Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Acta Parasitologica

4 Issues per year

IMPACT FACTOR 2017: 1.039
5-year IMPACT FACTOR: 1.121

CiteScore 2017: 1.17

SCImago Journal Rank (SJR) 2017: 0.641
Source Normalized Impact per Paper (SNIP) 2017: 0.738

See all formats and pricing
More options …
Volume 62, Issue 2


Morphological re-description of Electrotaenia malapteruri (Cestoda: Proteocephalidae) and Dujardinnascaris malapteruri (Nematoda: Heterocheilidae) infecting the Electric catfish Malapterurus electricus and heavy metal accumulation in host and parasites in relation to water and sediment analysis in Lake Manzala, North Delta, Egypt

Rewaida Abdel-Gaber / Fathy Abdel-Ghaffar / Mohamed Abdallah Shazly / Kareem Morsy / Saleh Al Quraishy / Sanna Mohamed / Heinz Mehlhorn
Published Online: 2017-04-18 | DOI: https://doi.org/10.1515/ap-2017-0040


Parasites are one of the most serious limiting factors in aquaculture. The Electric catfish Malapterurus electricus was subjected to study the prevalence and mean intensity of parasitic infections throughout the whole year of 2015. Heavy metals accumulation in host fish and parasites were determined in relation to water quality and sediments of two different sites of Lake Manzala (Manzala and Bahr El-Baqar), Egypt. A total of 100 specimens of Electric catfish were collected and examined for the presence of helminth parasites. Two parasite species were recovered and morphologically identified. These were cestoda Electrotaenia malapteruri and nematode Dujardinnascaris malapteruri. Heavy metal analysis in water and sediments showed that measured heavy metals in Bahr El-Baqar were found in risky levels higher than permissible limits and Manzala site. Sediments were found to contain a higher level of metals than water samples. Heavy metals accumulation in recovered parasites and their host were also determined and showed significantly higher concentrations in parasites compared to their host tissues. According to bioconcentration factors, E. malapteruri showed that highest accumulation rate for all recorded elements up to 302. Essential elements like Cu and Fe were found in significantly higher concentrations in D. malapteruri, whereas E. malapteruri accumulated elements Cd, Pb, Ni, Mn, Zn and Ca to a significantly higher degree. Accordingly, the ratios (C[D.malapteruri]/C[E. malapteruri]) for most essential elements were higher than 0.5. Therefore, fish cestodes can be regarded as useful bio-indicators more than nematodes when evaluating the environmental pollution of aquatic ecosystems by heavy metals.

Keywords: Electrotaenia spp.; Dujardinnascaris spp.; Malapterurus electricus; morphological studies; heavy metals accumulation; biological indicators


  • Abdel-Baky T.E., Hagras A.E, Hassan S.H., Zyadah M.A. 1998. Environmental impact assessment of pollution in Lake Manzala, 1-Distribution of some heavy metals in water and sediment. Journal of the Egyptian German Society of Zoology, 26, 25–38Google Scholar

  • Abdel-Gaber R., Abdel-Ghaffar F., Bashtar A.R., Morsy K., Saleh R. 2016. Interaction between the intestinal parasite Polyonchobothrium clarias (Cestode: Ptychobothriidae) from the African sharptooth catfish Clarias gariepinus and heavy metal pollutants in an aquatic environment in Egypt. Journal of Helminthology, 8, 1–11. CrossrefGoogle Scholar

  • Abdel-Ghaffar F., Abdel-Gaber R., Bashtar A.R., Morsy K., Mehlhorn H., Al Quraishy S., Saleh R. 2015. Hysterothylacium aduncum (Nematoda, Anisakidae) with a new host record from the common sole Solea solea (Soleidae) and its role as a biological indicator of pollution. Parasitology Research, 114, 513–22. CrossrefGoogle Scholar

  • Abdel-Ghaffar F., Bashtar A.R., Abdel-Gaber R., Morsy K., Mehlhorn H., Al Quraishy S., Mohammed S. 2014. Cucullanus egyptae sp. nov. (Nematoda, Cucullanidae) infecting the European eel Anguilla anguilla in Egypt. Morphological and molecular phylogenetic studies. Parasitology Research, 113, 3457–65. CrossrefGoogle Scholar

  • Akhtar Y.(Ed.) 2008. Feeding habits and nematode parasites of some fishes of Karachi coast. Department of Botany, Jinnah University for Women, Nazimabad, Karachi, Pakistan pp. 268.Google Scholar

  • Ali H.R., Arifin M.M., Sheikh M.A., Shazili N.A., Bakari S.S., Bachok Z. 2014. Contamination of diuron in coastal waters around Malaysian Peninsular. Marine Pollution Bulletin, 85, 287–91. CrossrefGoogle Scholar

