Published online 1 March 2006
Published in J Environ Qual 35:584-589 (2006)
DOI: 10.2134/jeq2005.0222
© 2006 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Organic Compounds in the Environment
Organochlorine Residues in Fish and Water Samples from Lake Victoria, Uganda
G. N. Kasozia,
B. T. Kiremireb,
F. W. B. Bugenyic,
N. H. Kirschb and
P. Nkedi-Kizzaa,*
a Soil and Water Science Department, University of Florida, Gainesville, FL 326111-0290
b Department of Chemistry, Makerere University, PO Box 7062, Kampala, Uganda
c Department of Zoology, Makerere University, PO Box 7062, Kampala, Uganda
* Corresponding author (Kizza{at}ifas.ufl.edu)
Received for publication June 3, 2005.
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ABSTRACT
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Nile tilapia and Nile perch samples from Lake Victoria were analyzed for lindane (gamma-1,2,3,4,5,6-hexachlorocyclohexane), aldrin (1,2,3,4,10,10-hexachloro-1,4,4a,5,8,8a-hexahydro-1,4:5,8-dimethanonaphthalene), 
-endosulfan (6,7,8,9,10,10-hexachloro-1,5,5a,6,9,9a-hexahydro-6,9-methano-2,4,3- benzo(e) dioxathiepin-3-oxide), dieldrin (1,2,3,4,10,10-hexachloro-6,7-epoxy-1,4,4a,5,6,7,8,8a-octahydro-1,4,5,8-dimethanonaphthalene), DDE (p,p'-1,1-dichloro-2,2-bis-(4-chlorophenyl)ethylene), and DDT (p,p'-1,1,1-trichloro-2,2-bis-(4-chlorophenyl)ethane). No significant difference ( = 0.05) in the residue levels between fish types for lindane, -endosulfan, p,p'-DDE, p,p'-DDT, and dieldrin was observed. The aldrin levels in Nile perch (Lates niloticus) were significantly higher than the levels in Nile tilapia (Oreochromis niloticus). No difference was observed in the distribution of residues in the different parts of Nile tilapia, although a difference for p,p'-DDE was observed in the Nile perch. No significant difference was observed in the average fat content of the tissue of Nile perch and Nile tilapia; however, the distribution of fat was significantly different in the different parts of the fish, with the abdominal portion having the highest amount of fat. There was no correlation observed in this study between fat content and organochlorine concentration. Lower p,p'-DDT residues levels compared with the p,p'-DDE levels observed in this study indicate that DDT is no longer in use. The levels of organochlorine pesticide residues found in fish samples in this study were below the FAO, U.S. FDA, Australian, and German extraneous residue limits and maximum residue limits. The concentration of organochlorine residues in surface water within the Napoleon Gulf of Lake Victoria was below detection limit (0.1 µg L–1).
Abbreviations: DDT, dichlorodiphenyltrichloroethane • DDE, p,p'-1,1-dichloro-2,2-bis-(4-chlorophenyl)ethylene; ERL, extreneous residue limit • MRL, maximum residue limit • OC, organochlorine pesticide
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INTRODUCTION
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ORGANOCHLORINE PESTICIDES (OCs) are halogenated organic compounds classified as dichlorodiphenylethanes, hexachlorocyclohexanes, cyclodienes, and chlorinated benzenes. They are characterized by high persistence, low polarity, low aqueous solubility, and high lipid solubility (lipophilicity) and as a result they have a potential to bioaccumulate in fatty tissues. In this study, lindane, aldrin, -endosulfan, dieldrin, p,p'-DDE and p,p'-DDT were analyzed. Aldrin, dieldrin, and DDT are classified as persistent organic pollutants. Some studies (Kishimba et al., 2004; Calamari et al., 1995) and surveys (FAO, 2001; Wejuli and Magunda, 1998; Kiremire et al., unpublished data, 2001) indicate current use of organochlorine pesticides for agricultural and vector control programs and presence of their stockpiles within the riparian zone of Lake Victoria. The high efficacy and lower cost of OCs compared with alternative pesticides (Osibanjo et al., 1994) is the reason for their continued use in developing countries and also within Lake Victoria's riparian zone. Many of the pesticides that have been used extensively for long periods in Uganda are organochlorines (National Environment Action Plan, 1992). The pesticides DDT, the cyclodienes, and lindane were widely used in agriculture, as well as in mosquito and tsetse fly control programs from the 1940s to mid-1960s (Wandiga, 2001; Mitema and Gitau, 1990; Sserunjogi, 1974). A previous study on OC concentrations in Uganda was conducted on 13 pilot lakes (Sserunjogi, 1974). This study therefore aimed at advancing knowledge of the current levels of OCs in Lake Victoria, Uganda. The continued use of OCs in developing countries is of international concern, since their ubiquitous nature is thought to result from their persistence and ability to undergo long-distance atmospheric transport, eventually getting deposited in areas far from the point of application (Smith et al., 1993).
