Skip to main content
Log in

PCBs in fish and their cestode parasites in Lake Victoria

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Polychlorinated biphenyls (PCBs) are classified as persistent organic pollutants (POPs) regulated by the Stockholm Convention (2001). Although their production and use was stopped almost three decades ago, PCBs are environmental persistent, toxic, and bioaccumulate in biota. We assessed the levels of 7 PCB congeners (IUPAC nos. 28, 52, 101, 118, 138, 153, and 180) in sediment and fish (Oreochromis niloticus, Lates niloticus, and Rastrineobola argentea) and evaluated the potential of cestode fish endoparasite (Monobothrioides sp., Proteocephalaus sp., and Ligula intestinalis) as biomonitors of PCBs in Lake Victoria, Kenya. The median concentration of Σ7PCBs in sediments and fish were 2.2–96.3 μg/kg dw and 300–3,000 μg/kg lw, respectively. At all the sampling sites, CB138, CB153, and CB180 were the dominant PCB congeners in sediment and fish samples. Compared to the muscle of the piscine host, Proteocephalaus sp. (infecting L. niloticus) biomagnified PCBs ×6–14 while Monobothrioides sp. (infecting O. niloticus) biomagnified PCBs ×4–8. Meanwhile, L. intestinalis (infecting R. argentea) biomagnified PCBs ×8–16 compared to the muscle of unparasitized fish. We demonstrate the occurrence of moderate to high levels of PCB in sediments and fish in Lake Victoria. We also provide evidence that fish parasites bioaccumulate higher levels of PCBs than their piscine hosts and therefore provide a promising biomonitor of PCBs. We urge further a long-term study to validate the use of the above cestode fish parasites as biomonitoring tools for PCBs.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Aksoy, A., Das, Y. K., Yavuz, O., Guvenc, D., Atmaca, E., & Agaoglu, S. (2011). Organochlorine pesticide and polychlorinated biphenyls levels in fish and mussel in van region Turkey. Bulletin of Environmental Contamination and Toxicology, 87, 65–69.

    Article  CAS  Google Scholar 

  • Barakat, A. O., Khairy, M., & Aukaily, I. (2013). Persistent organochlorine pesticide and PCB residues in surface sediments of Lake Qarun, a protected area of Egypt. Chemosphere, 90, 2467–2476.

    Article  CAS  Google Scholar 

  • Bellay, S., de Oliveira, E. F., Almeida-Neto, M., Abdallah, V. D., de Azevedo, R. K., Takemoto, R. M., et al. (2015). The patterns of organisation and structure of interactions in a fish-parasite network of a neotropical river. International Journal for Parasitology, 45, 549–557.

    Article  Google Scholar 

  • Berg, V., Zerihun, M. A., Jørgensen, A., Lie, E., Dale, O. B., Skaare, J. U., et al. (2013). High prevalence of infections and pathological changes in burbot (Lota lota) from a polluted lake (Lake Mjøsa, Norway). Chemosphere, 90, 1711–1718.

    Article  CAS  Google Scholar 

  • Blanchet−Letrouvé, I., Zalouk−Vergnoux, A., Vénisseau, A., Couderc, M., Le Bizec, B., Elie, P., et al. (2014). Dioxin-like, non-dioxin like PCB and PCDD/F contamination in European eel (Anguilla anguilla) from the Loire estuarine continuum: spatial and biological variabilities. Science of the Total Environment, 472, 562–571.

    Article  Google Scholar 

  • Brázová, T., Hanzelová, V., & Miklisová, D. (2012a). Bioaccumulation of six PCB indicator congeners in a heavily polluted water reservoir in eastern Slovakia: tissue-specific distribution in fish and their parasites. Parasitology Research, 111, 779–786.

    Article  Google Scholar 

  • Brázová, T., Hanzelová, V., Miklisová, D., Šalgovičová, D., & Turčeková, Ľ. (2012b). Biomonitoring of polychlorinated biphenyls (PCBs) in heavily polluted aquatic environment in different fish species. Environmental Monitoring and Assessment, 184, 6553–6561.

