Bioaccumulation of Some Potentially Toxic Heavy Metals in Freshwater Fish of River Shah Alam, Khyber Pakhtunkhwa, Pakistan

Hazrat Ali1,2,*, Ezzat Khan1,* and Muhammad Jamal Nasir3

1Department of Chemistry, University of Malakand, Chakdara 18800, Dir Lower, Khyber Pakhtunkhwa

2Green & Environmental Chemistry, Ecotoxicology and Ecology Laboratory, Department of Zoology, University of Malakand, Chakdara 18800, Dir Lower, Khyber Pakhtunkhwa

3Department of Geography, University of Peshawar, Peshawar, Khyber Pakhtunkhwa

ABSTRACT

The present study was designed to assess the concentrations of Cr, Ni, Cd and Pb in water, sediments and different fish species of River Shah Alam, a tributary of River Kabul in Khyber Pakhtunkhwa, Pakistan. The different environmental samples were collected from the river, downstream the city of Peshawar, and analyzed for the selected heavy metals by atomic absorption spectrophotometry. Heavy metal accumulation was studied in muscles of six fish species collected from the river. Heavy metal accumulation was also studied in other tissues such as skin, gills, liver and kidneys of two fish species i.e., Clupisoma naziri and Mastacembelus armatus. Cr concentrations in fish muscles ranged from 30.5±41.9 to 70.8±12.1 mg kg−1 wet weight, Ni from 16.7±10.2 to 103.5±114.1 mg kg−1 wet weight, Cd from 1.1±0.18 to 2.5±0.21 mg kg−1 wet weight and Pb from 29.7±18.3 to 97.7±95.4 mg kg−1 wet weight. Metal concentrations in muscle samples of the different six fish species showed random variations. Inter-species differences were statistically not significant, most probably due to more variance within samples. Comparative metal accumulation in the five different tissues of C. naziri and M. armatus did not show a consistent trend across the studied tissues.

Article Information

Received 17 November 2017

Revised 22 June 2018

Accepted 30 January 2019

Available online 20 January 2020

Authors’ Contributions

HA and EK conceived and designed the study. HA collected, prepared and analyzed the samples. HA analyzed the data and wrote the manuscript. MJN contributed to data analysis. EK supervised the research work.

Key words

Bioaccumulation, Fish, Heavy metals, River Shah Alam, Sediments, Water.

DOI: https://dx.doi.org/10.17582/journal.pjz/20171117161138

* Corresponding authors: hazrataliuom@gmail.com;

hazratali@uom.edu.pk; ekhan@uom.edu.pk

0030-9923/2020/0002-0603 $ 9.00/0

Copyright 2020 Zoological Society of Pakistan

Introduction

Heavy metals released into the environment from a variety of natural and anthropogenic sources. Vehicle traffic is among the major anthropogenic sources of heavy metals such as Cr, Zn, Cd and Pb (Ferretti et al., 1995). Environmental monitoring of river water is important for protecting aquatic life (Ebadi and Hisoriev, 2017). Assessment of heavy metal accumulation in fish is important from public health point of view because of their consumption by humans (Ali et al., 2017).

Cd and Pb are biologically non-essential heavy metals. Cd is among the most toxic heavy metals (Bernard, 2008). A recent study conducted in China on a large adult population has found an association between blood Pb levels and an increased prevalence of cardiovascular diseases (CVD) (Chen et al., 2017). Apart from affecting the fish consumers, heavy metals also affect the exposed fish. Exposure of fish to heavy metals disrupts secretion of reproductive hormones and causes pathological changes (Ebrahimi and Taherianfard, 2011). Cr causes biochemical, hematological and behavioral changes in fish (Aslam and Yousafzai, 2017). It has been found that exposure to Cr changed locomotor behavior in the fish Gambusia affinis. It also caused adverse effects such as morphological changes, necrosis and periodic hemorrhages in the gills of the exposed fish (Begum et al., 2006). It has been reported that exposure to Pb at sublethal concentrations has a potential immuno-suppressor effect on tilapia fish (Oreochromis mossambicus) (Kaya et al., 2013).

