Skip to main content Accessibility help

Levels of infection of gastric nematodes in a flock of great cormorants (Phalacrocorax carbo) from Lake Biwa, Japan

  • Kh.M. El-Dakhly (a1) (a2), E. El-Nahass (a1) (a3), S. Uni (a4), H. Tuji (a1), H. Sakai (a1) and T. Yanai (a1)...


A high prevalence (86.7%) of various species of nematodes was observed in the stomach of great cormorants living in Lake Biwa, Japan. There were varying numbers of adults belonging to two common genera, Eustrongylides Jagerskiold 1909 (Nematoda: Dioctophymatidae) and Contracaecum Railliet & Henry 1912 (Nematoda: Anisakidae). The first included common adenophorean nematodes comprising a single species, Eustrongylides tubifex and the second comprised ascaroid nematodes that contained four named species: Contracaecum rudolphii Hartwich, 1964, Contracaecum microcephalum Yamaguti, 1961, Contracaecum multipapillatum Drasche, 1882 and Contracaecum chubutensis Garbin, 2008. After the prevalence and intensity of the infection had been noted, both types of nematodes were frequently observed to penetrate the mucosa and intrude into the wall of the glandular stomach, where they caused gross haemorrhage and ulceration. The Eustrongylides sp. was predominantly found in a nodular lesion of the proventricular wall, while Contracaecum spp. were observed either free in the lumen of the proventriculus or, on occasion, deeply penetrating its wall. Of the Contracaecum spp., C. rudolphii was the most prevalent. Grossly, large numbers of nematodes were present in infected stomachs (for C. rudolphii intensity was 1–34 and 3–57 nematodes in male birds and 1–21 and 1–32 in females; for C. microcephalum 1–2 and 1 in male birds and 1–2 in females; for C. multipapillatum 2 in male cormorants and no infection in females; for C. chubutensis 1–2 and 1 in male birds and 1–5 and 1 in females and for E. tubifex 1–5 nematodes in male birds and 2–8 in females). Ulcerative inflammation and hyperaemia were the most common pathological presentations, especially in areas that had been invaded by parasites. Microscopically, varying degrees of granulomatous inflammatory reactions were seen, in addition to degenerated nematodes which appeared to have deeply penetrated mucosal surfaces and were surrounded by fibrous connective tissues.


Corresponding author

*Fax: +81-58-293-2943 E-mail:


