where fish was collected for the study.
2 Materials and Methods
2.1 Study area
The sewage rehabilitation project consists of three major ponds, located south of Khartoum state between lat. 15°35′ long., 32°33′ alt. (Figure 1). The dimensions of the primary pond were 100×170×3m; the secondary pond 239.1×785×1.2m and the tertiary pond 239.1×220×1.2m. The waste water from the tertiary pond is released in one common canal of 3m width. On its way this canal received the waste water from the military factories and flow straight to release its contents in the White Nile at Al-Ozozab city in Khartoum west.



Figure 1 Fish (St 1 & 5) and water sampling points (St1~5) from the wastewater of the sewage-treatment plant in south of Khartoum State.


2.2 Fish and water samples collection
Fish samples of the Nile Tilapia (Oreochromis niloticus, Linnaeus, 1758; Trewavas, 1983) of about the same size (length ±5”) were collected at two points (Figure 1): from the effluent discharge canals of the sewage treatment plant (St 1) and from the effluent discharge point of the sewage-treated water into the White Nile (St 5). Fish specimens were immediately preserved on ice prior to heavy metal analysis.
Water samples were collected from a depth 15 cm from four stations (Figure 1) in the sewage treatment canals (one sample from each) using automated water sampler (21 cc capacity) and stored in amber-coloured polyethylene bottles (1 L) pre-washed with 1 (N) HNO3 and deionised water. To prevent further oxidation or any fungal growth 5mL concentrated HNO3 was added to the sampled water.
2.3 Samples treatment and analysis
Fish muscle tissues and gills were taken from each specimen after removing the scales and skin, and each was cut into small pieces, ground well thoroughly to achieve homogeneity and used to prepare the ash solution for ICP-OES analysis. About 4g of the each sample were kept in muffle furnace on a hot plate at 550℃ for 3 hours to obtain the ash. Ash was dissolved in 10 ml of 20% HCl then filtered in a 100ml volumetric flask and the volume was completed with distilled water to 50ml. Each ash solution was analyzed for heavy metals: Cadmium (Cd), Chromium (Cr), Nickel (Ni), Lead (Pb), Copper (Cu), Zinc (Zn), Iron (Fe) and strontium (Sr) using ICP-OES.Water samples were not subjected to any further treatment and were also analyzed for the same heavy metals using ICP-OES. The concentration of each metal was detected in a triplicate ash samples of fish muscles and gills as well as water samples, and recorded in ppm (μg/g, μg/L) according to APHA (1998).

3 Results and Discussion
3.1 Concentrations of heavy metals in fish samples
The concentrations of heavy metals (Cd, Cr,Ni, Pb, Cu, Zn, Fe, and Sr) determined in fish muscle tissues and gills at the two sampling points are given in Table 1. The highest concentration of the heavy metal in muscle tissues and gills of was recorded for Sr, followed by Fe, Zn, Cu and Pb, where Sr and Fe recorded higher concentrations in the muscles compared to the gills of fish samples collected from both points: the main canal of treated waste-water, and the discharge area of the treated waste-water into the White Nile (Figure 2). The same trend was found in the other heavy metals.



Table 1 Concentration heavy metals ppm (µg/g) in muscle tissues and gills of O. niloticus at two sampling points.



Figure 2 Mean metal (Sr, Fe, Zn, Cu and Pb) concentrations (µg/g) in muscles and gills of fish collected from sewage-treatment canals (1) and the White Nile (2) at the discharge of sewage- treated waste water. 


3.2 Concentration of heavy metals in water samples
The water samples at each sampling point were also analyzed by using ICP-OES. The concentration of Fe and Sr was very high in all sampling stations (Table 2). The range of Fe was (10.6 – 11.6 ppm) with no significant difference between the four sampling stations, while the range of Sr was (6.32 – 7.86 pppm) with increased concentration in station 4, the discharge point of the treated waste-water (Figure 3). The concentration Zn and Cu was very low and below the detection limit in all sampling stations, while the concentration of Ni, Cr and Cd was a pit higher. Lead was detected in the four stations (0.11 – 0.2 ppm) with the highest level in station 3, the discharge point of industrial effluents.



Table 2 Concentration heavy metals (p.p.m.) in water from four sampling stations along the sewage-treatment canal.



Figure 3 Mean metal (Fe, Sr, Pb, Cr and Cd) concentrations (µg/L) in water samples from four stations along the canals of sewage-treatment.


