Skip to main content
Springer Nature Link
Log in

Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the oldfield mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the southeastern Nearctic with comments on tapeworm faunal diversity among deer mice

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A previously unrecognized species of hymenolepidid cestode attributable to Hymenolepis is described based on specimens in Peromyscus polionotus, oldfield mouse, from Georgia near the southeastern coast of continental North America. Specimens of Hymenolepis folkertsi n. sp. differ from those attributed to most other species in the genus by having testes arranged in a triangle and a scolex with a prominent rostrum-like protrusion. The newly recognized species is further distinguished by the relative position and length of the cirrus sac, shape of seminal receptacle, and relative size of external seminal vesicle and seminal receptacle. Hymenolepidid cestodes have sporadically been reported among the highly diverse assemblage of Peromyscus which includes 56 distinct species in the Nearctic. Although the host genus has a great temporal duration and is endemic to the Nearctic, current evidence suggests that tapeworm faunal diversity reflects relatively recent assembly through bouts of host switching among other cricetid, murid, and geomyid rodents in sympatry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Agosta SJ, Janz N, Brooks DR (2010) How generalists can be specialists: resolving the “parasite paradox” and implications for emerging infectious disease. Zoologia 27:151–162

    Article  Google Scholar 

  • American Society of Mammalogists (1998) Guidelines for the capture, handling, and care of mammals as approved by the American Society of Mammalogists. J Mammal 79:1416–1431

    Article  Google Scholar 

  • Arai H (1980) Biology of the Tapeworm Hymenolepis diminuta. New York Academic Press, New York

    Google Scholar 

  • Avise JC, Shapira JF, Daniel SW, Aquadro CF, Lansman RA (1983) Mitochondrial DNA differentiation during the speciation process in Peromyscus. Mol Biol Evol 1:38–56

    CAS  PubMed  Google Scholar 

  • Babero BB, Matthias D (1967) Protospirura peromysci n. sp. (Nematoda: Spiruridea) and other helminths from Peromyscus spp. in Nevada. Proc Helminthol Soc Wash 34:255–261

    Google Scholar 

  • Barker CM, Dyer WG, Feldhamer GA (1987) Helminths of Peromyscus leucopus, P. maniculatus and Blarina carolinensis from southern Illinois. Trans Ill Acad Sci 80:119–127

    Google Scholar 

  • Binkienė R, Kontrimavichus V, Hoberg EP (2011) Overview of the cestode fauna of European shrews of the genus Sorex with comments on the fauna in Neomys and Crocidura and an exploration of historical processes in post-glacial Europe. Helminthologia 48:207–228. doi:10.2478/s11687-011-0031-5

    Google Scholar 

  • Brooks DR, Hoberg EP, Boeger WA, Gardner SL, Galbreath KE, Herczeg D, Mejía-Madrid HH, Rácz SE, Dursahinhan AT (2014) Finding them before they find us: informatics, parasites, and environments in accelerating climate change. Comp Parasitol 81:155–164. doi:10.1654/4724b.1

    Article  Google Scholar 

  • Doran DJ (1954) A catalogue of the Protozoa and helminths of North American rodents. II. Cestoda. Am Midl Nat 52:469–480

    Article  Google Scholar 

  • Dragoo JW, Lackey JA, Moore KE, Lessa EP, Cook JA, Yates TL (2006) Phylogeography of the deer mouse (Peromyscus maniculatus) provides a predictive framework for research on hantaviruses. J Gen Virol 87:1997–2003. doi:10.1099/vir. 0.81576-0

    Article  CAS  PubMed  Google Scholar 

  • Dyer WG (1969) A checklist of the Protozoa and helminths of the deer mouse Peromyscus maniculatus in North America. Am Midl Nat 81:258–262

    Article  Google Scholar 

  • Erickson AB (1938) Parasites of some Minnesota Cricetidae and Zapodidae, and a host catalogue of helminth parasites of native American mice. Am Midl Nat 20:575–589