  • Ali M.H., Abdel-Satar A.M. 2005. Studies of some heavy metals in water, sediment, fish and fish diets in some fish farms in El-Fayoum province, Egypt. Egyptian Journal of Aquatic Research, 31, 261–273Google Scholar

  • Badawy M.I., Wahaab R.A. 1997. Environmental impact of some chemical pollutants on Lake Manzala. International Journal of Environmental Health Research, 7, 161–170Google Scholar

  • Baruš V., Jrkovský J., Prokeš M. 2007 Philometra ovata (Nematoda: Philometroidea): a potential sentinel species of heavy metal accumulation. Parasitology Research, 100, 929–933. CrossrefGoogle Scholar

  • Baylis H.A. 1923 Reports on collection of parasitic nematodes mainly from Egypt. Pt.1.Ascarida and Heterakidae; Pt. 11. Oxyuridae; Pt 111 Camallanidae etc. Parasitology, 15,1–38Google Scholar

  • Baylis H.A. 1947 The nematode genus Dujardinascaris (nom. nov. pro. Dujardinia) in Crocodilia with a description of a new species. The Annals and Magazine of Natural History, 14, 123–134Google Scholar

  • Bilqees F.M., Shabbir I., Haseeb M.F. 2004. Dujardinascaris karachiensis n. sp. (Heterocheilidae: Filopsularinae) from the fish Pomadasys olivaceus of Karachi coast. Proceedings of Parasitology, 38, 63–69Google Scholar

  • Bleeker P. 1858. De visschen van den Indischen Archipel. Beschreven en toegelicht. Siluri. Verhandelingen der Koninklijke Natuurkundige Vereeniging in Nederlandsch Indië [Acta Societatis Regiae Scientiarum Indo-Neêrlandicae], 4, i–xii + 1–370. [Also: Ichthyologiae Archipelagi Indici Prodromus, Vol 1. Siluri. Lange & Co., Batavia. xii + 370] ( In Duch)Google Scholar

  • Bush A.O., Lafferty K.D., Lotz J.M., Shostak W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583Google Scholar

  • Coetzee L., du Preez H.H., van Vuren J.H. 2002. Metal concentrations in Clarias gariepinus and Labeo umbratus from the Olifant and Klein Olifants River, Mpumalanga, South Africa: Zinc, copper, manganese, lead, chromium, nickel, aluminium and iron. Water SA, 28, 433–448Google Scholar

  • Courtney-Hogue C. 2016. Heavy metal accumulation in Lacistorhynchus dollfusi (Trypanorhyncha: Lacistorhynchidae) infecting Citharichthys sordidus (Pleuronectiformes: Bothidae) from Santa Monica Bay, Southern California. Parasitology, 143, 794–799. CrossrefGoogle Scholar

  • De Chambrier A., Scholz T., Ibraheem M.H. 2004. Redescription of Electrotaenia malapteruri Fritsch, 1886 (Cestoda: Proteocephalidae), a parasite of Malapterurus electricus (Siluriformes: Malapteruridae) from Egypt. Systematic Parasitology, 57, 97–109. CrossrefGoogle Scholar

  • Demirezen D., Uruc K. 2006. Comparative study of trace elements in certain fish, meat and meat products. Meat Science, 74, 255–260. CrossrefGoogle Scholar

  • Dick T.A., Choudhury A. 1995. Cestoidea (Phylum Platyhelminthes), dans P.T.K. Woo (Ed.), Fish diseases and disorders. 1 Protozoan and Metazoan Infection. CAB International, Oxon, UK, pp. 391–414Google Scholar

  • Dural M., Genc E., Sangun M.K., Güner, O. 2011. Accumulation of some heavy metals in Hysterothylacium aduncum (Nematoda) and its host sea bream, Sparus aurata (Sparidae) from North-Eastern Mediterranean Sea (Iskenderun Bay). Environmental Monitoring and Assessment, 174, 147–155. CrossrefGoogle Scholar

  • EHCW (Egyptian Higher Committee of Water). 1995. Egyptian standards for drinking and domestic water according to the Act 27/ 1978 in regulating of the public water supplies. Egyptian Governmental Press, EgyptGoogle Scholar

  • Eissa I.A.M. 2002. Text book of parasitic fish diseases in Egypt. Dar El-Nahdda El-Arabia, Cairo, Egypt Issa I.A.M., Ramadan A.F., Mohamed S.Y., Abdelmola H.I. 2010. Entero-parasitic infestation and the associated pathological lesions in Clarias gariepinus at Ismailia province. Journal of Agriculture and Veterinary Science, 3, 21–32Google Scholar

  • El-Seify M.A., Mahmoud N.A., Abou El-Wafa S.A., Abd El-Aal A.M.I. 1997. Studies on some enteric helminths of Nile fishes from Sharkia province, Lower Egypt. Egyptian Journal of Aquatic Biology and Fisheries, 1, 431–449Google Scholar

  • Fritsch G.(Ed.). 1886. Die Parasiten des Zitterwelses. Sitzungsberichte der Akademie der Wissenschaften zu Berlin, 6, 99–108. (In German)Google Scholar

  • Gedoeist L.(Ed.). 1916. Notes sur la Fauna parasitaira du Congo belge. Rev Zool Afric S, pp. 1–90. (In French)Google Scholar

  • Gmelin J.F. 1789. Caroli a Linné. Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species; cum Characteribus, Differentiis, Synonymis, Locis. Editio Decimo Tertia, Aucta, Reformata, Lipsiae. Fishes, 1, 3. (In French)Google Scholar

  • Hafesteinsson H., Rizvi S.S. 1987. A review of the sealworm problem: biology, implications and solutions. Journal of Food Production, 50, 70–84Google Scholar

  • Hoffman G.L. (2nd Ed.) 1970. Parasite of North American freshwater fishes. University of California Press, Berkeley, pp. 480Google Scholar

  • Ibrahim A.M., Bahnasawy M.H., Mansy S.E., El-Fayomy R.I. 1999. Heavy metal accumulation in water, sediment and some fishes in Lake Manzala, Egypt. Journal of Egyptian German Society of Zoology, 29, 43–58Google Scholar

  • Innes W.T. (19th Ed.). 1966. Exotic aquarium fishes. New Jersey, Aquarium Incorporated.Google Scholar

  • Khaleghzadeh-Ahangar H., Malek M., McKenzie K. 2011. The parasitic nematodes Hysterothylacium sp. type MB larvae as bioindicators of lead and cadmium: a comparative study of parasite and host tissues. Parasitology, 138, 1400–1405. CrossrefGoogle Scholar

  • Khalil L.F., Polling L. (2nd Ed.). 1997. Checklist of the helminth parasites of African freshwater fishes. Pietersburg: University of the North, pp.185Google Scholar

  • Khallaf E.A., Galal M., Authman M. 1998. Assessment of heavy metals pollution and their effects on Oreochromis niloticus in aquatic drainage canals. Journal of Egyptian German Society of Zoology, 26, 39–74Google Scholar

  • Klimpel S., Abdel-Ghaffar F., Al-Rasheid K.A., Aksu G., Fischer K., Strassen B., Mehlhorn H. 2011. The effects of different plant extracts on nematodes. Parasitology Research, 108, 1047–1054. CrossrefGoogle Scholar

  • La Rue G.R. 1911. A revision of the cestode family Proteocephalidae. Zoologischer Anzeiger, 38, 473–482Google Scholar

  • Mazhar R., Shazili N.A., Harrison F.S. 2014. Comparative study of the metal accumulation in Hysterothalycium reliquens (nematode) and Paraphilometroides nemipteri (nematode) as compared with their doubly infected host, Nemipterus peronii (Notched threadfin bream). Parasitology Research, 113, 3737-43. .CrossrefGoogle Scholar

  • Nachev M., Schertzinger G., Sures B. 2013. Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasites and Vectors, 6, 1–8. CrossrefGoogle Scholar

  • Nybelin O. (Ed.). 1942. Zur Helminthen Fauna der Süsswasserfische Schwedens. II. Die Cestodes des Welses. Bihang till Göteborgs Kungliga Vetenskaps-och Vitterhets-samhälles Handlingar, B1, 1–24 ( In German)Google Scholar

  • Page A.L., Miller R.H., Kenney D.R. 1982. Heavy metals determination, Methods of soil analysis, part 2, chemical and microbiological properties. American Society of Agronomy, Madison, pp.8Google Scholar

  • Palíková M., Baruš V. 2003. Mercury content in Aguillicola crassus (Nematoda) and its host Anguilla anguilla. Acta Veterinaria Brno, 72, 289–294Google Scholar

  • Pourang N. 1995. Heavy metal bioaccumulation in different tissues of two fish species with regards to their feeding habits and trophic levels. Environmental Monitoring and Assessment, 35, 207–219. CrossrefGoogle Scholar

  • Pradit S., Shazili N.A., Towatana P., Saengmanee W. 2016. Accumulation of Trace Metals in Anadara granosa and Anadara inaequivalvis from Pattani Bay and the Setiu Wetlands. Bulletin of Environmental Contamination and Toxicology, 96, 472–7. CrossrefGoogle Scholar