    Article  Google Scholar 

  • Breivik, K., Sweetman, A., Pacyna, J. M., & Jones, K. C. (2007). Towards a global historical emission inventory for selected PCB congeners—a mass balance approach—3. An update. Science of the Total Environment, 377, 296–307.

    Article  CAS  Google Scholar 

  • Brown, J. F., Lawton, R. W., & Morgan, C. B. (1994). PCB metabolism, persistence, and health effects after occupational exposure: implications for risk assessment. Chemosphere, 29, 2287–2294.

    Article  CAS  Google Scholar 

  • Campbell, L. M., Hecky, R. E., & Wandera, S. B. (2004). Stable isotope analyses of food web structure and fish diet in Napoleon and Winam gulfs, Lake Victoria, East Africa. Journal of Great Lakes Research, 29, 243–257.

    Article  Google Scholar 

  • Colombo, J., Cappelletti, N., Barreda, A., Migoya, M. C., & Skorupka, C. N. (2005). Vertical fluxes and accumulation of PCBs in coastal sediments of the Río de la Plata estuary, Argentina. Chemosphere, 61, 1345–1357.

    Article  CAS  Google Scholar 

  • de Souza, A. S., Torres, J. P., Meire, R. O., Neves, R. C., Couri, M. S., & Serejo, C. S. (2008). Organochlorine pesticides (OCs) and polychlorinated biphenyls (PCBs) in sediments and crabs (Chasmagnathus granulata, Dana, 1851) from mangroves of Guanabara Bay, Rio de Janeiro state, Brazil. Chemosphere, 73, 186–192.

    Article  Google Scholar 

  • Eckhardt, S., Breivik, K., Manø, S., & Stohl, A. (2007). Record high peaks in PCB concentrations in the Arctic atmosphere due to long-range transport of biomass burning emissions. Atmospheric Chemistry and Physics, 7, 4527–4536.

    Article  CAS  Google Scholar 

  • Eisenreich, S. J., Capel, P. D., Robbins, J. A., & Bourbonniere, R. (1989). Accumulation and diagenesis of chlorinated hydrocarbons in lacustrine sediments. Environmental Science & Technology, 23, 1116–1126.

    Article  CAS  Google Scholar 

  • Fang, J. K. H., Wu, R. S. S., Zheng, G. J., Au, D. W. T., Lam, P. K. S., & Shin, P. K. S. (2009). The use of muscle burden in rabbitfish Siganus oramin for monitoring of polycyclic aromatic hydrocarbons and polychlorinated biphenyls in Victoria harbour, Hong Kong and potential human health risk. Science of the Total Environment, 407, 4327–4332.

    Article  CAS  Google Scholar 

  • Frank, S. N., Godehardt, S., Nachev, M., Trubiroha, A., Kloas, W., & Sures, B. (2013). Influence of the cestode Ligula intestinalis and the acanthocephalan Polymorphus minutus on levels of heat shock protein 70 (HSP70) and metallothionein in their fish and crustacean intermediate hosts. Environmental Pollution, 180, 173–179.

    Article  CAS  Google Scholar 

  • Fu, C. T., & Wu, S. C. (2006). Seasonal variation of the distribution of PCBs in sediments and biota in a PCB-contaminated estuary. Chemosphere, 62, 1786–1794.

    Article  CAS  Google Scholar 

  • Hellar–Kihampa, H., De Wael, K., Lugwisha, E., Malarvannan, G., Covaci, A., & Van Grieken, R. (2013). Spatial monitoring of organohalogen compounds in surface water and sediments of a rural–urban river basin in Tanzania. Science of the Total Environment, 447, 186–197.

    Article  Google Scholar 

  • Hu, G., Sun, C., Li, J., Zhao, Y., Wang, H., & Li, Y. (2009). POPs accumulated in fish and benthos bodies taken from Yangtze River in Jiangsu area. Ecotoxicology, 18, 647–651.

