Systematic Parasitology

, Volume 96, Issue 3, pp 279–297 | Cite as

Two new cestode species of the family Hymenolepididae Perrier, 1897 (Cyclophyllidea) from passerine birds in Ethiopia, with the erection of Citrilolepis n. g.

  • Yana D. Dimitrova
  • Boyko B. Georgiev
  • Jean Mariaux
  • Gergana P. VasilevaEmail author
Part of the following topical collections:
  1. Cestoda


Two new cestode species of the family Hymenolepididae Perrier, 1897 are described from birds of the order Passeriformes at Wondo Genet, Ethiopia. Passerilepis zimbebel n. sp., a parasite of Terpsiphone viridis (Müller) (Monarchidae), is distinguished from its most similar congeners by its diorchoid rostellar hooks with length 37–38 μm, its median ovary consisting of three compact lobes, its compact vitellarium and the variable position of the terminal genital ducts passing mostly dorsally to the poral osmoregulatory canals. Citrilolepis n. g. is erected as monotypic for C. citrili n. sp., a parasite of Crithagra citrinelloides (Rüpell) (Fringillidae). The new genus is distinguished from the remaining avian and mammalian genera of the family Hymenolepididae by the presence of numerous (18) rostellar hooks, unilateral sinistral genital pores, ventral osmoregulatory canals with transverse anastomoses, 3 (rarely 4, in c.10% of proglottides) testes in number with variable positions in the proglottis and the sac-like uterus not extending beyond the osmoregulatory canals.



We are grateful to Professor Abebe Getahun of the Addis Ababa University for his support in organisation of the field studies as well as to Mr Yeneneh Teka of the Ethiopian Wildlife Conservation Authority (EWCA) for issuing the necessary permits for field studies. Field work assistance was provided by Mr Girma Ayalew and Mr Teklebrhan Kidane (EWCA) as well as by Mr Henok Getachew. We are especially grateful to Dr Andrea Waeschenbach (London) for sharing unpublished sequence data and depositing them in GenBank. We used facilities developed at the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, in the frames of the projects WETLANET (EC FP7, Programme CAPACITIES, Grant 229802) and CEBDER (National Science Fund of the Republic of Bulgaria, Grant DOO2–15/17.02.2009).


This work was funded by the National Science Foundation of the USA, PBI grants DEB 0818696 and DEB 0818823 (to Janine N. Caira and Kirsten Jensen).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed. The field study was permitted by Memorandum of Understanding signed by the Director, Wildlife Utilization Directorate, EWCA, and the research team on 20th November 2012 in Addis Ababa.


  1. Alexander, S., & McLaughlin, J. D. (1993). Microsomacanthus macrotesticulata n. sp. (Cestoda: Hymenolepididae) from South African waterfowl. Journal of Parasitology, 79, 843–846.CrossRefGoogle Scholar
  2. Alexander, S. J., & McLaughlin, J. D. (1996). Fimbriasacculus africanensis n. gen., n. sp. (Cestoda: Hymenolepididae) from Anas capensis, Anas undulata, and Anas erythrorhyncha (Anatidae) in South Africa. Journal of Parasitology, 82, 907–909.CrossRefPubMedGoogle Scholar
  3. Baer, J.-G. (1933). Contribution a l’étude de la Faune helminthologique africaine. Revue Suisse de Zoologie, 40, 31–84.CrossRefGoogle Scholar
  4. Baer, J., & Fain, A. (1955). Cestodes. In: Exploration du Parc National de l’Upemba, Fasc. 36, Mission G. F. de Witte. Bruxelles: Institut des Parc Nationaux du Congo Belge, 38 pp.Google Scholar
  5. Bondarenko, S. K., & Kontrimavichus, V. L. (2006). Aploparaksidae of wild and domesticated birds. In: Movsesyan, S. O. (Ed.), Fundamentals of Cestodology, Vol. 14. Moscow: Nauka, 443 pp (In Russian).Google Scholar
  6. Burt, D. R. R. (1944). New avian species of Hymenolepis from Ceylon. Ceylon Journal of Sciences (B), 22, 165–172.Google Scholar
  7. Canaris, A. G., & Gardner, S. L. (2003). Bibliography of helminth species described from African vertebrates 1800–1967. Faculty Publications from the Harold W. Manter Laboratory of Parasitology. Accessed 18 January 2019.
