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Distribution of the cestode Urocystis prolifer Villot, 1880 (Cyclophyllidea: Hymenolepididae) in the Palaearctic and new data on its postembryonic development

Published online by Cambridge University Press:  19 July 2021

S.A. Kornienko*
Affiliation:
Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, 11 Frunze Street, Novosibirsk 630091, Russia
L.A. Ishigenova
Affiliation:
Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, 11 Frunze Street, Novosibirsk 630091, Russia
*
Author for correspondence: S.A. Kornienko, E-mail: [email protected]

Abstract

Urocystis prolifer Villot, 1880 is an intestinal parasite of Sorex spp. In the Palaearctic. There are significant differences in the descriptions of both adults and stages of ontogenesis of U. prolifer as described by various authors. The experimental infection of intermediate hosts with cestodes has been conducted. An overview of the geographical distribution, infestation of the definitive hosts and the development of the metacestode stages of U. prolifer are presented. The cestode is characterized by an extensive geographic area in the Palaearctic, wide host specificity and very high rates of infection of its definitive host. Urocystis prolifer has been recorded mostly in the taiga and forest zones of Palaearctic. Fourteen species of Sorex were registered as the definitive host. Redescription of U. prolifer and an amended generic diagnosis are provided. A complete description of the ontogeny from oncosphere to fully developed metacestode is given. Features of development of the metacestode are an asexual larval reproduction, the absence of the anterior and posterior obturator valve in the cyst of the fully developed urocyst, as well as excretory bodies.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anikanova, VS, Bespyatova, LA and Bugmyrin, SB (2001) The parasites of common shrew (Sorex araneus L.) from south of Karelia. pp. 7885 in Yeshko, EP (Ed.) Ekologo-parazitologicheskie issledovaniya parazitov zhivotnych i rasteniy Evropeyskogo Severa, Petrazavodsk, Karelian Scientific Center of RAS.Google Scholar
Baer, J-C and Della Santa, E (1960) Matériaux pour server à une révision des espèces du genre Hymenolepis Weinland (Cestoda), parasites de Musaraignes. I. Hymenolepis prolifer (Villot, 1880) Stammer, 1955. Bulletin de la Société neuchâteloise des sciences naturelles 83, 7177.Google Scholar
Binkiene, R (2006) Helminth fauna of shrews (Sorex spp.) in Lithuania. Acta Zoologica Lituanica 16, 241245.CrossRefGoogle Scholar
Binkiene, R, Kontrimavichus, V and Hoberg, EP (2011) Overview of the Cestode fauna of European shrews of the genus Sorex with comments on the fauna in Neomys and Crocidura and an exploration of historical processes in post-glacial Europe. Helminthologia 48, 207228.CrossRefGoogle Scholar
Chervy, L (2002) The terminology of larval cestodes or metacestodes. Systematic Parasitology 52, 133.CrossRefGoogle Scholar
Czaplinski, B and Vaucher, C (1994) Family Hymenolepididae Ariola, 1899. pp. 595663 in Khalil, LF, Jones, A and Bray, RA (Eds) Keys to the cestode parasites of vertebrates. Wallingford, UK, CAB International.Google Scholar
Dokuchaev, NE, Melnikova, YA and Gulyaev, VD (2003) Cestodes of shrews in Kamchatka and adjacent areas. pp. 3942 in Chernyagina, OA (Eds) Conservation of biodiversity of Kamchatka and coastal waters. Petropavlovsk-Kamchatsky, Publ house KamchatNIRO.Google Scholar
Fedorov, KP (1986) Patterns of spatial distribution of parasitic worms. 256 pp. Novosibirsk, Nauka.Google Scholar
