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Dactylogyrids (Platyhelminthes, Monogenoidea) from the gills of Hoplias malabaricus (Characiformes: Erythrinidae) from coastal rivers of the Oriental Amazon Basin: species of Urocleidoides and Constrictoanchoratus n. gen.

Published online by Cambridge University Press:  15 May 2017

K.D.C. Ferreira
Affiliation:
Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros – Alameda Leandro Ribeiro s/n. Bairro Aldeia, 68.600–000 Bragança, PA, Brazil Programa de Pós-Graduação em Biologia Ambiental, Universidade Federal do Pará, Bragança, PA, Brazil
A.R.O. Rodrigues
Affiliation:
Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros – Alameda Leandro Ribeiro s/n. Bairro Aldeia, 68.600–000 Bragança, PA, Brazil
J.-M. Cunha
Affiliation:
Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros – Alameda Leandro Ribeiro s/n. Bairro Aldeia, 68.600–000 Bragança, PA, Brazil Programa de Pós-Graduação em Biodiversidade e Conservação, Universidade Federal do Pará, Bragança, PA, Brazil
M.V. Domingues*
Affiliation:
Universidade Federal do Pará, Campus Universitário de Bragança, Instituto de Estudos Costeiros – Alameda Leandro Ribeiro s/n. Bairro Aldeia, 68.600–000 Bragança, PA, Brazil Programa de Pós-Graduação em Biologia Ambiental, Universidade Federal do Pará, Bragança, PA, Brazil Programa de Pós-Graduação em Biodiversidade e Conservação, Universidade Federal do Pará, Bragança, PA, Brazil

Abstract

Five species of Urocleidoides (one new) and two new species of Constrictoanchoratus n. gen. are described in this study. All were collected from the gills of Hoplias malabaricus (Characiformes: Erythrinidae) captured in six localities of coastal rivers of the north-eastern sector the State of Pará (Oriental Amazon): Urocleidoides brasiliensis Rosim, Mendoza-Franco & Luque, 2011; Urocleidoides bulbophallus n. sp.; Urocleidoides cuiabai Rosim, Mendoza-Franco & Luque, 2011; Urocleidoides eremitus Kritsky, Thatcher & Boeger, 1986; Urocleidoides malabaricusi Rosim, Mendoza-Franco & Luque, 2011; Constrictoanchoratus lemmyi n. gen. n. sp.; and Constrictoanchoratus ptilonophallus n. gen. n. sp. This is the first reported occurrence of the four previously described species of Urocleidoides parasitizing H. malabaricus from streams in the Oriental Amazon Basin. The analysis of voucher specimens of U. eremitus parasitizing the gills of H. malabaricus from the Upper Paraná River floodplain in the limits of States of Paraná and Mato Grosso do Sul, Brazil, indicates that these specimens are members of a new species of Urocleidoides, described here as Urocleidoides paranae n. sp. Constrictoanchoratus n. gen. is proposed for the species with a male copulatory organ sclerotized, coiled, clockwise; ventral anchor with elongate superficial root, inconspicuous deep root; dorsal anchor with inconspicuous roots, and a constriction at the intersection between the shaft and the point. The host–parasite diversity scenario and host specificity of the species of Constrictoanchoratus n. gen. and Urocleidoides from the gills of H. malabaricus are also discussed in this study.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2017 

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References

Braga, M.P., Araújo, S.B.L. & Boeger, W.A. (2014) Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitology Research 113, 481490.CrossRefGoogle ScholarPubMed
Bertollo, L.A.C., Born, G.G., Dergam, J.A., Fenocchio, A.S. & Moreira-Filho, O. (2000) A biodiversity approach in the Neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations. Chromosome Research 8, 603613.Google Scholar
