Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-05-08T18:39:57.572Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeny and taxonomy of Potamotrygonocotyle Mayes, Brooks & Thorson, 1981 (Monogenoidea: Monocotylidae) with a description of four new species

Published online by Cambridge University Press:  19 November 2010

M.V. Domingues  and
F.P.L Marques
M.V. Domingues*
Affiliation:
Laboratório de Helmintologia Evolutiva, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, trav. 14, n° 101 Cidade Universitária, 05508-090, São Paulo, SP, Brazil
F.P.L Marques
Affiliation:
Laboratório de Helmintologia Evolutiva, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, trav. 14, n° 101 Cidade Universitária, 05508-090, São Paulo, SP, Brazil
*
*E-mail: mvdomingues71@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The marine-derived stingrays of Potamotrygonidae, endemic to South American river systems, host an interesting parasite fauna equally related to marine lineages. Among those lineages, the diversity and phylogenetic relationships within Potamotrygonocotyle – a monocotylid monogenoidean specific to potamotrygonids – are poorly known, since 9 of 10 species attributed to this genus have been described in the past 3 years. Here, we readdress the diversity of Potamotrygonocotyle after examining the gills of 436 potamotrygonid individuals representing 12 described and 14 potentially undescribed species of freshwater stingrays from 19 major river systems of South America (i.e. sub-basins). We recognized 12 valid species within the parasite genus, of which four are described in this study. Our taxonomic decisions were based on the phylogenetic analysis of 14 ingroup terminal taxa and 12 morphological characters, which resulted in the following hypothesis of sister-group relationships: ((P. dromedarius, P. tatianae sp. nov.), (P. rionegrense, P. auriculocotyle sp. nov., ((P. quadracotyle, P. umbella), (P. septemcotyle sp. nov., (P. chisholmae, P. uruguayense)), (P. tsalickisi, P. eurypotamoxenus, P. rarum, (P. tocantinsense sp. nov., P. aramasae))))). According to our hypothesis, the absence of autapomorphic features for some nominal species, and the re-evaluation of morphological variation among populations, led us to consider P. eurypotamoxenus and P. uruguayense as junior synonymys of P. tsalicksi and P. chisholmae, respectively. Finally, we address the importance of biogeographic and host representation, in order to fully understand the patterns of morphological variation and host specificity within this group. We found that hypotheses of species delimitation depend greatly on efforts to sample specimens throughout its distributional range and that host specificity within this genus varies dramatically among lineages.

Type
Research Papers
Information
Journal of Helminthology , Volume 85 , Issue 4 , December 2011 , pp. 353 - 380
Copyright
Copyright © Cambridge University Press 2010. This is a work of the U.S. Government and is not subject to copyright protection in the United States.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albert, J.S., Lovejoy, N.R. & Crampton, W.G.R. (2006) Miocene tectonism and the separation of cis- and trans-Andean river basins: Evidence from Neotropical fishes. Journal of South American Earth Sciences 21, 14–11.CrossRefGoogle Scholar
Boeger, W.A. & Kritsky, D.C. (2003) Parasites, fossils, geologic history: historical biogeography of the South America freshwater croakers, Plagioscion spp. (Teleostei: Sciaenidae). Zoologica Scripta 32, 3–11.CrossRefGoogle Scholar