Lake Victoria has an area of 68 800 km2 and is the largest lake in Africa and the second largest in the world. The lake is a shallow saucer-shaped basin with a maximum depth of 84 m, and mean depth of 40 m (Welch, 1996) and is located along the equator at 0°30' N, 3°00' E and 31°39' N, 34°53' E. The pollutants entering the lake are unlikely to be rapidly reduced by dilution or outflow since the lake has a single outlet into the Victoria Nile. The OC contamination pathways to water bodies within the Lake Victoria basin are likely to be nonpoint sources via runoff, atmospheric deposition, and leaching due to agricultural applications and vector control practices. The sediments can act as a sink for the persistent contaminants whose resuspension at the sediment–water interface, especially in storm events and during lake mixing, may increase pesticide bioavailability and accumulation in the food chain. Lake Victoria is a source of potable and recreational water as well as a source of cheap, affordable protein in the form of fish. Pesticide pollution to the lake is therefore likely to pose a danger to both aquatic organisms and humans. Generally it is believed that the contaminants taken in by aquatic organisms are from water, rather than from their food, and may vary with seasonal variation in contaminant availability within the water column (DeLorenzo et al., 2002). Fish act as nonpolar media that can adsorb hydrophobic organic chemicals within the water column. Since birds and humans consume fish, this makes fish good biomonitors for xenobiotic pollutants. The ingestion of foods contaminated with persistent lipophilic pesticides can result in the accumulation of these pesticides in humans. The potential for pesticide residues to cross placental barriers (Waliszewski et al., 2000) even in trace concentrations may cause serious neonatal damage and therefore the presence of the residues should be of concern. Already OCs have been implicated in a broad range of adverse human health and environmental effects including reproductive failures and birth defects (Edwards, 1987), immune system dysfunction, endocrine disruptions, and cancers (World Wildlife Fund, 1999; Garabrant et al., 1992; Edwards, 1987).
Uganda lacks a functional registration and legislative framework and, as a result, the importation of pesticides is largely uncontrolled. The only law governing pesticide use is the Agricultural Chemical Statute of 1989, which is only crop protective and lacks adequate measures regarding storage, disposal, and safe use (National Environment Action Plan, 1993). In addition, there are no pesticide residue monitoring programs. Uganda Revenue Authority, the government agency responsible for authorizing the entry of imported chemicals, has no laboratory facilities to identify the pesticides entering the market and only classifies the imported pesticides in general terms such as insecticide, herbicide, etc., mostly for purposes of import revenue collection. The control of pesticide residues in food and establishment of national maximum pesticide residue limits is the responsibility of the Government Chemist laboratory and the National Environmental Management Authority. The setup of the Government Chemist pesticide laboratory is underway. Currently, analysis of pesticide residues in fish for export is done at a private laboratory (Chemiphar Laboratory, Kampala, Uganda).