Genov, T (1984) Helminths of insectivorous and rodents in Bulgaria. 348 pp. Sofia, Publishing House of the Bulgarian Academy of Sciences.Google Scholar
Georgiev, BB, Bray, RA and Littlewood, DTJ (2006) Cestodes of small mammals: taxonomy and life cycles. pp. 2962 in Morand, S, Krasnov, B and Poulin, R (Eds) Micromammals and Macroparasites. From evolutionary ecology to management. Tokyo, Japan, Springer-Verlag.CrossRefGoogle Scholar
Gulyaev, VD (2000) On gemmation of Polycercus paradoxa (Rud., 1802) Spasskaja & Spassky, 1970 (Cestoda; Cyclophyllidea; Monopylidiidae). Zoologicheskii Zhurnal 79, 11131119.Google Scholar
Gulyaev, VD and Kornienko, SA (1998) On morphological peculiarities of cysticercoids Monocercus (Cestoda: Cyclophyllidea: Dilepididae). Parasitologiya 32, 141145.Google Scholar
Gulyaev, VD and Kornienko, SA (2009) The causes and mechanisms of emergence of miniature polymer Hymenolepididae (Cyclophyllidea, Cestoda), parasites of common shrews. Proceedings of the Zoological Institute of RAS 313, 249256.Google Scholar
Gulyaev, VD, Ishigenova, LA and Kornienko, SA (2010) Morphogenesis of Staphylocystis furcata cysticercoid (Cestoda, Hymenolepididae). Parasitologiya 44, 1221.Google Scholar
Haukisalmi, V (1989) Intestinal helminth communities of Sorex shrews in Finland. Annales Zoologici Fennici 26, 401409.Google Scholar
Haukisalmi, V (2015) Checklist of tapeworms (Platyhelminthes, Cestoda) of vertebrates in Finland. ZooKeys 533, 161.CrossRefGoogle Scholar
Haukisalmi, V, Hardman, LM, Foronda, P, Feliu, C, Laakkonen, J, Niemimaa, J, Lehtonen, JT and Henttonen, H (2010) Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zoologica Scripta 39, 631641.CrossRefGoogle Scholar
Irzhavsky, SV and Gulyaev, VD (2002) The cestode fauna of shrews (Soricidae) of Central Caucasus. pp. 7477 in Gulyaev, VD (Ed.) Parasitologicheskie issledovaniya v Sibiri i na Dal'nem Vostoke. Novosibirsk, Publ. Co. Lada.Google Scholar
Ishigenova, LA (2009) Morphogenesis of cysticercoid Urocystis prolifer Villot, 1880. pp. 114115 in Gulyaev, VD (Ed.) Parasitologicheskie issledovaniya v Sibiri i na Dal'nem Vostoke. Novosibirsk, Publ. Co. Lada.Google Scholar
Ishigenova, LA and Kornienko, SA (2013) Development of cysticercoids in Monocercus arionis (Cestoda, Dilepididae). Zoologicheskii Zhurnal 92, 13031308.Google Scholar
Jones, MF and Alicata, JE (1935) Development and morphology of the cestode, Hymenolepis cantaniana, in coleopteran and avian hosts. Journal of the Washington Academy of Science 25, 237247.Google Scholar
Joyeux, C (1922) Recherches sur l’Urocystis prolifer Villot. Note préliminaire. Bulletin de la Société Zoologique de France 47, 5358.Google Scholar
Kirillov, AA, Kirillova, NJ, Krasnobaev YuP, and Vekhnik, VP (2017) Parasitic worms of micromammalians of the Zhigulevsky Reserve (annotated list of species). 81 pp in Evlanov, IA and Pelgunov, AN (Eds) M: Publ. Commission of the RAS for the conservation of biological diversity. Tolyatti, IPEE RAS.Google Scholar
Kisielewska, K (1958) The life cycle of Choanotaenia crassiscolex (Linstow, 1890) (Dilepididae) and some data relating to the formation of its cysticercoids. Bulletin de L'Académie Polonaise Des Sciences 6, 7984.Google Scholar
Kisielewska, K (1959) A new intermediate host of Staphylocystis furcata (Stieda, 1862) Spassky, 1950, and some data on the formation of larvocysts of this tapeworm. Acta Parasitologica Polonica 7, 133142.Google Scholar
Kisielewska, K (1960) Life cycle of the tapeworm Pseudodiorchis prolifer (Villot, 1890) comb. nova (= Pseudodiorchis multispinosa Zarnowski, 1955). Acta Parasitologica Polonica 8, 197204.Google Scholar