Brooks, D.R. (1992) Origins, diversification, and historical structure of the helminth fauna inhabiting Neotropical freshwater stingrays (Potamotrygonidae). Journal of Parasitology 78, 588–595.CrossRefGoogle ScholarPubMed
Brooks, D.R. (1995) Neotropical freshwater stingrays and their parasites: a tale of an ocean and a river long ago. Journal of Aquaculture and Aquatic Sciences 7, 52–61.Google Scholar
Brooks, D.R. & Amato, J.F.R. (1992) Cestodes parasites in Potamotrygon motoro (Matterer) (Chondrichthyes: Potamotrygonidae) from southwestern Brazil, including, Rhinebothroides mclennanae n. sp. (Tetraphyllidea: Phyllobothriidae), and a revised host-parasite checklist for helminths inhabiting Neotropical stringrays. Journal of Parasitology 78, 393–398.CrossRefGoogle Scholar
Brooks, D.R. & McLennan, D. (1993) Parascript: parasites and the language of evolution. 429 pp. Washington and London, Smithsonian Institution Press.Google Scholar
Brooks, D.R., Thorson, T.B. & Mayes, M.A. (1981) Fresh-water stingrays (Potamotrygonidae) and their helmith parasites: testing hypothesis of evolution and coevolution. pp. 147–175in Funk, V.A. & Brooks, D.R. (Eds) Cladists: Proceedings of the First Meeting of the Willi Hennig Society. New York, USA, New York Botanical Garden.Google Scholar
Brooks, D.R., van Veller, M.G.P. & McLennan, D. (2001) How to do BPA, really. Journal of Biogeography 28, 345–358.CrossRefGoogle Scholar
Bueno, V.M. (2010) Delimitação de espécies em Rhinebothroides Mayes, Brooks & Thorson, 1981 (Cestoda: Tetraphyllidea) com ênfase no complexo Rhinebothroides freitasi (Rego, 1979). Unpublished MSc Thesis, Universidade de São Paulo, São Paulo.Google Scholar
Bychowsky, B.E. (1957) Monogenetic trematodes. Their systematics and phylogeny. 509 pp. Moscow, The Academy of Sciences of the USSR. Translated from Russian by P.C. Oustinoff in Hargis W.J. Jr (Ed.) Monogenetic trematodes. Their systematics and phylogeny. Washington DC, AIBS.Google Scholar
Caira, J.N. (1990) Metazoan parasites as indicator of elasmobranch biology. pp. 71–96in Pratt, H.L., Gruber, S.H. & Taniuchi, T. (Eds) Elasmobranchs as living resources: Advances in the biology, ecology, systematics, and behavior, and the status of fisheries. NOAA Technical Report 90. Seattle, USA, US Department of Commerce.Google Scholar
Caira, J.N. (1994) Parascript: Paragon or parody. Review of Parascript: Parasites and the language of evolution, by D.R. Brooks and D.A. Mclennan. Bioscience 44, 771–773.CrossRefGoogle Scholar
Caira, J.N., Jensen, K. & Healy, C. (2001) Interrelationships among tetraphyllidean and lecanicephalidean cestodes. pp. 135–158in Littlewood, D.T.J. & Bray, R.A. (Eds) Interrelationships of platyhelminthes. The Systematics Association Special Volume Series 60. London, Taylor & Francis.Google Scholar
Carreno, R.A. & Hoberg, E.P. (1999) Evolutionary relationships among the Protostrongylidae (Nematoda: Metastrongyloidea) as inferred from morphological characters, with consideration of parasite-host coevolution. Journal of Parasitology 85, 638–648.CrossRefGoogle ScholarPubMed
Carvalho, M.R. de, Lovejoy, N.R. & Rosa, R.S. (2003) Family Potamotrygonidae. pp. 22–29in Reis, R.E., Kullander, S.O. & Ferraris, C.J. (Eds) Checklist of the freshwater fishes of South and Central America (CLOFFSCA). Porto Alegre, Edipucrs.Google Scholar
Carvalho, M.R. de, Maisey, J.G. & Grande, L. (2004) Freshwater stingrays of the Green River Formation of Wyoming (Early Eocene), with the description of a new genus and species and an analysis of its phylogenetic relationships (Chondrichthyes: Myliobatiformes). Bulletin of the American Museum of Natural History, Nova York 284, 1–136.2.0.CO;2>CrossRefGoogle Scholar