Industrialization and urbanization as well as rapid population growth and economic development have caused deterioration of environmental quality and contamination of freshwater ecosystems with various toxic chemicals including heavy metals. Rivers are freshwater ecosystems, which are much vulnerable to environmental changes and pollution. River Shah Alam is a severely polluted tributary of River Kabul (Khan et al., 1999), which receives wastewaters from different industries including distilleries, ghee mills, paper mills, sugar mills, tanneries, and textile mills (Khan et al., 2011). The present study was designed to assess the concentrations of four heavy metals i.e., Cr, Ni, Cd and Pb in the water, sediments and different freshwater fish of River Shah Alam, Khyber Pakhtunkhwa, Pakistan. Accumulation of the selected heavy metals was studied in muscles because this tissue is the edible part of the fish and is the most important from human health point of view. However, comparative metal accumulation was also studied in different tissues of two fish species i.e., Clupisoma naziri and Mastacembelus armatus.

 

Materials and methods

River Shah Alam is a tributary of River Kabul, and receives sewage from Peshawar city through Ganda Erab and Budni Nalla and from 30 villages in the surroundings. Therefore, River Shah Alam is considered as a more polluted river (Khan et al., 2012). A map of the study area showing the sampling site is given in Supplementary Figure S1.

Water, sediment and fish samples were collected at the sampling site (34°04′04″N and 71°38′54″E) on River Shah Alam. This sampling site was selected because it is downstream to the point where Budni Nalla, carrying polluted water from Peshawar, joins River Shah Alam. The environmental samples were collected according to Csuros and Csuros (2002) and transported to the laboratory with proper care and arrangements. Water samples were prepared according to Malik and Maurya (2014), sediment samples were digested according to Jan et al. (2010) while the fish samples were digested according to Javed and Usmani (2016) with modifications. A 50 mL water sample was acidified with 5 mL concentrated HNO3 and evaporated at 80°C on a hot plate until its volume was reduced to 50 mL. After filtration, the water sample was taken in a 50 mL volumetric flask. Sediment samples were air dried and passed through a less than 2 mm sieve. A 0.5 g dried and finely powdered sediment sample was digested with 10 mL aqua regia (HCl:HNO3, 3:1 ratio). Fish muscle samples were taken from the dorsal side, behind the dorsal fin. A 1.0 g muscle sample (wet weight basis) was digested with a 10 mL mixture of HNO3 and HClO4, 3:1 ratio. Digestion was carried out at 80°C on a hot plate. The four selected heavy metals i.e., Cr, Ni, Cd and Pb were quantified in the prepared samples with Flame Atomic Absorption Spectrophotometer (Perkin-Elmer Model No. 2380). Quality assurance tests were done to establish the reliability of metal analysis (Supplementary Table I).

Results are shown as mean±standard deviation, from three independent experiments. Data were analyzed with SPSS version 16. Mean metal concentrations at different study sites were compared using One-Way ANOVA (Tukey Test). A p-value of 0.05 was considered for statistical significance.

 

Results and discussion

Table I shows the concentrations of the four heavy metals in the water and sediments of River Shah Alam. The concentrations of these metals in both water and sediments followed the order: Ni > Cr > Pb > Cd. Previously, Khan et al. (2011) have reported the concentrations (mg L−1) of heavy metals in water of River Shah Alam as: Cr (0.02), Ni (0.65), Cd (0.03), and Pb (0.09), which are lower than the current levels. Usman et al. (2017) have reported Cr, Cd and Pb concentrations of 0.04-2.0, 0.2-0.69 and 1.0-1.2 mg L−1, respectively in water of River Shah Alam, which are higher than our reported concentrations. Tabinda et al. (2013) have reported Cr and Ni concentrations of 0.16 ± 0.89 and 0.04 ± 0.03 mg L−1, respectively in water from River Sutlej, Pakistan, which are lower than our reported concentrations. Ebadi and Hisoriev (2017) have reported Cr, Cd and Pb concentrations of 2.1-4.6, 0.01-0.59 and 1.9-4.2 mg L−1, respectively in water from different sites of Tajan River, Iran; these values are also higher than our reported concentrations.