  8. Clerc, W. (1906). Notes sur les cestodes d’oiseaux de l’Oural. A. Sur quelques espèces d’Hymenolepis. Centralblatt für Bakteriologie. Parasitenkunde und Infektionskrankheiten. Erste Abteilung. Originale, 42, 532–536.Google Scholar
  9. Czaplinski, B., & Vaucher, C. (1986). Helminthes parasites du Paraguay VIII. Redescription de Fuhrmanacanthus propeteres (Fuhrmann, 1907) Spassky, 1966 (Syn. Lateriporus biuterinus Fuhrmann, 1908) (Cestoda: Hymenolepidiae) et remarques sur les genres Fuhrmanacanthus Spassky, 1966 et Hamatolepis Spassky, 1962. Systematic Parasitology, 8, 83–90.Google Scholar
  10. Czaplinski, B., & Vaucher, C. (1994). Family Hymenolepididae Ariola, 1899. In: Khalil, L. F., Jones, A. & Bray, R. A. (Eds), Keys to the Cestode Parasites of Vertebrates. Wallingford: CAB International, pp. 595–663.Google Scholar
  11. Deardorff, T. L., & Brooks, D. R. (1978). Passerilepis schmidti sp. n. (Cestoidea: Hymenolepididae) from the blue jay, Cyanocitta cristata L. in Nebraska. Proceedings of the Helminthological Society of Washington, 45, 190–192.Google Scholar
  12. Fuhrmann, O. (1906a). Die Hymenolepis-Arten der Vögel. I. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten. Erste Abteilung, Originale, 41, 440–452.Google Scholar
  13. Fuhrmann, O. (1906b). Die Hymenolepisarten der Vögel. II. Allgemeiner Teil. Centralblatt für Bakteriologie. Parasitenkunde und Infektionskrankheiten. Erste Abteilung, Originale, 42, 730–755.Google Scholar
  14. Fuhrmann, O. (1907). Bekannte und neue Arten und Genera von Vögeltänien. Centralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten, 45, 516–536.Google Scholar
  15. Fuhrmann, O. (1909). Vermes 2. Cestodes. Wissenschftliche Ergebnisse der Schwedischen Zoologischen Expedition nach dem Kilimandjaro, dem Meru und dem umgebenden Massaisteppen Deutsch Ostafrikas 1905–1906, 3, 11–22.Google Scholar
  16. Fuhrmann, O. (1918). Cestodes d’oiseaux de la Nouvelle-Calédonie et des Iles Loyalty. Nova Caledonia (Sarasin et Roux). A. Zoologie, 2, 399–449.Google Scholar
  17. Fuhrmann, O. (1943). Cestodes d’Angola. Revue Suisse de Zoologie, 50, 449–471.Google Scholar
  18. Fuhrmann, O., & Baer, J.-G. (1943). Mission biologique Sagan-Omo (Ethiopie méridionale), 1939, dirigée par le professeur Eduardo Zavattari. Cestodes. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 68, 113–140.Google Scholar
  19. Georgiev, B., Biserkov, V., & Genov, T. (1986). In toto staining method for cestodes with iron acetocarmine. Helminthologia, 23, 279–281.Google Scholar
  20. Graber, M., Blanc, P., & Delavenay, R. (1980). Helminthes des animaux sauvages dʼEthiopie. 2. Oiseaux. Bulletin de lʼInstitut Fondamental d’Afrique Noire, Série A, 42, 545–570.Google Scholar
  21. Greiman, S. E., & Tkach, V. V. (2012). Description and phylogenetic relationships of Rodentolepis gnoskei n. sp. (Cyclophyllidea: Hymenolepididae) from a shrew Suncus varilla minor in Malawi. Parasitology International, 61, 343–350.CrossRefPubMedGoogle Scholar
  22. Greiman, S. E., Tkach, V. V., & Cook, J. A. (2013). Description and molecular differentiation of a new Staphylocystoides (Cyclophyllidea: Hymenolepididae) from the Dusky Shrew Sorex monticolus in Southeast Alaska. Journal of Parasitology, 99, 1045–1049.CrossRefPubMedGoogle Scholar
  23. Gulyaev, V. D., & Makarikov, A. A. (2007). Relictolepis gen. n., a new cestode genus (Cyclophyllidea: Hymenolepididae) of rodents from Far East and the description R. feodorovi sp. n. Parasitologiya, 32, 399–405 (In Russian).Google Scholar