    Article  Google Scholar 

  • Freeman RS (1960) Another hymenolepidid with great morphological variation, Hymenolepis bennetti n. sp. (Cestoda) from Napaeozapus insignis algonquinensis Prince. Can J Zool 38:737–743

    Article  Google Scholar 

  • Gardner SL (1985) Helminth parasites of Thomomys bulbivorus (Richardson) (Rodentia: Geomyidae), with the description of a new species of Hymenolepis (Cestoda). Can J Zool 63:1463–1469

    Article  Google Scholar 

  • Gardner SL, Schmidt GD (1988) Cestodes of the genus Hymenolepis Weinland, 1858 sensu stricto from pocket gophers Geomys and Thomomys spp. (Rodentia: Geomyidae) in Colorado and Oregon, with a discriminant analysis of four species of Hymenolepis. Can J Zool 66:896–903

    Article  Google Scholar 

  • Gardner SL, Luedders BA, Duszynski DW (2014) Hymenolepis robertrauschi n. sp. from grasshopper mice Onychomys spp. in New Mexico and Nebraska, U.S.A. Occas Pap Mus Texas Tech Univ 322:1–10

    Google Scholar 

  • Greiman SE, Tkach VV (2012) Description and phylogenetic relationships of Rodentolepis gnoskei n. sp. (Cyclophyllidea: Hymenolepididae) from a shrew Suncus varilla minor in Malawi. Parasitol Int 61:343–350

  • Grundmann AW, Frandsen JC (1960) Definitive host relationships of the helminth parasites of the deer mouse, Peromyscus maniculatus, in the Bonneville Basin of Utah. J Parasitol 46:673–677

    Article  CAS  PubMed  Google Scholar 

  • Gulyaev VD, Mel’nikova YA (2005) New genus of Cestoda from moles Talpolepis gen. n. and the redescription of T. peipingensis (Hsü, 1935) comb. n. (Cyclophyllidea: Hymenolepididae). Probl Cestodol 3:130–139 (In Russian)

    Google Scholar 

  • Hansen MF (1950) A new dilepidid tapeworm and notes on other tapeworms of rodents. Am Midl Nat 43:471–479

    Article  Google Scholar 

  • Haukisalmi V, Wickström LM, Henttonen H, Hantula J, Gubányi A (2004) Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae). Zool Scr 33:277–290. doi:10.1111/j.0300-3256.2004.00148.x

    Article  Google Scholar 

  • Haukisalmi V, Hardman LM, Foronda P, Feliu C, Laakonen J, Niemimaa J, Lehtonen JT, Henttonen H (2010a) Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zool Scr 39:631–641. doi:10.1111/j.1463-6409.2010.00444.x

    Article  Google Scholar 

  • Haukisalmi V, Hardman LM, Henttonen H (2010b) Taxonomic review of the genus Catenotaenia Janicki, 1904 in Eurasia and molecular phylogeny of the Catenotaeniidae (Cyclophyllidea). Zootaxa 2489:1–33

    Google Scholar 

  • Haukisalmi V, Hardman LM, Hoberg EP, Henttonen H (2014) Phylogenetic relationships and taxonomic revision of Paranoplocephala Lühe, 1910 sensu lato (Cestoda, Cyclophyllidea, Anoplocephalidae). Zootaxa 3873:371–415. doi:10.11646/zootaxa.3873.4.3

    Article  PubMed  Google Scholar 

  • Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J Biogeogr 35:1533–1550. doi:10.1111/j.1365-2699.2008.01951.x

    Article  Google Scholar 

  • Hoberg EP, Pilitt PA, Galbreath KE (2009) Why museums matter: a tale of pinworms (Oxyuroidea: Heteroxynematidae) among pikas (Ochotona princeps and O. collaris) in the American west. J Parasitol 95:490–501. doi:10.1645/GE-1823.1

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Galbreath KE, Cook JA, Kutz SJ, Polley L (2012) Northern host-parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Adv Parasitol 79:1–97. doi:10.1016/B978-0-12-398457-9.00001-9

