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Natural Sciences Journal Articles

2020 Heavy metals bio-accumulation in and catfish in Lake Rukwa ecosystem Tanzania

Mapenzi,Levinus Leonard;Shimba, Moses Joel;Moto, Edward Angelo;Maghembe, Reuben Silas;Mmochi, Aviti John

Elsevier

Mapenzi, L. L., Shimba, M. J., Moto, E. A., Maghembe, R. S., & Mmochi, A. J. (2020). Heavy metals bio-accumulation in tilapia and catfish species in Lake Rukwa ecosystem Tanzania. Journal of Geochemical Exploration, 208, 106413. http://hdl.handle.net/20.500.12661/2465 Downloaded from UDOM Institutional Repository at The University of Dodoma, an open access institutional repository. Journal of Geochemical Exploration 208 (2020) 106413

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Journal of Geochemical Exploration

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Heavy metals bio-accumulation in tilapia and catfish species in Lake Rukwa ecosystem Tanzania T ⁎ Levinus Leonard Mapenzia,b, , Moses Joel Shimbaa, Edward Angelo Motoa, Reuben Silas Maghembec, Aviti John Mmochib a Department of Biology, College of Natural and Mathematical Sciences, P.O. Box 338, University of Dodoma, Tanzania b Institute of Marine Sciences, University of Dar es Salaam, P.O. Box 668, Zanzibar, Tanzania c Department of Biological and Marine Sciences, Marian University College, P.O. Box 47, Bagamoyo, Pwani, Tanzania

ARTICLE INFO ABSTRACT

Keywords: Investigation on accumulation of selected heavy metals of Zinc, Mercury, Copper, Lead, Chromium and Nickel in Bio-accumulation sediment, water and muscle tissues of Clarias gariepinus (African catfish) and (Singida Fisher folk tilapia) fish was done in Lake Rukwa, Tanzania. Samples were obtained from transects of 100 m long extending fi Cat sh from Luika and Songwe River mouths to offshore. Water and sediment samples were collected directly from the Singida tilapia study sites while fish were obtained from fisherfolk operating in the Lake. Sampling was done in dry and wet Heavy metals seasons. Heavy metals analysis was done using the Atomic Absorption Spectrophotometry. Concentration of heavy metals was higher in catfish than in tilapia (p < 0.05). There were no significant differences in metal concentration between seasons except for Zn (p < 0.05). In this study only Zn was above standard WHO concentrations in fish muscles. Likewise, the concentrations of heavy metals were within recommended limits in water except Pb. The detected metals in sediment were above recommended limits. Other heavy metals in particular Hg, Ni and Cr were not detected in all samples. Therefore, studied fish from Lake Rukwa may threaten human health upon consumption. The detected heavy metals in water were within the maximum residual levels (MRLs) permitted by WHO. Sustainable Lake Rukwa's fish, ecosystem management and conservation are re- commended to discourage heavy metals discharge from elevating beyond permissible limits and thus prevent harmful health effects to fish consumers and water users.

1. Introduction pollutants can easily reach human through bio-magnification up the food chain (Amundsen et al., 1997), leading to diseases (Al-Yousuf and Heavy metals produced by local and commercial miners may pose El-Shahawi, 1999). The prevalence of heavy metals in measurable negative effects to the environment and living organisms. Pollution amounts across all aquatic ecosystems (Authman et al., 2015) raises an from mining activities is among the most common sources of highly important environmental concern. toxic chemical substances in aquatic and terrestrial ecosystems (Henry Afshan et al. (2014) reported that heavy metals enter fish bodies and Mamboya, 2012). Mining pollution may be due to seepage of through gills, gastro intestinal tract and the body surfaces. The metals chemicals used for gold processing through soil in mining sites into impact fish growth and reproductive potential (Per-Arne et al., 1997), aquatic ecosystems. Heavy metals may also enter aquatic ecosystems deteriorate immunity and cause pathological changes (Authman et al., through atmospheric deposition, geological weathering, agricultural, 2015). Fish respond to heavy metals either by accumulating, elimina- domestic and industrial waste discharges (Demirak et al., 2006). Heavy tion or shifting them to higher trophic levels (Shah and Altindag, 2005). metals impact fish due to their toxicity further enhanced by bio-accu- The fate of accumulated heavy metals in fish is dependent on storage mulation and bio-magnification (Afshan et al., 2014). Contaminants in and/or elimination capacity (Abdallah and Morsy, 2013). Therefore, water enter the food chain leading to negative impacts and fish mor- higher uptake with low elimination results into high accumulation of tality (Akinmoladun, et al., 2007). Heavy metal bio-accumulation in contaminants in tissues and vice versa. fish is important because fish tissues have higher uptake levels of some Pollutants that have been reported to negatively affect fish include metals e.g. arsenic and mercury (Afshan et al., 2014). Accordingly, such mercury, chromium, copper, zinc, lead and nickel. Lake Rukwa hosts a