On the Ugandan side of Lake Victoria, pesticides rank high among the most imported and most abused chemicals (Kiremire, unpublished data, 1997). Pesticides contributed the greatest percentage (29%) of chemicals imported into Uganda during 1993–1994 (Wasswa, 1997). Until recently, eutrophication was reported as a major threat to Lake Victoria (Calamari et al., 1995; Bugenyi, 1983). Nutrient enrichment and its associated blue-green algal blooms (Ochumba and Kibaara, 1989) along with an increase in aquatic weeds (mainly water hyacinth [Eichhornia crassipes (Mart.) Solms]) that cause O2 depletion were in the past responsible for fish kills. In 1998, however, illegal use of a pesticide to kill pest birds (Aryamanya-Mugisha, 1993) and poisoning and harvesting of fish by fishermen (National Environment Action Plan, 1993) were reported. Laboratory analysis traced endosulfan as the pesticide that was being used to poison the fish by local fishermen (Kasozi, unpublished data, 1998). This unscrupulous practice posed a major threat not only to the aquatic ecosystem, but also to the economy as this led to a European Union ban on fish imports from Lake Victoria. Fortunately, the ban forced the government of Uganda to fight these practices. Outside Lake Victoria, dieldrin has been detected in water and sediments of Lake Kyoga (Sserunjogi, 1974), while DDT and DDE were detected in human adipose tissues in the Kampala area (Wassermann et al., 1974). The pesticides DDT, dieldrin, and lindane were detected in cow's milk (Ejobi et al., 1994).
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MATERIALS AND METHODS
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Sampling
Sampling was conducted for 1 yr in the Napoleon Gulf of Lake Victoria, starting January 1998. Five stations (Kakira, Masese, Walukuba, Ternary, and Kiryowa) were selected within the gulf for collection of water samples (Fig. 1). Napoleon gulf is located near the town of Jinja and is the lake's only outflow. Live Nile perch (37) and tilapia (43) were collected from within the selected stations. As much as possible, similar sized fish of each species were collected for tissue analysis. The total length of Nile tilapia collected ranged from 30 to 35 cm while Nile perch ranged from 60 to 80 cm. The fish were tagged and transferred on ice in a cooling box to the laboratory at Makerere University, where they were frozen until the tissue samples were extracted for pesticide residues. Water samples were collected in 2-L amber glass bottles. The samples were stored at 4°C and were analyzed within 1 wk of sampling.
Limnological Parameters
Water temperature, electrical conductivity, and pH were measured on site. Temperature and pH were measured using a calibrated Orion Model 250A pH meter, while electrical conductivity was measured using an Orion Model 122 conductivity meter (Thermo Electron Corp., Milford, MA).
Sample Processing
The extraction of OCs from water samples was done by liquid–liquid partition in dichloromethane. The extraction of OCs from fish samples was performed according to the method described by the U.S. Food and Drug Administration (U.S. Food and Drug Administration, 1994). Before the extraction, the bones were removed. A commercial meat chopper was used to macerate the fillet while still partially frozen, as this makes the skin more brittle. The skin was not removed before analysis because it is an edible portion of fish in Uganda. Two subsamples (10 and 25 g) of homogenized fish sample were taken. The 10-g portion was weighed into a crucible and used for determination of moisture content. The 25-g portion was used for solvent extraction and further analysis. The 25 g of fish tissue were macerated in a metallic blender at high speed with three consecutive volumes (150, 100, and 100 mL) of petroleum ether. The extracts from each portion were combined in a 250-mL volumetric flask and made up to volume. A portion (25 mL) of the combined extract was used to determine the extractable fat content, while 200 mL was evaporated to near dryness on a rotary evaporator. The residue in the flask was then transferred with three 1-mL portions of acetonitrile–dichloromethane mixture (25/75 v/v) to a centrifuge tube and frozen for 24 h. The frozen extract was centrifuged in a Heraeus Biofuge 22R centrifuge (Heraeus Instruments GmbH, Germany), operated at 15 000 rpm and 0°C, to precipitate the fat. The supernatant was transferred to a weighed flask. The precipitation step was repeated and the supernatants were combined. The combined extract, equivalent to 20 g of fish tissue, was loaded onto a column of 20 g florisil, activated in accordance with U.S. Food and Drug Administration (1994). The florisil was topped with 4 g of anhydrous Na2SO4. The column was eluted with 200 mL of 60 mL L–1 diethyl ether–petroleum ether and 200 mL of 150 mL L–1 diethyl ether–petroleum ether to give two fractions.
