Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-30T16:16:27.705Z Has data issue: false hasContentIssue false
  • English
  • Français

A morphological and molecular study of adults and metacercariae of Hysteromorpha triloba (Rudolpi, 1819), Lutz 1931 (Diplostomidae) from the Neotropical region

Published online by Cambridge University Press:  24 January 2018

A.L. Sereno-Uribe ,
A. López-Jimenez ,
L. Andrade-Gómez  and
M. García-Varela
A.L. Sereno-Uribe
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México
A. López-Jimenez
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México
L. Andrade-Gómez
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México
M. García-Varela*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México
*
Author for correspondence: M. García Varela, Fax: (525) 5550 0164, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Adults of Hysteromorpha triloba (Rudolpi, 1819), Lutz, 1931 inhabit primarily the intestine of cormorants across the globe, whereas metacercariae have been found in the body cavity of freshwater fishes of the families Cyprinidae, Ictaluridae, Ariidae, Pimelodidae and Catostomidae. In this study, adults and metacercariae identified as H. triloba were collected from the Neotropical cormorant (Nannopterum brasilianus) and from the Mexican tetra fish (Astyanax mexicanus) from the Gulf of Mexico and Pacific Ocean slopes in the Neotropical region. Partial DNA sequences of the mitochondrial gene cytochrome c oxidase subunit I (cox 1) and the internal transcribed spacers (ITS1, 5.8S and ITS2) of nuclear ribosomal DNA were generated for both developmental stages, and were compared with available sequences of H. triloba from the Nearctic region. The genetic divergence between metacercariae and adults of H. triloba from the Neotropical and Nearctic region (Canada) associated with the double-crested cormorant (Nannopterum auritus), ranged from 0 to 5.5% for cox 1 and from 0 to 0.2% for ITS. Phylogenetic analyses inferred with both molecular markers using maximum likelihood and Bayesian inference placed the adults and metacercariae in a single clade, confirming that both stages are conspecific. Our data confirmed that H. triloba is a widely distributed species across the Americas, parasitizing both the Neotropical and Nearctic cormorants in Argentina, Brazil, Venezuela, Mexico, USA and Canada.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 1 , January 2019 , pp. 91 - 99
Copyright
Copyright © Cambridge University Press 2018 