    Article  CAS  Google Scholar 

  • Huang, J., Amuzu-Sefordzi, B., & Li, M. (2015). Heavy metals and polychlorinated biphenyls (PCBs) sedimentation in the Lianhua Mountain reservoir, Pearl River Delta, China. Environmental Monitoring and Assessment, 187, 254.

    Article  Google Scholar 

  • Johnson, G. W., Chiarenzelli, J., Quensen, J. F., & Hamilton, M. C. (2006). Polychlorinated biphenyls. Environmental Forensic: A Contaminant Specific Guide, 10, 187–205.

    Google Scholar 

  • Karvonen, A., Lundsgaard-Hansen, B., Jokela, J., & Seehausen, O. (2013). Differentiation in parasitism among ecotypes of whitefish segregating along depth gradients. Oikos, 122, 122–128.

    Article  Google Scholar 

  • Lavandier, R., Quinete, N., Hauser-Davis, R. A., Dias, P. S., Taniguchi, S., Montone, R., et al. (2013). Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) in three fish species from an estuary in the southeastern coast of Brazil. Chemosphere, 90, 2435–2443.

    Article  CAS  Google Scholar 

  • Le, T. T. Y., Rijsdijka, L., Sures, B., & Hendriksa, A. J. (2014). Accumulation of persistent organic pollutants in parasites. Chemosphere, 108, 145–151.

    Article  Google Scholar 

  • Lima, D. P., Giacomini, H. C., Takemoto, R. M., Agostinho, A. A., & Bini, L. M. (2012). Patterns of interactions of a large fish–parasite network in a tropical floodplain. The Journal of Animal Ecology, 81, 905–913.

    Article  Google Scholar 

  • Liu, H., Zhang, Q., Wang, Y., Cai, Z., & Jiang, G. (2007). Occurrence of polychlorinated dibenzo-p-dioxins, dibenzofurans and biphenyls pollution in sediments from the Haihe River and Dagu Drainage River in Tianjin City, China. Chemosphere, 68, 1772–1778.

    Article  CAS  Google Scholar 

  • Manirakiza, P., Covaci, A., Nizigiymana, L., Ntakimazi, G., & P., S. (2002). Persistent chlorinated pesticides and polychlorinated biphenyls in selected fish species from Lake Tanganyika, Burundi, Africa. Environmental Pollution, 117, 447–455.

    Article  CAS  Google Scholar 

  • Marcogliese, D. J., & Pietrock, M. (2011). Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology, 27, 123–130.

    Article  Google Scholar 

  • McLeod, P. B., Luoma, S. N., & Luthy, R. G. (2008). Biodynamic modeling of PCB uptake by Macoma balthica and Corbicula fluminea from sediment amended with activated carbon. Environmental Science & Technology, 42, 484–490.

    Article  CAS  Google Scholar 

  • Meijer, N. S., Ockenden, A. W., Sweetman, A., Brevik, K., Grimalt, O. J., & Jones, C. K. (2003). Global distribution and budget of PCBs and HCB in background surface soils: implications for sources and environmental processes. Environmental Science & Technology, 37, 667–672.

    Article  CAS  Google Scholar 

  • Morrill, A., Provencher, J., & Forbes, M. (2014). Testing for dual impacts of contaminants and parasites on hosts: the importance of skew. Environmental Reviews, 22, 445–456.

    Article  Google Scholar 

  • Ojwang, W. O., Kaufman, L., Asila, A. A., Agembe, S., & Michener, B. (2004). Isotopic evidence of functional overlap amongst the resilient pelagic fishes. Hydrobiologia(529), 27–34.

  • Ondarza, P. M., Gonzalez, M., Fillmann, G., & Miglioranza, K. S. B. (2014). PBDEs, PCBs and organochlorine pesticides distribution in edible fish from Negro River basin, Argentinean Patagonia. Chemosphere, 94, 135–142.

    Article  CAS  Google Scholar 

  • Oyoo-Okoth, E., Admiraal, W., Osano, O., Hoitinga, L., & Kraak, M. H. S. (2010a). Metal specific partitioning in a parasite–host assemblage of the cestode Ligula intestinalis and the cyprinid fish Rastrineobola argentea. Science of the Total Environment, 408, 1557–1562.