    Article  PubMed  Google Scholar 

  • Hope AG, Takebayashi N, Galbreath KE, Talbot SL, Cook JA (2013) Temporal, spatial and ecological dynamics of speciation among amphi-Beringian small mammals. J Biogeogr 40:415–429. doi:10.1111/jbi.12056

    Article  Google Scholar 

  • Kinsella JM (1991) Comparison of helminths of three species of mice, Podomys floridanus, Peromyscus gossypinus, and Peromyscus polionotus, from southern Florida. Can J Zool 69:3078–3083

    Article  Google Scholar 

  • Kruidenier FJ, Gallicchio V (1956) A survey of cestodes in mammals from Grand Canyon National Park. J Parasitol 42:42

    Article  Google Scholar 

  • Kurtén B, Anderson E (1980) Pleistocene mammals of North America. Columbia University Press, New York

    Google Scholar 

  • Layne JN (1963) A study of the parasites of the Florida mouse, Peromyscus floridanus, in relation to host and environmental factors. Tulane Stud Zool 11:1–27

    Google Scholar 

  • Leiby PD (1961) Intestinal helminths of some Colorado mammals. J Parasitol 47:311

    Article  Google Scholar 

  • Leiby PD (1962) Helminth parasites recovered from some rodents in southeastern Idaho. Am Midl Nat 67:250

    Google Scholar 

  • Lubinsky G (1957) List of helminths from Alberta rodents. Can J Zool 35:623–627

    Article  Google Scholar 

  • Makarikov AA, Tkach VV (2013) Two new species of Hymenolepis (Cestoda: Hymenolepididae) from Spalacidae and Muridae (Rodentia) from eastern Palearctic. Acta Parasitol 58:37–49. doi:10.2478/s11686-013-0115-0

    Article  PubMed  Google Scholar 

  • Makarikov AA, Gardner SL, Hoberg EP (2012) New species of Arostrilepis (Eucestoda: Hymenolepididae) in members of Cricetidae and Geomyidae (Rodentia) from the Western Nearctic. J Parasitol 98:617–626. doi:10.1645/GE-2943.1

    Article  PubMed  Google Scholar 

  • Makarikov AA, Galbreath KE, Hoberg EP (2013a) Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia. Zootaxa 3608:401–439. doi:10.11646/zootaxa.3608.6.1

    Article  PubMed  Google Scholar 

  • Makarikov AA, Tkach VV, Bush SE (2013b) Two new species of Hymenolepis (Cestoda: Hymenolepididae) from murid rodents (Rodentia: Muridae) in the Philippines. J Parasitol 99:847–855. doi:10.1645/12-173.1

    Article  PubMed  Google Scholar 

  • Makarikov AA, Tkach VV, Villa SM, Bush SE (2015) Description of two new species of Hymenolepis Weinland, 1858 (Cestoda: Hymenolepididae) from rodents on Luzon Island, Philippines. Syst Parasitol 90:27–37. doi:10.1007/s11230-014-9528-x

    Article  PubMed  Google Scholar 

  • Mas-Coma S, Tenora F (1997) Proposal of Arostrilepis n. gen. (Cestoda: Hymenolepidae). Res Rev Parasitol 57:93–101

    Google Scholar 

  • Musser GG, Carleton MD (2005) Superfamily Muroidea. In: Wilson DE (ed) Reeder DM (eds) mammal species of the world: a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore, pp 894–1531

    Google Scholar 

  • Nims TN, Durden LA, Chandler CR, Pung OJ (2008) Parasitic and phoretic arthropods of the oldfield mouse (Peromyscus polionotus) from burned habitats with additional ectoparasite records from the eastern harvest mouse (Reithrodontomys humulis) and southern short-tailed shrew (Blarina carolinensis). Comp Parasitol 75:102–106. doi:10.1654/4273.1

    Article  Google Scholar 

  • Nowak RM (1999) Walker’s mammals of the world, vol 2. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pérez-Ponce de León G, Nadler SL (2010) What we don’t recognize can hurt us: a please for awareness about cryptic species. J Parasitol 96:453–464. doi:10.1645/GE-2260.1