 

Table I.- Concentrations (mean ± SD, n=3) of four potentially toxic heavy metals in water and sediments of River Shah Alam, Khyber Pakhtunkhwa, Pakistan.

Metal	Concentration in water (mg L−1)	Concentration in sediments (mg kg−1 dry weight)
Cr	0.80 ± 0.32	47.0 ± 20.9
Ni	2.4 ± 1.0	159.3 ± 150.8
Cd	0.05 ± 0.02	4.4 ± 0.42
Pb	0.44 ± 0.15	36.3 ± 19.1

 

Tabinda et al. (2013) have reported Cr and Ni concentrations of 35.0 ± 7.3 and 21.8 ± 5.2 ppm respectively in sediments from River Sutlej, Pakistan, which are lower than our reported concentrations. Miri et al. (2015) have reported Cd, Ni and Pb concentrations of 0.22-5.8, 10.0-17.6 and 5.6-14.9 ppm, respectively in sediments of Chabahar Bay, Iran, which are also lower than our reported concentrations. Metal concentrations in both water and sediments depend on several factors and fluctuate from site to site due to their variable natural and anthropogenic sources. The anthropogenic sources of the selected heavy metals in the study area are agricultural run-off, domestic sewage and industrial effluents.

Table II shows metal concentrations in muscles of the different fish species. Metal concentrations in muscle samples of the different six fish species showed random variations. A high degree of randomness in heavy metal distribution has also been reported in the muscles of different six fish species from five freshwater lakes of Pakistan (Tariq et al., 1991). Inter-species differences were statistically not significant, most probably due to more variance within samples. Table III shows a comparison of concentrations of the four potentially toxic heavy metals in muscles of fish reported by the present study with those reported in fish from some other freshwater bodies.

Our reported heavy metal concentrations in fish muscles are generally higher than or comparable to those reported by the above-mentioned studies. However, our reported heavy metal concentrations are lower than those reported by Siraj et al. (2014) in muscles of fish collected from River Kabul near Nowshera. Similarly, Ahmad et al. (2015) have reported heavy metal concentrations, much higher than our reported values, in muscles of different edible fish species from River Kabul. Thus, our reported concentrations are lower than those reported by these two studies from River Kabul, Pakistan, the most relevant river for River Shah Alam. As mentioned in the introduction, River Shah Alam is a tributary of River Kabul; both are relatively polluted water bodies in the province because they receive industrial effluents, domestic sewage and agricultural run-off from Peshawar and adjacent areas.

 

Table II.- Metal concentrations (mean ± SD, n = 3) in muscles of different fish species from River Shah Alam, Khyber Pakhtunkhwa, Pakistan.

Fish species	Metal concentration (mg kg−1 wet weight) in muscles
	Cr	Ni	Cd	Pb
Barilius vagra	40.2 ± 39.4	58.3 ± 39.9	1.9 ± 0.94	29.7 ± 18.3
Clupisoma naziri	31.0 ± 28.5	103.5 ± 114.1	2.5 ± 0.21	62.7 ± 51.9
Glyptothorax cavia	30.5 ± 41.9	78.0 ± 53.2	1.5 ± 0.52	57.2 ± 49.5
Glyptothorax punjabensis	32.2 ± 21.0	99.7 ± 44.3	2.0 ± 0.76	40.5 ± 30.1
Mastacembelus armatus	57.5 ± 12.5	72.7 ± 93.0	1.4 ± 0.28	97.7 ± 95.4
Notopterus chitala	70.8 ± 12.1	16.7 ± 10.2	1.1 ± 0.18	51.0 ± 46.5

 

Table III.- Comparison of concentrations of the four potentially toxic heavy metals in muscles of fish reported by the present study with those reported in fish from some other freshwater bodies.

