Skip to main content

Advertisement

SpringerLink
Log in

Assessment of pollution in sewage ponds using biomarker responses in wild African sharptooth catfish (Clarias gariepinus) in Tanzania

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The interactive effects of mixed pollutants in sewage wastewater on biomarker responses were investigated using wild male African sharptooth catfish (Clarias gariepinus) in Morogoro, Tanzania. A total of 58 fish were used, of which 21 were from Mindu dam (reference site) and 22, 9 and 10 from Mafisa, Mazimbu and Mzumbe sewage ponds, respectively. Liver somatic index (LSI) and gonadosomatic index (GSI) were significantly greater (two- to threefold) and (five- to sixfold), respectively, in fish from all sewage ponds. Haemoglobin concentration and gill filament 7-ethoxyresurufin O-deethylase (EROD) activities were significantly higher (1.2-fold and twofold, respectively) in fish from Mzumbe sewage ponds than in fish from Mindu dam, whereas liver EROD activity was significantly higher in fish from Mzumbe and Mafisa sewage ponds (5-fold). A HPLC method for determination of enzymatically formed p-nitrophenyl-glucuronide (PNPG) was developed and applied to measure UDP-glucuronosyl transferase (UGT) activities that was significantly higher in fish from all sewage ponds (2–2.5-fold) than in fish from Mindu dam. Kinetic characteristics and assay dependence of UGT were studied with microsomal preparations. Metallothionein (MT) content was significantly lower (three- to fourfold) in fish from sewage ponds than in fish from Mindu dam, and corresponded with cumulative levels of cadmium, lead and mercury. Condition factor, vitellogenin (Vtg), acetylcholinesterase (AChE) activities in plasma, eyes and brain, haematocrit, plasma protein and cytosolic glutathione S-transferase (GST) activities were comparable in fish from sewage ponds and Mindu dam. Although specific pollutants other than the metals were not identified by chemical analysis, application of a suite of biomarkers in C. gariepinus demonstrated that all sewage ponds were contaminated by pollutants of public health concern.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andersson T, Pesonen M, Johansson C (1985) Differential induction of cytochrome P-450-dependent monooxygenase, epoxide hydrolase, glutathione transferase and UDP glucuronosyltransferase activities in the liver of the rainbow trout by ß-naphthoflavone or Clophen A50. Biochem Pharmacol 34:3309–3314

    Article  CAS  Google Scholar 

  • Bagenal TB, Tesch FW (1978) Methods for assessment of fish production in fresh waters. In: Bagenal TB (ed) Age and growth. Blackwell, Oxford, pp 101–136

    Google Scholar 

  • Barber LB, Lee KE, Swackhamer DL, Schoenfuss HL (2007) Reproductive responses of male fathead minnows exposed to wastewater treatment plant effluent, effluent treated with XAD8 resin, and an environmentally relevant mixture of alkylphenol compounds. Aquat Toxicol 82:36–46

    Article  CAS  Google Scholar 

  • Benjamin MM (1978) Outline of veterinary clinical pathology, 3rd edn. The Iowa State University Press, Iowa, pp 60–75

    Google Scholar 

  • Beyer J, Sandvik M, Hylland K, Fjeld E, Egaas E, Aas E, Skåre JU, Goksøyr A (1996) Contaminant accumulation and biomarker responses in flounder (Platichthys flesus L.) and Atlantic cod (Gadus morhua L.) exposed by caging to polluted sediments in Sorfjorden, Norway. Aquat Toxicol 36:75–98

    Article  CAS  Google Scholar 

  • Beyer J, Sandvik M, Skare JU, Egaas E, Hylland K, Waagbo R, Goksoyr A (1997) Time- and dose-dependent biomarker responses in flounder (Platichthys flesus L.) exposed to benzo[a]pyrene, 2, 3, 3′, 4, 4′, 5-hexachlorobiphenyl (PCB-156) and cadmium. Biomarkers 2:35–44

    Article  CAS  Google Scholar 

  • Braathen M, Mdegela RH, Correia D, Rundberget T, Myburgh J, Botha C, Skaare JU, Sandvik M (2008) Vitellogenin in African sharptooth catfish (Clarias gariepinus): purification, characterization and ELISA development. J Toxicol Environ Health 72:173–183