    Article  Google Scholar 

  • Pospekhova NA (2009) Rostellar sac gland in Cloacotaenia megalops (Cestoda: Hymenolepididae). Invertebr Zool 6:33–46 (In Russian)

    Google Scholar 

  • Pung OJ, Durden LA, Patrick MJ, Conyers T, Mitchell LR (2000) Ectoparasites and gastrointestinal helminths of southern flying squirrels in southeast Georgia. J Parasitol 86:1051–1055. doi:10.1645/0022-3395(2000)086[1051:EAGHOS]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  • Rausch RL, Tiner JD (1949) Studies on the parasitic helminths of the north-central states. II. Helminths of voles (Microtus spp.) preliminary report. Am Midl Nat 41:665–694

    Article  Google Scholar 

  • Repenning CA (2001) Beringian climate during intercontinental dispersal: a mouse eye view. Quat Sci Rev 20:25–40

    Article  Google Scholar 

  • Ryzhikov KM, Gvozdev EV, Tokobaev MM, Shaldybin LS, Matzaberidze GV, Merkusheva IV, Nadtochii EV, Khohlova IG, Sharpilo LD (1978) Keys to the helminths of the rodent fauna of the USSR. Cestodes and trematodes. Izdatel’stvo Nauka, Moskva, 232 pp. (In Russian)

    Google Scholar 

  • Schad GA (1954) Helminth parasites of mice in northeastern Quebec and the coast of Labrador. Can J Zool 32:215–224

    Article  Google Scholar 

  • Schiller EL (1952) Studies on the helminth fauna of Alaska. X. Morphological variation in Hymenolepis horrida (von Linstow, 1901) (Cestoda: Hymenolepididae). J Parasitol 38:554–568. doi:10.2307/3273983

    Article  CAS  PubMed  Google Scholar 

  • Singh KS (1956) Hymenolepis vogeae n. sp., from an Indian Field Mouse, Mus buduga Thomas, 1881. Trans Am Microsc Soc 75:252–255, http://www.jstor.org/stable/3224018

    Article  Google Scholar 

  • Smith CF (1954) Four new species of cestodes of rodents from the high plains, central and southern Rockies and notes on Catenotaenia dendritica. J Parasitol 40:245–254

    Article  CAS  PubMed  Google Scholar 

  • Spassky AA (1963) Hymenolepidid cestodes—tapeworms of wild and domestic birds, vol 2. Izdatel’stvo Akademii Nauk SSSR, Moscow, 418 pp. (In Russian)

    Google Scholar 

  • Spassky AA (1992) To the phylogeny and systematics of hymenolepidoid tapeworms (Cestoda: Cyclophyllidea). Buletinul Academiei de Stiintea Republicii Moldova, Stiinte Biologice si Chimice 6:41–47 (In Russian)

    Google Scholar 

  • Spassky AA, Spasskaja LP (1954) Systematics of Hymenolepididae parasiting birds. Trudy Gel’mintologcheskoy Laboratorii Akademii Nauk SSSR 7:55–119, In Russian

    Google Scholar 

  • Specian RD, Lumsden RD (1980) The microanatomy and fine structure of the rostellum of Hymenolepis diminuta. Z Parasitenkd 63:71–88. doi:10.1007/bf00927728

    Article  CAS  PubMed  Google Scholar 

  • Specian RD, Lumsden RD (1981) Histochemical, cytochemical and autoradiographic studies on the rostellum of Hymenolepis diminuta. Z Parasitenkd 64:335–345. doi:10.1007/BF00927380

    Article  CAS  PubMed  Google Scholar 

  • Steppan SJ, Adkins RM, Anderson J (2004) Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53:533–553. doi:10.2307/4135423

    Article  PubMed  Google Scholar 

  • Tinkle DP (1972) Description and natural intermediate hosts of Hymenolepis peromysci n. sp., a new cestode from deer mice (Peromyscus). Trans Am Microsc Soc 91:66–69, http://www.jstor.org/stable/3224860