Boeger, W.A. & Kristky, D.C. (1989) Phylogeny, coevolution, and revision of the Hexabothriidae Price, 1942 (Monogenea). International Journal for Parasitology 19, 425440.Google Scholar
Boeger, W.A. & Kristky, D.C. (1997) Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology 27, 14951511.Google Scholar
Boeger, W.A. & Kristky, D.C. (2003) Parasites, fossils and geologic history: historical biogeography of the South American freshwater croakers, Plagioscion spp. (Teleostei, Sciaenidae). Zoologica Scripta 32, 311.CrossRefGoogle Scholar
Boeger, W.A. & Popazoglo, F. (1995) Neotropical Monogenoidea. 23. Two new species of Gyrodactylus (Gyrodactylidae) from a cichlid and an erythrinid fish from southeastern Brazil. Memórias do Instituto Oswaldo Cruz 90, 689694.Google Scholar
Boeger, W.A. & Vianna, R.T. (2006) Monogenoidea. pp. 42116 in Thatcher, V.E. (Ed.) Amazon fish parasites. 2nd edn. Sofia, Moscow, Pensoft Publishers.Google Scholar
Brooks, D.R. & Glen, D.R. (1982) Pinworms and primates: a case study in coevolution. Proceedings of the Helminthological Society of Washington 49, 7685.Google Scholar
Brooks, D.R. & McLennan, D. (1991) Phylogeny, ecology, and behavior: A research program in comparative biology. 434 pp. Chicago, University of Chicago Press.Google Scholar
Brooks, D.R. & McLennan, D. (1993) Parascript: Parasites and the language of evolution. 429 pp. Washington DC, Smithsonian Institution Press.Google Scholar
Brooks, D.R., Bandoni, S.M., MacDonald, C.M. & O'Grady, R.T. (1989) Aspects of the phylogeny of the Trematoda Rudolphy, 1808 (Platyhelminthes: Cercomeria). Canadian Journal of Zoology 67, 26092624.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, K.D. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Bychowsky, B.E. (1957) Monogenetic trematodes, their systematics and phylogeny. 509 pp. Moscow, Russia. (translated from Russian by AIBS, Washington, DC).Google Scholar
Cohen, S.C., Justo, C.N.M. & Kohn, A. (2013) South American Monogenoidea parasites of fishes, amphibians and reptiles. 663 pp. Rio de Janeiro, Oficina de livros.Google Scholar
Domingues, M.V. & Boeger, W.A. (2005) Neotropical Monogenoidea. 47. Phylogeny and coevolution of species of Rhinoxenus (Plathyhelminthes, Monogenoidea, Dactylogyridae) and their characiformes hosts (Teloestei, Ostariophysi) with description of four new species. Zoosystema 27, 441467.Google Scholar
Domingues, M.V. & Marques, F.P.L. (2011) Phylogeny and taxonomy of Potamotrygonocotyle Mayes, Brooks and Thorson, 1981 (Monogenoidea: Monocotylidae) with a description of four new species. Journal of Helminthology 85, 353380.Google Scholar
Fehlauer-Ale, K.H. & Littlewood, D.T.J. (2011) Molecular phylogeny of Potamotrygonocotyle (Monogenea, Monocotylidae) challenges the validity of some of its species. Zoologica Scripta 40, 638658.Google Scholar
Gasques, L.S., Graça, R.J., Prioli, S.M.A.P., Takemoto, R.M. & Prioli, A.J. (2015) Molecular characterization of Urocleidoides cuiabai and U. malabaricusi (Monogenea: Dactylogyridae) from the trahira fish Hoplias aff. malabaricus in the Paraná River, Brazil. Journal of Helminthology 90, 693697.Google Scholar
Graça, R.J., Ueda, B.H., Oda, F.H. & Takemoto, R.M. (2013) Monogenea (Platyhelminthes) parasites from the gills of Hoplias aff. malabaricus (Bloch, 1794) (Pisces: Erythrinidae) in the Upper Paraná River Floodplain, States of Paraná and Mato Grosso do Sul, Brazil. Check List 9, 14841487.Google Scholar
