Abstract
Species of two monotypic genera, Ephedrocephalus Diesing, 1850 and Zygobothrium Diesing, 1850 (Cestoda: Proteocephalidae), parasites of one of the most basal members of the catfish family Pimelodidae, the redtail catfish, Phractocephalus hemioliopterus, in the Neotropical Region, are redescribed based on the evaluation of type specimens and newly collected material. Generic diagnoses are amended to provide a robust baseline for the future re-arrangement of the classification of proteocephalid cestodes. Ephedrocephalus is typified by the medullary position of the ovary and uterus, the cortical distribution of vitelline follicles (dispersed throughout almost the entire ventral cortex) and the testes in one dorsal field. Zygobothrium is primarily characterized by its possession of a robust scolex bearing four uniloculate suckers with two openings each and by the tetralobed velum (laciniations) on every proglottid (two on the ventral and two on the dorsal side). The redtail catfish is the definitive host of as many as seven species of proteocephalid cestodes, which, however, do not represent a monophyletic group. Some species, including Z. megacephalum, are among the earliest diverged parasites of Neotropical catfishes, being closely related to African and North American proteocephalids from catfishes, whereas others such as E. microcephalus belong to more recently diverged taxa with uncertain interrelations. Unlike most proteocephalids of the redtail catfish, which almost always infect the anterior parts of the host intestine, E. microcephalus and Z. megacephalum occur exclusively in its posterior third. A key to the identification of the proteocephalid species parasitizing P. hemioliopterus is also presented.
References
- Alves, P.V., de Chambrier, A., Luque, J.L. & Scholz, T. (2017a) Reappraisal of Goezeella Fuhrmann, 1916 (Cestoda: Proteocephalidae), parasites of Neotropical catfishes (Siluriformes), with description of a new species from Pimelodella cristata (Heptapteridae). Revue suisse de Zoologie, 124, 335–350. - https://doi.org/10.5281/zenodo.893547 - Alves, P.V., de Chambrier, A., Luque, J.L. & Scholz, T. (2017b) Untangling convoluted taxonomy of Chambriella Rego, Chubb & Pavanelli, 1999 (Cestoda: Proteocephalidae), with erection of Riggenbachiella n. g. and description of a new species from pimelodid catfishes in the Neotropical Region. Systematic Parasitology, 94, 367–389. - https://doi.org/10.1007/s11230-017-9700-1 - Alves, P.V., de Chambrier, A., Scholz, T. & Luque, J.L. (2015) A new genus and species of proteocephalidean tapeworm (Cestoda), first parasite found in the driftwood catfish Tocantinsia piresi (Siluriformes: Auchenipteridae) from Brazil. Folia Parasitologica, 62, 6. - https://doi.org/10.14411/fp.2015.006 - Alves, P.V., de Chambrier, A., Scholz, T. & Luque, J.L. (2017c) Annotated checklist of fish cestodes from South America. ZooKeys, 650, 1–205. - https://doi.org/10.3897/zookeys.650.10982 - Arredondo, N.J., Alves, P.V. & Gil de Pertierra, A.A. (2017) A new genus of proteocephalid tapeworm (Cestoda) from the marbled swamp eel Synbranchus marmoratus Bloch (Synbranchiformes: Synbranchidae) in the River Paraná basin, Argentina. Folia Parasitologica, 64, 015. - https://doi.org/10.14411/fp.2017.015 - Brabec, J., Scholz, T., Králová-Hromadová, I., Bazsalovicsová, E. & Olson, P.D. (2012) Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of non-segmented tapeworms (Platyhelminthes). International Journal for Parasitology, 42, 259–267. 
 https://doi.org/10.1016/j.ijpara.2012.01.005- Caira, J.N. & Jensen, K. (2017) Planetary Biodiversity Inventory (2008–2017): tapeworms from vertebrate bowels of the Earth. Special Publication No. 25. University of Kansas, Natural History Museum, Lawrence, 463 pp. - Cañeda-Guzmán, I.C., de Chambrier, A. & Scholz, T. (2001) Thaumasioscolex didelphidis n. gen. and n. sp. (Eucestoda: Proteocephalidae) from the black-eared opossum Didelphis marsupialis from Mexico, the first proteocephalidean tapeworm from a mammal. Journal of Parasitology, 87, 639–647. - https://doi.org/10.1645/0022-3395(2001)087[0639:TDNGNS]2.0.CO;2 - Coquille, S.C. & de Chambrier, A. (2008) Cairaella henrii gen. n., sp. n., a parasite of Norops trachyderma (Polychrotidae) and Ophiotaenia nicolae sp. n. (Eucestoda: Proteocephalidea), a parasite of Thecadactylus rapicauda (Gekkonidae), in Ecuador. Folia Parasitologica, 55, 197–206. 
 https://doi.org/10.14411/fp.2008.027- de Chambrier, A. (2001) A new tapeworm from the Amazon, Amazotaenia yvettae gen. n., sp. n., (Eucestoda: Proteocephalidea) from the siluriform fishes Brachyplatystoma filamentosum and B. vaillanti (Pimelodidae). Revue suisse de Zoologie, 108, 303–316. - https://doi.org/10.5962/bhl.part.79632 - de Chambrier, A., Binh, T.T. & Scholz, T. (2012) 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. Systematic Parasitology, 81, 39–50. 
