Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-26T08:24:06.028Z Has data issue: false hasContentIssue false

Redescription and taxonomic position of Rodentolepis (sensu lato) asymmetrica (Janicki, 1904), with the erection of Kontrimavichusia n. g. (Eucestoda: Hymenolepididae) from arvicoline rodents (Rodentia: Cricetidae)

Published online by Cambridge University Press:  25 August 2022

A. A. Makarikov*
Affiliation:
Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, 11 Frunze Street, 630091 Novosibirsk, Russia
R. Binkienė
Affiliation:
Institute of Ecology of Nature Research Centre, Akademijos 2, Vilnius 08412, Lithuania
*
*Author for correspondence: Arseny A. Makarikov, E-mail: [email protected]

Abstract

Rodentolepis (sensu lato) asymmetrica (Janicki, 1904) is redescribed on the basis of materials from Microtus agrestis, Microtus arvalis and Myodes glareolus from Eastern Europe (Belarus, Lithuania, Latvia, Estonia, Ukraine and the north-eastern part of Russia). A new genus, Kontrimavichusia n. g., is proposed for it based on morphological and molecular evidence. The unique morphological diagnostic characters of this currently monotypic genus include the presence of an armature on the suckers, ventral osmoregulatory canals connected with irregularly spaced transverse anastomoses, an internal seminal vesicle with circular musculature and uterus with numerous diverticula, situated dorsally to the genital ducts, extending bilaterally beyond the longitudinal osmoregulatory canals. In addition, the new genus differs from morphologically related genera of the Rodentolepis clade by the structure of its vagina. The copulatory part of the vagina in specimens of Kontrimavichusia n. g. is surrounded by circular musculature and covered externally by a dense layer of intensely-stained cells; the conductive part of the vagina is clearly distinguishable from the seminal receptacle. Molecular analysis of the partial 28S rRNA gene fully supports the erection of Kontrimavichusia n. g. as a distinct lineage.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baer, J-G (1932) Contribution à la faune helminthologique de Suisse (Deuxieme partie) [Contribution to the helminthological fauna of Switzerland (Second part)]. Revue Suisse de Zoologie 39(1), 157. [In French.]Google Scholar
Baer, J-G and Tenora, F (1970) Some species of Hymenolepis (Cestoidea) from rodents and from primates. Acta Scientiarum Naturalium Academiae Scientiarum Bohemicae, Brno 4(9), 132.Google Scholar
Binkienė, R, Miliūtė, A and Stunžėnas, V (2019) Molecular data confirm the taxonomic position of Hymenolepis erinacei (Cyclophyllidea: Hymenolepididae) and host switching, with notes on cestodes of Palaearctic hedgehogs (Erinaceidae). Journal of Helminthology 93(2), 195202.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
Erhardová, B (1955) Die Helminthofauna der mäuseartigen Nagetiere des Nationalparks in der Roben Tatra [The helminthofauna of mouse-like rodents of the national park in the Robe Tatras]. Folia Zoologica et Entomologica 4(18), 353364. [In German.]Google Scholar
Erhardová, B (1958) Parasiticti cervi hlodavcu Československa [Parasiticity of the rodent cervi of Czechoslovakia]. Československá Parasitologie 5(1), 27103. [In Czech.]Google Scholar
Genov, T (1984) Helminths of insectivores and rodents in Bulgaria. 348 pp. Sofia, Izdatelstvo na Bulgarskata akademiya na naukite. [In Bulgarian.]Google Scholar
Greiman, SE and Tkach, VV (2012) Description and phylogenetic relationships of Rodentolepis gnoskei n. sp. (Cyclophyllidea: Hymenolepididae) from a shrew Suncus varilla minor in Malawi. Parasitology International 61(2), 343350.CrossRefGoogle Scholar
Greiman, SE, Tkach, VV and Cook, JA (2013) Description and molecular differentiation of a new Staphylocystoides (Cyclophyllidea: Hymenolepididae) from the dusky shrew Sorex monticolus in Southeast Alaska. The Journal of Parasitology 99(6), 10451049.CrossRefGoogle ScholarPubMed