    Article  CAS  Google Scholar 

  • Bucheli TD, Fent K (1995) Induction of cytochrome P450 as a biomarker for environmental contamination ion aquatic ecosystems. Crit Rev Environ Sci Technol 25:201–268

    Article  CAS  Google Scholar 

  • Buet A, Banas D, Vollaire Y, Coulet E, Roche H (2006) Biomarker responses in European eel (Anguilla anguilla) exposed to persistent organic pollutants. A field study in the Vaccares lagoon (Camargue, France). Chemosphere 65:1846–1858

    Article  CAS  Google Scholar 

  • Chen C, Liu MC, Shih ML, Yu S, Yeh C, Lee ST, Yang T, Hung S (2001) Microsomal monooxygenase activity in Tilapia (Oreochromis mossambicus) exposed to a bleached kraft mill effluent using different exposure systems. Chemosphere 45:581–588

    Article  CAS  Google Scholar 

  • Collier TK, Varanasi U (1991) Hepatic activities of xenobiotic metabolizing enzymes and biliary levels of xenobiotics in English sole (Parophrys vetulus) exposed to environmental contaminants. Arch Environ Contam Toxicol 20:462–473

    Article  CAS  Google Scholar 

  • Diniz MS, Peres I, Pihan JC (2005) Comparative study of the estrogenic response of mirror carp (Cyprinus carpio) exposed to treated municipal sewage effluent (Lisbon) during two periods in different seasons. Sci Total Environ 349:129–139

    Article  CAS  Google Scholar 

  • Dunnett CW (1980) Pairwise multiple comparisons in the homogeneous variance, unequal sample size case. J Am Stat Assoc 75:789–795

    Article  Google Scholar 

  • Ellman GL, Courtney KD, Andres VJ, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Esbensen KH (2000) Multivariate data analysis in practice. An introduction to multivariate data analysis and experimental design, 4th edn. CAMO, Oslo

    Google Scholar 

  • Farkas A, Salánki J, Specziár A (2003) Age- and size-specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Res 37:959–964

    Article  CAS  Google Scholar 

  • Gaworecki KM, Rice CD, van den Hurk P (2004) Induction of phenol-type sulfotransferase and glucuronosyltransferase in channel catfish and mummichog. Marine Environ Res 58:525–528

    Article  CAS  Google Scholar 

  • George SG (1989) Cadmium effects on plaice liver xenobiotic and metal detoxication systems: dose response. Aquat Toxicol 15:303–310

    Article  CAS  Google Scholar 

  • George S, Leaver M (2002) Allelic variations in the plaice UGT1B1 gene. Marine Environ Res 54:259–262

    Article  CAS  Google Scholar 

  • George SG, Young P (1986) The time course of effects of cadmium and 3-methylcholanthrene on activities of enzymes of xenobiotic metabolism and metallothionein levels in the plaice, Pleuronectes platessa. Comp Biochem Physio 83C:37–44

    Article  CAS  Google Scholar 

  • Grizzle JM, Horowitz SA, Strength DR (1988) Caged fish as monitors of pollution: effects of chlorinated effluent from as wastewater treatment plant. Water Resource Bull 24:951–959

    CAS  Google Scholar 

  • Grossbard ML, Boyer JL, Gordon ER (1987) The excretion pattern of biliverdin and bilirubin in bile of the small skate (Raja erinacea). J Comp Physiol 157:61–66

    CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jacoby WB (1974) Glutathione S-transferases. The first enzymic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Jedamski-Grymlas J, Kammann U, Tempelmann A, Karbe L, Siebers D (1995) Biochemical responses and environmental contaminants in breams (Abramis brama L.) caught in the River Elbe. Ecotoxicol Environ Saf 31:49–56

    Article  CAS  Google Scholar 

  • Jobling M (1988) A review of the physiological and nutritional energetics of cod, Gadus morhua L., with particular reference to growth under farmed conditions. Aquaculture 70:1–19

