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Citellinema (Nematoda: Heligmosomidae) from North America with descriptions of 2 new species from the red squirrel Tamiasciurus hudsonicus and 1 from the Canadian woodchuck, Marmota monax

Published online by Cambridge University Press:  27 May 2022

Haitham Alnaqeb Open the ORCID record for Haitham Alnaqeb [Opens in a new window] ,
Kurt E. Galbreath Open the ORCID record for Kurt E. Galbreath [Opens in a new window] ,
Anson V. Koehler ,
Mariel L. Campbell  and
F. Agustín Jiménez Open the ORCID record for F. Agustín Jiménez [Opens in a new window]
Haitham Alnaqeb
Affiliation:
School of Biological Sciences, Southern Illinois University, Carbondale, Illinois 62901-6501, USA
Kurt E. Galbreath
Affiliation:
Department of Biology, Northern Michigan University, Marquette, Michigan 49855, USA
Anson V. Koehler
Affiliation:
Department of Veterinary Biosciences, Melbourne Veterinary School, The University of Melbourne, Parkville, Victoria 3010, Australia
Mariel L. Campbell
Affiliation:
Division of Genomic Resources, Museum of Southwestern Biology, University of New Mexico, Albuquerque, New Mexico 87131, USA
F. Agustín Jiménez*
Affiliation:
School of Biological Sciences, Southern Illinois University, Carbondale, Illinois 62901-6501, USA
*
Author for correspondence: F. Agustín Jiménez, Email: [email protected]
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Abstract

Citellinema Hall, 1918 includes 6 valid species of gastrointestinal nematodes of sciurids. Two species occur in the Palearctic and 4 in the Nearctic, 3 of which occur minimally across Colorado, Idaho and Oregon and 1, Citellinema bifurcatum, has a wide distribution across North America. Members of the genus are didelphic, possess a cephalic vesicle, a terminal spine-like process in females and feature robust spicules, consisting of a proximal end fused and semicylindrical shaft connected to a lamina supported by 2 terminal filiform processes. Typically, the size of the spicules is used to differentiate species. As part of the Beringian Coevolution Project, specimens provisionally identified as C. bifurcatum were collected through intensive field sampling of mammals and associated parasites from across localities spanning the Holarctic. These specimens revealed considerable genetic variability at both mitochondrial and nuclear loci, supporting the identification of deeply divergent clades. Examination of these new specimens, along with the holotypes of C. bifurcatum and Citellinema quadrivittati indicates that Citellinema monacis (previously synonymized with C. bifurcatum) should be resurrected and 3 additional species described. We suggest that the apparent bifurcated nature of the spicule should be considered a generic diagnostic trait, while the proportional length of the lamina relative to that of the spicule is used as a specific character. We demonstrate the critical need for continued inventory of often poorly known assemblages of hosts and parasites, contributing to a growing baseline of archival specimens, collections and information that make explorations of faunal structure and diversity possible.