Country	Freshwater body	Fish species	Concentration (μg g−1)				Reference
			Cr	Ni	Cd	Pb
Bangladesh	Buriganga river	Puntius ticto ww	5.5 ± 1.5	1.6 ± 0.27	—	—	Ahmed et al. (2016b)
		Puntius sophore ww	4.3 ± 1.4	1.2 ± 0.30	—	—
		Puntius chola ww	3.6 ± 1.6	1.0 ± 0.52	—	—
		Labeo rohita ww	18.8 ± 1.7	6.6 ± 0.24	—	—
		Glossogobius giuris ww	5.1 ± 1.0	0.73 ± 0.19	—	—
India	River Ganga	Mastacembelus armatus ww	19.7 ± 1.1	4.6 ± 0.9	4.4 ± 0.9	30.3 ± 6.4	Pandey et al. (2017)
Pakistan	Tarbela Lake	Catla catla	0.17 ± 0.03	0.26 ± 0.06	—	0.16 ± 0.04	Ahmed et al. (2016a)
		Cyprinus carpio	0.23 ± 0.07	0.22 ± 0.05	—	0.23 ± 0.03
		Tor putitora	0.18 ± 0.02	0.18 ± 0.02	—	0.18 ± 0.02
Pakistan	River Swat	Oncorhynchus mykiss	0.23 ± 0.06	0.19 ± 0.02	—	0.16 ± 0.04	Ahmed et al. (2016a)
Pakistan	River Kabul	Wallago attu	533.3 ± 206.1	106.7 ± 6.8	68.0 ± 15.0	599.3 ± 188.3	Ahmad et al. (2015)
		Cyprinus carpio	489.0 ± 49.7	74.7 ± 17.3	53.3 ± 2.9	226.3 ± 222.2
		Labeo dyocheilus	647.3 ± 105.1	117.7 ± 33.5	66.7 ± 8.5	528.7 ± 236.4
Pakistan	River Kabul	Aorichthys seenghala ww	565.3 ± 148.7	94.7 ± 33.3	60.7 ± 17.2	350.7 ± 37.2	Siraj et al. (2014)
		Ompok bimaculatous ww	703.0 ± 125.3	135.0 ± 52.6	71.7 ± 12.1	407.0 ± 126.6
Pakistan	River Sutlej	Cirrhina mrigala	2.0 ± 0.74	1.3 ± 0.67	—	—	Tabinda et al. (2013)
		Labeo rohita	1.8 ± 0.84	1.2 ± 0.50	—	—
		Catla catla	1.5 ± 0.49	1.1 ± 0.72	—	—
Pakistan	Freshwater lakes	Six fish species ww	0.12-2.3	0.14-2.7	0.02-1.2	0.06-4.1	Tariq et al. (1991)
Pakistan	River Shah Alam	Six fish species ww	30.5-70.8	16.7-103.5	1.1-2.5	29.7-97.7	Present study

ww, wet weight.

 

Apart from assessment of heavy metal levels in fish muscles from natural water bodies such as rivers and lakes, some studies have investigated levels of heavy metals in fish from commercial fish farms. For example, Nawaz et al. (2010) have reported Cd concentrations in fish muscles as 0.40 and 0.35 µg g−1 in edible and non-edible fish respectively from River Ravi, Pakistan while 0.45 µg g−1 in edible farmed fish from fish farms at Manawan, Lahore. Their reported Pb concentrations in fish muscles were 2.7 and 2.1 µg g−1 in edible and non-edible fish, respectively from River Ravi, Pakistan while 3.0 µg g−1 in edible farmed fish from fish farms at Manawan, Lahore.