 https://doi.org/10.1007/s11230-011-9320-0- de Chambrier, A., Coquille, S.C., Mariaux, J. & Tkach, V. (2009a) 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. Systematic Parasitology, 73, 49–64. - https://doi.org/10.1007/s11230-009-9178-6 - de Chambrier, A. & Gil de Pertierra, A.A. (2002) Redescription of Travassiella avitellina Rego & Pavanelli, 1987 (Proteocephalidea: Monticelliidae, Zygobothriinae), a parasite of Paulicea luetkeni (Siluriformes) from South America. Memórias do Instituto Oswaldo Cruz, 97, 657–661. - https://doi.org/10.1590/S0074-02762002000500013 - de Chambrier, A., Kuchta, R. & Scholz, T. (2015b) Tapeworms (Cestoda: Proteocephalidea) of teleost fishes from the Amazon River in Peru: additional records as an evidence of unexplored species diversity. Revue suisse de Zoologie, 122, 149–163. https://doi.org/10.5281/zenodo.14580 - de Chambrier, A., Rego, A.A. & Mariaux, J. (2004b) Redescription of Brooksiella praeputialis and Goezeella siluri (Eucestoda: Proteocephalidea), parasites of Cetopsis coecutiens (Siluriformes) from the Amazon and proposition of Goezeella danbrooksi sp. n. Revue suisse de Zoologie, 111, 111–120. - https://doi.org/10.5962/bhl.part.80230 - de Chambrier, A., Rego, A.A. & Vaucher, C. (1999) Euzetiella tetraphylliformis n. gen., n. sp., (Eucestoda: Proteocephalidae), parasite du poisson d’eau douce Néotropical Paulicea luetkeni (Siluriforme, Pimelodidae). Parasite, 6, 43–47. - https://doi.org/10.1051/parasite/1999061043 - de Chambrier, A., Scholz, T., Beletew, M. & Mariaux, J. (2009b) A new genus and species of proteocephalidean (Cestoda) from Clarias catfishes (Siluriformes: Clariidae) in Africa. Journal of Parasitology, 95, 160–168. - https://doi.org/10.1645/GE-1594.1 - de Chambrier, A., Scholz, T., Kuchta, R., Posel, P., Mortenthaler, M. & Guardia, C.C. (2006) Tapeworms (Cestoda: Proteocephalidea) of fishes from the Amazon River in Peru. Comparative Parasitology, 73, 111–120. - https://doi.org/10.1654/4182.1 - de Chambrier, A., Scholz, T., Mariaux, J. & Kuchta, R. (2017) Onchoproteocephalidea I Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. In: Caira, J.N. & Jensen, K. (Eds.), Planetary Biodiversity Inventory (2008–2016): Tapeworms from vertebrate bowels of the Earth. Special Publication No. 25. University of Kansas, Natural History Museum, Lawrence, pp. 251–277. - de Chambrier, A. & Vaucher, C. (1997) Révision des cestodes (Monticelliidae) décrits par Woodland (1934) chez Brachyplatystoma filamentosum avec redéfinition des genres Endorchis Woodland, 1934 et Nomimoscolex Woodland, 1934. Systematic Parasitology, 37, 219–233. - https://doi.org/10.1023/A:1005863808627 - de Chambrier, A., Waeschenbach, A., Fisseha, M., Scholz, T. & Mariaux, J. (2015a) A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda). ZooKeys, 500, 25–59. - https://doi.org/10.3897/zookeys.500.9360 - de Chambrier, A., Zehnder, M., Vaucher, C. & Mariaux, J. (2004a) The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Systematic Parasitology, 57, 159–171. 
 https://doi.org/10.1023/B:SYPA.0000019083.26876.34- de Chambrier, S. & de Chambrier, A. (2010) Two new genera and two new species of proteocephalidean tapeworms (Eucestoda) from reptiles and amphibians in Australia. Folia Parasitologica, 57, 263–279. - https://doi.org/10.14411/fp.2010.033 - Chervy, L. (2009) Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitologica, 56, 199–230. 
 https://doi.org/10.14411/fp.2009.025- Conn, D.B. & Swiderski, Z. (2008) A standardised terminology of the embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes: Cestoda). Folia Parasitologica, 55, 42–52. 
 https://doi.org/10.14411/fp.2008.006- Diesing, K.M. (1850) Systema Helminthum. Vol. I. Braumüller, Vienna, 679 pp. - Diesing, K.M. (1855) Sechzehn Gattungen von Binnenwürmern und ihre Arten. Denkschriften der Kaiserlichen Akademie der Wissenschaften, Mathematisch Naturwissenschaftliche Classe, 9, 171–185. - Freze, V.I. (1965) [Proteocephalata in fish, amphibians and reptiles]. Essentials of Cestodology. Vol. V. Nauka, Moscow, 538 pp. [in Russian: English translation, Israel Program of Scientific Translation, 1969, Cat. No. 1853. v + 597 pp.)] - Froese, R. & Pauly, D. (Eds.) (2017) FishBase. World Wide Web electronic publication. Version 06/2017. Available from: http://www.fishbase.org (accessed 1 September 2017) - Fuhrmann, O. (1934) Vier Diesing’sche Typen (Cestoda). Revue suisse de Zoologie, 41, 545–564. - Gil de Pertierra, A.A. (2009) Luciaella ivanovae n. g., n. sp. (Eucestoda: Proteocephalidea: Peltidocotylinae), a parasite of Ageneiosus inermis (L.) (Siluriformes: Auchenipteridae) in Argentina. Systematic Parasitology, 73, 71–80. 