    Article  CAS  Google Scholar 

  • Oyoo-Okoth, E., Admiraal, W., Osano, O., Kraak, M. H. S., Ngure, V., Makwali, J., et al. (2010b). Use of fish endoparasite Ligula intestinalis in an intermediate cyprinid host (Rastrineobola argentea) in biomonitoring contaminant metals (Pb, Cd, Cr and Cu) in Lake Victoria, Kenya. Lakes & Reservoirs: Research & Management, 15, 63–73.

    Article  CAS  Google Scholar 

  • Oyoo-Okoth, E., Admiraal, W., Osano, O., Kraak, M. H. S., Ngure, V., Makwali, J., et al. (2010c). Use of the fish endoparasite Ligula intestinalis (L., 1758) in an intermediate cyprinid host (Rastrineobola argentea) for biomonitoring heavy metal contamination in Lake Victoria, Kenya. Lake. Reserv. Manage, 15, 63–73.

    Article  CAS  Google Scholar 

  • Oyoo-Okoth, E., Admiraal, W., Osano, O., & Kraak, M. H. S. (2012). Element profiles in hair and nails of children reflect the uptake from food and the environment. Environmental Toxicology and Chemistry, 31, 1461–1469.

    Article  CAS  Google Scholar 

  • Persson, M., Larsson, P., & Stenroth, P. (2007). Biomagnification and polychlorinated biphenyl congener distribution in an aquatic predator–prey, host–parasite system. Environmental Toxicology and Chemistry, 26, 837–843.

    Article  CAS  Google Scholar 

  • Pizarro−Aránguiz, N., Galbán-Malagón, C. J., Ruiz-Rudolph, P., Araya-Jordan, C., Maddaleno, A., & San Martin, B. (2015). Occurrence, variability and human exposure to polychlorinated Dibenzo-p-dioxins (PCDDs), polychlorinated Dibenzofurans (PCDFs) and dioxin-like polychlorinated biphenyls (DL-PCBs) in dairy products from Chile during the 2011–2013 survey. Chemosphere, 126, 78–87.

    Article  Google Scholar 

  • Ribas-Fito, N., Sala, M., Kogevinas, M., & Sunyer, J. (2001). Polychlorinated biphenyls (PCBs) and neurological development in children: a systematic review. Journal of Epidemiology and Community Health, 55, 537–546.

    Article  CAS  Google Scholar 

  • Seppälä, O., Karvonen, A., Valtonen, E. T., & Jokela, J. (2009). Interactions among co-infecting parasite species: a mechanism maintaining genetic variation in parasites? Proceedings of the Royal Society B, 276, 691–697.

    Article  Google Scholar 

  • Ssebugere, P., Sillanpää, M., Kiremire, B. T., Kasozi, G. N., Wang, P., Sojinu, S. O., et al. (2014a). Polychlorinated biphenyls and hexachlorocyclohexanes in sediments and fish species from the Napoleon gulf of Lake Victoria, Uganda. Science of the Total Environment, 48, 55–60.

    Article  Google Scholar 

  • Ssebugere, P., Sillanpää, M., Wang, P., Li, Y., Kiremire, B. T., Kasozi, G. N., et al. (2014b). Polychlorinated biphenyls in sediments and fish species from the Murchison Bay of Lake Victoria, Uganda. Science of the Total Environment, 482–483, 349–357.

  • Sun, Y. X., Hao, Q., Xu, X. R., Luo, X. J., Wang, S. L., Zhang, Z. W., et al. (2014). Persistent organic pollutants in marine fish from Yongxing Island, South China Sea: levels, composition profiles and human dietary exposure assessment. Chemosphere, 98, 84–90.

    Article  CAS  Google Scholar 

  • Sures, B. (2001). The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems, a review. Aquatic Ecology, 35, 245–255.

    Article  CAS  Google Scholar 

  • Sures, B. (2004). Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology, 20, 170–177.