⁎ Corresponding author at: Department of Biology, College of Natural and Mathematical Sciences, P.O. Box 338, University of Dodoma, Tanzania. E-mail address: [email protected] (L.L. Mapenzi). https://doi.org/10.1016/j.gexplo.2019.106413 Received 29 October 2018; Received in revised form 26 June 2019; Accepted 4 November 2019 Available online 06 November 2019 0375-6742/ © 2019 Elsevier B.V. All rights reserved. L.L. Mapenzi, et al. Journal of Geochemical Exploration 208 (2020) 106413

Fig. 1. A map of Lake Rukwa showing the sampling stations, data source Institute of Marine Sciences, GIS lab. variety of catfish species including Clarias gariepinus and tilapiines like heavy metals in C. gariepinus, O. esculentus, sediments and water in Lake Oreochromis rukwaensis and Oreochromis esculentus declared vulnerable Rukwa and its river inlets in Songwe District (former Chunya District), according to Cota, (2018). Therefore, the present study focused at both Songwe Region, Tanzania. We studied the metal accumulation on the sustainable management and conservation of fish resources in Lake fish species in Lake Rukwa, the work is important to the food safety and Rukwa by assessing the extent of heavy metal contamination. The environmental protection primary objective of the study was to determine the concentration of

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2. Description of the study site Table 1 Detection limits of heavy metals in fish, sediment and water. 2 Lake Rukwa is an inland lake covering an area of about 5760 km . S/No Metal Detection limit Major inlets into the Lake are Luika, Songwe, Kikamba and Yeye Rivers. The Lake lying between 8°00′S and 32°25′E is close to abandoned and 1. Hg 0.01 mg/l ongoing gold mining sites. The present study was done in the Southern 2. Cr 0.00 2 mg/l ff 3. Ni 0.009 mg/l part of the Lake covering Luika and Songwe River Mouths and o shore 4. Cu 0.001 mg/l (Fig. 1). Socio-economic activities of communities along Lake Rukwa 5. Pb 0.005 mg/l include agriculture, livestock keeping, fishing and gold mining. The lake is surrounded by varieties of terrestrial wildlife and plant species. The Lake is also gifted with aquatic biodiversity that include Table 2 hippopotamus, crocodiles, turtles and fish species. The lake experiences Maximum limits of heavy metals in fish, sediment and water as per WHO re- two seasons that are dry and wet annually. commendations. Maximum limit WHO/FEPA