  24. Joyeux, C., & Baer, J.-G. (1928). Cestodes. (pp. 17–54). In: Joyeux, C., Gendre, E. & Baer, J.-G. (Eds), Recherches sur les helminthes de l’Afrique occidentale française. (Collection de la Société de Pathologie Exotique, Monographie II.). Masson et Cie, Éditeurs, Paris, 120 pp.Google Scholar
  25. Joyeux, C., & Baer, J.-G. (1940). Sur quelques cestodes. Revue Suisse de Zoologie, 47, 381–388.Google Scholar
  26. Joyeux, C., Baer, J.-G., & Martin, R. (1936). Sur quelques cestodes de Somalie-Nord. Bulletin de la Société de Pathologie Exotique, 29, 82–95.Google Scholar
  27. Khalil, L. F., Jones, A., & Bray, R. A. (Eds) (1994). Keys to the Cestode Parasites of Vertebrates. Wallingford, UK: CAB International, 751 pp.Google Scholar
  28. Krabbe, H. (1869). Bidrag til Kundskab om Fuglenes Baendelorme. Videskabelige Selskab Skrifter, 5. Raekhe, Naturvidenskabelig og Mathematisk Afdel, 8, 249–363.Google Scholar
  29. Krabbe, H. (1879). The Turkestan expedition of A. P. Fedchenko. Part II. Vermes. Izvestiya Imperatorskogo Obshchestva Lyubiteley Estestvoznania, Antropologii i Etnografii, 34, 1–23 (In Russian).Google Scholar
  30. Kuchta, R., Burianová, A., Jirků, M., de Chambrier, A., Oros, M., Brabec, J., et al. (2012). Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa, including erection of Kirstenella n. gen. and description of Tetracampos martinae n. sp. Zootaxa, 3309, 1–35.CrossRefGoogle Scholar
  31. Lepage, D. (2019). Avibase, the World Bird Database. Accessed 4 January 2019.
  32. Mahon, J. (1954). Contributions to the helminth fauna of tropical Africa: Tapeworms from the Belgian Congo. Annales du Musée Royal du Congo Belge, C, Zoologie Série, 1, 137–263.Google Scholar
  33. Mahon, J. (1958). Helminth parasites of reptiles, birds and mammals of Egypt. V. Avian Cestodes. Canadian Journal of Zoology, 36, 577–605.CrossRefGoogle Scholar
  34. Makarikov, A. A. (2017). A taxonomic review of hymenolepidids (Eucestoda, Hymenolepididae) from dormice (Rodentia, Gliridae), with descriptions of two new species. Acta Parasitologica, 62, 1–21.CrossRefPubMedGoogle Scholar
  35. Makarikov, A. A., & Gulyaev, V. D. (2009). [Pararodentolepis gen. n. - a new cestode genus from rodents and the description of P. sinistra sp. n. (Cyclophyllidea: Hymenolepididae).] Parazitologiya, 43, 454–459 (In Russian).Google Scholar
  36. Makarikov, A. A., Gulyaev, V. D., & Krivopalov, A. V. (2010). Nomadolepis (Cyclophyllidea, Hymenolepididae), a new genus of cestodes from rodents. Zoologicheskiy Zhurnal, 89, 948–955 (In Russian).Google Scholar
  37. Makarikova, T. A., & Makarikov, A. A. (2012). First report of Potorolepis Spassky, 1994 (Eucestoda: Hymenolepididae) from China, with description of a new species in bats (Chiroptera: Rhinolophidae). Folia Parasitologica, 59, 272–278.CrossRefPubMedGoogle Scholar
  38. Makarikova, T. A., & Makarikov, A. A. (2013). Sawadalepis prima n. g., n. sp. (Cestoda: Cyclophyllidea) from the Schreiber’s bent-winged bat Miniopterus schreibersii Kuhl (Chiroptera: Vespertilionidae) from China. Systematic Parasitology, 86, 59–68.CrossRefPubMedGoogle Scholar
  39. Makarikova, T. A., Gulyaev, V. D., Tiunov, M. P., & Feng, J. (2010). Cestodes Paramilina nishidai (Sawada, 1982) gen. n., comb. n. and Hymenolepis magna sp. n. (Cyclophyllidea: Hymenolepididae) from Chiroptera in China. Zoolgicheskiy Zhurnal, 89, 131–139 (In Russian).Google Scholar