Figure 1 shows the comparative accumulation of the four heavy metals in different tissues of C. naziri and M. armatus. Among fish tissues, usually higher metal accumulation is observed in metabolically active tissues such as liver, kidneys and gills as compared to muscles. In this study, metal concentrations in different tissues of the two studied fish species followed the following order; for C. naziri: Cr, gills > kidneys > liver > skin = muscles; Ni, skin > liver > gills > kidneys > muscles; Cd, muscles > liver > kidneys > skin > gills; Pb, muscles > liver > gills > skin > kidneys; for M. armatus: Cr, kidneys > gills > muscles > skin > liver; Ni, kidneys > gills > muscles > liver > skin; Cd, kidneys > liver > gills > muscles @ skin; Pb, kidneys > muscles > liver > skin > gills.

Rauf et al. (2009) have reported highest Cd and Cr accumulation in liver among six fish tissues for three major carps from River Ravi, Pakistan. Mohammadi-Rouzbahani (2017) has also reported gills and liver as the target tissues for accumulation of heavy metals in two fish species from the Persian Gulf, Iran. Khan et al. (2012) have reported heavy metal concentrations in different fish tissues as: liver ≥ gills > muscles. Ahmed et al. (2016a) have found higher heavy metal accumulation in liver and skin than in gills and muscles.

Yousafzai and Shakoori (2008) have reported heavy metals concentrations (µg g−1 wet weight) in gills of the freshwater fish Tor putitora at control, polluted site 1 and polluted site 2 respectively of River Kabul, Pakistan as: Cr (5.3±0.18, 6.6±0.07 and 6.0±0.38); Ni (53.3±8.4, 128±8.8 and 133±7.3); Pb (219.3±31.4, 313.7±29.9 and 321±9.8). These values are lower (Cr), comparable to (Ni) and higher than (Pb) our reported metal concentrations in gills of C. naziri and M. armatus.

 

Conclusions

Metal concentrations in muscle samples of the different six fish species showed random variations. A high degree of randomness in heavy metal distribution has also been reported in the muscles of different fish species from other freshwater bodies of Pakistan. Inter-species differences were statistically not significant, most probably due to more variance within samples.

Comparison with similar studies done in Pakistan shows that heavy metal levels reported in fish muscles by this study are generally higher than or comparable to those reported from other neighborhood rivers. However, our reported concentrations are lower than those reported by two studies from River Kabul, Pakistan, the most relevant river for River Shah Alam. As mentioned in the introduction, River Shah Alam is a tributary of River Kabul; both are relatively polluted water bodies in the province because they receive industrial effluents, domestic sewage and agricultural run-off from Peshawar and adjacent areas. Regarding tissue-specific metal accumulation, the five different tissues of C. naziri and M. armatus did not show a consistent trend across the studied tissues.

 

Acknowledgements

The authors are thankful to Prof. Dr. Rup Lal, Professor at Department of Zoology, University of Delhi, India, for gifting a copy of standard literature keys for fish identification and to Mr. Abdur Rahman, Lecturer in Zoology, and Fisheries Specialist at Department of Zoology, University of Malakand, for his help in fish identification. Dr. Muhammad Anwar Sajad, Department of Botany, Islamia College Peshawar, is also gratefully acknowledged for his cooperation in metal analysis. The authors are also thankful to the anonymous reviewer whose comments and suggestions greatly improved the quality of the manuscript.

 

Supplementary material

There is supplementary material associated with this article. Access the material online at: https://dx.doi.org/10.17582/journal.pjz/20171117161138

 

Statement of conflict of interest

The authors declare no conflict of interest.

 

References

Ahmad, H., Yousafzai, A.M., Siraj, M., Ahmad, R., Ahmad, I., Nadeem, M.S., Ahmad, W., Akbar, N. and Muhammad, K., 2015. Pollution problem in River Kabul: Accumulation estimates of heavy metals in native fish species. BioMed Res. Int., 2015. Article ID 537368. https://doi.org/10.1155/2015/537368

Ahmed, M., Ahmad, T., Liaquat, M., Abbasi, K.S., Farid, I.B.A. and Jahangir, M., 2016a. Tissue specific metal characterization of selected fish species in Pakistan. Environ. Monitor. Assess., 188: 212. https://doi.org/10.1007/s10661-016-5214-6

