New species of Kontrimavichusia Makarikov & Binkienė, 2022 (Eucestoda: Hymenolepididae) from arvicoline rodents (Rodentia: Cricetidae) from the North Caucasus
Abstract
Two previously unrecognized species attributable to the genus Kontrimavichusia Makarikov & Binkienė, 2022 in arvicoline rodents from the North Caucasus are described. Kontrimavichusia testiculata sp. nov. is described from Microtus majori (Thomas, 1906) from the northwestern Caucasus (Republic of Adygeya and Karachay-Cherkess Republic, Russia) and Kontrimavichusia hobergi sp. nov. is described from Microtus daghestanicus (Shidlovsky, 1919) from the central Caucasus (Republic of North Ossetia, Russia). Kontrimavichusia testiculata is readily distinguishable from K. asymmetrica (Janicki, 1904) and K. hobergi in having a larger number of testes (4–6 per proglottis), larger suckers and a longer cirrus and cirrus-sac. In addition, the new species differs from its congeners by the position of the cirrus-sac with regard to the poral osmoregulatory canals and position of distal end of the rostellar pouch relative to the posterior margins of the suckers. Kontrimavichusia hobergi can be readily distinguished from its congeners by the arrangement of the testes in a triangle and the position of the cirrus-sac with regard to the poral osmoregulatory canals. In addition, this previously unrecognized species differs from K. asymmetrica and K. testiculata by the smaller dimensions of the fully developed strobila and a narrower ovary. The cirrus-sac of K. hobergi is larger than that in K. asymmetrica but smaller than that in K. testiculata. We also used partial sequences of the nuclear ribosomal 28S rRNA gene and mitochondrial nad1 gen to justify the generic arrangement and independent status of these two new species which are characterized in the current manuscript.
References
Baer J.-G. & Tenora F. 1970. Some species of Hymenolepis (Cestoidea) from rodents and from primates. Acta Scientiarum Naturalium Academiae Scientiarum Bohemicae, Brno 4: 1–32.
Binkienė R., Miliūtė A. & 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: 195–202. https://doi.org/10.1017/S0022149X18000056
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: 595–663. CAB International, Wallingford, UK.
Erhardová B. 1955. Die Helminthofauna der mäuseartigen Nagetiere des Nationalparks in der Roben Tatra. Folia Zoologica et Entomologica 4: 353–364.
Galbreath K.E., Makarikov A.A., Bell K.C., Greiman S.E., Allen J.M., Haas G.M.S., Li C., Cook J.A. & Hoberg E.P. 2023. Late Cenozoic history and the role of Beringia in assembling a Holarctic cestode species complex. Molecular Phylogenetics and Evolution 183: e107775. https://doi.org/10.1016/j.ympev.2023.107775
Genov T. 1984. Helminths of Insectivores and Rodents in Bulgaria. Izdatelstvo na Bulgarskata akademiya na naukite, Sofia. [In Bulgarian.]
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. https://doi.org/10.1016/j.parint.2012.01.003
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. The Journal of Parasitology 99: 1045–1049. https://doi.org/10.1645/13-302.1
Gulyaev V.D. & Chechulin A.I. 1996. [Composition and morphological criteria of the tribe Sudarikovinini (Cestoda: Cyclophyllidea: Hymenolepididae).] Parasitologiya 30: 495–503. [In Russian.]
Haas G.M.S., Hoberg E.P., Cook J.A., Henttonen H., Makarikov A.A., Gallagher S.R., Dokuchaev N.E. & Galbreath K.E. 2020. Taxon pulse dynamics, episodic dispersal and host colonization across Beringia drive diversification of a Holarctic tapeworm assemblage. Journal of Biogeography 47: 2457–2471. https://doi.org/10.1111/jbi.13949
Hall T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
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. https://doi.org/10.1111/j.1463-6409.2010.00444.x
Janicki C. 1904. Zur Kenntnis einiger Säugetiercestoden. Zoologischer Anzeiger 27: 770–782.
Janicki C. 1906. Studien an Säugetiercestoden. Zeitschrift für wissenschaftliche Zoologie 81: 503–597.
