Folia Parasitologica, vol. 63 (2016)

Folia Parasitologica 63:017 (2016) | DOI: 10.14411/fp.2016.017

Scanning and transmission electron microscopy of the histopathological impact of Macrogyrodactylus clarii (Monogenea: Gyrodactylidae) on the gills of catfish, Clarias gariepinus

Mohammed Mohammed El-Naggar1,2, Joanne Cable2, Safaa Zaky Arafa1,3, Samir Ahmed El-Abbassy1, Graham C. Kearn4
1 Zoology Department, Faculty of Science, Mansoura University, Mansoura, Egypt;
2 School of Biosciences, Cardiff University, UK;
3 Biology Department, College of Medicine, University of Dammam, Kingdom of Saudi Arabia;
4 School of Biological Sciences, University of East Anglia, Norwich, UK

Scanning and transmission electron microscopy (TEM) were used to study the histopathological effects of the monogenean Macrogyrodactylus clarii Gussev, 1961 on the gills of the catfish Clarias gariepinus (Burchell). Suction generated during attachment created 'footprints' on host surfaces in which the host tissues were elevated above the general gill surface. 'Footprints' were bordered by four clefts caused by the muscular flaps on the anterior, lateral and posterior margins of the haptor. The hamuli points penetrate the gill tissue but no evidence was found for the insertion of the marginal hooklets. At the site of attachment, host cells adjacent to the lateral flaps often appeared compressed and widely spaced with large intercellular spaces. Desquamation of these surface epithelia was also apparent and some of the widely spaced epithelial cells had pseudopodium-like processes. Cells within the upper surface epithelial layer of the host were vacuolated and necrotic. Ruptured blood capillaries (blood spaces) in the secondary gill lamellae contained atypical compressed erythrocytes, agranular and granular leucocytes and evidence of haemorrhaging. Cells with fibrotic cytoplasm, putative phagocytes and host mucous cells were evidence of a host response at the site of parasite attachment. The possible role of these cells is discussed in relation to host resistance against infection.

Keywords: ultrastructure, histopathology, fish disease, aquatic health, monogeneans

Received: January 14, 2016; Accepted: April 26, 2016; Published online: June 2, 2016


References

  1. Abdelmonem A.A., Metwally M.M., Hussein H.S. 2010: Gross and microscopic pathological changes associated with parasitic infection in European eel (Anguilla anguilla Linnaeus, 1758). Parasitol Res. 106: 463-469. Go to original source... Go to PubMed...
  2. Ali M.Z. 2001: Dietary protein and energy interactions in African catfish Clarias gariepinus (Burchell, 1822). PhD Thesis, Institute of Aquaculture, University of Stirling, Stirling, 217 pp.
  3. Aly S., Mayberry L., El-Melegy A., El-Gwady H. 1995a: Pathological studies on parasitic infections in Tilapia nilotica. Egypt. J. Comp. Pathol. Clinic. Pathol. 8: 147-157.
  4. Aly S., Mayberry L., El-Melegy A., El-Gwady H. 1995b: Pathological studies on parasitic infections in common carp. Egypt. J. Comp. Pathol. Clinic. Pathol. 8: 123-130.
  5. Amatyakul C. 1972: Parasites of pond-raised Clarias in Thailand. FAO Aquacult. Bull. 5: 16-17.
  6. Arafa S.Z., El-Naggar M.M., El-Abbassy S.A. 2009: Mode of attachment and histopathological effects of Macrogyrodactylus clarii, a monogenean gill parasite of the catfish Clarias gariepinus, with a report on host response. Acta Parasitol. 54: 103-112. Go to original source...
  7. Arafa S.Z., El-Naggar M.M., Kearn G.C. 2003: Scanning electron microscope observations on the monogenean skin parasite Macrogyrodactylus congolensis (Prudhoe, 1957) Yamaguti, 1963. Acta Parasitol. 48: 163-171.
  8. Bishai H.M., Khalil M.T. 1997: Freshwater Fishes of Egypt. Publication of the National Biodiversity Unit No. 9, Department of Natural Protectorate, Egyptian Environmental Affairs Agency, Cario, 229 pp.
  9. Buchmann K., Bresciani J. 1998: Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitol. Res. 84: 17-24. Go to original source... Go to PubMed...
  10. Cable J., Harris P.D. 2002: Gyrodactylid developmental biology: historical review, current status and future trends. Int. J. Parasitol. 32: 255-280. Go to original source... Go to PubMed...
  11. Cone D.K., Beverley-Burton M., Wiles M., McDonald T.E. 1983: The taxonomy of Gyrodactylus (Monogenea) parasitizing certain salmonid fishes of North America, with a description of G. nerkae n. sp. Can. J. Zool. 61: 2587-2597. Go to original source...
  12. Cone D.K., Odense P.H. 1984: Pathology of five species of Gyrodactylus von Nordmann, 1832 (Monogenea). Can. J. Zool. 62: 1084-1088. Go to original source...
  13. Dezfuli B.S., Giari L., Simoni E., Menegatti R., Shinn A.P., Manera M. 2007: Gill histopathology of cultured European sea bass, Dicentrarchus labrax (L.), infected with Diplectanum aequans (Wagener 1857) Diesing 1958 (Diplectanidae: Monogenea). Parasitol. Res. 100: 707-713. Go to original source... Go to PubMed...
  14. El-Naggar M.M., Hagras A.E., Ogawa K., Hussein A.B., El-Naggar A.M. 2001: Attachment of Cichlidogyrus monogenean species to the gills of the Nile fish Oreochromis niloticus and their local pathological impact on them. J. Egypt. Ger. Soc. Zool. 35: 143-155.
  15. El-Naggar M.M., Serag H.M. 1987: Redescription of Macrogyrodactylus clarii Gussev 1961, a monogenean gill parasite of Clarias lazera in Egypt. Arab. Gulf J. Sci. Res. Agric. Biol. Sci. 5: 257-271.
  16. El-Seify M., Soliman M.K., Mahfouz N.B. 1998: Effect of parasitism on certain immunological parameters of cultured fishes. Egypt. J. Aquat. Biol. Fish. 2: 379-405.
  17. Elsheikh E.H. 2013: Scanning electron microscopic studies of gill arches and rakers in relation to feeding habits of some fresh water fishes. J. Basic Appl. Zool. 66: 121-130. Go to original source...
  18. Evans D.L., Gratzek J.B. 1989: Immune defense mechanisms in fish protozoan and helminth infections. Am. Zool. 29: 409-418. Go to original source...
  19. FAO 1997: Aquaculture production, 1986-1995, FAO Fish Circ. No 815 (FIDID/815-Rev.9), FAO, Italy.
  20. Harris P.D. 1983: The morphology and life-cycle of the oviparous Gyrodactylus farlowellae gen. et sp. nov. (Monogenea: Gyrodactylidae). Parasitology 87: 405-420. Go to original source...
  21. Harris P.D., Cable J., Tinsley R.C. 1997: Detection of sperms within Gyrodactylus (Platyhelminthes, Monogenea) tissues using fluorescence and transmission electron microscopy. Parasitol. Res. 83: 533-538. Go to original source... Go to PubMed...
  22. Hogendoorm H. 1983: The African catfish, (Clarias lazera C. & V., 1840) a new species for aquaculture. PhD thesis, Wageningen Agricultural University, Wageningen, 135 pp.
  23. Johnsen B.O., Jensen A. 1986: Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers. J. Fish Biol. 29: 233-241. Go to original source...
  24. Kearn G.C. 2004: Leeches, Lice and Lampreys. A Natural History of Skin and Gill Parasites of Fishes. Springer, Dordrecht, 432 pp.