Ahmed, M.K., Baki, M.A., Kundu, G.K., Islam, M.S., Islam, M.M. and Hossain, M.M., 2016b. . Human health risks from heavy metals in fish of Buriganga river, Bangladesh. SpringerPlus, 5: 1697. https://doi.org/10.1186/s40064-016-3357-0

Ali, H., Ali, W., Ullah, K., Akbar, F., Ahrar, S., Ullah, I., Ahmad, I., Ahmad, A., Ilahi, I. and Sajad, M.A., 2017. Bioaccumulation of Cu and Zn in Schizothorax plagiostomus and Mastacembelus armatus from River Swat, River Panjkora and River Barandu in Malakand Division, Pakistan. Pakistan J. Zool., 49: 1555-1561. https://doi.org/10.17582/journal.pjz/2017.49.5.1555.1561

Ali, H. and Khan, E., 2018. Environmental chemistry in the twenty-first century. Environ. Chem. Lett., 15: 329-346. https://doi.org/10.1007/s10311-016-0601-3

Ali, H. and Khan, E., 2017b. What are heavy metals? long-standing controversy over the scientific use of the term ‘heavy metals’—proposal of a comprehensive definition. Toxicol. environ. Chem., 100: 6-19. https://doi.org/10.1080/02772248.2017.1413652

Aslam, S. and Yousafzai, A.M., 2017. Chromium toxicity in fish: A review article. J. Ent. Zool. Stud., 5: 1483-1488.

Begum, G., Rao, J.V. and Srikanth, K., 2006. Oxidative stress and changes in locomotor behavior and gill morphology of Gambusia affinis exposed to chromium. Toxicol. environ. Chem., 88: 355-365. https://doi.org/10.1080/02772240600635985

Bernard, A., 2008. Cadmium and its adverse effects on human health. Ind. J. med. Res., 128: 557-564.

Chen, C., Li, Q., Nie, X., Han, B., Chen, Y., Xia, F., Zhai, H., Wang, N. and Lu, Y., 2017. Association of lead exposure with cardiovascular risk factors and diseases in Chinese adults. Environ. Sci. Pollut. Res., 24: 22275-22283. https://doi.org/10.1007/s11356-017-9200-5

Csuros, M. and Csuros, C., 2002. Environmental sampling and analysis for metals. Lewis Publishers, Boca Raton. https://doi.org/10.1201/9781420032345

Ebadi, A.G. and Hisoriev, H., 2017. Metal pollution status of Tajan River – Northern Iran. Toxicol. environ. Chem., 99: 1358-1367. https://doi.org/10.1080/02772248.2017.1345191

Ebrahimi, M. and Taherianfard, M., 2011. The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iran. J. Fish. Sci., 10: 13-24.

Ferretti, M., Cenni, E., Bussotti, F. and Batistoni, P., 1995. Vehicle-induced lead and cadmium contamination of roadside soil and plants in Italy. Chem. Ecol., 11: 213-228. https://doi.org/10.1080/02757549508039072

Jan, F.A., Ishaq, M., Khan, S., Ihsanullah, I., Ahmad, I. and Shakirullah, M., 2010. A comparative study of human health risks via consumption of food crops grown on wastewater irrigated soil (Peshawar) and relatively clean water irrigated soil (lower Dir). J. Hazard. Mater., 179: 612-621.

Javed, M. and Usmani, N., 2016. Accumulation of heavy metals and human health risk assessment via the consumption of freshwater fish Mastacembelus armatus inhabiting, thermal power plant effluent loaded canal. SpringerPlus, 5: 776. https://doi.org/10.1186/s40064-016-2471-3

Kaya, H., Akbulut, M., Çelik, E.Ş. and Yılmaz, S., 2013. Impacts of sublethal lead exposure on the hemato-immunological parameters in tilapia (Oreochromis mossambicus). Toxicol. environ. Chem., 95: 1554-1564. https://doi.org/10.1080/02772248.2013.869332

Khan, A.R., Akif, M., Wadud, S. and Khan, K., 1999. Pollution studies of Kabul River and its tributes for the assessment of organic strength and fecal coliform. J. chem. Soc. Pak., 21: 41-47.

