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Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America

  • Immunology and Host-Parasite Interactions - Original Paper
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Abstract

Species of the genus Arostrilepis were discovered and definitively identified for the first time in rodents from geographically disparate localities along the Appalachian Mountain range of eastern North America (West Virginia, Virginia, and Maine). These are the first confirmed records for species of Arostrilepis occurring east of the Rocky Mountains and the Mississippi River in North America. Arostrilepis gardneri n. sp. is described on the basis of specimens obtained from two phylogenetically divergent rodent hosts: Southern Red-Backed Vole Myodes gapperi (Cricetidae: Arvicolinae) (from West Virginia) and the Woodland Jumping Mouse Napaeozapus insignis (Dipodidae: Zapodinae) (West Virginia, Virginia, and Maine). Additionally, in a mixed infection, specimens of Arostrilepis insperata n. sp. were also found in a Southern Red-Backed Vole from West Virginia. These previously unknown species are primarily distinguished from congeners based on shape, dimensions, and spination (pattern, shape, and size of spines) of the cirrus. Specimens of A. gardneri n. sp. are further characterized by the relative position and length of the cirrus-sac, arrangement of the testes, and relative size of the external seminal vesicle and seminal receptacle. Specimens of A. insperata n. sp. are structurally most similar to A. macrocirrosa from the western Nearctic and Palearctic but with consistently greater dimensions for the cirrus-sac, testes, and seminal receptacle. Phylogenetic analysis of Arostrilepis spp. using partial sequences of the mitochondrial cytochrome b gene and the nuclear second ribosomal internal transcribed spacer strongly supported the status of A. gardneri n. sp. and A. insperata n. sp. within an unresolved clade of congeners in Red-Backed Voles (Myodini and species of Myodes). Our observations extend the known geographic distribution for species of Arostrilepis to the Appalachian Mountains in either a disjunct or possibly continuous but patchy range across North America. Prior observations, summarizing field and museum collections, had suggested that geographic ranges for a diverse assemblage of Arostrilepis in North America were largely restricted to the north-western region of the continent, with historical connections to Beringia and Eurasia. Recognition of a more extensive distribution is consistent with a history of episodic biotic expansion and isolation under a dynamic of taxon pulses for arvicoline rodents and an associated parasite fauna in the Nearctic during the Quaternary. Occurrence in a dipodid rodent represents an event of host colonization from an arvicoline source.

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Acknowledgments

Dr. Alfred L. Gardner contributed to field collections in Virginia and Maine and prepared the symbiotype host specimens for deposition in the mammal collections of National Museum of Natural History. We thank the Virginia Division of Game and Inland Fisheries, the West Virginia Division of Natural Resources, and the Maine Division of Natural Resources for granting Scientific Collecting Permits. Funding which contributed to field collections was also provided from the Washington Biologists Field Club (to RPE).

Funding

AAM was supported in part by the Federal Fundamental Scientific Research Program for 2013–2020, grant no. VI.51.1.5 (АААА-А16-116121410121-7) and the Russian Foundation for Basic Research (Project No. 17-04-00227-a). RPE received partial funding for field collections from the Washington Biologists Field Club. Our study represents a continuing contribution of the Beringian Coevolution Project and the Integrated Inventories of Biomes of the Arctic through grants from the National Science Foundation (USA) to Joseph A. Cook, EPH, and KEG (DEB- 0196095, 0415668, 1250810, and 1256943).

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Authors and Affiliations

  1. Institute of Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences, Frunze Str. 11, Novosibirsk, Russian Federation, 630091

    Arseny A. Makarikov

  2. Department of Biology, Northern Michigan University, 1401 Presque Isle Avenue, Marquette, MI, 49855, USA

    Kurt E. Galbreath

  3. Mathematics, Science and Engineering Division, Northern Virginia Community College, Annandale, VA, 22003, USA

    Ralph P. Eckerlin

  4. Museum of Southwestern Biology, Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    Eric P. Hoberg

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Mammal specimens were collected under state scientific collector permits (Maine, Virginia, and West Virginia) and guidelines of the National Museum of Natural History Institutional Animal Care and Use Committee and American Society of Mammalogists (Sikes and The Animal Care and Use Committee of the American Society of Mammalogists 2016).

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The authors carefully reviewed the ethical standards of the journal and hereby certify that the procedures used with the investigated species comply fully with those standards. All applicable institutional, national, and international guidelines for the care and use of animals were followed.

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Makarikov, A.A., Galbreath, K.E., Eckerlin, R.P. et al. Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America. Parasitol Res 119, 567–585 (2020). https://doi.org/10.1007/s00436-019-06584-4

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