Hide All
Abollo, E., Gestal, C. & Pascual, S. (2001) Anisakid infection in the European shag Phalacrocorax aristotelis aristotelis. Journal of Helminthology 75, 209214.
Abou Znada, N.Y. (1993) First record and prevalence of the caecal nematodes, Heterakis gallinarum and Subulura suctoria from the Guinea Fowl, Numedia meliagris, in Saudi Arabia. Journal of King Saud University 5, 5965.
Anderson, R.C. (1992) Nematode parasites of vertebrates: their development and transmission. Oxford, CAB International.
Armas de Conroy, G. (1986) Investigaciones sobre la fagicolosis en lisas (Mugilidae) de aguas americanas I. Estudios taxonomicos de Phagicola sp. (Trematoda: Heterophyidae) en mugilidos sudamericanos. Revista Iberica de Parasitologia 46, 3946.
Asakawa, M., Kimoto, Y. & Murata, K. (1997) First record of Eustrongylides tubefix (Dioctophymatidae) from Little Grebe, Tachybaptus ruficollis in Japan. Journal of Veterinary Medical Science 59, 955956.
Bancroft, J.D. & Stevens, A. (1996) Theory and practice of histological techniques. 4th edn.New York, Churchill Livingstone.
Barson, M. & Marshall, B.E. (2004) First record of Contracaecum spp. (Nematoda: Anisakidae) in fish-eating birds from Zimbabwe. Journal of South Africa Veterinary Association 75, 7478.
Bartlett, C.M. (1996) Morphogenesis of Contracaecum rudolphii (Nematoda: Ascaridoidea), a parasite of fish-eating birds, in its copepod precursor and fish intermediate hosts. Parasite 4, 367376.
Buendia, E. (1997) Anisakis, anisakidosis and allergy to Anisakis. Allergy 52, 481482.
Cancrini, G., Magro, G. & Giannone, G. (1997) Primo caso di anisakiosi extragastrointestinale nelluomo diagnosticato in Italia. Parasitologia 39, 1317.
Corn, J.L., Barre, N., Thiebot, B., Creekmore, T.E., Garris, G.I. & Nettles, V.F. (1993) Potential role of cattle egrets, Bulbucus ibis (Ciconiformes: Ardeide), in the dissemination of Amblyomma variegatum (Acari: Ixodidae) in the eastern Caribbean. Journal of Medical Entomology 30, 10291037.
Dick, T.A., Papst, M.H. & Paul, H.C. (1987) Rainbow trout (Salmo gairdneri) stocking and Contracaecum spp. Journal of Wildlife Diseases 23, 242247.
Dziekonska-Rynko, J. & Rokicki, J. (2007) Life cycle of nematode Contracaecum rudolphii Hartwig, 1964 (sensu lato) from northern Poland under laboratory conditions. Helminthologia 44, 95102.
Dziekonska-Rynko, J. & Rokicki, J. (2008) Infestation of the black cormorants (Phalacrocorax carbo sinensis L.1758) from the colony on the Selment Wielki, with the nematode Contracaecum rudolphii Hartwich, 1964 (Nematoda, Anisakidae). International Journal of Oceanography and Hydrobiology 37, 6171.
Fagerholm, H.P. (1988) Incubation in rats of a nematodal larva from cod to establish its specific identity: Contracaecum osculatum (Rudolphi). Parasitology Research 75, 5763.
Fagerholm, H.P., Overstreet, R.M. & Humphrey-Smith, I. (1996) Contracaecum magnipapillatum (Nematoda, Ascaroidoidea): resurrection and pathogenic effect of a common parasite from the proventriculus of Anous minutus from the Great Barrier Reef, with a note on C. variegatum. Helminthologia 33, 195207.
Friend, M. (1981) Waterfowl management and waterfowl disease: independent or cause and effect relationships? Transactions of the North American Wildlife Natural Resources Conference 46, 94103.
Hartwich, G. (1964) Revision der vogelparasitischen nematoden mitteleuropas, II. Di Gattung Contracaeum Railliet & Henry, 1912. Mitteilungen aus dem Zoologisches Museum Berlin 40, 1553.
Hartwich, G. (1974) Keys to genera of the Ascaridoidea. pp. 115in Chaubaud, A.G., Anderson, C.R.C. & Willmott, S. (Eds) CIH keys to the nematode parasites of vertebrates, Vol. 2. Farnham Royal, Commonwealth Agricultural Bureau.
Howard, R. & Moore, A. (1984) A complete checklist of the birds of the world. London, Macmillan.
Huizinga, H.W. (1966) Studies on the life cycle and development of Contracaecum spiculigerum (Rudolphi, 1809) (Ascaroidea: Heterocheilidae) from marine piscivorous birds. Journal of Elisha Mitchell Scientific Society 82, 181195.
Huizinga, H.W. (1971) Contracaecinasis in pelicaniformes birds. Journal of Wildlife Diseases 7, 198204.
Kanarek, G. & Bohdanowicz, J. (2009) Larval Contracaecum sp. (Nematoda: Anisakidae) in the Great Cormorant {Phalacrocorax carbo (L., 1758)} from north-eastern Poland: A morphological and morphometric analysis. Veterinary Parasitology 166, 9097.