Korneva, Z, Kornienko, SA and Jones, M (2012) Fine structure of the uteri in two hymenolepidid tapeworm Skrjabinacanthus diplocoronatus and Urocystis prolifer (Cestoda: Cyclophyllidea) parasitic in shrews that display different fecundity of the strobilae. Parasitology Research 111, 15231530.CrossRefGoogle ScholarPubMed
Kornienko, SA (2001) Cestodes of shrews from North-Eastern Altai (taxonomy, systematic and ecology). 23 pp. PhD thesis, Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Science, Novosibirsk.Google Scholar
Kornienko, SA and Ishigenova, LA (2012) Intermediate host beetles for cestodes of the genus Staphylocystis Villot, 1877 (Cestoda, Cyclophyllidea, Hymenolepididae), the parasites of shrews (Soricomorpha). Euroasian Entomological Journal 11, 569574.Google Scholar
Kornienko, SA, Zubova, ОA, Gulyaev, VD and Dokuchaev, NE (2008) Cestodes of the shrews from Kunashir Island. pp. 7577 in Galaktionov, KV and Dobrovolskij, AA (Eds) Parasitology in XXI century – problems, methods, solutions. St. Peterburg, Lema.Google Scholar
Kornienko, SA, Dokuchaev, NE and Odnokurtsev, VA (2018) Shrew’ cestodes of the Central and Southern Yakutia. Zoologicheskii Zhurnal 97, 11101120.Google Scholar
Lefebvre, F, Georgiev, BB, Bray, RA and Littlewood, DTJ (2009a) Developing a dedicated cestode life cycle database: lessons from the hymenolepidids. Helminthologia 46, 2127.CrossRefGoogle Scholar
Lefebvre, F, Georgiev, BB, Bray, RA and Littlewood, DTJ (2009b) Cestode life cycle database. Available at www.nhm.ac.uk/research-curation/scientificresources/taxonomy-systematics/cestode-life-cycle/index.htmlGoogle Scholar
Mariaux, J, Tkach, VV, Vasileva, GP, et al. (2017) Cyclophyllidea van Beneden in Braun, 1900. pp. 77148 in Caira, JN and Jensen, K (Eds) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. Lawrence, KS, University of Kansas, Natural History Museum, Special Publication No. 25.Google Scholar
Movsessian, SO, Chubarian, FA and Nikogosian, MA (2006) Fauna of the south of the low Caucasus Cestodes. 331 pp. Moscow, Nauka.Google Scholar
Novikov, MV (1995) Cestodes of shrews (Insectivora, Soricidae) from the Magadan region, North-East Siberia. Acta Parasitologica Polonica 40, 3742.Google Scholar
Obushenkov, IN and Rudzhanskaite, AF (1984) The development Hymenolepis scutigera and Cucurbilepis skrjabini (Cestoda, Hymenolepididae) from insectivorous mammals. Parasitologiya 18, 321324.Google Scholar
Procopič, I, Dimitrova, E, Genov, T and Karapchanski, N (1970) Cysticercoids of cestodes from insectivorous mammals in Bulgaria. Bulletin of the Central Helminthological Laboratory 14, 173184.Google Scholar
Prokopic, J (1968a) Oeceoptoma thoracica L., a new intermediate host of the cestode Neoskrjabinolepis singularis (Cholodkowsky, 1912). Folia Parasitologica 15, 105.Google Scholar
Prokopic, J (1968b) A description of the cysticercoid of the cestode Vigisolepis spinulosa (Cholodkowsky, 1906) found in Collembola. Folia Parasitologica 15, 268.Google Scholar
Prokopič, J and Matsaberidze, GV (1972) Cestodes parasites new for the parasite fauna of Micromammalians from Georgia. Věstník Československé společnosti zoologické 36, 214220.Google Scholar
Quentin, J-C and Beaucournu, J-C (1966) Cysticercoïdes d'Hymenolepididae parasites d'Insectivores chez des Siphonaptères. Comptes Rendus de l'Académie des Sciences (Serie D) 262, 20592062.Google Scholar
Rawson, D and Rigby, JE (1960) The functional anatomy of the cysticercoid of Choanotaenia crassiscolex (Linstow, 1890) (Dilepididae) from the digestive gland of Oxychilus cellarius (Müller) (Stylommatophora) with some observations on developmental stages. Parasitology 50, 453468.CrossRefGoogle Scholar