Gas–Liquid Chromatography Analysis
An HP5890 Series II gas chromatograph (Hewlett-Packard, Waldbronn, Germany) equipped with a 63Ni ECD (electron capture detector) was used. A low polar HP-5 column of 30-m length, 0.53-mm i.d. and 0.88-µm film thickness was used. Hydrogen–helium was used as a carrier gas at a flow rate of 10 mL min–1 and N2 as an auxiliary gas for the ECD (flow rate 60 mL min–1). Data were processed via an HP 3396 integrator.
Operating parameters were as follows: injector temperature set at 250 and 350°C for the detector; column temperature program: initial column temperature maintained at 110°C for 1 min, then raised (at 20°C min–1) to 150°C and maintained for 0.5 min. The temperature was again raised (at 3°C min–1) to 205°C and maintained for 1 min, and finally raised (at 35°C min–1) to 280°C, where it was maintained for 4 min.
Confirmation of Results
Tentative confirmation was done using a medium polar Chromepack CP-SIL 24 CB (50/50 phenyl–dimethylpolysiloxane) column 30 m by 0.53-mm i.d. with 1-µm film thickness. The operating conditions were: temperature set at 250°C for the injector and 320°C for the detector; column temperature program: initial column temperature 110°C and maintained for 1 min, then raised (at 20°C min–1) to 165°C and maintained for 0.5 min, again raised (at 2°C min–1) to 235°C and maintained for 1 min, and finally raised (at 35°C min–1) to 280°C and maintained for 4 min. Helium was used as the carrier gas at 10 mL min–1 flow rate and N2 as the auxiliary gas for the ECD at 50 mL min–1 flow rate.
Statistical Analysis
Statistical analyses were conducted using SAS Version 6.11 for Windows software (SAS Institute, 1996). The data were checked for normality using the univariate procedure for SAS. The results showed that the continuous variables studied were not normally distributed. Nonparametric methods were, therefore, used for the statistical analysis. A Wilcoxon rank-sum (Mann–Whitney) test for two independent samples was used for comparison of means for both Nile perch and Nile tilapia. Exact p values were determined using the NPAR1WAY procedure in SAS. Organochlorines are believed to readily partition in the fat; therefore, the Spearman correlation coefficient was used to assess this association. Arithmetic means and standard errors were determined and, in all cases, the differences are considered significant if the exact p value was 
0.05.
Quality Control and Quality Assurance
To ensure quality of the residue data, blanks, duplicates, and spikes were included in the analysis and recalibration standards were run frequently to check the integrity of the calibration curve. The individual reference standards (purity 
980 g kg–1) used to identify and quantify the levels of residues were purchased from Dr. Ehrenstorfer GmbH (Augsburg, Germany).
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RESULTS AND DISCUSSION
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Summary of Limnological Data for Napoleon Gulf, Lake Victoria
The pH of the water was generally alkaline and the electrical conductivity averaged 0.1 mS cm–1 (Table 1). The lowest temperature (25.3°C) and conductivity (0.094 mS cm–1) in this study were both recorded in August and the highest temperature (28.6°C) and conductivity (0.105 mS cm–1) were in December.
Analysis of Water and Fish Samples
Blank samples were collected from Lake Nabugabo, Masaka. This lake was considered pristine since it is in a remote area, far from major agricultural and industrial activities. Juvenile fish were collected for this purpose. The blank samples contained no detectable amount of pesticides. Mean recoveries for spiked water samples exceeded 80% except dieldrin, which gave poor recoveries of 52%. Results were not corrected for recoveries.