The above data indicated the order of heavy metals accumulation in fish muscles and gills was Sr > Fe > Zn > Cu > Pb > Ni > Cr > Cd for samples of fish from both points of collection, while the concentrations of heavy metals in the water collected from four stations through the waste-treatment canal had the order Fe > Sr > Pb > Cr > Cd > Ni > Cu > Zn. The trend of accumulation suggested deposition was maximum for Sr and iron, and minimum for cadmium in the muscles and gills of fish samples. In water samples, the concentration of Fe and Sr was very high in St (1), the beginning of the canal, where effluent from different sources are discharged, then the level came down at St (2), the end of the waste-water canal. At St (3) the industrial effluents from the military factory are released into the canal. This situation explains why the concentrations of these metals were high at St (3), and consequently, their levels in the water increase at St (4), which is released into the White Nile.  The water condition was also very muddy caused by the effluent discharge into the water. 
Although some metals such as Zn and Cu were high in the tissues and gills of the fish, they are very low and below the detected limits in the water from where the fish samples were collected. This however is in agreement with a study in Turkey andMalaysia, where the concentration of heavy metals in fish was high even the concentration of heavy metals in the water was low (Ismaniza and Saleh, 2012). It was reported that Ca, Mg, Fe, Cu, Zn and Pb exhibited bio-accumulation from water to fish (Kalfakakon and Akrida-Demertai, 2000; Irwandi and Farida, 2009). They demonstrate that metal concentrations in fish are higher than in water, which indicates the bio-accumulation. The main reason is the long-term disposal of sewage-treated water into the Nile, which results in the accumulation of toxic heavy metals in river water, and may adversely affect the growth of various aquatic vertebrates and invertebrates including fishes. Ayotunde and Offen (2012) found a level of (0.02 to 0.04 mg/kg) of lead in muscle tissues of some species of freshwater fish from Cross River in Nigeria and Oladimeji and Offen (1989) noticed in O. niloticus, that the gills consistently accumulated higher amount of lead as lead nitrate. Lead is highly toxic to aquatic organisms, especially fish (Rompala et al., 1984). The biological effects of sublethal concentrations of lead include delayed embryonic development, suppressed reproduction, and inhibition of growth, increased mucous formation, neurological problems, enzyme inhalation and kidney dysfunction (Leland and Kuwabara, 1985). The level of lead in muscle and gills of O. niloticus was below the (0.5μg/g) limits. The accumulation of both cadmium and chromium was higher in muscles compared to fish gills. Dural et al. (2007) reported highest levels of cadmium, lead, copper, zinc and iron in the liver and gills of fish species viz. Sparus aurata, Dicentrachus labrax, Mugil cephalus and Scomberomorus cavalla. Yilmaz et al. (2007) reported maximum accumulations of cadmium, cobalt and copper in the liver and gills of Leuciscus cephalus and Lepornis gibbosus, while these accumulations were least in the fish muscle. However, as could be deduced from the present study, the muscles accumulate more of these metals. Both Cd and Cr are toxic elements which have no known biological function and show their carcinogenic effect on aquatic biota and humans. Cadmium is widely distributed at low levels in the environment and is not an essential element for humans, animals and plants. The European and National Drinking Water Quality Standards maximum residue limit (MRL) permitted in fish is 0.3 µg/g for Pb and 0.1 µg/g for Cd (WHO, 1996).
High level of Cu was also detected in both muscle and fish gills. For the gills samples, it may be due to the fact that freshwater fish’s gills might be expected to be the primary route for the uptake of water borne pollutants. WHO (1989) reported that copper toxicity in fish is taken up directly from the water via gills and stored in the liver, the present study showed accumulation of copper in the gills and muscles.
However, toxic heavy metals are available to aquatic environment from various sources of industrial effluents. Fish may uptake heavy metals from water, food or sediment and therefore can easily enter or transported to the food chains (Kalfakakon and Akrida-Demertzi, 2000). The efficiency of metal uptake from contaminated water may differ in relation to ecological needs, metabolisms, and the contamination gradient of water, food and sediment as well as other environmental factors such as salinity, temperature and interacting agent (Al-Weher, 2008; Rauf et al., 2009). When fish are exposed to elevated metal levels in an aquatic environment, they can absorb the available metals directly from the environment via the gills and skin or through the ingestion of contaminated water and food, thus accumulates them in their tissues and enter the food chains and extent to many other problems to humans (Ahmad and Othman, 2010).
Although, the concentrations of heavy metals Zn, Cu, Pb, Ni, Cr and Cd determined were very low and below the detection limit, the continuous discharge from the sewage treatment plant into the White Nile might be the contributor of heavy metal accumulation and other possible pollutants in the fish samples. The high load of heavy metals is due to the presence of major sources of metal pollution, intensive human activity and discharge of municipal waste and industrial effluents. In conclusion, the levels of Fe, Sr, Zn, Cu, Pb, Cr and Cd observed would have harmful effect on the health of the community in the study area. Heavy meals are one of the more serious pollutants in our natural environment due to their toxicity, persistence and bioaccumulation problems, thus fish species will not be safe for human consumption. Despite its extensive treatment processes for heavy metal removal from wastewater residues, heavy metals remain in the waster and absorbed by fish. The concentrations of heavy metal in the tissue of freshwater fish vary considerably among different studies.Therefore, there should be a continuous assessment of pollution with metals from the mentioned sources in the Nile water and other commercial Nile fish, with a view to reducing the level of pollution via education and public enlightenment. Fish can be considered as an index of metal pollution in the aquatic bodies (Dural et al., 2007; Anim et al., 2011), and therefore, could be a useful tool to study the biological role of metals present at higher concentrations in different species of the Nile fish.
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