Gulyaev, VD (2000) Acceleration of scolex morphogenesis in phylogenesis of tapeworms (Plathelminthes, Cestoda, Eucestoda). Zoolgicheskii Zhurnal 79(11), 12531259. [In Russian.Google Scholar
Haas, GMS, Hoberg, EP, Cook, JA, Henttonen, H, Makarikov, AA, Gallagher, SR, Dokuchaev, NE and Galbreath, KE (2020) Taxon pulse dynamics, episodic dispersal and host colonization across Beringia drive diversification of a Holarctic tapeworm assemblage. Journal of Biogeography 47(11), 24572471.CrossRefGoogle Scholar
Hall, T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41(1), 9598.Google 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(6), 631641.CrossRefGoogle Scholar
Janicki, C (1904) Zur Kenntnis einiger Säugetiercestoden [On the knowledge of some mammalian cestodes]. Zoologischer Anzeiger 27(25), 770782. [In German.]Google Scholar
Janicki, C (1906) Studien an Säugetiercestoden [Studies on mammalian cestodes]. Zeitschrift für Wissenschaftliche Zoologie 81, 505597.Google Scholar
Joyeux, C and Baer, J-G (1936) Faune de France. 30. Cestodes [Fauna of France. 30. Cestodes]. 613 pp. Paris, P. Lechevalier. [In French.]Google Scholar
Kornienko, SA, Gulyaev, VD and Mel'nikova, Y (2006) On the morphology and systematics of cestodes of the genus Neoskrjabinolepis Spassky, 1947 (Cyclophyllidea, Hymenolepididae). Zoologicheskii Zhurnal 85(1), 134145. [In Russian.Google Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA x: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35(6), 15471549.CrossRefGoogle ScholarPubMed
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78(2), 155171.CrossRefGoogle Scholar
Makarikov, AA (2017) A taxonomic review of hymenolepidids (Eucestoda, Hymenolepididae) from dormice (Rodentia, Gliridae), with descriptions of two new species. Acta Parasitologica 62(1), 121.CrossRefGoogle Scholar
Makarikov, AA and Gulyaev, VD (2009) Pararodentolepis n. gen., - a new cestode genus from rodents and the description of P. sinistra sp. n. (Cyclophyllidea: Hymenolepididae). Parazitologiya 43(6), 454459. [In Russian.Google Scholar
Makarikov, AA and Tkach, VV (2013) Two new species of Hymenolepis (Cestoda: Hymenolepididae) from Spalacidae and Muridae (Rodentia) from eastern Palearctic. Acta Parasitologica 58(1), 3749.CrossRefGoogle ScholarPubMed
Makarikov, AA, Gulyaev, VD and Chechulin, AI (2005) Arvicolepis gen. n., a new cestode genus from rodents and redescription of Arvicolepis transfuga (Spassky et Merkusheva, 1976) comb. nov. (Cyclophyllidea, Hymenolepididae). pp. 178186. In Alimov, AF (Ed.) Problemy tsestodologii 3 [Problems of cestodology 3]. St. Petersburg, Izdatel'stvo Zoologicheskogo Instituta RAN. [In Russian.]Google Scholar
Makarikov, AA, Gulyaev, VD and Krivopalov, AV (2010) Nomadolepis (Cyclophyllidea: Hymenolepididae) - a new cestode genus from rodents. Zoolgicheskii Zhurnal 89(8), 948955. [In Russian.]Google Scholar
Makarikov, AA, Galbreath, KE and Hoberg, EP (2013) Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia. Zootaxa 3608(6), 401439.CrossRefGoogle ScholarPubMed
Makarikov, AA, Mel'nikova, YA and Tkach, VV (2015) Description and phylogenetic affinities of two new species of Nomadolepis (Eucestoda, Hymenolepididae) from Eastern Palearctic. Parasitology International 64(5), 453463.CrossRefGoogle ScholarPubMed
Makarikov, AA, Stakheev, VV and Tkach, VV (2018) Phylogenetic relationships of the genus Armadolepis Spassky, 1954 (Eucestoda, Hymenolepididae), with descriptions of two new species from Palaearctic dormice (Rodentia, Gliridae). Systematic Parasitology 95(1), 6579.CrossRefGoogle 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
Mas-Coma, S and Galan-Puchades, MT (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(1–4), 139173.Google Scholar
Murai, E (1974) Review of tapeworms in Microtinae from Hungary. Parasitologia Hungarica 7(1), 111141.Google Scholar
Murai, E (1989) Ceratozetes gracilis (Michael, 1884) (Acari: Oribatida), an intermediate host of Vampirolepis asymmetrica (Janicki, 1904) (Cestoda: Hymenolepididade). Miscellanea Zoologica Hungarica 5(1), 1319.Google Scholar
