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A taxonomic review of hymenolepidids (Eucestoda, Hymenolepididae) from dormice (Rodentia, Gliridae), with descriptions of two new species

Arseny A. Makarikov
From the journal Acta Parasitologica


In present study the systematic and taxonomic position of hymenolepidids parasitizing rodents of the family Gliridae from Europe and Central Asia is discussed. Hymenolepis myoxi is redescribed on the basis of the type material from the fat dormouse Glis glis deposited in the collection of the Museum für Naturkunde, Berlin, Germany. Significant corrections of morphologically distinctive characters attributable to H. myoxi include: (1) recognition of a rudimentary rostellar apparatus; (2) absence of rostellar hooks and spination on the suckers; and (3) tissues of the scolex and neck filled with numerous “firm elements”. Hymenolepis sulcata was recognised as a synonym of H. myoxi (sensu stricto). The generic allocation of true H. myoxi and validity of the genus Armadolepis is clarified. Specimens from Eliomys quercinus originally designated as H. myoxi by Baer (1932) are described as a new species, Armadolepis jeanbaeri n. sp. The taxonomy has potentially been confused as Spassky (1954) designated misidentified specimens of H. myoxi sensu Baer (1932) as the type species of the genus Armadolepis. In the current article, this error is corrected and A. jeanbaeri n. sp. is fixed as the type of the genus Armadolepis. An additional new species of Armadolepis, A. tenorai n. sp., is described from Dryomys nitedula from Almaty Province, Kazakhstan. The generic diagnosis of Armadolepis is amended. Armadolepis (sensu stricto) is subdivided into two subgenera; the nominotypical subgenus includes species having well developed rostellar apparatus armed by rostellar hooks and A. (Bremserilepis) n. subgen. includes species with rudimentary and unarmed rostellar apparatus.

Funding statement: A substantial portion of the work was funded by the by the Russian Fund for Fundamental Research (Project No. 14-04-00871-a and 17-04-00238). Further support for AAM was provided by the Federal Fundamental Scientific Research Program for 2013-2020 (VI.51.1.7.). This study was funded in part by the US National Science Foundation grants DEB 0818696 and 0818823

Compliance with ethical standards

  1. Conflict of interest statement. The author declares that he has no conflict of interest.

    Ethical approval. The author carefully reviewed the ethical standards of the journal and hereby certifies that the procedures used with the investigated species comply fully with those standards. The methods used in the current study were approved by the ethics committee of the Institute of Systematics and Ecology of Animals, Novosibirsk, Russia (ISEA).


I wish to thank the curators of the helminthological collections, Dr. Birger Neuhaus (Museum für Naturkunde, Berlin, Germany) and Dr. Jean Mariaux (Natural History Museum, Geneva, Switzerland) for assistance in assembling cestode specimens for the current study. I also thank Dr. Helmut Sattmann (Naturhistorisches Museum, Vienna, Austria) for assistance in obtaining critical literature and for providing valuable comments on the biography of J. Bremser. Dr. Voitto Haukisalmi (Finnish Museum of Natural History, Helsinki, Finland) provided the information about voucher specimens from dormice. I am grateful to Dr. Anatoly V. Barkalov (ISEA) who kindly discussed issues of zoological nomenclature for the present study. Dr. Vasyl Tkach (University of North Dakota, Grand Forks, ND, USA) shared access to unpublished data on genetic diversity of Armadolepis. I sincerely thank Dr. Eric P. Hoberg (U.S. National Parasite Collection, Beltsville, MD, USA) and Dr. Boyko B. Georgiev (Institute of Biodiversity and Ecosystem Research Bulgarian Academy of Sciences, Sofia, Bulgaria) for their useful comments and checking the English in the manuscript. Helminths from rodents from southeastern Kazakhstan were collected within the framework of a comprehensive expedition which was organized in 2012 by Institute of Systematics and Ecology of Animals SB RAS. I am grateful to Dr. Victor V. Glupov and Dr. Anatoly V. Barkalov for their great contribution in organization of the comprehensive expedition.