Guidelli, G., Tavechio, W.L.G., Takemoto, R.M. & Pavanelli, G.C. (2006) Fauna parasitária de Leporinus lacustris e Leporinus friderici (Characiformes, Anostomidae) da planície de inundação do alto rio Paraná, Brazil. Acta Scientiarium, Biological Sciences 28, 281290.Google Scholar
Hoberg, E.P. (1992) Congruent and synchronic patterns in biogeography and speciation among seabirds, pinnipeds, and cestodes. Journal of Parasitology 78, 601615.Google Scholar
Humason, G.L. (1979) Animal tissue techniques. 503 pp. San Francisco, WH Freeman.Google Scholar
Iannacone, J. & Luque, J.L. (1993) New records on helminths parasitic on Peruvian Amazonian. fishes (Osteichthyes). Revista de Biologia Tropical 41, 303305.Google Scholar
Jogunoori, W., Kritsky, D.C. & Venkatanarasaiah, J. (2004) Neotropical Monogenoidea. 46. Three new species from the gills of introduced aquarium fishes in India, the proposal of Heterotylus n. g. and Diaphorocleidus n. g., and the reassignment of some previously described species of Urocleidoides Mizelle & Price, 1964 (Polyonchoinea: Dactylogyridae). Systematic Parasitology 58, 115124.Google Scholar
Klassen, G.J. (1992) Coevolution: a history of the macroevolutiorary approach to studyng host–parasite associations. Journal of Parasitology 78, 573587.Google Scholar
Kritsky, D.C. & Thatcher, V. (1974) Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater fishes of Colombia, South America. Journal of Helminthology 48, 5966.Google Scholar
Kritsky, D.C., Thatcher, V.E. & Boeger, W.A. (1986) Neotropical Monogenea. 8. Revision of Urocleidoides (Dactylogyridae, Ancyrocephalinae). Proceedings of the Helminthological Society of Washington 53, 137.Google Scholar
Lambert, A. & El Gharbi, S. (1995) Monogenean host specificity as a biological and taxonomic indicator for fish. Biological Conservation 72, 227235.CrossRefGoogle Scholar
León-Règagnon, V., Guillén-Hernández, S. & Arizmendi-Espinosa, M.A. (2005) Intraspecific variation of Haematoloechus floedae Harwood, 1932 (Digenea: Plagiorchiidae), from Rana spp. in North and Central America. Journal of Parasitology 91, 915921.Google Scholar
Mackenzie, K. (1987) Parasites as indicators of host populations. International Journal for Parasitology 17, 345352.Google Scholar
Mackenzie, K. (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitology 124, 153163.Google Scholar
Marques, D.F., Santos, F.A., Silva, S.S., Sampaio, I. & Rodrigues, L.R.R. (2013) Cytogenetic and DNA barcoding reveals high divergence within the trahira Hoplias malabaricus (Chariciformes: Erythrinidae) from the lower Amazon River. Neotropical Ichthyology 11, 459466.CrossRefGoogle Scholar
Mendoza-Franco, E.F. & Reina, R.G. (2008) Five new species of Urocleidoides (Monogenoidea) (Mizelle and Price 1964) Kritsky, Thatcher and Boeger, 1986, parasitizing the gills of Panamanian freshwater fishes. Journal of Parasitology 94, 793802.CrossRefGoogle ScholarPubMed
Mendoza-Franco, E.F., Scholz, T., Vivas-Rodrigues, C. & Vargas-Vazquez, J. (1999) Monogeneans of freshwater fishes from cenotes (sinkholes) of the Yucatan Peninsula, Mexico. Folia Parasitologica 46, 267273.Google Scholar
Mendoza-Franco, E.F., Aguirre-Macedo, M.L. & Vidal-Martínez, V.M. (2007) New and previously described species of Dactylogyridae (Monogenoidea) from the gills of Panamanian freshwater fishes (Teleostei). Journal of Parasitology 93, 761771.Google Scholar
Mendoza-Franco, E.F., Caspeta-Mandujano, J.M., Salgado-Maldonado, G. & Matamoros, W.A. (2015) Two new species of Urocleidoides Mizelle et Price, 1964 (Monogenoidea) from the gill lamellae of profundulids and poeciliids from Central America and southern Mexico. Folia Parasitologica 62, 059. doi:10.14411/fp.2015.059.Google Scholar