    Article  CAS  PubMed  Google Scholar 

  • Vaughn JW (2013) Parasite fauna of 3 sympatric Montana rodents. Unpublished Masters of Science Thesis, Western Illinois University, pp 1-23

  • Voge M (1952) Variation in some unarmed Hymenolepididae (Cestoda) from rodents. Univ Calif Publ Zool 57:1–52

    Google Scholar 

  • Whitaker JO, Jr (1968) Parasites. In: King JA (ed) Biology of Peromyscus (Rodentia). Special Publication American Society of Mammalogy, No. 2, pp 254-311

  • Whitaker JO Jr, Hamilton WJ Jr (1998) Mammals of the Eastern United States. Cornell University Press, Ithaca, 583 pp

    Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world a taxonomic and geographic reference, 3rd edn. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Yarinsky A (1952) Hymenolepis pitymi n. sp., a hymenolepidid cestode from the pine mouse. J Tenn Acad Sci 27:150–152

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Jean Mariaux (Natural History Museum, Geneva, Switzerland), Dr. Patricia Pilitt (US National Parasite Collection, Beltsville, MD, USA), and Dr. Scott L. Gardner (Harold W. Manter Laboratory of Parasitology, Lincoln, NE, USA), for specimen loans and/or providing conditions and laboratory space for examination of the type and voucher specimens. We thank Dr. Oscar Pung (Georgia Southern University (GSU), Statesboro, GA, USA) for his assistance with the mouse dissections. We thank The Nature Conservancy in Georgia for allowing access to their managed lands. We are grateful for access to the Arctos database through the Museum of Southwestern Biology, University of New Mexico, and a summary of inventory for parasites in species of Peromyscus prepared by Mariel Campbell. We sincerely thank Dr. Scott L. Gardner and an anonymous reviewer for their detailed comments that improved our manuscript. Research by AAM was supported in part by the Russian Fund for Fundamental Research (Project No. 14-04-00871-a). Further support for AAM was provided by the National Science Foundation (DEB 0819696 and 0818823) through grants addressing cestode diversity coordinated by Dr. Janine Caira, University of Connecticut. This is also a contribution to understanding history and diversity of mammalian helminth faunas supported by NSF through the Beringian Coevolution Project (DEB 0196095 and 0415668) and the Integrated Inventory of Biomes of the Arctic (DEB-Biodiversity Discovery and Analysis-1258010) to J.A. Cook (University of New Mexico), EPH, and KEG. Portions of this study were approved by the Institutional Animal Care and Use Committee (IACUC) at Georgia Southern University, permitted by the Georgia Department of Natural Resources, and done in partial completion of a Master of Science in Biology at GSU by TNN.

Author information

Authors and Affiliations

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

    Arseny A. Makarikov

  2. Science Department, Georgia Perimeter College, 239 Cedar Lane, Covington, GA, 30014, USA

    Todd N. Nims

  3. Department of Biology, Northern Michigan University, 1401 Presque Isle Ave., Marquette, MI, 49855, USA

    Kurt E. Galbreath

  4. United States National Parasite Collection, Animal Parasitic Disease Laboratory, USDA Agricultural Research Service, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, MD, 20705, USA

    Eric P. Hoberg

Authors
  1. Arseny A. Makarikov
    View author publications

    Search author on:PubMed Google Scholar

  2. Todd N. Nims
    View author publications

    Search author on:PubMed Google Scholar

  3. Kurt E. Galbreath
    View author publications

    Search author on:PubMed Google Scholar

  4. Eric P. Hoberg
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Arseny A. Makarikov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Makarikov, A.A., Nims, T.N., Galbreath, K.E. et al. Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the oldfield mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the southeastern Nearctic with comments on tapeworm faunal diversity among deer mice. Parasitol Res 114, 2107–2117 (2015). https://doi.org/10.1007/s00436-015-4399-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4399-x

Keywords

Profiles

  1. Arseny A. Makarikov View author profile