 https://doi.org/10.1007/s11230-009-9174-x- Gil de Pertierra, A.A. & de Chambrier, A. (2000) Rudolphiella szidati sp. n. (Proteocephalidea: Monticelliidae, Rudolphiellinae) parasite of Luciopimelodus pati (Valenciennes, 1840) (Pisces: Pimelodidae) from Argentina with new observations on Rudolphiella lobosa (Riggenbach, 1895). Revue suisse de Zoologie, 107, 81–95. - https://doi.org/10.5962/bhl.part.80119 - Gil de Pertierra, A.A. & Viozzi, G.P. (1999) Redescription of Cangatiella macdonaghi (Szidat y Nani, 1951) comb. nov. (Cestoda: Proteocephalidae) a parasite of the atheriniform fish Odontesthes hatcheri (Eigenmann, 1909) from the Patagonian region of Argentina. Neotrópica, 45, 13–20. - Hypša, V., Škeříková, A. & Scholz, T. (2005) Phylogeny, evolution and host–parasite relationships of the order Proteocephalidea (Eucestoda) as revealed by combined analysis and secondary structure characters. Parasitology, 130, 359–371. https://doi.org/10.1017/S0031182004006638 - Lundberg, J.G. & Aguilera, O. (2003) The late Miocene Phractocephalus catfish (Siluriformes: Pimelodidae) from Urumaco, Venezuela: additional specimens and reinterpretation as a distinct species. Neotropical Ichthyology, 1, 97–109. - https://doi.org/10.1590/S1679-62252003000200004 - Lundberg, J.G., Sullivan, J.P. & Hardman, M. (2011) Phylogenetics of the South American catfish family Pimelodidae (Teleostei: Siluriformes) using nuclear and mitochondrial gene sequences. Proceedings of the Academy of Natural Sciences of Philadelphia, 161, 153–189. 
 https://doi.org/10.1635/053.161.0110- Mola, P. (1906) Di alcune specie poco studiate o mal note di Cestodi. Annuario del Museo Zoologico della R. Università di Napoli, 2, 1–12. - Mola, P. (1929) Descriptio platodorum sine exstis. Zoologischer Anzeiger, 86, 101–113. - Olson, P.D., Littlewood, D.T.J., Bray, R.A. & Mariaux, J. (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution, 19, 443–467. - https://doi.org/10.1006/mpev.2001.0930 - Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. & Thollesson, M. (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371. - https://doi.org/10.1016/j.ympev.2008.03.024 - Rego, A.A. (1984) Proteocefalídeos (Cestoda) de Phractocephalus hemioliopterus, peixe da Amazônia. Memórias do Instituto Oswaldo Cruz, 79, 257–261. - https://doi.org/10.1590/S0074-02761984000200013 - Rego, A.A. (1994) Order Proteocephalidea Mola, 1928. In: Khalil, L.F., Jones, A. & Bray, R.A. (Eds.), Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, pp. 257–293. - Rego, A.A., Chubb, J.C. & Pavanelli, G.C. (1999) Cestodes in South American freshwater teleost fishes: keys to genera and brief description of species. Revista Brasileira de Zoologia 16, 299–367. - https://doi.org/10.1590/S0101-81751999000200003 - Ruedi, V. & de Chambrier, A. (2012) Pseudocrepidobothrium ludovici sp. n. (Eucestoda: Proteocephalidea), a parasite of Phractocephalus hemioliopterus (Pisces: Pimelodidae) from Brazilian Amazon. Revue suisse de Zoologie, 119, 137–147. - https://doi.org/10.5962/bhl.part.150326 - Schmidt, G.D. (1986) CRC Handbook of tapeworm identification. CRC Press, Boca Raton, 675 pp. - Scholz, T., de Chambrier, A., Kuchta, R., Littlewood, D.T.J. & Waeschenbach, A. (2013) Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): example of convergent evolution. Zootaxa, 3640 (3), 485–499. - https://doi.org/10.11646/zootaxa.3640.3.12 - Woodland, W.N.F. (1933) On the anatomy of some fish cestodes described by Diesing from the Amazon. Quarterly Journal of Microscopical Science, 76, 175–208. - Zehnder, M.P. & Mariaux, J. (1999) Molecular systematic analysis of the order Proteocephalidea (Eucestoda) based on mitochondrial and nuclear rDNA sequences. International Journal for Parasitology, 29, 1841–1852. 
 https://doi.org/10.1016/S0020-7519(99)00122-8
 
		