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Type: Articles
Published: 2013-01-23
Page range: 401–439
Abstract views: 37
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Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia

Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Frunze Str. 11, 630091 Novosibirsk, Russia
Department of Biology, Northern Michigan University, 1401 Presque Isle Avenue, Marquette, Michigan, USA 49855
United States National Parasite Collection, Animal Parasitic Disease Laboratory, USDA, Agricultural Research Service, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland, USA 20705
Platyhelminthes Cestoda Hymenolepididae Arostrilepis gulyaevi Arostrilepis cooki Arostrilepis rauschorum new species comparative morphology cytochrome b rodents Beringia

Abstract

Previously unrecognized species of hymenolepidid cestodes attributable to Arostrilepis Mas-Coma & Tenora, 1997 in arvicoline rodents from the greater Beringian region and western North America are described. Discovery and characterization of these tapeworms contributes to the recognition of a complex of cryptic species distributed across the Holarctic region. Three species are proposed: Arostrilepis gulyaevi sp. n. is named for cestodes in Myodes rufocanus from the Republic of Buryatia, southeastern Siberia and from the Khabarovskiy Kray, Chukotka Autonomous Okrug, and Magadanskaya Oblast’, Russian Far East (western Beringia); A. cooki sp. n. is named for cestodes in Myodes gapperi from British Columbia, Canada and Montana, USA; and A. rauschorum sp. n. is named for cestodes in Microtus oeconomus, M. longicaudus, M. pennsylvanicus and M. xanthognathus from the Brooks Range, Seward Peninsula, north-central interior, and Arctic coastal plains of Alaska (eastern Beringia) and Montana, USA. Consistent with recent studies defining diversity in the genus, the form, size, and spination (pattern, shape and size) of the cirrus are diagnostic; species are further distinguished by the relative position and length of the cirrus sac, and arrangement of the testes. Assessment of genetic data from the cytochrome b gene of mitochondrial DNA complements differentiation of this complex based on morphological attributes and confirms known species diversity within the genus. New data for geographical distribution and host specificity of known Arostrilepis spp. indicate that 3 of 12 recognized species have Holarctic distributions extending across Beringia. These include Arostrilepis beringiensis (Kontrimavichus & Smirnova, 1991) in lemmings (species of Lemmus and Synaptomys), A. cf. janickii Makarikov & Kontrimavichus, 2011 in root voles (M. oeconomus) MAKARIKOV ET AL. 402 · Zootaxa 3608 (6) © 2013 Magnolia Press and A. macrocirrosa Makarikov, Gulyaev & Kontrimavichus, 2011 in red backed voles (species of Myodes) and less often other rodent host species.

References

  1. Asakawa, M., Tenora, F. & Koubkova, B. (2002) Arostrilepis horrida (Linstow, 1901) (Cestoda: Hymenolepididae) from Eothenomys spp. (Rodentia) in Japan. Biogeography, 4, 51–55.

    Chaline, J. & Graf, J.-D. (1988) Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence. Journal of Mammalogy, 69, 22–33. http://dx.doi.org/10.2307/1381744

    Conroy, C.J., & Cook, J.A. (1999) Mt DNA evidence for repeated pulses of speciation within arvicoline and murid rodents.Journal of Mammalian Evolution, 6, 221–245. http://dx.doi.org/10.1023/A:1020561623890

    Cook, J.A., Hoberg, E.P., Koehler, A., Henttonen, H., Wickström, L., Haukisalmi, V., Galbreath, K., Chernyavski, F., Dokuchaev, N., Lahzuhtkin, A. et al. (2005) Beringia: Intercontinental exchange and diversification of high latitude mammals and their parasites during the Pliocene and Quaternary. Mammal Study, 30, 33–44. http://dx.doi.org/10.3106/1348-6160(2005)30[33:BIEADO]2.0.CO;2

    Cook, J.A., Runck, A.M. & Conroy, C. (2004) Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Molecular Phylogenetics and Evolution, 30, 767–777. http://dx.doi.org/10.1016/S1055-7903(03)00248-3

    Dogel’, V.A. (1962) General Parasitology. Izdatel’stvo Leningradskogo Universiteta, Leningrad, 464 pp. [In Russian.]

    Fedorov, K.P. (1986) Patterns of spatial distribution of parasitic worms. Izdatel’stvo Nauka, Novosibirsk, 256 pp. [In Russian.]