Andreiko O.F. 1965. Some results of the studies on helminthfauna of dormice (Myoxidae) in Moldavia. In: (Ed. A.A. Spassky) Parasites of animals and plants. Vol. 1. Izdatel’stvo Kartya Moldovenyaske, Kishinev, pp. 53-60 (In Russian)Search in Google Scholar

Anonymous Schreibers C., Bremser J., Natterer J.d. Jüngere. 1811. Nachricht von einer beträchtlichen Sammlung thierischer Eingeweidewürmer, und Einladung zu einer literarischen Verbindung, um dieselbe zu vervollkommnen, und sie für die Wissenschaft und die Liebhaber allgemein nützlich zu machen. K. K. Naturalienkabinets – Direktion in Wien, 31Search in Google Scholar

Baer J.G. 1932. Contribution á la faune helminthologique de Suisse (Deuxieme partie). Revue Suisse de Zoologie, 39, 1–57Search in Google Scholar

Blanchard R. 1891. Histoire zoologique et médicale des Téniadés du genre “Hymenolepis” Weinland. Paris, pp.111Search in Google Scholar

Casanova J.C., Santalla F., Durand P., Vaucher C., Feliu C., Renaud F. 2001. Morphological and genetic differentiation of Rodentolepis straminea (Goeze, 1752) and Rodentolepis microstoma (Dujardin, 1845) (Hymenolepididae). Parasitology Research, 87, 439–44. 10.1007/s004360100379Search in Google Scholar PubMed

Chowdhury N., De Rycke P.H. 1977. Structure, formation, and functions of calcareous corpuscles in Hymenolepis microstoma. Zeitschrift für Parasitenkunde, 53, 59–16910.1007/BF00380461Search in Google Scholar PubMed

Czaplinski B., Vaucher C. 1994. Family Hymenolepididae Ariola, 1899. In: (Eds. L.F. Khalil, A. Jones and R.A. Bray) Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, UK, 595–663Search in Google Scholar

Erhardová B. 1958. Parasiticti cervi hlodavcu Československa. Československá Parasitologic, 5, 27-103 (In Czech)Search in Google Scholar

Faivre J.P., Vaucher C. 1978. Redescription de Hymenolepis sulcata (von Linstow, 1879), parasite du loir Glis glis (L.). Bulletin de la Societé Neuchateloise des Sciences Naturelles, 101, 53–58Search in Google Scholar

Fataliev G.G. 2009. Helminthfauna of rodents (Rodentia) in Azerbaijan and ways of its formation. The South of Russia: ecology, development, 4, 139–144 (In Russian)Search in Google Scholar

Genov T. 1984. Helminths of insectivores and rodents in Bulgaria. Izdatelstvo na Bulgarskata akademiya na naukite, Sofia, 348 pp. (In Bulgarian)Search in Google Scholar

Georgiev B.B., Sánchez M.I., Green A.J., Nikolov P.N., Vasileva G.P., Mavrodieva R.S. 2005. Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: a systematic survey. Acta Parasitologica, 50, 105–117Search in Google Scholar

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. in Google Scholar PubMed

Gulyaev V.D., Ishigenova L.A., Kornienko S.A. 2010. Morphogenesis of the Staphylocystis furcata cysticercoid (Cyclophyllidea, Hymenolepididae). Parazitologiya, 44, 12–21 (In Russian)Search in Google Scholar

Hartwich G., Kilias I. 1992. Die Typen der Cercomeromorphae (Plathelminthes) des Zoologischen Museums in Berlin. Mitteilungen aus dem Zoologischen Museum in Berlin, 68, 209–24810.1002/mmnz.19920680204Search in Google Scholar

Haukisalmi V., Hardman L.M., Foronda P., Feliu C., Laakkonen J., Niemimaa J., Lehtonen J.T., Henttonen H. 2010. Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zoologica Scripta, 39, 631–641. in Google Scholar

ICZN 1999. International Code of Zoological Nomenclature, 4th Edition. xxix + 306 pp. International Trust for Zoological Nomenclature, c/o The Natural History Museum, London.Search in Google Scholar

Janicki C. 1904. Zur Kenntnis einiger Säugetiercestoden. Zoologischer Anzeiger, 27, 770–782. (In German)Search in Google Scholar