Keywords

CitellinemaHeligmosomoideaNematodascientific collectionsTamiasciurus hudsonicus
Type
Research Article
Information
Parasitology , Volume 149 , Issue 9 , August 2022 , pp. 1199 - 1218
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Alnaqeb, H, Greiman, S, Vandegrift, KJ, Campbell, ML, Meagher, S and Jiménez, FA (2022) A molecular reconstruction of Holarctic Heligmosomidae reveals a new species of Heligmosomoides (Nematoda: Heligmosomidae) in Peromyscus maniculatus (Neotominae) from Canada. Systematics and Biodiversity 20, 1–19. doi: 10.1080/14772000.2022.2046199.CrossRefGoogle Scholar
Colella, JP, Bates, J, Burneo, SF, Camacho, MA, Carrion Bonilla, C, Constable, I, D'Elía, G, Dunnum, JL, Greiman, S and Hoberg, EP (2021) Leveraging natural history biorepositories as a global, decentralized, pathogen surveillance network. PLoS Pathogens 17, e1009583.CrossRefGoogle ScholarPubMed
Cook, JA, Hoberg, EP, Koehler, A, Henttonen, H, Wickström, L, Haukisalmi, V, Galbreath, K, Chernyavski, F, Dokuchaev, N and Lahzuhtkin, A (2005) Beringia: intercontinental exchange and diversification of high latitude mammals and their parasites during the Pliocene and Quaternary. Mammal Study 30, S33–S44.CrossRefGoogle Scholar
Cook, JA, Galbreath, KE, Bell, KC, Campbell, ML, Carrière, S, Colella, JP, Dawson, NG, Dunnum, JL, Eckerlin, RP and Fedorov, V (2016) The Beringian coevolution project: holistic collections of mammals and associated parasites reveal novel perspectives on evolutionary and environmental change in the North. Arctic Science 3, 585–617.CrossRefGoogle Scholar
Dikmans, G (1938) A consideration of the nematode genus Citellinema with description of a new species, Citellinema columbianum. Proceedings of the Helminthological Society of Washington 5, 55–58.Google Scholar
Dunnum, JL, Yanagihara, R, Johnson, KM, Armien, B, Batsaikhan, N, Morgan, L and Cook, JA (2017) Biospecimen repositories and integrated databases as critical infrastructure for pathogen discovery and pathobiology research. PLoS Neglected Tropical Diseases 11, e0005133.CrossRefGoogle ScholarPubMed
Durette-Desset, MC (1969) Remarques sur un Citellinema sp., Nématode Trichostrongylide parasite d'un Glaucomys sabrinus en Californie. Bulletin du Muséum National d'Histoire Naturelle 41, 940–945.Google Scholar
Fleming, W, Georgi, J and Caslick, J (1979) Parasites of the woodchuck (Marmota monax) in central New York State. Proceedings of the Helminthological Society of Washington 46, 115–127.Google Scholar
Galbreath, KE, Hoberg, EP, Cook, JA, Armién, B, Bell, KC, Campbell, ML, Dunnum, JL, Dursahinhan, AT, Eckerlin, RP, Gardner, SL, Greiman, SE, Henttonen, H, Jiménez, FA, Koehler, AVA, Nyamsuren, B, Tkach, VV, Torres-Pérez, F, Tsvetkova, A and Hope, AG (2019) Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites. Journal of Mammalogy 100, 382–393.CrossRefGoogle ScholarPubMed
Haas, GM, 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, 2457–2471.CrossRefGoogle Scholar
Hall, MC (1916) Nematode parasites of mammals of the orders Rodentia, Lagomorpha, and Hyracoidea. Proceedings of the United States National Museum 50, 1–258.CrossRefGoogle Scholar
Hebert, PDN, Cywinska, A, Ball, SL and DeWaard, JR (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hoberg, EP and Soudachanh, KM (2021) Diversity of Tetrabothriidae (Eucestoda) among Holarctic Alcidae (Charadriiformes): resolution of the Tetrabothrius jagerskioeldi cryptic species complex – cestodes of Alcinae – provides insights on the dynamic nature of tapeworm and marine bird faunas under the Stockholm paradigm. MANTER: Journal of Parasite Biodiversity 16, 1–76. doi: 10.32873/unl.dc.manter16Google Scholar
Hoberg, EP, Galbreath, KE, Cook, JA, Kutz, SJ and 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.CrossRefGoogle ScholarPubMed
Hoberg, EP, Agosta, SJ, Boeger, WA and Brooks, DR (2015) An integrated parasitology: revealing the elephant through tradition and invention. Trends in Parasitology 31, 128–133.CrossRefGoogle ScholarPubMed
Hope, AG, Malaney, JL, Bell, KC, Salazar-Miralles, F, Chavez, AS, Barber, BR and Cook, JA (2016) Revision of widespread red squirrels (genus: Tamiasciurus) highlights the complexity of speciation within North American forests. Molecular Phylogenetics and Evolution 100, 170–182.CrossRefGoogle ScholarPubMed
Jiménez, FA, Gardner, SL, Navone, GT and Ortí, G (2012) Four events of host-switching in Aspidoderidae (Nematoda) involve convergent lineages of mammals. Journal of Parasitology 98, 1166–1175.CrossRefGoogle ScholarPubMed
Lichtenfels, JR (1971) Citellinema grisei sp. n. (Nematoda: Trichostrongylidae) from the western gray squirrel, Sciurus griseus. Proceedings of the Helminthological Society of Washington 38, 257–261.Google Scholar
Maddison, W (2018) Mesquite: a modular system for evolutionary analysis. Version 3.51. Available at http://www.mesquiteproject.org.Google Scholar
Manter, HW (1930) Two new nematodes from the woodchuck, Marmota monax canadensis. Transactions of the American Microscopical Society 49, 26–33.CrossRefGoogle Scholar
Mayer, F, Dietz, C and Kiefer, A (2007) Molecular species identification boosts bat diversity. Frontiers in Zoology 4, 4.CrossRefGoogle ScholarPubMed
Pyziel, AM, Laskowski, Z, Demiaszkiewicz, AW and Höglund, J (2017) Interrelationships of Dictyocaulus spp. in wild ruminants with morphological description of Dictyocaulus cervi n. sp. (Nematoda: Trichostrongyloidea) from red deer, Cervus elaphus. Journal of Parasitology 103, 506–518.CrossRefGoogle Scholar
Sievers, F, Wilm, A, Dineen, D, Gibson, TJ, Karplus, K, Li, W, Lopez, R, McWilliam, H, Remmert, M and Söding, J (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539.CrossRefGoogle ScholarPubMed
Swofford, D (2002) PAUP* [Phylogenetic Analysis Using Parsimony (and other methods)]. Version 4. Sunderland, Sinauer Associates, 4.Google Scholar
Zaleśny, G, Hildebrand, J, Paziewska-Harris, A, Behnke, JM and Harris, PD (2014) Heligmosomoides neopolygyrus Asakawa & Ohbayashi, 1986, a cryptic Asian nematode infecting the striped field mouse Apodemus agrarius in Central Europe. Parasites & Vectors 7, 457–466.CrossRefGoogle ScholarPubMed