    Article  Google Scholar 

  • Johansson-Sjøbeck ML, Larsson Å (1978) The effect of cadmium on the hematology and on the activity of [delta]-aminolevulinic acid dehydratase (ALA-D) in blood and hematopoietic tissues of the flounder, Pleuronectes flesus L. Environ Res 17:191–204

    Article  Google Scholar 

  • Jönsson M (2003) A gill filament EROD assay: development and application in environmental monitoring. PhD Thesis, Uppsala University, Sweden, pp 35–37

  • Jönsson EM, Brandt I, Brunstrom B (2002) Gill filament-based EROD assay for monitoring waterborne dioxin-like pollutants in fish. Environ Sci Technol 36:3340–3344

    Article  CAS  Google Scholar 

  • Kendall RJ, Anderson TA, Baker RJ, Bens CM, Carr JA, Chiodo LA, Cobb GP III, Dickerson RL, Dixon KR, Frame LT, Hooper MJ, Martin CF, McMurry ST, Patino R, Smith EE, Theodorakis CW (2001) Ecotoxicology. In: Klaassen CD (ed) Casarett and Doull’s toxicology: the basic science of poisons, 6th edn. Division of McGraw-Hill Companies Inc., New York, pp 1013–1045

    Google Scholar 

  • Kosmala A, Migeon BM, Flammarion P, Garric J (1998) Impact assessment of a wastewater treatment plant effluent using the fish biomarker Ethoxyresorufin-O-Deethylase: field and on-site experiments. Ecotoxicol Environ Saf 41:19–28

    Article  CAS  Google Scholar 

  • Krahn MM, Burrows DG, Macleod WD, Malins DC (1987) Determination of individual metabolites of aromatic compounds in hydrolyzed bile of English sole (Parophrys vetulus) from polluted sites in Puget sound, Washington. Arch Environ Contam Toxicol 16:511–522

    Article  CAS  Google Scholar 

  • Lin JH, Wong BK (2002) Complexities of glucuronidation affecting in vitro–in vivo extrapolation. Curr Drug Metab 3:623–646

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Ma T, Wan X, Huang Q, Wang Z, Liu J (2005) Biomarker responses and reproductive toxicity of the effluent from a Chinese large sewage treatment plant in Japanese medaka (Oryzias latipes). Chemosphere 59:281–288

    Article  CAS  Google Scholar 

  • Mayer FL, Verteeg DJ, McKee MJ, Folmar LC, Graney RL, McCume DC, Rattner BA (1992) Physiological and non-specific biomarkers. In: Hugget RJ, Kimerle RA, Mehrle PM, Bergman HL (eds) Biomarkers: biochemical, physiological and histological markers of anthropogenic stress. Lewis Publishers, Michigan, pp 5–87

    Google Scholar 

  • McCormick SD, Bern HA (1989) In vitro stimulation of Na + -K + -ATPase activity and ouabain binding by cortisol in coho salmon gill. Am J Physiol 256:R707–R715

    CAS  Google Scholar 

  • Mdegela RH, Myburgh J, Correia D, Braathen M, Ejobi F, Botha B, Sandvik M, Skaare JU (2006a) Evaluation of the gill filament-based EROD assay in African sharptooth catfish (Clarias gariepinus) as a monitoring tool for waterborne PAH-type contaminants. Ecotoxicol 15:51–59

    Article  CAS  Google Scholar 

  • Mdegela RH, Braathen M, Correeia D, Mosha RD, Skaare JU, Sandvik M (2006b) Influence of EE2 on CYP1A, GST and biliary FACs responses in male African Sharptooth catfish (Clarias gariepinus) exposed to waterborne Benzo[a]pyrene. Ecotoxicol 15:629–637

    Article  CAS  Google Scholar 

  • Mdegela RH, Braathen M, Pereka A, Mosha R, Sandvik M, Skaare J (2009) Heavy metals and organochlorine residues in water, sediments, and fish in aquatic ecosystems in urban and peri-urban areas in Tanzania. Water Air Soil Pollut 203:369–379

    Article  CAS  Google Scholar 

  • Muchuweti M, Birkett JW, Chinyanga E, Zvauya R, Scrimshaw MD, Lester JN (2006) Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: implications for human health. Agric Ecosyst Environ 112:41–48