Charvet-Almeida, P. (2001) Ocorrência, Biologia e Uso das Raias de Água Doce na Baía de Marajó (Pará, Brasil), com Ênfase na Biologia de Plesiotrygon iwamae (Chondrichthyes: Potamotrygonidae) Dissertação de Mestrado, Belém, Universidade Federal do Pará e Museu Paraense Emílio Goeldi.Google Scholar
Chisholm, L.A. & Whittington, I.R. (2000) Heliocotyle ewingi sp. nov. (Monogenea: Monocotylidae) from the gills of Myliobatis australis (Myliobatididae) from Tasmania, Australia. Folia Parasitologica 47, 100–104.CrossRefGoogle Scholar
Chisholm, L.A. & Whittington, I.R. (2004) Two new species of Myliocotyle (Monogenea: Monocotylidae) from the gills of Aetomylaeus maculates and A. nichofii (Elasmobranchii: Myliobatidae) from Sarawak, Borneo, Malaysia. Folia Parasitologica 51, 304–310.CrossRefGoogle Scholar
Chisholm, L.A., Wheeler, T.A. & Beverley-Burton, M. (1995) A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Systematic Parasitology 32, 159–191.CrossRefGoogle Scholar
Deets, G.B. (1987) Phylogenetic analysis and revision of Kroyerina Wilson, 1932 (Sophonostomatoida: Kroyeriidae), copepods parasitic on chondrichthyans, with descriptions of four new species and the erection of a new genus, Prokroyeria. Canadian Journal of Zoology 65, 2121–2148.CrossRefGoogle Scholar
Deynat, P. (2006) Potamotrygon marinae n. sp., a new species of freshwater stingrays from French Guiana (Myliobatiformes, Potamotrygonidae). Comptes Rendus Biologies 329, 483–490.CrossRefGoogle Scholar
Dolezel, D., Koudela, B., Jirku, M., Hypsa, V., Obornik, M., Votypka, J., Modry, D., Slapeta, J.R. & Lukes, J. (1999) Phylogenetic analysis of Sarcocystis spp. of mammals and reptiles supports the coevolution of Sarcocystis spp. with their final hosts. International Journal for Parasitology 29, 795–798.CrossRefGoogle ScholarPubMed
Domingues, M.V. & Marques, F.P.L. (2007) Revision of Potamotrygonocotyle Mayes, Brooks & Thorson, 1981 (Platyhelminthes, Monogenea, Monocotylidae) with descriptions of four new species from the gills of freshwater stingrays, Potamotrygon spp. (Rajiformes, Potamotrygonidae) from the La Plata river basin. Systematic Parasitology 67, 157–174.CrossRefGoogle Scholar
Domingues, M.V., Pancera, N.C.M. & Marques, F.P.L. (2007) Monogenoidean parasites of freshwater stingrays (Rajiformes: Potamotrygonidae) from the Rio Negro, Amazon, Brazil: species of Potamotrygonocotyle (Monocotylidae) and Paraheteronchocotyle (Hexabothriidae). Folia Parasitologica 54, 177–190.CrossRefGoogle Scholar
Domning, D.P. (1982) Evolution of manatees, a speculative history. Journal of Paleontology 56, 599–619.Google Scholar
Farris, J.S. (1989) The retention index and rescaled consistency index. Cladistics 5, 417–419.CrossRefGoogle ScholarPubMed
Fink, S.V. & Fink, W.L. (1979) Central Amazonia and its fishes. Comparative Biochemistry and Physiology 62, 13–29.CrossRefGoogle Scholar
Géry, J. (1969) The freshwater fishes of South America. pp. 828–848in Fittkau, E.J., Illies, J., Klinge, H., Shwabe, G. & Sioli, H. (Eds) Biogeography and ecology in South America. Vol. 2. The Hague, Junk.Google Scholar
Goloboff, P., Farris, J. & Nixon, K. (2008) TNT, a free program for phylogenetic analysis. Cladistics 24, 1–13.CrossRefGoogle Scholar
Grabert, H. (1983) Der Amazonas - Geschichte eines stromes zwischen Pazifik und Atlantic. Natur und Museum 113, 61–71.Google Scholar
Hafner, M.S. & Nadler, S.A. (1990) Cospeciation in host-parasite assemblages: comparative analysis of rates of evolution and timing of cospeciation events. Systematic Zoology 39, 192–204.CrossRefGoogle Scholar
Hoberg, E.P. (1992) Congruence and synchronic patterns in biogeography and speciation among seabirds, pinnipeds, and cestodes. Journal of Parasitology 78, 601–615.CrossRefGoogle ScholarPubMed