  25. Khalil L. 1964: On the biology of Macrogyrodactylus polypteri Malmberg, 1956, a monogenetic trematode on Polypterus senegalus in the Sudan. J. Helminthol. 38: 219-222. Go to original source... Go to PubMed...
  26. Kritsky D.C. 1990: Synonymy of Paraquadriacanthus Ergens, 1988 (Monogenea: Dactylogyridae) and their type species. Folia Parasitol. 37: 76.
  27. Lester R.J.G. 1972: Attachment of Gyrodactylus to Gasterosteus and host response. J. Parasitol. 58: 717-772. Go to original source... Go to PubMed...
  28. Molnár K. 1972: Studies on gill parasitosis of the grass carp (Ctenopharyngodon idella) caused by Dactylogyrus lamellatus Achmerov, 1952. IV. Histopathological changes. Acta Vet. Acad. Sci. Hung. 22: 9-24. Go to PubMed...
  29. Obiekezie A.I., Taege M. 1991: Mortality in hatchery reared fry of the African catfish Clarias gariepinus (Burchell) caused by Gyrodactylus groschafti Ergens, 1973. Bull. Eur. Ass. Fish Pathol. 11: 82-85.
  30. Ogawa K., Egusa S. 1980: Gyrodactylus infections of cultured eels (Anguilla japonica and A. anguilla) in Japan. Fish Pathol. 15: 95-99. Go to original source...
  31. Paladini G., Cable J., Fioravanti M.L., Faria P.J., Cave D.D. 2009: Gyrodactylus orecchiae sp. n. (Monogenea: Gyrodactylidae) from farmed populations of gilthead seabream (Sparus aurata) in the Adriatic Sea. Folia Parasitol. 56: 21-28. Go to original source... Go to PubMed...
  32. Perera K.M.L. 1992: Ultrastructure of the primary gill lamellae of Scomber australasicus infected by a didymozoid parasite. Dis. Aquat. Organ. 13: 111-121. Go to original source...
  33. Perera K.M.L. 1994: Light and electron microscopic study of the pathology of a species of didymozoid (Trematoda, Digenea) infecting the gill arches of Scomber australasicus (Teleostei, Scombridae). Dis. Aquat. Organ. 18: 119-127. Go to original source...
  34. Pottinger T.G., Pickering A.D., Biackstock N. 1984: Ectoparasite-induced changes in epidermal mucification of the brown trout Salmo trutta L. J. Fish Biol. 25: 123-126. Go to original source...
  35. Ramadan N.F., El-Banhawy M.A., Abdel Salam M.A. 1995: Parasitological investigation on two monogenetic trematodes and their pathological impact on the grass carp Ctenopharyngodon idella in Egypt. J. Egypt. Germ. Soc. Zool. 17: 17-37.
  36. Reda E.S., El-Naggar A.M. 2003: Mode of attachment of the monogenean Protoancylodiscoides mansourensis El-Naggar, 1987 to gills of the longfin catfish Chrysichthys auratus, with reference to host-parasite interface, Egypt. J. Aquat. Biol. Fish. 7: 359-380.
  37. Robertson D.A., Roberts R.J., Bullock A.M. 1981: Pathogenesis and autoradiographic studies of the epidermis of the salmonids infested with Ichthyobodo necator (Henneguy, 1883). J. Fish Dis. 4: 113-125. Go to original source...
  38. Rohde K. 1984: Diseases caused by metazoans: helminths. Dis. Mar. Animal 4: 193-320.
  39. Roubal F.R., Bullock A.M., Robertson D.A., Roberts R.J. 1987: Ultrastructural aspects of infestation by Ichthyobodo necator (Henneguy, 1883) on the skin and gills of the salmonids Salmo salar L. and Salmo gairdneri Richardson. J. Fish. Dis. 10: 181-192. Go to original source...
  40. Sakai D.K. 1992: Repertoire of complement in immunological defense mechanisms of fish. Ann. Rev. Fish Dis. 2: 223-247. Go to original source...
  41. Saoud M.F., Mageed A. 1969: Host parasite relationship of Macrogyrodactylus polypteri (Trematoda: Monogenea) in some fishes of the Sudan. Curr. Sci. 38: 209-210.
  42. Senger M., Yadav L., Gopesh A. 2011: Fine structure of the gill epithelia of the African catfish Clarias gariepinus (Bur.) ESEM and TEM study of principal cell types. Nat. Acad. Sci. Let. 34: 285-291.
  43. St. Louis-Cormier E.A., Osterland C.K., Anderson P.D. 1984: Evidence for a cutaneous secretory immune system in rainbow trout (Salmo gairdneri). Develop. Comp. Immunol. 8: 715-780. Go to original source...
  44. Sterud E., Harris P.H., Bakke T.A., 1998. The influence of Gyrodactylus salaris Malmberg, 1957 (Monogenea) on the epidermis of Atlantic salmon, Salmo salar L., and brook trout, Salvelinus fontinalis (Mitchill), experimental studies. J. Fish Dis. 21: 257-263. Go to original source...
  45. Wells P.R., Cone D.K. 1990: Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on the density of the mucous cells in the epidermis of fry of Oncorhynchus mykiss. J. Fish Biol. 37: 5995-5603. Go to original source...
  46. Wilson J.M., Laurent P. 2002: Fish gill morphology: inside out. J. Exp. Zool. 293: 192-213. Go to original source... Go to PubMed...
  47. Yano T. 1996: The nonspecific immune system: humoral defense. In: G. Iwama and T. Nakanishi (Eds.), The Fish Immune System: Organism, Pathogen and Environment. Academic Press, New York, pp. 106-157.