    Article  CAS  Google Scholar 

  • Olafson RW, Ollson PE (1991) Electrochemical detection of metallothionein. Meth Enzym 205:205–216

    Article  CAS  Google Scholar 

  • Olsson M (1996) Mercury levels as a function of age and size in northern pike one and five years after the mercury ban in Sweden. Ambio 5:73–76

    Google Scholar 

  • Olsson PE, Zafarullah M, Gedamu L (1989) A role of metallothionein in zinc regulation after oestradiol induction of vitellogenin synthesis in rainbow trout, Salmo gairdneri. Fish Physiol Biochem J 257:555–559

    CAS  Google Scholar 

  • Pathiratne A, George S (1996) Comparison of xenobiotic metabolizing enzymes of Tilapia with those of other fish species and interspecies relationships between gene families. Mar Environ Res 42:293–296

    Article  CAS  Google Scholar 

  • Pettersson M, Adolfsson-Erici M, Parkkonen J, Forlin L, Asplund L (2006) Fish bile used to detect estrogenic substances in treated sewage water. Sci Tot Environ 366:174–186

    Article  CAS  Google Scholar 

  • Prosi F (1981) Heavy metals in aquatic organisms. In: Förstner U, Wittmann GTW (eds) Metal pollution in the aquatic environment. Springer, Berlin, pp 271–323

    Google Scholar 

  • Rattan RK, Datta SP, Chhonkar PK, Suribabu K, Singh AK (2005) Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater—a case study. Agric Ecosyst Environ 109:310–322

    Article  CAS  Google Scholar 

  • Rebers FEM, Hassing GAM, van Dijk W, van Straaten HJ, Goos HJ, Schulz RW (2002) Gonadotropin-releasing hormone does not directly stimulate luteinizing hormone biosynthesis in male African catfish. Biol Reprod 66:1604–1611

    Article  CAS  Google Scholar 

  • Ronisz D, Larsson DGJ, Förlin L (1999) Seasonal variations in the activities of selected hepatic biotransformation and antioxidant enzymes in eelpout (Zoarces viviparous). Comp Biochem Physiol C 124:271–279

    CAS  Google Scholar 

  • Sandvik M, Beyer J, Goksøyr A, Hylland K, Egaas E, Skaare JU (1997) Interaction of benzo[a]pyrene, 2, 3, 3′, 4, 4′, 5-hexachlorobiphenyl (PCB-156) and cadmium on biomarker responses in flounder (Platichthys flesus L.). Biomarkers 2:153–160

    Article  CAS  Google Scholar 

  • Sarakinos HC, Bermingham N, White PA, Rasmussen JB (2000) Correspondence between whole effluent toxicity and the presence of priority substances in complex industrial effluents. Environ Toxicol Chem 19:63–71

    Article  CAS  Google Scholar 

  • Shailaja MS, D’Silva C (2003) Evaluation of impact of PAH on a tropical fish, Oreochromis mossambicus using multiple biomarkers. Chemosphere 53:835–841

    Article  CAS  Google Scholar 

  • Skelton PH (2000) A complete guide to freshwater fishes of Southern Africa. Southern Book Publishers, Zimbabwe, pp 229–230

    Google Scholar 

  • Slooff W, Van Kreijl CF, Baars AJ (1983) Relative liver weights and xenobiotic-metabolizing enzymes of fish from polluted surface water in the Netherlands. Aquat Toxicol 4:1–14

    Article  CAS  Google Scholar 

  • Sturm A, Hodson PV, Carey JH, Hansen P (1999) Hepatic UDP-glucuronosyltransferase in rainbow trout (Oncorhynchus mykiss) and preliminary assessment of response to pulp mill cooking liquor. Bull Environ Contam Toxicol 62:608–615

    Article  CAS  Google Scholar 

  • Szefer P, Domagala-Wieloszewska M, Warzocha J, Garbacik-Wesolowska A, Ciesielski T (2003) Distribution and relationships of mercury, lead, cadmium, copper and zinc in perch (Perca fluviatilis) from the Pomeranian Bay and Szczecin Lagoon, southern Baltic. Food Chem 81:73–83