  • Radwan S., Kowalik W., Kornijow R. 1990. Accumulation of heavy metals in a lake ecosystem. The Science of the Total Environment, 96, 121–129Google Scholar

  • Railliet A., Henry A. 1905. Un nouveau sclerotomien (Triodontophorus deminutus Nov. sp.) parasite de’I’ homme. Comptes Rendus De La Societe De Biologie, 58, 569–571. (In French)Google Scholar

  • Rego A.A. 1994. Order Proteocephalidea Mola, 1928. In: Khalil LF, Jones A, Bray RA (Eds) Keys to the cestode parasites of vertebrates. Wallingford: CAB International, pp. 257–293Google Scholar

  • Schludermann C., Konecny R., Laimgruber S., Lewis J.W., Schiemer F., Chovanec A., Sures B. 2003. Fish macroparasites as indicators of heavy metal pollution in river sites in Austria. Parasitology, 123, S61–S69Google Scholar

  • Shakweer L.M. 1998. Concentration levels of some trace metals in Oreochromis niloticus at highly and less polluted areas of Mariut Lake. Journal of Egyptian German Society of Zoology, 25, 125–144Google Scholar

  • Sprent J.F.A. 1990. Some ascaridoid nematodes of fishes: Heterocheilinae. Systematic Parasitology, 16, 149–161. CrossrefGoogle Scholar

  • Sures B., Steiner W., Rydlo M., Taraschewski H. 1999. Concentrations of 17 elements in the zebra mussel (Dreissena polymorpha), in different tissues of perch (Perca fluviatilis), and in perch intestinal parasites (Acanthocephalus lucii) from the subalpin lake Mondsee (Austria). Environmental Toxicology and Chemistry, 18, 2574–2579. CrossrefGoogle Scholar

  • Tenora F., Baruš V., Kráčmar S., Dvořáček J. 2000. Concentration of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometra ovate (Nematoda) compared to some their hosts (Osteichthyes). Helminthologia, 37, 15–18Google Scholar

  • Torres J., Eira C., Miquel J., Ferrer-Maza D., Delgado E., Casadevall M. 2015. Effect of Intestinal Tapeworm Clestobothrium crassiceps on Concentrations of Toxic Elements and Selenium in European Hake Merluccius merluccius from the Gulf of Lion (Northwestern Mediterranean Sea). Journal of Agricultural and Food Chemistry, 63, 9349–56. CrossrefGoogle Scholar

  • UNEP/FAO/IOC/IAEA. 1984. Sampling of selected marine organisms and sample preparation for trace metal analysis: Reference methods for marine pollution studies. Revision, 2, 19Google Scholar

  • USEPA. 1986. United States Environmental Protection Agency. Quality criteria for water. EPA 440 15-86-001Google Scholar

  • Vidal-Martinez V.M., Pech D., Sures B., Purucker T., Poulin R. 2010. Can parasites really reveal environmental impact?. Trends Parasitol, 26, 44–51. CrossrefGoogle Scholar

  • WHO–IPCS–Environmental Health. 1987. International program of chemical safety. WHO–IPCS–Environmental Health Criteria Report, with ILO and UNEP. Geneva, Switzerland, WHOGoogle Scholar

  • Woo P.T.K. (2nd Ed.) 1995. fish diseases and disorders Vol. 1 (Protozoan and Metazoan infections) CAB, Int., Wallingford, Oxan, UKGoogle Scholar

  • Yamaguti S. 1941. Studies on the helminth fauna of Japan. Part II. Nematodes of fishes. Japanese Journal of Zoology, 9, 343–396Google Scholar

  • Yamaguti S. 1941. Studies on the helminth fauna of Japan. Part II. Nematodes of fishes. Japanese Journal of Zoology, 9, 343–396Google Scholar

  • Yamaguti S. (2nd Ed.) 1961. Systema Helminthum. Vol. III. The Nematodes of Vertebrates. Part I and II. Interscience Publishers, Inc., New York and LondonGoogle Scholar

  • Yılmaz A.B. 2005. Comparison of heavy metal levels of grey mullet (Mugil cephalus) and sea bream (Sparus aurata) caught in İskenderun Bay (Turkey). Turkish Journal of Veterinary and Animal Sciences, 29, 257–262Google Scholar

About the article

Received: 2016-09-14

Revised: 2017-01-17

Accepted: 2017-01-19

Published Online: 2017-04-18

Published in Print: 2017-06-01

Conflict of Interest. The authors have indicated that they have no conflict of interest regarding the content of this article.

Citation Information: Acta Parasitologica, Volume 62, Issue 2, Pages 319–335, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0040.

Export Citation

© 2017 W. Stefański Institute of Parasitology, PAS.Get Permission

Comments (0)

Please log in or register to comment.
Log in