2.1. Sampling methods Water mg/L Sediment mg/kg Fish mg/kg

Zn 3 0.0123 30 Five transects were established for sampling in the South of Lake Cu 1 0.025 3 Rukwa including Luika and Songwe River mouths. The rivers flow Pb 0.01 0.04 2 through abandoned mines areas; current mining and artisanal fisheries are taking place. Sampling was done twice during the dry (September–October 2016) and wet (March–May 2017) seasons. Choice 2.3. Statistical data analysis of the wet seasons based on the fact that probability that uptake of metals would be high due to River discharges and surface runoffs. All data for water quality and fish abundance were pooled followed Transects (100 m long) on the lake shore and river mouths were used by Kolmogorov–Smirnov normality and Levene homoscedasticity tests for water and sediment sampling. On each transect one sampling point respectively. The concentration of heavy metals in water, sediment, fish was set in the middle. Water samples were collected from the water tissues and water quality were found to be normally distributed and surface using three water bottles each with a capacity of 0.5 l. A grab behaved homoscedastically. Therefore, statistical analysis of the data sampler was used for sediment sampling on the shoreline of the lake. was done using one-way ANOVA in Statistica 10 software. Fish sampling was randomly done by purchasing fresh fish from fish- Accumulation of heavy metals in fish was analysed between the two erfolk while they were still fishing. Sediment sampling was done close fish species (African catfish and Singida tilapia) which are the com- to river mouths where the two rivers meet (SS1), Luika (SS2) and mercial and subsistence fish species in Lake Rukwa. Spearman corre- Songwe (SS3) river mouths stations. lation between water and heavy metals accumulation in fish was also Water quality parameters were measured in situ. These involved conducted. Fish diversity index was analysed using Primer 6 software. − conductivity (μScm1), salinity, turbidity and temperature (°C). Significant variation in heavy metals concentration of the tested sam- Salinity was measured using a hand-held salinometer (Model: YSI # 85/ ples was done following Turkey tests. 10 FT, USA), pH by a hand-held pH/mV meter (Model: SX 711), tur- bidity by secchi disc and coordinates by using GPS. The samples were 3. Results preserved in cool boxes with ice blocks and transported to the University of Dar es Salaam, Institute of Marine Sciences where they 3.1. Seasonal and spatial variability in heavy metals were stored in a freezer at −21 °C. Cu showed significant seasonal variation (p < 0.04, Table 3) with the highest concentration during the wet season. Zinc and lead did not 2.2. Laboratory analysis reveal any significant variation among seasons (p > 0.05, Table 3) while Hg, Cr and Ni were not detected in the water. On the overall, At S4 and S5 sampling stations we did not obtain sediment samples there were no significant variations in heavy metals among stations hence such two stations were not included in all analyses. All analyses (p > 0.05, Table 3). lied on S1, S2 and S3. Laboratory analyses of fish, sediments and water Lower mean temperature values were recorded during dry than the samples were done at the University of Dar es Salaam, Chemistry wet season (Fig. 2). Higher conductivity was recorded in the dry season Department. Fish tissue samples were dried at 80 °C for 12 h. Dried compared to the wet season. The water chemistry differed temporally samples were then ground in a mortar. About 5 g of dried samples were with respect to most of the parameters. However, no physical variables weighed into beakers. Then 10 ml of concentrated nitric acid was added showed any significant variation between the dry and wet seasons. followed by 10 ml concentrated sulphuric acid. The reaction was left to proceed for 30 min. Where the reaction was slow, the beaker was placed 3.2. Seasonal variability of heavy metals in sediments on a hot plate and heated at 60 °C. The mixture was allowed to cool before adding 10 ml of concentrated nitric acid followed by heating at Variation of heavy metal concentrations in sediments referred 120–150 °C until the brown fumes are finished. The reaction was al- (Fig. 3). The concentrations of heavy metals in Lake Rukwa sediments lowed to cool after which 5 ml of H2O2 was added and heated for 5 min. differed between seasons. These variations were insignificant This was repeated several times until the fumes are finished. Samples (p > 0.05; Fig. 3). The trend was Zn > Pb > Cu > Hg with Cr and were then filtered into a 50 ml volumetric flask, diluted to the mark Ni showing no detectable amounts in both seasons. Across sampling with de-ionized water prior to analysis using Atomic Absorption stations, the trend of Zn concentration was SS2 > SS3 > SS1 in dry Spectrometer (Spectrum Thermo Scientific ICE 3000 series). Maximum season while during wet season it was SS3 > SS1 > SS2. The trend of limits for heavy metals concentration in fish, water and sediments as Hg was SS2 > SS3 > SS1 during wet season and SS1 > SS2 > SS3 recommended by WHO are indicated (Table 2). The following detection during dry season. The concentration trend of Cu was SS2 > SS1 > limits were used to detect heavy metals concentration in fish tissues, SS3 during dry season and SS1 > SS2 > SS3 during wet season sediment and water (Table 1). whereas that of Pb was SS2 > SS1 > SS3 during dry season and

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Table 3 Seasonal and spatial concentrations of heavy metals (mg/L) in water where; DS and WS denote dry and wet seasons while SS1-SS3 denote sampling stations.