    Article  CAS  Google Scholar 

  • UKWIR (2001a) Diet Toxicity Assessment (DTA) demonstration programme technical guidance addressing water quality problems in catchments where acute toxicity is an issue. Steering group to the environmental regulators. Report ref. No 00/TX/01/07

  • UKWIR (2001b) Diet Toxicity Assessment (DTA) demonstration programme recommendations from the steering group to the environmental regulators. Report ref. No 00/TX/02/06

  • URT (2002). Tanzania population and housing census. http://www.tanzania.go.tz/census

  • US EPA (1998) Guidelines for ecological risk assessment. The United States Environmental Protection Agency, Washington D.C. EPA/630/R-95/002F

  • van der Oost R, Beyer J, Vermeulen PE (2003) Fish Bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • van Veld PA, Vogelbein WK, Cochran MK, Goksøyr A, Stegeman JJ (1997) Route-specific cellular expression of cytochrome P4501A (CYP1A) in fish (Fundulus heteroclitus) following exposure to aqueous and dietary Benzo[a]pyrene. Toxicol Appl Pharmacol 142:348–359

    Article  Google Scholar 

  • Vigano L, Arillo A, Falugi C, Melodia F, Polesello S (2001) Biomarkers of exposure and effect in flounder (Platichthys flesus) exposed to sediments of the Adriatic Sea. Mar Poll Bull 42:887–894

    Article  CAS  Google Scholar 

  • Werner J, Wautier K, Evans RE, Baron CL, Kid K, Place V (2003) Waterborne ethynylestradiol induces vitellogenin and alters metallothionein expression in lake trout (Salvelinus namaycush). Aquat Toxicol 62:321–328

    Article  CAS  Google Scholar 

  • Whyte JJ, Jung RE, Schmitt CJ, Tilltitt DD (2000) Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev in Toxicol 30:347–570

    Article  CAS  Google Scholar 

  • Williams TD, Gensberg K, Minchin SD, Chipman JK (2003) A DNA expression array to detect toxic stress response in European flounder (Platichthys flesus). Aquat Toxicol 65:141–157

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was kindly funded by the Norwegian Universities’ Committee for Development Research and Education (NUFU) PRO 08/2002. We are grateful to the management and staff of Morogoro Urban Water and Sewerage Authority (MORUWASA) and Mzumbe University for granting permission to use their sewage facilities and for kind support during sampling. We thank A. Ruus, K. Hylland, T.F. Holth, T. Waaler, A. Kitime, P. Mkuchu, A. Chambo, A. Mjema and H. Mbena for their technical support and assistance.

Author information

Authors and Affiliations

  1. Faculty of Veterinary Medicine, Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, P. O. Box 3021, Morogoro, Tanzania

    Robinson H. Mdegela

  2. Department of Pharmacology, Microbiology and Food Hygiene, Norwegian School of Veterinary Science, P. O. Box 8156, Dep., 0033, Oslo, Norway

    Marte Braathen & Janneche U. Skaare

  3. Faculty of Veterinary Medicine, Department of Veterinary Physiology, Biochemistry, Pharmacology and Toxicology, Sokoine University of Agriculture, P. O. Box 3017, Morogoro, Tanzania

    Resto D. Mosha

  4. National Veterinary Institute, Ullevålsveien 68, Pb 750 Sentrum, 0106, Oslo, Norway

    Janneche U. Skaare & Morten Sandvik

  5. Det Norske Veritas AS, 1322, Høvik, Norway

    Marte Braathen

Authors
  1. Robinson H. Mdegela
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marte Braathen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Resto D. Mosha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Janneche U. Skaare
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Morten Sandvik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Morten Sandvik.

Additional information

Robinson H. Mdegela and Marte Braathen have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mdegela, R.H., Braathen, M., Mosha, R.D. et al. Assessment of pollution in sewage ponds using biomarker responses in wild African sharptooth catfish (Clarias gariepinus) in Tanzania. Ecotoxicology 19, 722–734 (2010). https://doi.org/10.1007/s10646-009-0449-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-009-0449-4

Keywords

Search

Navigation