Khan, T., Muhammad, S., Khan, B. and Khan, H., 2011. Investigating the levels of selected heavy metals in surface water of Shah Alam River (A tributary of River Kabul, Khyber Pakhtunkhwa). J. Himalayan Earth Sci., 44: 71-79.

Khan, B., Khan, H., Muhammad, S. and Khan, T., 2012. Heavy metals concentration trends in three fish species from Shah Alam River (Khyber Pakhtunkhwa Province, Pakistan). J. Nat. environ. Sci., 3: 1-8.

Malik, D.S. and Maurya, P.K., 2014. Heavy metal concentration in water, sediment, and tissues of fish species (Heteropneustis fossilis and Puntius ticto) from Kali River, India. Toxicol. environ. Chem., 96: 1195-1206.

Miri, M., Nabavi, S.M.B., Doustshenas, B., Safahieh, A.R. and Loghmani, M., 2015. Levels of heavy metals in sediments in the vicinity of Chabahar Bay desalination plant. Iran. J. Fish. Sci., 14: 876-884.

Mohammadi-Rouzbahani, M., 2017. Heavy metal concentrations in different tissues of Euryglossa orientalis, Chirocentrus nudus and sediments in Bahrekan Bay (the northwest of Persian Gulf). Iran. J. Fish. Sci., 16: 945-958.

Morgan, A.J., 1986. Calcium-lead interactions involving earthworms: an hypothesis. Chem. Ecol., 2: 251-261. https://doi.org/10.1080/02757548608080730

Nawaz, S., Nagra, S.A., Saleem, Y. and Priydarshi, A., 2010. Determination of heavy metals in fresh water fish species of the River Ravi, Pakistan compared to farmed fish varieties. Environ. Monitor. Assess., 167: 461-471. https://doi.org/10.1007/s10661-009-1064-9

Pandey, M., Pandey, A.K., Mishra, A. and Tripathi, B.D., 2017. Assessment of metal bioaccumulation in Mastacembelus armatus (eel) and exposure evaluation in human. Environ. Nanotechnol. Monitor. Manage., 7: 103-109.

Rauf, A., Javed, M. and Ubaidullah, M., 2009. Heavy metal levels in three major carps (Catla catla, Labeo rohita and Cirrhina mrigala) from the river Ravi, Pakistan. Pak. Vet. J., 29: 24-26.

Siraj, M., Shaheen, M., Sthanadar, A.A., Khan, A., Chivers, D.P. and Yousafzai, A.M., 2014. A comparative study of bioaccumulation of heavy metals in two fresh water species, Aorichthys seenghala and Ompok bimaculatous at River Kabul, Khyber Pakhtunkhwa, Pakistan. J. Biodiver. environ. Sci., 4: 40-54.

Tabinda, A.B., Bashir, S., Yasar, A. and Munir, S., 2013. Heavy metals concentrations in water, sediment and fish in River Sutlej at Sulemanki Headworks. Pakistan J. Zool., 45: 1663-1668.

Tariq, J., Jaffar, M. and Ashraf, M., 1991. Levels of selected heavy metals in commercial fish from five freshwater lakes, Pakistan. Toxicol. environ. Chem., 33: 133-140. https://doi.org/10.1080/02772249109357755

Usman, K., Zaib-un-Nisa, Gul, S., Gul, S., Rehman, H.U., Asad, M., Waqar, M., Ullah, K. and Ishaq, H.K., 2017. Contamination of heavy metals in River Shah Alam Peshawar: (A tributary of River Kabul) Khyber Pakhtunkhwa Pakistan. J. Ent. Zool. Stud., 5: 510-512.

Yousafzai, A.M. and Shakoori, A.R., 2008. Heavy metal accumulation in the gills of an endangered South Asian fresh water fish as an indicator of aquatic pollution. Pakistan J. Zool., 40: 423-430.