The residue levels in all the water samples collected from Napoleon Gulf, including those collected near the leather tanning industry, were below the limit of detection (0.1 µg L–1).
The average moisture content for the Nile perch was 769 g kg–1 and 762 g kg–1 for Nile tilapia, while the fat content averaged 20.9 g kg–1 in Nile perch and 19.3 g kg–1 in Nile tilapia (Table 2). Statistical analysis showed no difference ( = 0.05) in either the moisture content or fat content of the tissue of Nile tilapia and Nile perch.
The mean pesticide residue concentrations detected were <2 µg kg–1 (fresh-weight basis) (Table 2). A previous study of pilot lakes in Uganda by Sserunjogi (1974) reported a dieldrin concentration in fish of 5 µg kg–1 while another in Winam Gulf, Lake Victoria, reported an average of 0.83 µg kg–1 (Calamari et al., 1995).
The lindane residue levels ranged between not detectable (limit of detection = 0.1 µg kg–1) to 3.16 µg kg–1 (fresh-weight basis) in Nile tilapia and not detectable to 1.83 µg kg–1 in Nile perch. The maximum detected concentration for aldrin was 1.17 µg kg–1 in Nile tilapia and 1.79 µg kg–1 in Nile perch. For -endosulfan, 7.59 µg kg–1 were detected in Nile tilapia and 6.00 µg kg–1 in Nile perch. The maximum concentration for p,p'-DDE was 6.10 µg kg–1 in Nile perch and 3.44 µg kg–1 in Nile tilapia and, for p,p'-DDT, the maximum was 7.34 µg kg–1 in Nile tilapia and 4.30 µg kg–1 in Nile perch. In the fish from Winam Gulf, Lake Victoria, an average of 4.4 and 3 µg kg–1 were reported for p,p'-DDE and p,p'-DDT, respectively (Calamari et al., 1995). The concentrations of OCs reported from the Kenyan side of Lake Victoria (Luanda and Mbita), for fish that were sampled in 1988, generally were higher (Mitema and Gitau, 1990) than those obtained in this study. The concentrations, however, were below the set extraneous residue limits.
The maximum concentration for dieldrin in Nile tilapia was 2.22 µg kg–1 and 1.88 µg kg–1 in Nile perch. Sserunjogi (1974) reported dieldrin concentrations in fish averaging 27 µg kg–1. We would like to remind the reader that Sserunjogi studied different lakes. Since his is the only other work on Ugandan waters since the 1970s, however, if comparison is made with his findings, it would appear that the residue levels have decreased.
The concentration levels for lindane, aldrin, dieldrin, p,p'-1,1-dichloro-2,2-bis(p-chlorophenyl)ethane (DDD, a metabolite of DDT), p,p'-DDE, and p,p'-DDT found in this study were below the extraneous residue limit of 5 ppm (5000 µg kg–1) set by the Codex Alimentarious Commission of FAO–WHO (1997). Figure 2 shows the concentration of OCs in Nile perch and Nile tilapia.
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Fig. 2. Variation of mean organochlorine pesticide residues in Nile perch and Nile tilapia of the Napoleon Gulf, Lake Victoria.
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A Wilcoxon rank-sum (Mann–Whitney) test for two independent samples showed no difference in pesticide residue levels between the fish types for lindane, -endosulfan, p,p'-DDE, p,p'-DDT or dieldrin ( = 0.05). A Kruskal–Wallis test (nonparametric version of one-way ANOVA) showed no difference in the distribution of lindane between different fish types. Analysis of pesticide residues in the different parts of fish showed a significant difference in the distribution of p,p'-DDE, with higher levels in the abdominal portion of the fish. The aldrin levels were significantly higher ( = 0.05) in Nile perch than the levels found in Nile tilapia. The difference suggests a higher accumulation potential for aldrin by Nile perch. No significant correlation was observed between lipid content and OC concentration. The Spearman correlation coefficients were r2 = –0.021 for lindane, r2 = 0.0956 for aldrin, r2 = 0.0234 for endosulfan, r2 = 0.0397 for dieldrin, r2 = 0.2331 for p,p'-DDE, and r2 = 0.1672 for p,p'-DDT). Campbell et al. (2000) observed a similar trend with the exception of lake trout (Salvelinus namaycush) where a significant correlation was reported between lipids and OC concentrations.