Hoberg, E.P., Brooks, D.R., Molina-Ureña, H. & Erbe, E. (1998) Echinocephalus janzeni n. sp. (Nematoda: Gnathostomatidae) in Himantura pacifica (Chondrichthyes: Myliobatiformes) from the Pacific coast of Costa Rica and Mexico, with historical biogeographic analysis of the genus. Journal of Parasitology 84, 571–581.CrossRefGoogle Scholar
Hubert, N. & Renno, J. F. (2006) Historical biogeography of South American freshwater fishes. Journal of Biogeography 33, 1414–1436.CrossRefGoogle Scholar
Humason, G.L. (1979) Animal tissue techniques. 4th edn. 468 pp. San Francisco, USA, W.H. Freeman.Google Scholar
Klassen, G.L. (1992) Coevolution: a history of the macroevolutionary approach to studying host-parasite associations. Journal of Parasitology 78, 573–587.CrossRefGoogle ScholarPubMed
Klassen, G.L. & Beverley-Burton, M. (1988) North American fresh water ancyrocephalids (Monogenea) with articulating haptoral bars: host-parasite coevolution. Systematic Zoology 37, 179–189.CrossRefGoogle Scholar
Kluge, A.G. & Farris, J.S. (1969) Quantitative phyletics and the evolution of anurans. Systematic Zoology 18, 1–32.CrossRefGoogle Scholar
Llewellyn, J. (1982) Host specifity in monogenetic trematodes. Bulletin de la Société Neuchâteloise des Sciences Naturelles 32, 199–212.Google Scholar
Lovejoy, N.R. (1997) Stingrays, parasites and Neotropical biogeography: a closer look at Brooks et al. hypotheses concerning the origins of Neotropical freshwater rays (Potamotrygonidae). Systematic Biology 46, 219–230.CrossRefGoogle Scholar
Lovejoy, N.R., Bermingham, E. & Martin, A.P. (1998) Marine incursion into South America. Nature 396, 421–422.CrossRefGoogle Scholar
Lovejoy, N.R., Albert, J.S. & Crampton, W.G.R. (2006) Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes. Journal of South American Earth Science 21, 5–13.CrossRefGoogle Scholar
Lovejoy, N.R., Lester, K., Crampton, W.G.R., Marques, F.P.L. & Albert, J.S. (2010) Phylogeny, biogeography, and electric signal evolution of Neotropical knifefishes of the genus Gymnotus (Osteichthyes: Gymnotidae). Molecular Phylogenetics and Evolution 54, 278–290.CrossRefGoogle ScholarPubMed
Luchetti, N.M., Marques, F.P.L. & Charvet-Almeida, P. (2008) A new species of Potamotrygonocestus Brooks and Thorson, 1976 (Eucestoda: Tetraphyllidea) from Plesiotrygon iwamae Rosa, Castello and Thorson, 1987 (Mylliobatoidea: Potamotrygonidae) and redescription of Potamotrygonocestus chaoi Marques, Brooks and Araujo, 2003. Systematic Parasitology 70, 131–145.CrossRefGoogle Scholar
Marlier, G. (1967) Hydrobiology in the Amazon Region. Atas do Simpósio sobre a Biota Amazônica 3, 1–7.Google Scholar
Marques, F.P.L. (2000) Evolution of Neotropical freshwater stingrays and their parasites: taking into account space and time. PhD Dissertation, University of Toronto, Ontario, Canada.Google Scholar
Marques, F.P.L. & Brooks, D.R. (2003) Taxonomic review of Rhinebothroides (Eucestoda: Tetraphyllidea: Phyllobothriidae), parasites of freshwater stingrays (Rajiformes: Myliobatoidei: Potamotrygonidae). Journal of Parasitology 89, 944–1017.CrossRefGoogle ScholarPubMed
Marques, F.P.L., Brooks, D.R. & Araújo, M.L.G. (2003) Systematics and phylogeny of Potamotrygonocestus (Platyhelminthes, Tetraphyllidea, Onchobothriidae) with descriptions of three new species from freshwater potamotrygonids (Myliobatoidea, Potamotrygonidae). Zoologica Scripta 32, 367–396.CrossRefGoogle Scholar
Metcalf, M.M. (1923) The opalinid ciliate infusorians. Bulletin of the U.S. National Museum 120, 1–484.Google Scholar
Metcalf, M.M. (1929) Parasites and the aid they give in problems of taxonomy, geographic distribution, and paleogeography. Smithsonian Miscellaneous Collection 81, 1–36.Google Scholar