Seasonal variation Variation in sampling stations

Metal DS WS p SS1 SS2 SS3 p

Zn 0.75 ± 0.23 0.49 ± 0.07 0.35 0.49 ± 0.08 0.86 ± 0.33 0.49 ± 0.14 0.45 Cu 0.02 ± 0.01 0.01 ± 0.01 0.04 0.01 ± 0.004 0.014 ± 0.01 0.003 ± 0.001 0.55 Pb 0.38 ± 0.07 0.29 ± 0.04 0.36 0.3 ± 0 0.32 ± 0.03 0.37 ± 0.15 0.85

SS3 > SS1 > SS2 in the wet season. behavior (Nzeve et al., 2014). Catfish also have high percentage of fat, which leads to easier accumulation in the blubber. Accumulation of 3.3. Fish abundance and diversity heavy metals in fish also depends on exposure time and concentration of metals in the water column (Authman, 2015). In the present study Zn Common fish species were African catfish, Chiloglanis rukwaensis concentrations were about four times higher in dry season and there- (Kolokolo), Chelaethiops rukwaensis (Lake Rukwa Sardine), Singida ti- fore concentration dropped to about twice above recommended limits lapia and Rukwa tilapia. A total of 1000 individuals of the above species for both catfish and tilapia. On the other hand, Cu and Pb concentration were collected. The abundance was 600 Singida tilapia, 150 catfish, in tilapia remained within WHO recommended standard limits during 100 Rukwa, 90 kolokolo and 60 Lake Rukwa sardine, indicating that all seasons while Pb concentration was three times higher than the Singida tilapia that was introduced to the Lake is now more abundant normal recommended limits for catfish in all seasons. than other fish species (including the native – Rukwa tilapia followed Water quality parameters are essential for fish life. The highest by catfish. Shanon Wiener diversity index was used in determination of water temperature at station sampling station 4 (SS4) can be due to the fish species diversity in Primer 6 software. A one-way Analysis of heating effect as it was located afar from the lake shores (shallow wa- Similarities (ANOSIM) showed very little difference (Global R = 0.21, ters). Temperature as one of the most important water physical para- p < 0.001). However, the R values were weak and hence the post-hoc meters is closely related to latitude, altitude and season (Shimba and analysis (the similarity of percentages (SIMPER)) was not computed. Jonah, 2016). Lower temperature recorded at station SS5 was due to good cover by riparian vegetation at that location. Vegetation cover 3.4. Heavy metals concentration in fish limits solar radiation reaching the water, thus contributing to minimal fluctuations of temperature (Shimba and Jonah, 2016). The range of Heavy metals concentration was determined for the commercially temperature seen at stations SS1–SS5 was probably due to the variable important African catfish and Singida tilapia. The African catfish and heating effect of the sun. The mean pH values observed in this are in Singida tilapia samples showed significant variation in concentrations agreement with those reported in Rau, Pangani and Mkondoa River of Zn (p < 0.05, Table 4) between seasons, with higher concentration Mouths (Kaaya et al., 2015; Shimba, 2017). On the other hand, higher observed in the wet season. However, Cu and Pb concentrations were turbidity recorded may be due to heavy rainfall along with the in- not significantly different between dry and wet seasons (p > 0.05, creased run-off from nutrient rich agricultural and mining lands. Sea- Table 4). All detected heavy metals were relatively higher in wet than sonal higher conductivity values during the dry season may be due to dry season. Catfish heavy metal concentrations varied significantly poor dilution compared to the wet season. Agricultural activities have between seasons (p < 0.05, Table 4). Catfish muscles recorded sig- potential for increased ionic substances such as nitrate, chloride and nificantly higher concentration of heavy metals as compared to tilapia phosphate from fertilizers (Kaaya et al., 2015). These are more con- (p < 0.05, Table 4). centrated during dry season compared to the wet season due to dilution effect (Kaaya et al., 2015; Shimba and Jonah, 2016). Furthermore, 4. Discussion higher values of Zn, Pb and Cu in water in wet season may be due to erosion and transportation of sediments with adsorbed metals by rain ff Zn and Cu are essential for enzymatic reactions at low concentra- runo s(Obasohan et al., 2008). The concentrations of Zn and Cu in tions. People near Lake Rukwa and the associated rivers consume the water were within WHO allowable limits while Pb concentration was fish as source of food and protein. Fish species vary in the ability to bio- above recommended limits. fi accumulate heavy metals. When heavy metals accumulate in fish, there In each season, Zn concentration in sediment was signi cantly is a possibility of leading to human health concerns upon consumption. higher levels than the rest of heavy metals (Verma and Pradesh, 2015). Higher levels of heavy metals in catfish than tilapia in this study agree Zn is a vital co-factor in metabolic pathways across all forms of biodi- with Sani (2011), who reported differences in heavy metal concentra- versity. However, at levels above normal range, Zn has been linked to ff tions between the two species. Furthermore, carnivorous fish were re- eco-toxicological e ects (De Schamphelaere et al., 2004) manifested in fl ported to accumulate high levels of Pb than omnivorous (Hashim et al., phototoxicity to aquatic ora and fauna (Shaziya et al., 2015; Tytler 2014). Catfish feeds on smaller fish of other species unlike tilapia which and Ehinmidu, 2016). Accordingly, Zn concentration in the current feeds on phytoplankton (Nzeve et al., 2014). Therefore, difference in study is a course for concern and need for further monitoring of the Zn, Cu and Pb concentration in studied fish is due to their feeding ecological status of Lake Rukwa biota. The higher concentration of Zn