Janicki C. 1906. Studien an Säugetiercestoden. Zeitschrift für wissenschaftliche Zoologie, 81, 503–597. (In German)Search in Google Scholar

Joyeux C., Baer J.G. 1936. Faune de France. 30. Cestodes. P. Lechevalier, Paris, pp. 613. (In French)Search in Google Scholar

Joyeux C.H., Foley H. 1930. Les helminthes de Meriones shawi shawi Rozet dans le nord de L’Algérie. Bulletin de la Société Zoologique de France, 55, 353–374. (In French)Search in Google Scholar

Kirshenblat Ya.D. 1948. Materials on helminth fauna of rodents in Georgia. In: Trudy Zoologicheskogo Instituta Akademii Nauk Gruzinskoi SSR. Vol. 8. Tbilisi, pp. 317-339 (In Russian)Search in Google Scholar

Konjević D., Špakulová M., Beck R., Goldová M., Severin K., Margaletić J., Pintur K., Keros T., Perić S. 2007. First evidence of Paraheligmonina gracilis and Hymenolepis sulcata among fat dormice (Glis glis L.) from Croatia. Helminthologia, 44, 34-36. 10.2478/s11687-006-0054-5Search in Google Scholar

Kontrimavichus V.L., Smirnova L.V. 1991. Hymenolepis beringiensis sp. n. from the Siberian lemming (Lemmus sibiricus Kerr) and the problem of the sibling species in helminthology. In: (Eds. G.P. Krasnosohekov, V.A. Roitman, M.D. Sonin and L.V. Chesnova) Evoljucia parazitov. Materialy I Vsesojuznogo Simpoziuma. Akademiya Nauk SSSR, Tol’yatti, pp. 90–104 (In Russian)Search in Google Scholar

Linstow O. 1879. Helminthologische Untersuchungen. Jahresheft des Vereins fur Vaterlandische Naturjunde. Württemberg, 35, 313–342. (In German)Search in Google Scholar

Mackiewicz J.S., Ehrenpris M.B. 1980. Calcareous corpuscles distribution in caryophyllid cestodes: possible evidence of cryptic segmentation. Proceedings of the Helminthological Society of Washington, 47, 1–7Search in Google Scholar

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)Search in Google Scholar

Makarikov A.A., Gulyaev V.D., Kontrimavichus V.L. 2011. A redescription of Arostrilepis horrida (Linstow, 1901) and descriptions of two new species from Palaearctic microtine rodents, Arostrilepis macrocirrosa sp. n. and A. tenuicirrosa sp. n. (Cestoda: Hymenolepididae). Folia Parasitologica, 58, 108–120. 10.14411/fp.2011.011Search in Google Scholar PubMed

Makarikov A.A., Tkach V.V. 2013. Two new species of Hymenolepis (Cestoda: Hymenolepididae) from Spalacidae and Muridae (Rodentia) from eastern Palearctic. Acta Parasitologica, 58, 37–49. 10.2478/s11686-013-0115-0Search in Google Scholar PubMed

Makarikov A.A., Galbreath K.E., Hoberg E.P. 2013. Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia. Zootaxa, 3608, 401–439. in Google Scholar PubMed

Makarikov A.A., Mel’nikova Y.A., Tkach V.V. 2015. Description and phylogenetic affinities of two new species of Nomadolepis (Eucestoda, Hymenolepididae) from Eastern Palearctic. Parasitology International, 64, 453–463. in Google Scholar PubMed

Mas-Coma S., Feliu C., Rey J.M. 1978. Contribucion al conocimiento de la helmintofauna de micromamiferos Ibericos. 6. Parasitos de Glis glis Linnaeus, 1766 (Rodentia: Gliridae). Revista Iberica de Parasitologia, 38, 579–584. (In Spanish)Search in Google Scholar

Mas-Coma S., Tenora F., Gallego J. 1980. Consideraciones sobre los Hymenolepididos inermes de Roedores, con especial referencia a la problematica entorno a Hymenolepis diminuta. Circular Farmaceutica, Barcelona, 38, 137–152. (In Spanish)Search in Google Scholar