    Galbreath, K.E. & Hoberg, E.P. (2012) Return to Beringia: Parasites reveal cryptic biogeographic history of North American pikas. Proceedings of the Royal Society B, 279, 371–378. http://dx.doi.org/10.1098/rspb.2011.0482

    Grönlund, E. & Melander, O. (eds.). (1995) Swedish-Russian Tundra Ecology-Expedition -94. A cruise report. Swedish Polar Research Secretariat, Stockholm, 462 pp.

    Gulyaev, V.D. & Chechulin, A.I. (1997) Arostrilepis microtis n. sp. (Cyclophyllidea: Hymenolepididae), a new cestode species from Siberian rodents. Research and Reviews in Parasitology, 57, 103–107.

    Haukisalmi, V. & Henttonen, H. (2001) Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with description of Paranoplocephala fellmani n. sp. (Cestoda: Anoplocephalidae) from the Norweigian lemming L. lemmus (Linnaeus). Systematic Parasitology, 49, 7–22. http://dx.doi.org/10.1023/A:1010778504559

    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. http://dx.doi.org/10.1111/j.1463-6409.2010.00444.x

    Hoberg, E.P. & Brooks, D.R. (2008) A macroevolutionary mosaic: Episodic host-switching, geographic colonization and diversification in complex host-parasite systems. Journal of Biogeography, 35, 1533–1550. http://dx.doi.org/10.1111/j.1365-2699.2008.01951.x

    Hoberg, E.P. & Brooks, D.R. (2010) Beyond vicariance: Integrating taxon pulses, ecological fitting and oscillation in historical biogeography and evolution. In: Morand, S. & Krasnov, B.R. (Eds.), The Geography of Host-Parasite Interactions. Oxford University Press, Oxford, pp. 7–20.

    Hoberg, E.P., Galbreath, K.E., Cook, J.A., Kutz, S.J. & Polley, L. (2012) Northern host-parasite assemblages: History and biogeography on the borderlands of episodic climate and environmental transition. Advances in Parasitology, 79, 1–97.

    Hoberg, E.P., Kutz, S.J., Galbreath, K.E. & Cook, J. (2003) Arctic biodiversity: From discovery to faunal baselines- revealing the history of a dynamic ecosystem. Journal of Parasitology, 89, 84–95.

    Hoberg, E.P., Pilitt, P.A. & Galbreath, K.E. (2009) Why museums matter: a tale of pinworms (Oxyuroidea: Heteroxynematidae) among pikas (Ochotona princeps and O. collaris) in the American west. Journal of Parasitology, 95, 490–501. http://dx.doi.org/10.1645/GE-1823.1

    Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: a program for the Bayesian inference of phylogeny. Available from http://mrbayes.csit.fsu.edu/ (accessed 19 August 2001)

    Hwang, Y.T., Gardner, S.L. & Millar, J.S. (2007) Hymenolepis horrida (Cestoda: Hymenolepididae) and Catenotaenia peromysci (Cestoda: Anoplocephalidae) in voles from the Canadian Rockies. Comparative Parasitology, 74, 160–163. http://dx.doi.org/10.1654/4256.1

    Johri, G.N. (1956) On a new cestode from the palm squirrel, Funambulus palmarum Linn. Proceedings of the National Academy of Sciences of Allahabad, 26 (series B), 274–277.

    Kinsella, J.M. (1967) Helminths of Microtinae in western Montana. Canadian Journal of Zoology, 45, 269–274. http://dx.doi.org/10.1139/z67-038

    Kontrimavichus, V.L. (1969) Helminths of Mustelids and Trends in Their Evolution. Akademiia Nauk, Moscow. [English Translation 1985, Amerind Publishing Compnay, New Delhi, India].

    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: Krasnosohekov, G.P., Roitman, V.A., Sonin, M.D. & Chesnova, L.V. (Eds.), Evoljucia parazitov, Materialy I Vsesojuznogo simpoziuma. Tol’yatti, Akademiya Nauk SSSR, pp. 90–104.

    Kuns, M.L., & Rausch, R.L. (1950) An ecological study of helminths of some Wyoming voles (Microtus spp.) with a description of a new species of Nematospiroides (Heligmosomidae: Nematoda). Zoologica, 35, 181–188.

    Linstow, O. (1901) Taenia horrida, Tetrabothrium macrocephalum, und Heterakis distans. Archiv für Naturgeschichte, Berlin, 67, 1–10.