Table 4 ANOVA results for variation of Zn, Cu and Pb metals in catfish and Singida tilapia with standard error of the mean. Differential superscripts indicate significant variation in concentration.

Catfish Tilapia

Metal Dry season Wet season p Metal Dry season Wet season p

Conc. (mg/kg) Zn 141.2 ± 17.3a 74.37 ± 8.05b 0.001 Conc. (mg/kg) Zn 133.5 ± 12.2a 64.05 ± 4.14b 0.03 Cu 3.71 ± 1.39a 2.45 ± 0.32b 0.02 Cu 1.52 ± 0.16a 0.25 ± 0.02b 0.01 Pb 7.79 ± 1.32a 7.56 ± 2.72a 0.07 Pb 1.51 ± 0.16a 1.03 ± 1.17a 0.08

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− Fig. 2. Seasonal variations of physical parameters (mean ± SE) of the study area: A) temperature (°C); B) pH; C) Conductivity (μScm 1); D) Turbidity (NTU).

Anike, 2009; Leppänen et al., 2017). In this study sampling stations in Luika and Songwe River mouths which flow through mining sites ex- hibited higher Zn levels than the other areas (Leppänen et al., 2017). All detected heavy metal concentrations in sediment were above the re- commended limits by WHO. The results prove the impact of mines on the contamination of sediments and fish.

5. Conclusions

The average concentrations of heavy metals in fish and sediments in this study were above the WHO standards particularly Zn and Pb. The detected heavy metals of Zn, Cu and Pb are considered to be due to seepage from agricultural fields, current mining sites and abandoned mines in Songwe and Luika River Basins. A more detailed follow up study on heavy metal concentration in Lake Rukwa ecosystem is crucial to critically investigate the fate of heavy metals in fish, sediment and water. With the current results careful management of both the Lake and Rivers should be undertaken to avoid further contaminations.

Fig. 3. Variability of heavy metal concentrations in sediments across sampling Acknowledgement stations during both dry and wet seasons. This work was supported by the United Nations Educational, Scientific and Cultural Organization, UNESCO [Grant number may be from natural sources depending on the concentration in the 4500309532] to facilitate sampling expeditions and analysis of the rocks. However, higher than normal levels of Zn could also be attrib- samples under the “Abandoned Mines” project. The authors greatly uted to anthropogenic activities such as mining activities (Ezeh and appreciate the support. The authors also like to appreciate the role

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