Tapeworms of the genus Ophiotaenia La Rue, 1911 parasitize herptiles (= amphibians and 'reptiles') throughout the world, with about 100 species recognised as valid. In the present work, the North American species found in watersnakes (Colubridae) are reviewed. An examination of the holotype of Ophiotaenia perspicua La Rue, 1911, the type species of the genus, and other specimens from Nerodia rhombifer (Hallowell) revealed that two species were used for the species description. The 'true' O. perspicua has a small scolex and small, round suckers. This species is redescribed based on new material from Oklahoma, USA. The other species from N. rhombifer, Ophiotaenia laruei n. sp., has a larger scolex and larger, almost triangular suckers. Examination of the types of O. variabilis (Brooks, 1978) from N. rhombifer and N. cyclopion (Duméril, Bibron et Duméril) from Louisiana, USA has revealed that it is a mixture of two or more species. Because of poor quality of these specimens, it is not possible to adequately characterise O. variabilis, which is considered a species inquirenda. In addition, two new species are described from Nerodia fasciata confluens (Blanchard). Ophiotaenia currani n. sp. from Mississippi, USA is characterised by elongate, narrow proglottids, few testes, and a relatively long cirrus sac. Ophiotaenia tkachi n. sp. from Louisiana, USA is characterised by relatively short and wide proglottids, more testes, and an unusual terminal part of the vagina with folds. Morphologically similar tapeworms of N. fasciata confluens, N. erythrogaster (Förster), N. sipedon (Linnaeus), and Agkistrodon piscivorus (Lacépède) (Viperidae) from Arkansas and Oklahoma, USA, which are genetically nearly identical, are considered to be conspecific with O. tkachi n. sp. The present data suggest a high, previously undescribed species diversity of proteocephalid tapeworms in watersnakes in North America, and generally strict host specificity of these tapeworms.

Department of Invertebrates Natural History Museum P O Box 6434 CH 1211 Geneva 6 Switzerland

Division of Natural Sciences Northeast Texas Community College Mt Pleasant TX 75455 USA

Institute of Ecology Nature Research Centre Akademijos 2 08412 Vilnius Lithuania

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Branišovská 31 370 05 České Budějovice Czech Republic

Zobrazit více v PubMed

Alves P.V., de Chambrier A., Luque J.L., Scholz T. Integrative taxonomy reveals hidden cestode diversity in Pimelodus catfishes in the Neotropics. Zool. Scripta. 2020;50:210–224.

Alves P.V., de Chambrier A., Luque J.L., Takemoto R.M., Tavares L.E.R., Scholz T. New arrangement of three genera of fish tapeworms (Cestoda: Proteocephalidae) in catfishes (Siluriformes) from the Neotropical Region: taxonomic implications of molecular phylogenetic analyses. Parasitol. Res. 2021;120:1593–1603. PubMed

Anderson M.G. Some intestinal parasites of Natrix sipedon Linn., with notes on the identity of Ophiotaenia (Taenia) lactea Leidy with Ophiotaenia perspicua LaRue. Ohio J. Sci. 1935;35:78–80.

Blasco-Costa I., Cutmore S.C., Miller T.L., Nolan M.J. Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Syst. Parasitol. 2016;93:295–306. PubMed

Brabec J., Rochat E.C., Knudsen R., Scholz T., Blasco-Costa I. Mining various genomic resources to resolve old alpha-taxonomy questions: a test of the species hypothesis of the Proteocephalus longicollis species complex (Cestoda: Platyhelminthes) from salmonid fishes. Int. J. Parasitol. 2023;53:197–205. PubMed

Brooks D.R. Systematic status of proteocephalid cestodes fom reptiles and amphibians in North America with description of three new species. Proc. Helminthol. Soc. Wash. 1978;45:1–28.

Caira J.N., Jensen K., Georgiev B.B., Kuchta R., Littlewood D.T.J., Mariaux J., Scholz T., Tkach V.V., Waeschenbach A. In: Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Caira J.N., Jensen K., editors. University of Kansas, Natural History Museum, Special Publication No. 25; Lawrence, Kansas: 2017. An overview of tapeworms from vertebrate bowels of the earth; pp. 1–20.

de Chambrier A., Scholz T. An emendation of generic diagnosis of the monotypic Glanitaenia (Cestoda: Proteocephalidae), with notes on the geographical distribution of G. osculata, a parasite of invasive wels catfish. Rev. Suisse Zool. 2016;123:1–9.

de Chambrier A., Vaucher C. Proteocephalidae et Monticelliidae (Eucestoda: Proteocephalidea) parasites de Poissons d’eau douce du Paraguay avec descriptions d’un genre nouveau et de dix espèces nouvelles. Rev. Suisse Zool. 1999;106:165–240.