  40. Mariaux, J. (1994). Avian cestodes of the Ivory Coast. Journal of the Helminthological Society of Washington, 61, 50–56.Google Scholar
  41. Mariaux, J., & Vaucher, C. (1989). Cestodes d’oiseaux de Côte-d’Ivoire. II. Parasites de Coraciiformes et Piciformes. Systematic Parasitology, 14, 117–133.CrossRefGoogle Scholar
  42. Mariaux, J., & Vaucher, C. (1991). A new species of Staphylepis Spassky & Oshmarin, 1954 (Cestoda: Hymenolepididae) found in West African nectariniid birds. Revue Suisse de Zoologie, 98, 261–268.CrossRefGoogle Scholar
  43. Mariaux, J., Bona, F. V., & Vaucher, C. (1992). A new genus of Metadilepididae (Cestoda: Cyclophyllidea) parasitic in Terpsiphone rufiventer (Aves: Muscicapidae) from the Ivory Coast. Journal of Parasitology, 78, 309–313.CrossRefPubMedGoogle Scholar
  44. Mariaux, J., Tkach, V. V., Vasileva, G. P., Waeschenbach, A., Beveridge, I., Dimitrova, Y. D., et al. (2017). Cyclophyllidea van Beneden in Braun, 1900. In: Caira, J. N. & Jensen, K. (Eds), Planetary Biodiversity Inventory (2008–2017): Tapeworms from vertebrate bowels of the earth, Special Publication 25. Lawrence, KS: University of Kansas, Natural History Museum, pp. 77–148.Google Scholar
  45. Meggitt, F. J. (1927). Report on a collection of Cestoda, mainly from Egypt. Part II. Cyclophyllidea: Family Hymenolepididae. Parasitology, 19, 420–450.CrossRefGoogle Scholar
  46. Ortlepp, R. J. (1938). South African helminths. Part IV. Cestodes from Columbiformes. Onderstepoort Journal of Veterinary Science and Animal Industry, 11, 51–61.Google Scholar
  47. Ortlepp, R. J. (1963). Observations on cestode parasites of Guinea-fowl from southern Africa. Onderstepoort Journal of Veterinary Research, 30, 95–118.Google Scholar
  48. Parona, C. (1885). Di alcuni elminti raccolti nel Sudan orientale da O. Beccari e P. Malgretti. Annali del Museo Civico de Storia Naturale di Genova, 22, 424–445.Google Scholar
  49. Ryšavý, B. (1955). Cizopasní červi pěvců (Passeriformes) Lednické reservace. Věstník Československé Zoologické Společnosti, 19, 99–118.Google Scholar
  50. Sawada, I., & Kugi, G. (1980). Studies on the helminth fauna of Kyushu. Part 6. Cestode parasites of wild birds from Oita Prefecture. Annotationes Zoologicae Japonenses, 53, 269–279.Google Scholar
  51. Schmidt, G. D. (1986). Handbook of Tapeworms Identification. Boca Raton, Florida: CRC Press, 675 pp.Google Scholar
  52. Scholz, T., de Chambrier, A., Kuchta, R., Littlewood, D. T. J., & Waeschenbach, A. (2013). Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): example of convergent evolution. Zootaxa, 3640, 485–499.CrossRefPubMedGoogle Scholar
  53. Singh, K. S. (1952). Cestodes parasites of birds. Indian Journal of Helminthology, 4, 1–72.Google Scholar
  54. Skrjabin, K. I., & Mathevosian, E. M. (1945). Tapeworms - Hymenolepididae of domestic and Game Birds. Moscow: Sel’khozgiz, 488 pp (In Russian).Google Scholar
  55. Southwell, T., & Lake, F. (1939). On a collection of Cestoda from the Belgian Congo. Annals of Tropical Medicine and Parasitology, 33, 107–123.CrossRefGoogle Scholar
  56. Spasskaya, L. P. (1966). Cestodes of birds of the USSR. Hymenolepididae. Moscow: Nauka, 698 pp (In Russian).Google Scholar
  57. Spasskii, A. A. (1954). [Classification of mammalian hymenolepidids.] Trudy Gel’mintologicheskoy Laboratorii Akademii Nauk SSSR, 7, 120–167 (In Russian).Google Scholar