Mendoza-Palmero, C.A. & Aguilar-Aguilar, R. (2008) Record of Urocleidoides vaginoclaustrum Jogunoori, Kritsky and Venkatanarasaiah, 2004 (Monogenea: Dactylogyridae) from a freshwater fish in Mexico. Parasitology Research 103, 12351236.Google Scholar
Mizelle, J.D. (1936) New species of trematodes from the gills of Illinois fishes. American Midland Naturalist 17, 785806.Google Scholar
Mizelle, J.D. & Klucka, A.R. (1953) Studies on monogenetic trematodes. XVI. Dactylogyridae from Wisconsin fishes. American Midland Naturalist 49, 720733.Google Scholar
Mizelle, J.D. & Price, C.E. (1964) Studies on monogenetic trematodes. XXVII. Dactylogyrid species with the proposal of Urocleidoides gen. n. Journal of Parasitology 50, 579584.Google Scholar
Molnar, K., Hanek, G. & Fernando, C.H. (1974) Ancyrocephalids (Monogenea) from freshwater fishes of Trinidad. Journal of Parasitology 60, 914920.Google Scholar
Moreira, J., Scholz, T. & Luque, J.L. (2015) First data on the parasites of Hoplias aimara (Characiformes): description of the two new species of gill monogeneans (Dactylogyridae). Acta Parasitologica 60, 254260.Google Scholar
Nadler, S.A. & Pérez-Ponce de Léon, G. (2011) Integrating molecular and morphological approaches for characterizing parasites cryptic species: implications for parasitology. Parasitology 138, 16881709.Google Scholar
Oyakawa, O.T. (2003) Family Erythrinidae, pp. 238240 in Reis, R.E., Kullander, S.O. & Ferraris, C.J. Jr (Eds) Check list of the freshwater fishes of South America. 742 pp. Porto Alegre, Edipucrs.Google Scholar
Oyakawa, O.T. & Mattox, G.M.T. (2009) Revision of the Neotropical trahiras of the Hoplias lacerdae species-group (Ostariophysi: Characiformes: Erythrinidae) with descriptions of two new species. Neotropical Ichthyology 7, 117140.Google Scholar
Rasband, W.S. (1997– 2016) ImageJ. US National Institutes of Health, Bethesda, Maryland, USA. Available at http://imagej.nih.gov/ij/.Google Scholar
Rosim, D.F., Mendoza-Franco, E.F. & Luque, J.L. (2011) New and previously described species of Urocleidoides (Monogenoidea: Dactylogyridae) infecting the gills and nasal cavities of Hoplias malabaricus (Characiformes: Erythinidae) from Brazil. Journal of Parasitology 97, 406417.Google Scholar
Santos, U., Volcker, C.M., Belei, F.A., Cioffi, M.B., Bertollo, L.A.C., Paiva, S.R. & Dergam, J.A. (2009) Molecular and karyotypic phylogeography in the Neotropical Hoplias malabaricus (Erythrinidae) fish in eastern Brazil. Journal of Fish Biology 75, 23262343.Google Scholar
Santos-Neto, J.F., Rodrigues, A.R.O. & Domingues, M.V. (2015) Proposal of Whittingtonocotyle n. gen. (Dactylogyroidea: Dactylogyridae), with the description of two new species from the gills of Hoplerythrinus unitaeniatus (Characiformes: Erythrinidae) in Brazil. Zootaxa 3937, 191200.CrossRefGoogle Scholar
Suriano, D.M. (1997) The genus Urocleidoides Mizelle & Price, 1964 (Monogenea: Ancyrocephalidae) parasitizing characoidei fishes in Argentina. Physis – Seccion B – las aguas continentales y sus organismos 53, 16.Google Scholar
Takemoto, R.M., Pavanelli, G.C., Lizama, M.A.P., Lacerda, A.C.F., Yamada, F.H., Moreira, L.H.A., Ceschini, T.L. & Bella, Y.S. (2009) Diversity of parasites of fish from the Upper Paraná River floodplain, Brazil. Brazilian Journal of Biology 69, 691705.Google Scholar
Tirard, C., Berrebi, P., Raibaut, A. & Frenaud, F. (1992) Parasites as biological markers: evolutionary relationships in the heterospecific combination of helminths (monogeneans) and teleosts (Gadidae). Biological Journal of the Linnean Society 47, 173182.Google Scholar