de Chambrier A., Vaucher C., Renaud F. Etude des caractères morpho-anatomiques et des flux géniques chez quatre Proteocephalus (Cestoda: Proteocephalidae) parasites de Bothrops jararaca du Brésil et description de trois espèces nouvelles. Syst. Parasitol. 1992;23:141–156.

de Chambrier A., Zehnder M.P., Vaucher C., Mariaux J. The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Syst. Parasitol. 2004;57:159–171. PubMed

de Chambrier A., Coquille S.C., Brooks D.R. Ophiotaenia bonneti sp. n. (Eucestoda: Proteocephalidea), a parasite of Rana vaillanti (Anura: Ranidae) in Costa Rica. Folia Parasitol. 2006;53:125–133. PubMed

de Chambrier A., Coquille S.C., Mariaux J., Tkach V. Redescription of Testudotaenia testudo (Magath, 1924) (Eucestoda: Proteocephalidea), a parasite of Apalone spinifera (Le Sueur) (Reptilia: Trionychidae) and Amia calva L. (Pisces: Amiidae) in North America and erection of the Testudotaeniinae n. subfam. Syst. Parasitol. 2009;73:49–64. PubMed

de Chambrier A., Binh T.T., Scholz T. Ophiotaenia bungari n. sp. (Cestoda), a parasite of Bungarus fasciatus (Schneider) (Ophidia: Elapidae) from Vietnam, with comments on relative ovarian size as a new and potentially useful diagnostic character for proteocephalidean tapeworms. Syst. Parasitol. 2012;81:39–50. PubMed

de Chambrier A., Waeschenbach A., Fisseha M., Scholz T., Mariaux J. A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda) ZooKeys. 2015;500:25–59. PubMed PMC

de Chambrier A., Scholz T., Mariaux J., Kuchta R. In: Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Caira J.N., Jensen K., editors. Special Publication No. 25. University of Kansas, Natural History Museum; Lawrence, Kansas: 2017. Onchoproteocephalidea I Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014; pp. 251–277.

de Chambrier A., Alves P.V., Schuster R., Scholz T. Ophiotaenia echidis n. sp. (Cestoda: Proteocephalidae) from the saw-scaled viper, Echis carinatus (Schneider) (Ophidia: Viperidae), one of the world's deadliest snakes, from the United Arab Emirates. Int. J. Parasitol.: Parasit. Wildlife. 2021;14:341–354. PubMed PMC

Collins R.F. The helminths of Natrix spp. and Agkistrodon piscivorus piscivorus (Reptilia: Ophidia) in eastern North Carolina. J. Elisha Mitchell Sci. Soc. 1969;85:141–144.

Coquille S.C., de Chambrier A. Cairaella henrii gen. n., sp. n., a parasite of Norops trachyderma (Polychrotidae), and Ophiotaenia nicoleae sp. n. (Eucestoda: Proteocephalidea), a parasite of Thecadactylus rapicauda (Gekkonidae), in Ecuador. Folia Parasitol. 2008;55:197–206. PubMed

Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012;9:772. PubMed PMC

Detterline J.L., Jacob J.S., Wilhelm W.E. A comparison of helminth endoparasites in the cottonmouth (Agkistrodon piscivorus) and three species of watersnakes (Nerodia) Trans. Am. Microsc. Soc. 1984;103:137–143.

Diard L., de Chambrier A., Waeschenbach A., Scholz T. A new species of tapeworm from Compsophis infralineatus (Pseudoxyrhophiidae), an endemic snake of Madagascar: scratching the surface of undiscovered reptilian parasite diversity. Parasitol. Int. 2022;88 PubMed

Ernst C.H., Ernst E.M. Synopsis of helminths endoparasitic in snakes of the United States and Canada. SSAR Herpetol. Circ. 2006;34:1–86.

Fantham H.B., Porter A. The endoparasites of some North American snakes and their effects on the Ophidia. Proc. Zool. Soc. Lond. 1954;123:867–898.

Flores-Barroeta L., Hidalgo-Escalante E., Montero-Gei F. Céstodos de vertebrados VIII. Rev. Biol. Trop. 1961;9:187–207.

Fontenot L.W., Font W.F. Helminth parasites of four species of aquatic snakes from two habitats in southeastern Louisiana. J. Helminthol. Soc. Wash. 1996;63:66–75.

Freze V.I. Nauka; Moscow: 1965. Essentials of Cestodology. Vol. V. Proteocephalata in Fish, Amphibians and Reptiles; p. 538. (In Russian: English translation: Israel Program of Scientific Translation, Jerusalem, 1969, Cat. No. 1853, v + p. 597)

García-Prieto L. Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México; México: 1986. Estudio taxonómico de algunos céstodos de vertebrados de México. Bachelor Thesis; p. 75.