  58. Spasskii, A. A. (1965). On the life-cycle and morphology of Passerilepis crenata (Cestoda: Hymenolepidiae). Parazity Zhivotnykh i Rastenii, 1, 113–118 (In Russian).Google Scholar
  59. Spasskii, A. A., & Spasskaya, L. I. (1954). Systematics of Hymenolepididae parasitizing birds. Trudy Gel’mintologicheskoy Laboratorii, 7, 55–119 (In Russian).Google Scholar
  60. Spasskii, A. A., & Spasskaya, L. P. (1964). The genus Passerilepis and the genus Variolepis (Cestoda: Hymenolepididae). Československá Parazitologie, 11, 247–255 (In Russian).Google Scholar
  61. Spasskii, A. A., Ngui, D. V., & Jurpalova, N. M. (1963). Three new hymenolepidid species of wild and domestic birds in Vietnam. In: A. A. Spasskii (Ed.) Parazity Zhivotnykh i Rastenii Moldavii. Kishinev: Shtiintsa, pp. 75–83 (In Russian).Google Scholar
  62. Sudarikov, V. E. (1950). New cestodes from birds from middle flow of Volga River. Trudy Gel’mintologicheskoy Laboratorii, 3, 142–151 (In Russian).Google Scholar
  63. Swan, D. C. (1936). Berlese’s Fluid: Remarks upon its preparation and use as a mounting medium. Bulletin of Entomological Research, 27, 389–391.CrossRefGoogle Scholar
  64. Tkach, V. V. (1998). Neomylepis gen. n., a new genus of hymenolepidid tapeworms (Cestoda, Cyclophyllidea), parasites of water shrews. Vestnik Zoologii, 32, 90–93.Google Scholar
  65. Tkach, V. V., & Kornyushin, V. V. (1997). On the systematic position of Hymenolepis blarinae Rausch & Kuns, 1950 (Cestoda, Hymenolepididae), with a re-description of the holotype. Systematic Parasitology, 37, 21–25.CrossRefGoogle Scholar
  66. Tkach, V. V., & Velikanov, V. P. (1991). Pseudhymenolepis turkestanica sp. n. (Cestoda: Hymenolepididae), a new cestode from shrews. Annales de Parasitologie Humaine et Comparée, 66, 54–56.CrossRefPubMedGoogle Scholar
  67. Tkach, V. V., Vasileva, G. P., & Genov, T. (2003). Description of Vaucherilepis trichophorus sp. nov., gen. nov. (Cyclophyllidea, Hymenolepididae) from water shrews and gammarid crustaceans in Bulgaria and Ukraine. Acta Parasitologica, 48, 87–97.Google Scholar
  68. Tkach, V. V., Makarikov, A. A., & Kinsella, J. M. (2013). Morphological and molecular differentiation of Staphylocystis clydesengeri n. sp. (Cestoda, Hymenolepididae) from the vagrant shrew, Sorex vagrans (Soricomorpha, Soricidae), in North America. Zootaxa, 3691, 389–400.CrossRefPubMedGoogle Scholar
  69. von Linstow, O. (1903). Entozoa des Zoologischen Museums der Kaiserlichen Akademie der Wissenschaften zu St. Petersburg. Annuaire Musée Zoologique de l’Académie Impériale des Sciences, 8, 19–297.Google Scholar
  70. Yamaguti, S. (1956). Parasitic Worms mainly from Celebes. Part II. Cestodes of Birds. Japanese Journal of Medical Science and Biology, 4, 27–44.Google Scholar
  71. Yamaguti, S. (1959). Systema helminthum. Volume 2. The Cestodes of Vertebrates. New York: Interscience Publischers Inc., 860 pp.Google Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  • Yana D. Dimitrova
    • 1
  • Boyko B. Georgiev
    • 1
  • Jean Mariaux
    • 2
    • 3
  • Gergana P. Vasileva
    • 1
    Email author
  1. 1.Institute of Biodiversity and Ecosystem ResearchBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Muséum d’Histoire Naturelle de GenèveGeneva 6Switzerland
  3. 3.Department of Genetics and EvolutionUniversity of GenevaGenevaSwitzerland

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