Mas-Coma S., Galan-Puchades M.T. 1991. A methodology for the morpho-anatomic and systematic study of the species of the family Hymenolepididae Railliet et Henry, 1909 (Cestoda: Cyclophyllidea). Research and Reviews in Parasitology, 51, 139–173Search in Google Scholar

Merkusheva I.V., Bobkova A.F. 1981. Helminths of domesticated and wild animals in Belarus. Nauka i Tehnika, Minsk, pp. 120. (In Russian)Search in Google Scholar

McCullough J.S., Fairweather I. 1987. The structure, composition, formation and possible functions of calcareous corpuscles in Trilocularia acanthiaevulgaris Olsson 1867 (Cestoda, Tetraphyllidea). Parasitology Research, 74, 175–182. 10. 1007/BF00536030Search in Google Scholar

Movsessian S.O., Chubarian F.A., Nikoghosian A.A. 2006. Fauna of the south of the Low Caucasus. Cestodes. (Ed. A.N. Pelgunov). Institute of Parasitology RAS. Nauka, Moskva, pp 331. (In Russian)Search in Google Scholar

Murai E., Tenora F. 1977. Hymenolepis sulcata (von Linstow, 1879): Occurrence in Glis glis (Rodentia) in Hungary. Parasitologica Hungarica, 10, 63–66Search in Google Scholar

Rudolphi C.A. 1819. Entozoorum Synopsis, cui accedunt mantissa duplex et indices locupletissimi. Sumtibus Augusti Rücker, Berolini, Berlin, pp. 811. (In Spanish)10.5962/bhl.title.9157Search in Google Scholar

Ryzhikov K.M., Gvozdev E.V. Tokobaev M.M. Shaldybin L.S. Matzaberidze G.V., Merkusheva I.V., Nadtochii E.V., Khohlova I.G., Sharpilo L.D. (Ed.). 1978. Keys to the helminths of the rodent fauna of the USSR. Cestodes and trematodes. Izdatel’stvo Nauka, Moskva, pp. 232. (In Russian)Search in Google Scholar

Sattmann H., Konecny R., Stagl V. 1999. Die Geschichte der Helminthensammlung am Naturhistorischen Museum in Wien Teil 1 (1797–1897). Mitteilungen der Österreichischen Gesellschaft für Tropenmedizin und Parasitologie, 21, 83–92. (In German)Search in Google Scholar

Sattmann H. 2000. Profile: Johann Gottfried Bremser (1767–1827). Systematic Parasitology, 47, 231–23210.1023/A:1017247007661Search in Google Scholar

Shaikenov B. 1981. Helminths of rodents of Kazakhstan. Izdatel’stvo Nauka, Alma-Ata, pp. 172. (In Russian)Search in Google Scholar

Shimalov V.T., Shimalov V.V. 2000. Helminth fauna of dormice (Rodentia: Gliridae) in Belarus. Vestsi Natsyyanal’nai Akademii Navuk Belarusi. Seryya Biyalagichnykh Navuk, 2, 123–125.Search in Google Scholar

Shults R.S., Gvozdev Ye.V. 1970. Osnovy obshchei gel’mintologii (The principles of general helminthology), Izdatel’stvo Nauka, Moskva, Vol. 1, pp. 492 (In Russian)Search in Google Scholar

Skrjabin K.I., Matevosyan E.N. 1945. Tapeworms-Hymenolepidae of domestic and game birds. Izdatel’stvo Sel’khozgiz, Moskva, pp. 488. (In Russian)Search in Google Scholar

Skrjabin K.I., Matevosyan E.M. 1948. Hymenolepidids of mammals. In: Trudy Gel’mintologcheskoy Laboratorii, Vol. 1, pp. 15–92 (In Russian)Search in Google Scholar

Sludskiy A.A., Bekenov A., Borisenko V.A., Grachev Y.A., Ismagilov M.I., Kapitonov V.I., Strautman E.I., Fedosenko A.K., Shubin I.G. 1977. Mammals of Kazakhstan. Vol. 1, part 2. Izdatel’stvo “Nauka” of KazSSR, Alma-Ata, pp. 536. (In Russian)Search in Google Scholar