Gibson J.B., Rabalais F.C. Helminth parasites of Natrix sipedon sipedon and Thamnophis sirtalis sirtalis from the Ottawa National Wildlife Refuge, Ohio. Am. Midl. Nat. 1973;89:239–241.

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. PubMed

Harwood P.D. The helminths parasitic in the Amphibia and Reptilia of Houston, Texas and vicinity. Proc. U. S. Natl. Mus. 1932;81:1–71.

Herde A. Early development of Ophiotaenia perspicua La Rue. Trans. Am. Microsc. Soc. 1938;57:282–291.

International Code of Zoological Nomenclature . The International Trust for Zoological Nomenclature 1999. fourth ed. c/o The Natural History Museum; London, U.K.: 1999. p. 306.

Leidy J. Notices of some tape worms. Proc. Acad. Nat. Sci, Philadelphia. 1855;7:443–444.

de Luna M., García-Barrios R., Barton D.P., García-Vázquez L. Adult tapeworm (Platyhelminthes: Cestoda) parasites of North American herpetofauna: checklist of species and identification key to families and genera. J. Parasitol. 2023;109:377–400. PubMed PMC

MacCallum G.A. Studies in helminthology. Part 1. Trematodes. Part 2. Cestodes. Part 3. Nematodes. Zoopathologica. Sci. Contr. New York Zool. Soc. Dis. Anim. 1921;1:135–284.

McAllister C.T., Bursey C.R. New host and distributional records for helminth parasites (Trematoda, Cestoidea, Nematoda) of herpetofauna from southeastern Oklahoma. Proc. Okla. Acad. Sci. 2012;92:29–35.

McAllister C.T., Bursey C.R., Trauth S.E. New host and geographic distribution records for some endoparasites (Myxosporea, Trematoda, Cestoidea, Nematoda) of amphibians and reptiles from Arkansas and Texas. U.S.A. Comp. Parasitol. 2008;75:241–254.

Pérez-Ponce de León G., Jiménez-Ruiz A., Mendoza-Garfias B., García-Prieto L. Helminths parasites of garter snakes and mud turtles from several localities of the Mesa Central of Mexico. J. Helminthol. Soc. Wash. 2001;61:139–141.

Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P., Thollesson M. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol. Phylogenet. Evol. 2008;48:369–371. PubMed

Rambaut A. 2012. FigTree V1. 4. Molecular Evolution, Phylogenetics and Epidemiology.http://tree.bio.ed.ac.uk/software/figtree/

Rego A.A. In: Keys to the Cestode Parasites of Vertebrates. Khalil L.F., Jones A., Bray R.A., editors. CAB International; Wallingford: 1994. Order Proteocephalidea Mola, 1928; pp. 257–293.

Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., Huelsenbeck J.P. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. PubMed PMC

La Rue G.R. A revision of the cestode family Proteocephalidae. Zool. Anz. 1911;38:473–482.

La Rue G.R. A revision of the cestode family Proteocephalidae. Ill Biol. Monogr. 1914;1:1–350. + 16 pls.

Schmidt G.D. CRC Press; Boca Raton, Florida: 1986. CRC Handbook of Tapeworm Identification; p. 675.

Scholz T., Barčák D., Waeschenbach A., McAllister C.T., Choudhury A. Tapeworms (Cestoda) of ictalurid catfishes (Siluriformes) in North America: redescription of type species of two genera and proposal of Essexiellinae n. subfam. J. Parasitol. 2020;106:444–463. PubMed

Scholz T., de Chambrier A., McAllister C.T., Tkach V.V., Kuchta R. Tapeworms (Cestoda: Ophiotaenia) from the northern cottonmouth (Agkistrodon piscivorus) J. Parasitol. 2023;109:464–479. PubMed

Scholz T., de Chambrier A., Kudlai O., Tkach V.V., McAllister C.T. A global survey of tapeworms (Cestoda: Proteocephalidae) of ‘true’ frogs (Amphibia: Ranidae), including a tabulated list of all proteocephalids parasiting amphibians. Folia Parasitol. 2023;70:9. PubMed

Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol. Biol. Evol. 2021;38:3022–3027. PubMed PMC

Thomas L.J. The life cycle of Ophiotaenia perspicua La Rue, a cestode of snakes. Rev. Med. Trop. Parasitol. Clin. Lab. 1941;7:74–78.

Uetz P., Freed P., Aguilar R., Hošek J., editors. The Reptile Database. 2023. http://www.reptile-database.org

Three new species of Ophiotaenia La Rue, 1911 (Cestoda: Proteocephalidae) from dipsadine snakes (Squamata: Colubridae) in Ecuador