Musser, GG and Carelton, MD (2005) Superfamily Muroidea. pp. 8941522. In Wilson, DE and Reeder, DM (Eds) Mammal species of the world: a taxonomic and geographic reference. 3rd edition. Baltimore, Maryland, Johns Hopkins University Press.Google Scholar
Neov, B, Vasileva, GP, Radoslavov, G, Hristov, P, Littlewood DT, J and Georgiev, BB (2019) Phylogeny of hymenolepidid cestodes (Cestoda: Cyclophyllidea) from mammalian hosts based on partial 28S rDNA, with focus on parasites from shrews. Parasitology Research 118(1), 7388.CrossRefGoogle ScholarPubMed
Nkouawa, A, Haukisalmi, V, Li, T, Nakao, M, Lavikainen, A, Chen, X, Henttonen, H and Ito, A (2016) Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitology International 65(2), 8386.CrossRefGoogle ScholarPubMed
Ryzhikov, KM, Gvozdev, EV, Tokobaev, MM, Shaldybin, LS, Matzaberidze, GV, Merkusheva, IV, Nadtochii, EV, Khohlova, IG and Sharpilo, LD (1978) Keys to the helminths of the rodent fauna of the USSR. Cestodes and trematodes. 232 pp. Moscow, Izdatel'stvo Nauka. [In Russian.]Google Scholar
Sambrook, J and Russell, DW (2002) Molecular cloning: a laboratory manual. 3rd edition. New York, Cold Spring Harbor Laboratory Press.Google Scholar
Santalla, F, Casanova, JC, Durand, P, Vaucher, C, Renaud, F and Feliu, C (2002) Morphometric and genetic variability of Rodentolepis asymmetrica (Hymenolepididae) from the Pyrenean mountains. Journal of Parasitology 88(5), 983988.CrossRefGoogle ScholarPubMed
Schmidt, GD (1986) Handbook of tapeworm identification. 675 pp. Boca Raton, Florida, CRC Press.Google Scholar
Skrjabin, KI and Matevosyan, EM (1948) Hymenolepidids of mammals. Trudy Gel'mintologcheskoy Laboratorii, Akademii Nauk SSSR 1(1), 1592. [In Russian.]Google Scholar
Spassky, AA (1954) Classification of hymenolepidids of mammals. Trudy Gel'mintologcheskoy Laboratorii, Akademii Nauk SSSR 7(1), 120167. [In Russian.]Google Scholar
Spassky, AA (1992) To the phylogeny and systematics of hymenolepidoid tapeworms (Cestoda: Cyclophyllidea). Izvestya Akademii nauk respubliki Moldava. Biologicheskikie i chimicheskie nauki 6(1), 4147. [In Russian.]Google Scholar
Tenora, F and Murai, E (1972) Recent data on five species of the genus Hymenolepis (Weinland) (Cestoidea, Hymenolepididae) parasitizing rodents in Hungary. Acta Zoologica Academiae Scientiarum Hungaricae 18(1), 129145.Google Scholar
Tkach, VV, Makarikov, AA and Kinsella, JM (2013) Morphological and molecular differentiation of Staphylocystis clydesengeri n. sp. (Cestoda, Hymenolepididae) from the vagrant shrew, Sorex vagrans (Soricimorpha, Soricidae), in North America. Zootaxa 3691(3), 389400.CrossRefGoogle Scholar
Vainio, EJ, Korhonen, K and Hantula, J (1998) Genetic variation in Phlebiopsis gigantea as detected with random amplified microsatellite (RAMS) markers. Mycological Research 102(2), 187192.CrossRefGoogle Scholar
Vaucher, C (1967) Contribution à l’étude des cestodes et des trématodes parasites des micromammifères de Suisse 1 [Contribution to the study of parasitic cestodes and trematodes of micromammals in Switzerland 1]. Bulletin de la Société Neuchâteloise des Sciences Naturelles 90(1), 161184. [In French.]Google Scholar
Waeschenbach, A, Webster, BL, Bray, RA and Littlewood, DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution 45(1), 311325.CrossRefGoogle ScholarPubMed
Widmer, VC, Georgiev, BB and Mariaux, J (2013) A new genus of the family Hymenolepididae (Cestoda) from Sephanoides sephaniodes (Apodiformes, Trochilidae) in Northern Patagonia (Chile). Acta Parasitologica 58(1), 105111.CrossRefGoogle 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(13), 279368. [In Polish.]Google Scholar
Zehnder, MP and Mariaux, J (1999) Molecular systematic analysis of the order Proteocephalidea Mola, 1928 (Eucestoda) based on mitochondrial and nuclear rDNA sequences. International Journal for Parasitology 29(11), 18411852.CrossRefGoogle Scholar