Juvenile Nile perch mainly feed on zooplankton but later shift to a piscivorous diet consisting of silver pelagic cyprinid (Rastrineobola argentea Pellegrin), Nile tilapia, and juvenile Nile perch. Nile tilapia mainly feed on phytoplankton and detritus. Because of the difference in the trophic levels (Campbell et al., 2003), it would be expected that levels of OCs would be higher in Nile perch than in Nile tilapia. In this study, however, despite the difference in the diets of Nile perch and tilapia, no difference ( = 0.05) in the accumulation of OCs was observed for the two species except for aldrin, an observation that does not seem to implicate fish diet as a pathway for bioaccumulation. Sserunjogi (1974) did not observe accumulation of dieldrin residues by fish. By comparing the levels of OCs in fish and in surface water, a bioconcentration factor of 111 was observed for Nile perch and 116 for Nile tilapia. Since our study did not investigate the levels of OCs in the entire food web, it cannot be concluded that the accumulation of OCs is from the water column rather than another source within the food chain. Therefore these bioconcentration factors should be interpreted with caution. Nevertheless, the presence of persistent and hydrophobic OC residues in water, even at low concentrations, poses a risk to health of the biota because such residues have a higher affinity for partitioning into sediment and aquatic organisms. Chemicals with long half-life values and a high solubility in lipids (fats, oils, or waxes) will tend to accumulate in fatty tissue. Such lipophilic chemicals easily move into cells and are sequestered in fat, where they become more persistent.
By expressing pesticide residue levels on a lipid basis (Table 3), the residue levels found in this study were 10 to 300 times lower in Nile tilapia and Nile perch than the recommended German MRLs, the Australian MRLs, U.S. FDA action limits, and FAO–WHO limits.
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Table 3. Comparison of the levels in this study with some cited extraneous residue limits (residue levels expressed on a lipid basis).
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CONCLUSIONS
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The levels of OC residues found in this study for fish samples analyzed from the Napoleon Gulf of Lake Victoria are below the FAO, U.S. FDA, and Australian and German ERLs and MRLs. Based on these set standards, the fish from lake Victoria were found fit for human consumption. However, all the samples analyzed contained lindane residues and 98% of the samples contained endosulfan. This seems to indicate current use of lindane and endosulfan. The levels of lindane and endosulfan found were very low, suggesting rapid degradation of the pesticides in the tropical climate. On the other hand, only 53% of the samples analyzed were found to contain DDT. The ratio of DDT to that of its metabolite DDE found in this study suggests no current use of DDT in Uganda but is rather indicative of previous use of the compound.
Considering the previous and present use of some chlorinated hydrocarbons in agriculture and for vector control in Uganda and East Africa in general, the levels of pesticide residues found in fish in this study were very low. These low levels suggest a high degradation rate of the OCs in the tropical environment. Several researchers have found variations in pesticide dynamics in the tropical and subtropical environment compared with a temperate environment (Pandit et al., 2001; Laabs et al., 2000). However, due to their bioaccumulation tendencies and their ubiquitous nature, resulting from global transport and redeposition, the use of OCs has global implications, making their use unsuitable even in the tropical climate of Uganda.
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ACKNOWLEDGMENTS
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Financial support for this work was provided by NUFU Norway and the International Program in Chemical Sciences (IPICS) Sweden. We would like to acknowledge the Faculty of Veterinary Medicine, Makerere University; GTZ; Department of Chemistry, Makerere University; Fisheries Resources and Research Institute, Jinja; Dr. J.W. Jones (FDA) for the FDA manuals, Dr. Edward Bagu, and Mr. Moses Magumba.
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ABSTRACT
INTRODUCTION