Neifar, L., Euzet, L. & Ben Hassine, O.K. (1999a) Myliocotyle pteromylaei gen. et sp. n. (Monogenea: Monocotylidae) parasite branchial de Pteromylaeus bovines (Euselachii: Myliobatinae) en Tunisie. Parasite 6, 323–327.CrossRefGoogle Scholar
Neifar, L., Euzet, L. & Ben Hassine, O.K. (1999b) Helicotyle kartasi gen. et sp. n. (Monogenea: Monocotylidae) parasitic on Pteromylaeus bovines (Euselachii: Myliobatinae) from Tunisia. Folia Parasitologica 46, 29–32.Google Scholar
Nixon, K.C. (1999–2002) WinClada ver. 1.00.08. Published by the author, Ithaca, NY, USA.Google Scholar
Nuttal, C.P. (1990) A review of the Terciary non-marine molluscans faunas of the Pebasian and other inlands basins of north-western South America. Bulletin of the British Museum of Natural History (Geology) 45, 165–371.Google Scholar
Page, R.D.M. & Charleston, M.A. (1998) Trees within trees: phylogeny and historical associations. Trends in Ecology and Evolution 13, 356–359.CrossRefGoogle ScholarPubMed
Paterson, A.M. & Banks, J. (2001) Analytical approaches to measuring cospeciation of host and parasites: through a glass darkly. International Journal for Parasitology 31, 1012–1022.CrossRefGoogle ScholarPubMed
Paterson, A.M., Wallis, G.P., Wallis, L.J. & Gray, R.D. (2000) Seabird and louse coevolution: Complex histories revealed by 12S rRNA sequences and reconciliation analyses. Systematic Biology 49, 383–399.CrossRefGoogle ScholarPubMed
Reis, R.E., Kullander, S.O. & Ferraris, C.J. Jr(Org.) (2003) Check list of the freshwater fishes of South and Central America. 742 pp. Porto Alegre, Brazil, EDIPUCRS.Google Scholar
Reyda, F.B. (2007) Patterns of diversity and host specificity in the cestodes of neotropical freshwater stingrays. PhD Dissertation, University of Connecticut, Storrs, Connecticut.Google Scholar
Ribeiro, A.C. (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotropical Ichthyology 4, 225–246.CrossRefGoogle Scholar
Roberts, T.R. (1972) Ecology of fishes in the Amazon and Congo Basin. Bulletin of Museum of Comparative Zoology 143, 117–142.Google Scholar
Rosa, R.S., Menezes, N.A., Britski, H.A., Costa, W.J.E.M. & Groth, F. (2003) Diversidade, padrões de distribuição e conservação dos peixes da Caatinga. pp. 135–180in Leal, I.R., Tabarelli, M. & da Silva, J.M.C. (Eds) (Org.)Ecologia e conservação da Caatinga. 1st edn. São Paulo, Editora Universitária UFPE.Google Scholar
Rosa, R.S., de Carvalho, M.R. & Wanderley, C.A. (2008) Potamotrygon boesemani (Chondrichthyes: Myliobatiformes: Potamotrygonidae), a new species of neotropical freshwater stingray from Surinam. Neotropical Ichthyology 6, 1–8.CrossRefGoogle Scholar
Straney, D.O. (1982) Review of: Advances in cladistics. Systematic Zoology 31, 337–341.CrossRefGoogle Scholar
Thorson, T.B., Brooks, D.R. & Mayes, M.A. (1983) The evolution of freshwater adaptation in stingrays. National Geographic Society, Research Reports 15, 663–694.Google Scholar
von Ihering, H. (1891) On the ancient relations between New Zealand and South America. Transactions and Proceedings of the Royal Society of the New Zealand Institute 24, 431–445.Google Scholar
von Ihering, H. (1902) Die helminthen als Hilfsmittel der zoogeographischen Forschung. Zoologischer Anzeiger 26, 42–51.Google Scholar
Webb, S. (1995) Biological implications of the Mid-Miocene seaway. Science 268, 361–362.CrossRefGoogle Scholar
Zamparo, D., Brooks, D.R. & Barriga, R. (1999) Pararhinebothroides hobergi n. gen. n. sp. (Eucestoda: Tetraphyllidea) in Urobatis tumbesensis (Chondrichthyes: Myliobatiformes) from Coastal Ecuador. Journal of Parasitology 85, 534–539.CrossRefGoogle Scholar