Jia Y.Q., Yan W.C., Du S.Z., Song J.K., Zhao W., Zhao Y.X., Cheng W.Y. & Zhao G.H. 2016. Pseudanoplocephala crawfordi is a member of genus Hymenolepis based on phylogenetic analysis using ribosomal and mitochondrial DNA sequences. Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis 27: 1688–1692. https://doi.org/10.3109/19401736.2014.958729
Kornienko S.A., Stakheev V.V. & Makarikov A.A. 2021. Cestodes of shrews (Soricidae) in the North Caucasus. Zoolgicheskii Zhurnal 100: 867–876. https://doi.org/10.31857/S0044513421060076
Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev/msy096
Littlewood D.T.J., Waeschenbach A. & Nikolov P.N. 2008. In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda) – a test study with Davaineidae. Acta Parasitologica 53: 133–144. https://doi.org/10.2478/s11686-008-0029-4
Lockyer A.E., Olson P.D. & Littlewood D.T.J. 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: 155–171. https://doi.org/10.1046/j.1095-8312.2003.00141.x
Makarikov A.A. & Binkienė R. 2022. 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). Journal of Helminthology 96: E63. https://doi.org/10.1017/S0022149X22000505
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. https://doi.org/10.11646/ZOOTAXA.3608.6.1
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. https://doi.org/10.1016/j.parint.2015.06.009
Makarikov A.A., Stakheev V.V. & Orlov V.N. 2017. On helminth fauna of rodents from the Northwest Caucasus. Parasitologiya 52: 317–328. [In Russian.]
Makarikov A.A., Stakheev V.V. & Tkach V.V. 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: 65–79. https://doi.org/10.1007/s11230-017-9765-x
Makarikov A.A., Galbreath K.E., Eckerlin R.P. & Hoberg E.P. 2020. Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America. Parasitology Research 119: 567–585. https://doi.org/10.1007/s00436-019-06584-4
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: 139–173.
Murai E. 1974. Review of tapeworms in Microtinae from Hungary. Parasitologia Hungarica 7: 111–141.
Murai E. 1989. Ceratozetes gracilis (Michael, 1884) (Acari: Oribatida), an intermediate host of Vampirolepis asymmetrica (Janicki, 1904) (Cestoda: Hymenolepididade). Miscellanea Zoologica Hungarica 5: 13–19.
Musser G.G. & Carelton M.D. 2005. Superfamily Muroidea. In: Wilson D.E. & Reeder D.M. (eds) Mammal Species of the World: a Taxonomic and Geographic Reference, 3rd Edn: 894–1522. Johns Hopkins University Press, Baltimore, Maryland.
Neov B., Vasileva G.P., Radoslavov G., Hristov P., Littlewood D.T.J & Georgiev B.B. 2019. Phylogeny of hymenolepidid cestodes (Cestoda: Cyclophyllidea) from mammalian hosts based on partial 28S rDNA, with focus on parasites from shrews. Parasitology Research 118: 73–88. https://doi.org/10.1007/s00436-018-6117-y
Nkouawa A., Haukisalmi V., Li T., Nakao M., Lavikainen A., Chen X., Henttonen H. & Ito A. 2016. Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitology International 65: 83–86. https://doi.org/10.1016/j.parint.2015.10.009
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. 1978. Keys to the helminths of the rodent fauna of the USSR. Cestodes and trematodes. Izdatel’stvo Nauka, Moscow. [In Russian.]
Santalla F., Casanova J.C., Durand P., Vaucher C., Renaud F. & Feliu C. 2002. Morphometric and genetic variability of Rodentolepis asymmetrica (Hymenolepididae) from the Pyrenean mountains. Journal of Parasitology 88: 983–988. https://doi.org/10.1645/0022-3395(2002)088[0983:magvor]2.0.co;2
Schmidt G.D. 1986. Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida.
Skrjabin K.I. & Matevosyan E.N. 1945. Tapeworms-Hymenolepidae of Domestic and Game Birds. Izdatel’stvo Sel’khozgiz, Moscow. [In Russian.]
Sokolov V.E. & Tembotov A.K. 1989. Mammals of the Caucasus. Insectivora. Nauka Press, Moscow. [In Russian.]
Spassky A.A. 1954. Classification of hymenolepidids of mammals. Trudy Gel’mintologcheskoy Laboratorii, Akademii Nauk SSSR 7: 120–167. [In Russian.]
Tkach V. & Pawlowski J. 1999. A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica 44: 147–148.
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 (Soricimorpha, Soricidae), in North America. Zootaxa 3691: 389–400. https://doi.org/10.11646/zootaxa.3691.3.7
Vaucher C. 1967. Contribution à l’étude des cestodes et des trématodes parasites des micromammifères de Suisse 1. Bulletin de la Société Neuchâteloise des Sciences Naturelles 90: 161–184.
Zehnder M.P. & 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: 1841–1852. https://doi.org/10.1016/S0020-7519(99)00122-8
Copyright (c) 2024 Arseny A. Makarikov, Valeriy V. Stakheev
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT PERMITTED to post their submitted work online (e.g., in institutional repositories or on personal websites) prior to publication, as it may lead to nomenclatural issues.