    Makarikov, A.A. (2008) Cestodes of the family Hymenolepididae Perrier, 1897 in rodents from the Asian part of Russia. Dissertatsija Kandidata Biologicheskikh Nauk, Rossiiskaja Akademija Nauk Sibirskoe Otdelenie Institut Sistematiki I Ekologii Zhivotnikh, Novosibirsk, Russia, 178 pp.

    Makarikov, A.A., Gulyaev, V.D. & Kontrimavichus, V.L. (2011) A redescription of Arostrilepis horrida (Linstow, 1901) and descriptions of two new species from Palearctic microtine rodents, Arostrilepis macrocirrosa sp. n. and Arostrilepis tenuicirrosa sp. n. (Cestoda: Hymenolepididae). Folia Parasitologica, 58, 108–120.

    Makarikov, A.A. & Kontrimavichus, V.L. (2011) A redescription of Arostrilepis beringiensis (Kontrimavichus et Smirnova, 1991) and descriptions of two new species from Palearctic microtine rodents, Arostrilepis intermedia sp. n. and A. janickii sp. n. (Cyclophyllidea: Hymenolepididae). Folia Parasitologica, 58, 289–301.

    Makarikov, A.A., Gardner, S.L. & Hoberg, E.P. (2012) New species of Arostrilepis (Eucestoda: Hymenolepididae) in members of Cricetidae and Geomyidae (Rodentia) from the Western Nearctic. Journal of Parasitology, 98, 617–626. http://dx.doi.org/10.1645/GE-2943.1

    Mas-Coma, S., Tenora, F. & Gallego, J. (1980) Consideraciones sobre los Hymenolepídidos inermes de Roedores, con especial referencia a la problemática entorno a Hymenolepis diminuta. Circular Farmacéutica. Barcelona, 38, 137–152.

    Mas-Coma, S. & Tenora, F. (1997) Proposal of Arostrilepis n. gen. (Cestoda: Hymenolepididae). Research and Reviews in Parasitology, 57, 93–101.

    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 Edition. Johns Hopkins University Press, Baltimore, Maryland, pp. 894–1522.

    Rambaut, A. & Drummond, A.J. (2009) Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer (accessed 2 December 2009)

    Rausch, R.L. (1950) Observations on the cyclic decline of lemmings (Lemmus) on the Arctic coast of Alaska during the spring of 1949. Arctic, 3, 166–177.

    Rausch, R.L. (1952) Studies on the helminth fauna of Alaska. XI. Helminth parasites of microtine rodents – taxonomic considerations. Journal of Parasitology, 38, 415–444. http://dx.doi.org/10.2307/3273922

    Rausch, R.L. (1994) Transberingian dispersal of cestodes in mammals. International Journal for Parasitology, 24, 1203–1212. http://dx.doi.org/10.1016/0020-7519(94)90191-0

    Repenning, C.A. (2001) Beringian climate during intercontinental dispersal: a mouse eye view. Quaternary Science Reviews, 20, 25–40. http://dx.doi.org/10.1016/S0277-3791(00)00133-5

    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, Moskva, Russia, 232 pp.

    Schad, G.A. (1954) Helminth parasites of mice in northeastern Quebec and the coast of Labrador. Canadian Journal of Zoology, 32, 215–224. http://dx.doi.org/10.1139/z54-021

    Schiller, E.L. (1952) Studies on the helminth fauna of Alaska. X. Morphological variation in Hymenolepis horrida (von Linstow, 1901) (Cestoda: Hymenolepididae). Journal of Parasitology, 38, 554–568. http://dx.doi.org/10.2307/3273983

    Swofford, D.L. (2000) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, USA.

    Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739. http://dx.doi.org/10.1093/molbev/msr121

    Tanabe, A.S. (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources, 11, 914–921. http://dx.doi.org/10.1111/j.1755-0998.2011.03021.x

    Tavrovskii, V.A., Egorov, O.V., Krivosheev, V.G., Popov, M.V. & Labutin, U.V. (1971) Mammals of Yakutia. Izdatel’stvo Nauka, Moskva, 659 pp.

    Voge, M. (1952) Variation in some unarmed Hymenolepididae (Cestoda) from rodents. In: Kirby, H., Eakin, R.M., Miller, A. & Stern, C. (Eds.), University of California Publications in Zoology, Vol. 57. University of California Press, Berkeley, California, pp. 1–52.

    Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Unpublished Ph.D. Dissertation, University of Texas at Austin.