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

Abstract

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Alexander, S., & McLaughlin, J. D. (1993). Microsomacanthus macrotesticulata n. sp. (Cestoda: Hymenolepididae) from South African waterfowl. Journal of Parasitology, 79, 843–846.

    Article  Google 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.

    Article  CAS  PubMed  Google Scholar 

  3. Baer, J.-G. (1933). Contribution a l’étude de la Faune helminthologique africaine. Revue Suisse de Zoologie, 40, 31–84.

    Article  Google 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.

  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).

  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. http://digitalcommons.unl.edu/parasitologyfacpubs/3. 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.

  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.

  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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

  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).

  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.

    Article  Google Scholar 

  31. Lepage, D. (2019). Avibase, the World Bird Database. http://avibase.bsc-eoc.org/. 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.

    Article  Google 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.

    Article  PubMed  Google 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).

    CAS  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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  Google 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.

  45. Meggitt, F. J. (1927). Report on a collection of Cestoda, mainly from Egypt. Part II. Cyclophyllidea: Family Hymenolepididae. Parasitology, 19, 420–450.

    Article  Google 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.

    Article  PubMed  Google 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).

  55. Southwell, T., & Lake, F. (1939). On a collection of Cestoda from the Belgian Congo. Annals of Tropical Medicine and Parasitology, 33, 107–123.

    Article  Google Scholar 

  56. Spasskaya, L. P. (1966). Cestodes of birds of the USSR. Hymenolepididae. Moscow: Nauka, 698 pp (In Russian).

  57. Spasskii, A. A. (1954). [Classification of mammalian hymenolepidids.] Trudy Gel’mintologicheskoy Laboratorii Akademii Nauk SSSR, 7, 120–167 (In Russian).

  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).

  59. Spasskii, A. A., & Spasskaya, L. I. (1954). Systematics of Hymenolepididae parasitizing birds. Trudy Gel’mintologicheskoy Laboratorii, 7, 55–119 (In Russian).

  60. Spasskii, A. A., & Spasskaya, L. P. (1964). The genus Passerilepis and the genus Variolepis (Cestoda: Hymenolepididae). Československá Parazitologie, 11, 247–255 (In Russian).

  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).

  62. Sudarikov, V. E. (1950). New cestodes from birds from middle flow of Volga River. Trudy Gel’mintologicheskoy Laboratorii, 3, 142–151 (In Russian).

  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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

Download references

Acknowledgements

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).

Funding

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).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gergana P. Vasileva.

Ethics declarations

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.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as 51AF63BB-9A07-4C4C-B0E5-DB7D6C6726C2. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the Version of Record.

This article is part of the Topical Collection Cestoda.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dimitrova, Y.D., Georgiev, B.B., Mariaux, J. et al. Two new cestode species of the family Hymenolepididae Perrier, 1897 (Cyclophyllidea) from passerine birds in Ethiopia, with the erection of Citrilolepis n. g.. Syst Parasitol 96, 279–297 (2019). https://doi.org/10.1007/s11230-019-09846-y

Download citation