    Article  CAS  Google Scholar 

  • Sures, B. (2007). Host-parasite interactions from an ecotoxicological perspective. Parassitologia, 49, 173–176.

    CAS  Google Scholar 

  • Sures, B. (2008). Host–parasite interactions in polluted environments. Journal of Fish Biology, 73, 2133–2142.

    Article  Google Scholar 

  • Sures, B., Siddall, R., & Taraschewski, H. (1999). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today, 50, 16–21.

    Article  Google Scholar 

  • UNEP (2009). Stockholm convention on persistent organic pollutants (POPs). Geneva: Published by the Secretariat of the Stockholm Convention on Persistent Organic Pollutants.

    Google Scholar 

  • Verhaert, V., Covaci, A., Bouillon, S., Abrantes, K., Musibono, D., Bervoets, L., et al. (2013). Baseline levels and trophic transfer of persistent organic pollutants in sediments and biota from the Congo River basin (DR Congo). Environment International, 59, 290–302.

    Article  CAS  Google Scholar 

  • Wafo, E., Sarrazin, L., Diana, C., Schembri, T., Lagadec, V., & Monod, J. L. (2006). Polychlorinated biphenyls and DDT residues distribution in sediments of Cortiou (Marseille, France). Marine Pollution Bulletin, 52, 104–107.

    Article  CAS  Google Scholar 

  • Wang, H. S., Du, J., Leung, H. M., Leung, A. O. W., Liang, P., Giesy, J. P., et al. (2011). Distribution and source apportionments of polychlorinated biphenyls (PCBs) in mariculture sediments from the Pearl River Delta, South China. Marine Pollution Bulletin, 63, 516–522.

    Article  CAS  Google Scholar 

  • Xing, Y., Lu, Y., Dawson, R. W., Shi, Y., Zhang, H., Wang, T., et al. (2005). A spatial temporal assessment of pollution from PCBs in China. Chemosphere, 60, 731–739.

    Article  CAS  Google Scholar 

  • Yamaguchi, N., Gazzard, D., Scholey, G., & Macdonald, D. W. (2003). Concentrations and hazard assessment of PCBs, organochlorine pesticides and mercury in fish species from the upper Thames: river pollution and its potential effects on top predators. Chemosphere, 50, 265–273.

    Article  CAS  Google Scholar 

  • Yamaguti, S. (1959). Systema Helminthum. II. The Cestodes of vertebrates. New York & London: Interscience Publishers.

    Google Scholar 

  • Yang, F., Wilcox, B., Jin, S., Aguirre, A. A., Rougée, L., Xu, Y., et al. (2008). Detection and quantitative analysis of polychlorinated biphenyls in tilapia from Hawaiian waters. Chemosphere, 73, 133–137.

    Article  CAS  Google Scholar 

  • Yang, Z., Shen, Z., Gao, F., Tang, Z., & Niu, J. (2009). Occurrence and possible sources of polychlorinated biphenyls in surface sediments. Chemosphere, 74, 1522–1530.

    Article  CAS  Google Scholar 

  • Zhang, Q., Ye, J., Chen, J., Xu, H., Wang, C., & Zhao, M. (2014). Risk assessment of polychlorinated biphenyls and heavy metals in soils of an abandoned e-waste site in China. Environmental Pollution, 185, 258–265.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by grants from the The Netherlands Government through NWO-WOTRO (grant no. W 01.83.2004.023) and partial funds from the Global Livestock Collaborative Research Support Program (GL-CRSP Grant No. LAG-G-00-96-90015-00. The lead also author also obtained additional funds from the Kenyan government through the National Council for Science and Technology (NCST) and Moi University Research Fund (MURF). We are grateful to ILRI who assisted in laboratory sample preparation and analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elijah Oyoo-Okoth.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oluoch-Otiego, J., Oyoo-Okoth, E., Kiptoo, K.K.G. et al. PCBs in fish and their cestode parasites in Lake Victoria. Environ Monit Assess 188, 483 (2016). https://doi.org/10.1007/s10661-016-5483-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-016-5483-0

Keywords

Navigation