Spassky A.A. 1954. Classification of hymenolepidids of mammals. In: Trudy Gel’mintologcheskoy Laboratorii, Vol. 7, pp. 120–134 (In Russian)Search in Google Scholar

Spassky A.A. 1963. Hymenolepidid cestodes – tapeworms of wild and domestic birds. Vol. 2. Izdatel’stvo Akademii Nauk SSSR, Moscow, pp. 418. (In Russian)Search in Google Scholar

Spassky A.A. 1992. To the phylogeny and systematics of hymenolepidoid tapeworms (Cestoda: Cyclophyllidea). Izvestya Akademii nauk respubliki Moldava. Biologicheskikie i chimicheskie nauki, 6, 41–47 (In Russian)Search in Google Scholar

Spassky A.A. 1995. On structure and generic composition of hymenolepidids (Cestoda: Cyclophyllidea). Izvestya Akademii nauk respubliki Moldava. Biologicheskikie i chimicheskie nauki, 6, 23–28 (In Russian)Search in Google Scholar

Tenora F., Baruš V. 1958. Armadolepis spasskii n. sp. eine neue Bandwurmart aus Nagern der Fam. Myoxidae. Folia Zoologica, 4, 339–342. (In German)Search in Google Scholar

Tenora F. 1965. Supplementary notes on hymenolepidid tapeworms parasitizing glirid dormice in south Slovakian limestone area Czechoslovakia. Ceskoslovenska Parasitologie, 12, 299–303.Search in Google Scholar

Tenora F., Baruš V., Koubková B. 1999a. Remarks on tapeworms of the family Hymenolepididae (Cyclophyllidea) parasitizing dormice (Gliridae: Rodentia) in Europe. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 47, 13–23Search in Google Scholar

Tenora F., Koubkova B., Baruš V. 1999b. Is Armadolepis spasskii, 1954 (Cestoda) a valid genus? In: Proc. of 8th Helminthological Days, Helminthological Section of the Czech Parasitological Society, Dolni V ěstonice, May 17–20, 1999, Helminthologia, 36, 130Search in Google Scholar

Tinnin D.S., Ganzorig S., Gardner S.L. 2011. Helminths of Small Mammals (Erinaceomorpha, Soricomorpha, Chiroptera, Rodentia, and Lagomorpha) of Mongolia. Special Publications of the Museum of Texas Tech University, Number 59, pp.5010.5962/bhl.title.142892Search in Google Scholar

Tokobajev M.M. 1976. Gel’minty dikich mlekopitayuschih Sredney Azii. Izdatel’stvo Ilim, Frunze, pp. 179 (In Russian)Search in Google Scholar

Vargas-Parada L., Laclette J.P. 1999. Role of the calcareous corpuscles in cestode physiology: a review. Revista Latinoamericana de Microbiologia, 41, 303–307Search in Google Scholar

Vaucher C., Quentin J.C. 1975. Présence du cysticercoïde de Hymenolepis myoxi (Rud., 1819) chez la Puce du Lérot et redescription du Ver adulte. Bulletin de la Société Neuchâteloise des Sciences Naturelles, 98, 27–34. (In Spanish)Search in Google Scholar

Wilson D.E., Reeder D.M. 2005. Mammal species of the world. A taxonomic and geographic reference. 3th ed., The Johns Hopkins University Press, Baltimore, pp.2142Search in Google Scholar

Yamaguti S. 1959. Systema helminthium. Vol. II. The cestodes of vertebrates. Interscience Publishers, New York, pp. 415–420Search in Google Scholar

Zhaltsanova D.-S.D. 1992. Gel’minty mlekopitayuschih basseina Ozera Baikal. Izdatel’stvo Nauka, Moskva, pp. 204. (In Russian)Search in Google Scholar

Žarnowski E. 1955. Parasitic worms of forest micromammalians (Rodentia and Insectivora) of the environment of Pulawy (district Lublin). I. Cestoda. Acta Parasitologica Polonica, 3, 279–368 (In Polish)Search in Google Scholar

Received: 2016-3-31
Revised: 2016-8-23
Accepted: 2016-8-26
Published Online: 2016-12-28
Published in Print: 2017-3-1

© 2017 W. Stefański Institute of Parasitology, PAS

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