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

American Ornithologists’ Union (1998) Check-list of North American birds. 7th edn. Washington DC, AOU.Google Scholar
Blasco-Costa, I and Locke, SA (2017) Life history, systematics and evolution of the Diplostomoidea Poirier, 1886: progress, promises and challenges emerging from molecular studies. Advances in Parasitology 98, 167–225.Google Scholar
Blasco-Costa, I, Faltynková, A, Goergieva, S, Skirnisson, K, Scholz, T and Kostadinova, A (2014) Fish pathogens near the Arctic Circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology 44, 703–715.Google Scholar
Blasco-Costa, I, Poulin, R and Presswell, B (2017) Morphological description and molecular analyses of Tylodelphys sp. (Trematoda: Diplostomidae) newly recorded from freshwater fish Gobiomorphus cotidianus (common bully) in New Zealand. Journal of Helminthology 9, 332–345.Google Scholar
Bowles, J and McManus, DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular Biochemical Parasitology 57, 231–239.Google Scholar
Chibwana, FD, Blasco-Costa, I, Georgieva, S, Hosea, KM, Nkwengulila, G, Scholz, T and Kostadinova, A (2013) A first insight into the barcodes for African diplostomids (Digenea: Diplostomidae): brain parasites in Clarias gariepinus (Siluriformes: Clariidae). Infection Genetics and Evolution 17, 62–70.Google Scholar
Chibwana, FD, Nkwengulila, G, Locke, SA, McLughlin, JD and Marcogliese, DJ (2015) Completion of the life cycle of Tylodelphys mashonense (Sudarikov, 1971) (Digenea: Diplostomidae) with DNA barcodes and rDNA sequences. Parasitology Research 114, 3675–3682.Google Scholar
Ciurea, I (1930) Contributions à l´étude morphologique et biologique de quelques strigéidés des oiseaux ichtyophages de la faune de Roumanie (Recherches expérimentales). Archives Roumaines de Pathologie Experimentale et de Microbiologie (Bucuresti) 3, 227–323.Google Scholar
Drago, FB, Lunaschi, LI and Schenone, M (2011) Digenean parasites of the Neotropic cormorant, Palacrocorax brasilianus (Gmelin, 1789) (Aves: Phalacrocoracidae) from Argentina: distribution extension and new host records. Check List 6, 871–875.Google Scholar
Dubois, G (1970) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mémoires de la Société de Sciences Naturelles de Neuchatel 10, 259–727.Google Scholar
Fedynich, AM, Pence, DB and Bergan, JF (1997) Helminth community structure and pattern in sympatric populations of double-crested and neotropic cormorants. Journal of the Helminthological Society of Washington 64, 176–182.Google Scholar
García-Varela, M, Sereno-Uribe, AL, Pinacho-Pinacho, CD, Hernández-Cruz, E and Pérez-Ponce de León, G (2016) An integrative taxonomic study reveals a new species of Tylodelphys Diesing, 1950 (Digenea: Diplostomidae) in central and northern Mexico. Journal of Helminthology 90, 668–679.Google Scholar
Georgieva, S, Soldánová, M, Pérez-Del-Olmo, A, Dangel, DR, Sitko, J, Sures, B and Kostadinova, A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 52–72.Google Scholar
Goss, OM (1940) Platyhelminth and Acanthocephalan parasites of local shags. Journal of the Royal Society of Western Australia 26, 1–14.Google Scholar
Gupta, R (1963) On two new diplostome parasites of birds, with a note on Hysteromorpha triloba (Rud., 1819) Lutz, 1931 from India (Trematoda: Diplostomidae). Revista de Biología Tropica 11, 75–87.Google Scholar
Hérnandez-Mena, DI, García-Varela, M and Pérez Ponce de León, G (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 94, 833–848.Google Scholar
Howell, SNG and Webb, S (1995) A guide to the birds of Mexico and Northern Central America. Oxford, New York, Oxford University Press.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MrBayes: Bayesian inference of phylogeny. Biometrics 17, 754–755.Google Scholar
Hugghins, EJ (1954) Life history of a Strigeid trematode, Hysteromorpha triloba (Rudolphi, 1819) Lutz, 1931. Transactions of the American Microscopical Society 3, 221–236.Google Scholar
Locke, SA, McLaughlin, JD, Lapierre, AR, Johnson, PT and Marcogliese, DJ (2011) Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. Journal of Parasitology 97, 846–851.Google Scholar
López-Jimenez, A, Pérez-Ponce de León, G and García-Varela, M (2017) Molecular data reveal high diversity of Uvulifer (Trematoda: Diplostomidae) in Middle America, with the description of a new species. Journal of Helminthology 11, 1–15.Google Scholar
Lutz, A (1931) Contribucao ao conhecimiento da ontogenia das Strigeida. I. Ontogenia de Hemistomum trilobum (Rudolphi, 1819). Memorias do Instituto Oswaldo. 25, 333–342.Google Scholar
Miller, RR, Minckley, WL and Norris, SM (2005) Freshwater fishes of Mexico. Chicago, The University of Chicago Press.Google Scholar
Monteiro, CM, Amato, JF and Amato, SB (2011) Helminth parasitism in the neotropical cormorant, Phalacrocorax brasilianus, in southern Brazil: effect of host size, weight, sex, and maturity state. Parasitology Research 109, 849–855.Google Scholar
Moszczynska, A, Locke, SA, McLaughlin, JD, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, 75–82.Google Scholar
O'Hear, M, Pote, L, Yost, M, Doffitt, C, King, T and Panuska, C (2014) Morphologic and molecular identifications of digenetic trematodes in double-crested cormorants (Phalacrocorax auritus) from the Mississippi delta, USA. Journal Wildlife Disease 50, 42–49.Google Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.Google Scholar
Ostrowski de Nuñez, M (1970) Estudios sobre la fauna parasitaria del biguá. Phalacrocorax b. brasilianus. II. Trematodes pertenecientes a la familia Diplostomatidae Poirier, 1886. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia Zoología 10, 199–214.Google Scholar
Otachi, EO, Locke, SA, Jirsa, F, Fellner-Frank, C and Marcogliese, DJ (2015) Morphometric and molecular analyses of Tylodelphys sp. metacercariae (Digenea: Diplostomidae) from the vitreous humour of four fish species from Lake Naivasha, Kenya. Journal of Helminthology 4, 1–11.Google Scholar
Pérez-Ponce de León, G, García Prieto, L and Mendoza Garfías, B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1–247.Google Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.Google Scholar
Posada, D (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Rambaut, A (2006) FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh.Google Scholar
Selbach, C, Soldánová, M, Georgieva, S, Kostadinova, A and Sures, B (2015) Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasites & Vectors 8, 300.Google Scholar
Sheehan, KL, Hanson-Dorr, KC, Dorr, BS, Yarrow, GK and Johnson, RJ (2016) The influence of geographical location, host maturity and sex on intestinal helminth communities of the double-crested cormorant Phalacrocorax auritus from the eastern United States. Journal of Helminthology 28, 1–8.Google Scholar
Stamatakis, A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.Google Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Thompson, JD, Gibson, TJ, Plewniak, F and Jeanmougin, F (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar