Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-19T12:57:31.860Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular and morphological characterization of Austrodiplostomum ostrowskiae Dronen, 2009 (Digenea: Diplostomatidae), a parasite of cormorants in the Americas

Published online by Cambridge University Press:  04 March 2015

M. García-Varela ,
A.L. Sereno-Uribe ,
C.D. Pinacho-Pinacho ,
O. Domínguez-Domínguez  and
G. Pérez-Ponce de León
M. García-Varela*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Distrito Federal, México
A.L. Sereno-Uribe
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Distrito Federal, México
C.D. Pinacho-Pinacho
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Distrito Federal, México
O. Domínguez-Domínguez
Affiliation:
Laboratorio de Biología Acuática, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, México
G. Pérez-Ponce de León
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Distrito Federal, México
*
*Fax: (525) 5550 0164 E-mail: garciav@unam.mx; garciav@ib.unam.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

The diplostomid genus Austrodiplostomum currently contains two species, i.e. A. mordax and A. ostrowskiae. Adults of these species inhabit the intestine of cormorants of the genus Nannopterum, whereas larval forms (metacercariae) are found in the eyes (vitreous humor) of freshwater fishes. Records of both species have been established across a wide geographic range in the Americas. Diplostomid adults and metacercariae were collected from a wide geographical range that spans from south-eastern Mexico, southwards to Central and South America. Even though the diplostomid has been largely reported in Mexico as Diplostomum (Austrodiplostomum) compactum, our specimens were identified morphologically as A. ostrowskiae. Sequences of the mitochondrial gene cytochrome c oxidase (cox 1) were obtained for 86 individuals, including 15 adults recovered from the intestine of Nannopterum brasilianus, in five localities, and 71 metacercariae from the eyes of ten fish species, in 13 localities. Sequences were used to evaluate the genetic diversity, and to test conspecificity of these specimens with the available sequence of A. ostrowskiae. Sequences were aligned with another 12 taxa representing five genera of Diplostomatidae, forming a dataset of 104 taxa with 478 nucleotides. The genetic divergence estimated among the 86 sequenced individuals, and that of A. ostrowskiae from the double-crested cormorant, Nannopterum auritus, in the USA, was very low, ranging from 0 to 0.8%. The maximum likelihood (ML) and Bayesian consensus trees showed that all sequences nested within a monophyletic lineage, with strong bootstrap and Bayesian posterior probability support values (100/1.0). In conclusion, a link between the metacercariae in fish and the adults in cormorants was established, indicating also that a single species is found in the distribution range comprising southern USA, southwards to Venezuela. Previous records of this species, particularly from Mexico, need to be corrected.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 2 , March 2016 , pp. 174 - 185
Copyright
Copyright © Cambridge University Press 2015 

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 (AOU). (1998) Check-list of North American birds. 7th edn. 829 pp. Washington, DC, AOU.Google Scholar
Bandelt, H.J., Forster, P. & Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Faltynková, A., Goergieva, S., Skirnisson, K., Scholz, T. & 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.CrossRefGoogle ScholarPubMed
Caballero, Y.C.E. & Winter, H.W. (1954) Metacercarias de Diplostomum spathaceum (Rudolphi, 1819) Braun, 1893 en peces de agua dulce de México. Ciencia 14, 77–80.Google Scholar
Chibwana, F.D., Blasco-Costa, I., Georgieva, S., Hosea, K.M., Nkwengulila, G., Scholz, T. & 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.CrossRefGoogle ScholarPubMed
Drago, F.B., Lunaschi, L.I. & Schenone, M. (2011) Digenean parasites of the Neotropical Cormorant, Palacrocorax brasilianus (Gmelin, 1789) (Aves: Phalacrocoracidae) from Argentina: distribution extension and new host records. Check List 6, 871–875.CrossRefGoogle Scholar
Dronen, N.O. (2009) Austrodiplostomum ostrowskiae n. sp. (Digenea: Diplostomidae: Diplostominae) from the double-crested cormorant, Phalacrocorax auritus (Phalacrocoracidae) from the Galveston, Texas area of the Gulf of Mexico, U.S.A. Comparative Parasitology 76, 34–39.CrossRefGoogle 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
Dubois, G. & Macko, J. (1972) Contribution à l'étude des Strigeata La Rue, 1926 (Trematoda: Strigeida) de Cuba. Annales de Parasitologie Humaine et Comparée 47, 51–75.CrossRefGoogle Scholar
Fedynich, A.M., Pence, D.B. & Bergan, J.F. (1997) Helminth community structure and pattern in sympatric populations of double-crested and neotropical cormorants. Journal of the Helminthological Society of Washington 64, 176–182.Google Scholar
Galazzo, D.E., Dayanandan, S., Marcogliese, D.J. & McLaughlin, J.D. (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
Georgieva, S., Soldánová, M., Pérez-del-Olmo, A., Dangel, R.D., Sitko, J., Sures, B. & Kostadinova, A. (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 52–72.CrossRefGoogle ScholarPubMed
Howell, S.N.G. & Webb, S. (1995) A guide to the birds of Mexico and Northern Central America. 851 pp. New York, Oxford University Press.CrossRefGoogle Scholar
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogeny. Biometrics 17, 754–755.Google Scholar
Kennedy, M. & Spencer, H.G. (2014) Classification of the cormorants of the world. Molecular Phylogenetics and Evolution 79, 249–257.CrossRefGoogle ScholarPubMed
Locke, S.A., McLaughlin, J.D., Dayanandan, S. & Marcogliese, D.J. (2010a) Diversity, specificity and evidence of hybridization in Diplostomum spp. metacercariae in freshwater fishes is revealed by DNA barcodes and ITS sequences. International Journal for Parasitology 40, 333–343.CrossRefGoogle Scholar
Locke, S.A., McLaughlin, D.J. & Marcogliese, D.J. (2010b) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.CrossRefGoogle Scholar
Lutz, A. (1928) Estudios de zoología y parasitología Venezolanas. 133 pp. Brazil, Rio de Janeiro.Google Scholar
Machado, P.M., Takemoto, R.M. & Pavanelli, G.C. (2005) Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) (Platyhelminthes, Digenea) metacercariae in fish from the floodplain of the Upper Paraná River, Brazil. Parasitology Research 97, 436–444.CrossRefGoogle Scholar
Miller, R.R., Minckley, W.L. & Norris, S.M. (2005) Freshwater fishes of Mexico. 559 pp. Chicago, The University of Chicago Press.Google Scholar
Moszczynska, A., Locke, S.A., McLaughlin, J.D., Marcogliese, D.J. & Crease, T.J. (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminthes. Molecular Ecology Resource 9, 75–82.CrossRefGoogle Scholar
Nasir, P. & Díaz, M.T. (1972) Avian flukes of Venezuela. Rivista di Parassitologia 33, 245–276.Google Scholar
Niewiadomska, K. (2002) Family Strigeidae, 1919. pp. 231–260 in Gibson, D.I., Jones, A. & Bray, R.A. (Eds) Keys to the Trematoda. Vol. I. London, The Natural History Museum.CrossRefGoogle Scholar
Niewiadomska, K. & Laskowski, Z. (2002) Systematic relationships among six species of Diplostomum Nordmann, 1832 (Digenea) based on morphological and molecular data. Acta Parasitologica 47, 20–28.Google Scholar
O'Hear, M., Pote, L., Yost, M., Doffitt, C., King, T. & Panuska, C. (2014) Morphologic and molecular identifications of digenetic trematodes in double-crested cormorants (Phalacrocorax auritus) from the Mississippi delta. Journal Wildlife Disease 50, 42–49.CrossRefGoogle ScholarPubMed
Ostrowski de Núñez, M. (1970) Estudios sobre la fauna parasitaria del biguá. II. Trematodes pertenecientes a la familia Diplostomatidae. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia Zoología 10, 199–214.Google Scholar
Ostrowski de Núnez, M. (1977) El ciclo biológico de Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois 1970 (Austrodiplostomum mordax Szidat y Nani 1951) (Trematoda, Diplostomatidae). Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia Parasitología 2, 7–63.Google Scholar
Ostrowski de Núnez, M. (1982) Die Entwicklungszyklen von Diplostomum (A) compactum (Lutz, 1928) Dubois, 1970 und D. (A.) mordax (Szidatt und Nani, 1951 n. comb) in Südamerika. Zoologischer Anzeiger 208, 393–404.Google Scholar
Otachi, E.O., Locke, S.A., Jirsa, F., Fellner-Frank, C. & Marcogliese, D.J. (2014) 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. & Mendoza Garfías, B. (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1–247.CrossRefGoogle Scholar
Pineda-López, R. (1985) Infección por metacercarias (Platyhelminthes: Trematoda) en peces de agua dulce de Tabasco. Universidad Ciencia 2, 47–60.Google Scholar
Pineda-López, R., Andrade-Salas, O., Páramo-Delgadillo, S., Trejo-Pérez, L., Pérez-Méndez, M.A., Almeyda-Artigas, J., Osorio-Sarabia, D. & Pérez-Ponce de León, G. (1985) Estudio del control sanitario de la piscifactoría Benito Juárez y en los vasos de las presas Malpaso y La Angostura, Chiapas. 309 pp. Mexico City, Universidad Juárez Autónoma de Tabasco-Secretaría de Pesca.Google Scholar
Pinto, H.A. & Melo, A.L. (2013) Biomphalaria straminea and Biomphalaria glabrata (Mollusca: Planorbidae) as a new intermediate hosts of the fish eyefluke Austrodiplostomum compactum (Trematoda: Diplostomidae) in Brazil. Journal of Parasitology 99, 729–733.CrossRefGoogle ScholarPubMed
Posada, D. & Crandall, K.A. (1988) Modeltest: Testing the model of DNA substitution. Bioinformatics 9, 817–818.Google Scholar
Rambaut, A. (2006) FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh.Google Scholar
Ramos, I.P., Franceschini, L., Zago, A.C., Oliveira de Penha Zica, E., Wunderlich, A.C., Carvalho, E.D. & da Silva, R.J. (2013) New host records and a checklist of fishes infected with Austrodiplostomum compactum (Digenea: Diplostomidae) in Brazil. Revista Brasileira de Parasitologia Veterinária 4, 511–518.CrossRefGoogle Scholar
Ramos-Ramos, P. (1995) Algunos tremátodos de vertebrados de la Presa Miguel Alemán, en Temascal, Oaxaca, México. Anales del Instituto de Biología Universidad Nacional Autónoma de México 66, 241–246.Google Scholar
Rietschel, G. & Werding, B. (1978) Trematodes of birds from northern Colombia. Zeitschrift für Parasitenkundes 57, 57–82.CrossRefGoogle Scholar
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.CrossRefGoogle ScholarPubMed
Szidat, L. & Nani, A. (1951) Diplostomiasis cerebralis del Pejerrey. Una grave epizootia que afecta a la economia nacional producida por las de trematodes que destruyen el cerebro de los pejerreyes. Revista Nacional del Instituto de Investigaciones de las Ciencias Naturales anexo al Museo Argentino de Ciencias Naturales de Bernardino Rivadavia 1, 323–394.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thompson, J.D., Gibson, T.J., Plewniak, F. & Jeanmougin, F. (1994) The Clustal windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
Violante-González, J., García-Varela, M., Rojas-Herrera, A. & Guerrero, S.G. (2009) Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitology Research 105, 803–807.CrossRefGoogle ScholarPubMed