Ribas, A, Casanova, JC, Feliu, C, Fons, R and Magnanous, E (2003) About Hymenolepidids parasites of Sorex araneus (Insectivora, Soricidae) in Pyrenean mountains. p. 31 in Abstracts of Ninth International Helminthological Symposium, Slovakia.Google Scholar
Rybicka, K (1958) Pseudodiorchis kampinosi n.sp. (Cestoda, Hymenolepididae) a new cestode from the shrew Sorex araneus L. Bulletin L'Académie Polonaise des Science 6, 339345.Google Scholar
Ryšavý, B (1989) Orthoptera as intermediate hosts of Staphylocystis furcata (Stieda, 1862) (Cestoda: Hymenolepididae). Folia Parasitologica 36, 4347.Google Scholar
Ryšavý, B and Prokopič, J (1965) Neue Zwischenwirte des Bandwurmes Staphylocystis furcata Stieda, 1862 (Hymenolepididae). Zeitschrift für Parasitenkunde 25, 371374.CrossRefGoogle Scholar
Sadovskaja, NP (1965) Cestode fauna of insectivores in the Primorsk region. pp. 290297 in Leonov, VA, Mamaev, YL and Oshmarin, PG (Eds) Paraziticheskie chervi domashnikh i dikikh zhivotnych. Vladivostok, Dal'nevostochnii Gosudarstvennii Universitet.Google Scholar
Sato, H, Kamiya, H and Ohbayashi, M (1988) Hymenolepidid and Dilepidid cestodes with armed rostellum in shrews, Sorex spp., from Hokkaido, Japan. Japanese Journal of Veterinary Research 36, 119131.Google ScholarPubMed
Sheykina, ZV and Zhigileva, ON (2018) Helminthes of shrews (Soricidae) in the «Malaya Sosva» Nature Reserve (Russia). Nature Conservation Research 3, 2836.CrossRefGoogle Scholar
Shimalov, VV (2012) Monitoring of the helminth of insectivorous of meliorative canal banks in Belorussian Polesie. Parasitologiya 46, 472478.Google ScholarPubMed
Skolka, M, Fãgăras, M and Paraschiv, G (2004) Biodiversitatea Dobrogei. 396 pp. Constanta, Romania, Ovidius University Press.Google Scholar
Skrjabin, KI and Mathevossian, EM (1942) Stages in the postembryonic development of cestodes of the family Hymenolepididae and an attempt to establish morphological types of their larvicysts. Doklady Akademii Nauk SSSR 10, 8385.Google Scholar
Spassky, AA and Andrejko, OF (1970) Cestodes of insectivorous mammals from Moldova. Parazity Zhivotnyh i Rasteniy 5, 4459.Google Scholar
Stammer, HJ (1955) Die parasiten deutscher Kleinsauger. Verhandlungen der Deutschen Zoologischen Gesellschaft 19, 362390.Google Scholar
Vaucher, C (1971) Les Cestodes parasites des Soricidae d'Europe. Etude anatomique, révision taxonomique et biologie. Revue Suisse Zoologie 78, 1113.CrossRefGoogle Scholar
Villot, FCA (1880) Sur une nouvelle forme de ver vésiculaire, à bourgeonnement exogène. Comptes rendus de l'Académie des Sciences 91, 938940.Google Scholar
Wardle, RA and McLeod, JA (1952) The zoology of tapeworms. 780 pp. Minneapolis, University of Minnesota Press.Google Scholar
Yushkov, VF (1995) Helminths of mammals. Fauna of the European Western North of Russia. III. 201 pp. St. Petersburg, Nauka.Google Scholar
Zarnowski, E (1955) Robaki pasozytnicze drobnych ssakòw lesnych (Rodentia i Insectivora) okolicy Pulaw (woj. Lubelskie). I. Cestoda. Acta Parasitologica Polonica 3, 281357.Google Scholar
Zubova, ОA, Kornienko, , Gulyaev, VD and Dokuchaev, NE (2008a) Cestodes of the shrews of the Sakhalin Island. pp. 265268 in Galaktionov, KV and Dobrovolskii, AA (Eds) Parasitology in XXI century – problems, methods, solutions. St. Peterburg, Lema.Google Scholar
Zubova, ОA, Kornienko, SA, Gulyaev, VD and Dokuchaev, NE (2008b) Cestodes of the shrews of the Hokkaido (Japan). pp. 135138 in Movsessian, SO (Ed.) Biodiversity and ecology of parasites of terrestrial and water cenoses. Moscow, Nauka.Google Scholar