Kanarek, G. & Rokichi, J. (2005) The status of the studies on the helminth fauna of the Great Cormorant (Phalacrocorax carbo sinensis) in northern Poland. Wiadomości Parazytologiczne 51, 165.
Kanarek, G., Rolbiecki, L., Sitko, J., Barus, V. & Rokichi, J. (2002) The occurrence of Contracaecum rudolphii Hartwig 1964 in the cormorant (Phalacrocorax carbo sinensis) in northern Poland. 5 Slovenske a ceske parasitologicke dni 28–31 maja 2002, Starta Lesna, Slovenska Republika. Program a zbornik abstractov, 22.
Karmanova, E.M. (1968) Dioctophymatoidea of animals and man and diseases caused by them. Fundamentals of nematology. 383 pp. Academy of Sciences of the USSR. Translated and published for the U.S. Department of Agriculture, Vol. 20. New Delhi, Amerind Publishing.
Kuiken, T., Leighton, F.A., Wobeser, G. & Wagner, B. (1999) Causes of morbidity and mortality and their effect on reproductive success in double-crested cormorants from Saskatchewam. Wildlife Diseases Association 35, 331346.
Mace, T.F. & Anderson, R.C. (1975) Development of the giant kidney worm, Dioctophyma renale (Goeze, 1782) (Nematoda: Dioctophymatoidea). Zoologicheskii Zhurnal 62, 113117(in Russian).
Malacalza, V., Poretti, T.I. & Bertellotti, M. (1994) La dieta de Phalacrocorax albiventer en Punta Leon (Chubut, Argentina) durante la temporada reproductiva. Ornitologia Neotropical 5, 9197.
Measures, L. (1988a) Revision of the genus Eustrongylides Jagerskiold, 1909 (Nematoda: Dioctophymatoidea) of piscivorous birds. Canadian Journal of Zoology 66, 885895.
Measures, L. (1988b) The development of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) in oligochaetes. Journal of Parasitology 74, 294304.
Measures, L. (1988c) Epizootiology, pathology, and description of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) in fish. Canadian Journal of Zoology 66, 22122222.
Measures, L. (1988d) The development and pathogenesis of Eustrongylides tubifex (Nematoda: Dioctophymatoidea) in piscivorous birds. Canadian Journal of Zoology 66, 22232232.
Mozgovoy, A.A., Shakhmatova, W.I. & Semenova, M.K. (1965) [Study of the life cycle of Contracaecum spiculigerum (Ascaridata: Anisakidae), a nematode of fish-eating birds]. Materials of the Scientific Conference of the All-Union Society of Parasitologists, Pt 4, pp. 169–174 (in Russian).
Mozgovoy, A.A., Shakhmatova, W.I. & Semenova, M.K. (1968) Life cycle of Contracaecum spiculgerum (Ascaridata: Anisakidae), a parasite of domestic and game birds. Trudy Gelmintologiczeskoj Labolatori 19, 129136.
National Wildlife Health Center, (1987) National Wildlife Health Center quarterly mortality report. April 1987–June 1987. Wildlife Disease Newsletter Supplement. Journal of Wildlife Diseases 23, 1011.
Pinto, R.M., Barros, L.A., Tortelly, L., Teixeira, R.F. & Gomes, D.C. (2004) Prevalence and pathology of ciconiiform birds from the Brazilian swamplands. Journal of Helminthology 78, 259264.
Sick, H. (2001) Ornitologia Brasileria. 912 pp. Rio de Janeiro, Editoria Nova Fronteira.
Spalding, M.G. (1990) Antemortem diagnosis of eustrongylidosis in wading birds (Ciconiiformes). Colonial Water Birds 13, 7577.
Spalding, M.G. & Forrester, D.J. (1993) Pathogenesis of Eustrongylides ignotus (Nematoda: Dioctophymatoidea) in Ciconiiformes. Journal of Wildlife Diseases 29, 250260.
Thomas, L.J. (1937a) On the life cycle of Contracaecum spiculigerum (Rud). Journal of Parasitology 23, 429431.
Thomas, L.J. (1937b) Further studies on the life cycle of Contracaecum spiculigerum. Journal of Parasitology 23, 572.
Wiese, J.H., Davidson, W.R. & Nettles, V.F. (1977) Large scale mortality of nestling ardeids caused by nematode infection. Journal of Wildlife Diseases 13, 376382.
Yamaguti, S. (1961) Systema Helminthum. Vol. III. The nematodes of vertebrates. Part 1. New York, Interscience.
Yang, T.B., Liao, X.H. & Zeng, B.P. (2000) Population ecology of Contracaecum rudolphii in the host Gymnocypris przewalski in the Qinghai Lake. Acta Hydrobiologica Sinica 24, 213218.
Yang, T.B., Miao, S.Y., Liao, X.H. & Wang, Z.J. (2001) Studies on the dynamic mechanism of cavity helminths in Gymnocypris przewalski in the Qinghai Lake. Acta Hydrobiologica Sinica 25, 268273.


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed