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Review of five species of cyclocoelids (Digenea: Cyclocoelidae) from aquatic birds in Mexico with notes on their interspecific variation

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Abstract

Based on a morphological approach, five species of cyclocoelids (Digenea: Cyclocoelidae) are revised based on material from birds in Mexico. The species studied are: Cyclocoelum cf. leidyi Harrah, 1922 from the black-necked stilt Himantopus mexicanus Müller (Recurvirostridae); Cyclocoelum mutabile (Zeder, 1800) from the northern jacana Jacana spinosa L. (Jacanidae) and the willet Tringa semipalmata Gmelin (Scolopacidae); Cyclocoelum pseudomicrostomum Harrah, 1922 from the American coot Fulica americana Gmelin (Rallidae); Selfcoelum lamothei Blend & Dronen, 2008, from the long-billed curlew Numenius americanus Bechstein (Scolopacidae); and Neohaematotrephus arayae Zamparo, Brooks, Causey & Rodriguez, 2003 from J. spinosa. New morphological data, illustrations and measurements are presented for these trematodes. Three species, insufficiently described, i.e. C. cf. leidyi, C. mutabile and C. pseudomicrostomum, are redescribed in detail. Our results indicate morphological variation in some important features used in the diagnosis of Cyclocoelum Brandes, 1892 (i.e. the presence or absence of oral sucker, the position of the genital pore relative to the pharynx, and the posterior extension of the uterus) and Selfcoelum Dronen, Gardner & Jiménez, 2006 (i.e. anterior extension of vitelline follicles). Finally, this study provides the first molecular data for the large subunit of the ribosomal RNA (28S rRNA) gene for N. arayae.

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References

  • American Ornithologist’s Union. (1998). Check-list of North American Birds. 7th Edition. American Ornithologists’ Union. Lawrence: Allen Press Inc., 829 pp.

  • Bashkirova, E. I. (1950). Family Cyclocoelidae Kossack, 1911. Osnovy Trematodologii, 4, 329–493 (In Russian).

    Google Scholar 

  • Besprozvannykh, V. V., Ngo, H. D., Ha, N. V., Hung, N. M., Rozhkovan, K. V., & Ermolenko, A. V. (2013). Descriptions of digenean parasites from three snail species, Bithynia fuchsiana (Morelet), Parafossarulus striatulus Benson and Melanoides tuberculata Müller, in North Vietnam. Helminthologia, 50, 190–204.

    Article  Google Scholar 

  • Blend, C. K., & Dronen, N. O. (2008). Selfcoelum lamothei n. sp. (Digenea: Cyclocoelidae: Cyclocoelinae) from the air sacs of the long-billed curlew, Numenius americanus (Scolopacidae), from the Galveston, Texas area, USA. Revista Mexicana de Biodiversidad, 79, 41S–48S.

    Google Scholar 

  • Caballero, C. E., & Flores-Barroeta, L. (1952). Presencia de Cyclocoelum mutabile (Zeder, 1800) Stossich, 1902 en aves acuáticas de México. Revista Iberica de Parasitologia, 12, 297–300.

    Google Scholar 

  • Canaris, A., Ortiz, R., & Canaris, G. (2010). A predictable suite of helminth parasites in the long-billed dowitcher, Limnodromus scolopaceus, from the Chihuahua desert in Texas and Mexico. Journal of Parasitology, 96, 1060–1065.

    Article  Google Scholar 

  • Chapin, J. (1922). Note on monostomes. Journal of Parasitology, 9, 44.

    Google Scholar 

  • Coil, W. H. (1957). Parastrigea mexicanus sp. nov., a strigeid trematode from the avocet. Transactions of the American Microscopical Society, 76, 70–72.

    Article  Google Scholar 

  • Dronen, N. O. (2007). Revision of the family Cyclocoelidae Stossich, 1902 with the proposal of two new subfamilies and the description of a new species of Morishitium Witenberg, 1928 from the common snipe, Gallinago gallinago, from Texas, U.S.A. Zootaxa, 1563, 55–68.

    Google Scholar 

  • Dronen, N. O., & Blend, C. K. (2015). Updated keys to the genera in the subfamilies of Cyclocoelidae Stossich, 1902, including a reconsideration of species assignments, species keys and the proposal of a new genus in Szidatitreminae Dronen, 2007. Zootaxa, 4053, 1–100.

    Article  Google Scholar 

  • Dronen, N. O., Al-Kassar, N. R., Ali, A. H., Abdulhameed, M. F., Abdullah, B. H., & Al-Mayah, S. H. (2017). Intraspecific variation in adult Uvitellina iraquensis Dronen, Ali & Al-Amura, 2013 (Cyclocoelidae: Haematotrephinae) from two collection sites of white-tailed lapwing, Vanellus leucurus (Lichtenstein) (Charadriiformes: Charadriidae), in Iraq. Zootaxa, 4242, 1–33.

    Article  Google Scholar 

  • Dubois, G. (1959). Revision des Cyclocoelidae Kossack 1911 (Trematoda). Revue Suisse de Zoologie, 66, 67–147.

    Article  Google Scholar 

  • García-Varela, M., & Nadler, S. A. (2005). Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology, 91, 1401–1409.

    Article  Google Scholar 

  • Gibson, D. I., Bray, R. A., & Harris, E. A. (Compilers). (2005). Host-parasite database of the Natural History Museum, London. http://www.nhm.ac.uk/research-curation/scientific-resources/taxonomy-systematics/host-parasites/database/index.jsp

  • Griffin, M. J., Khoo, L. H., Quiniou, S. M., O’Hear, M. M., Pote, L. M., Greenway, T. E., & Wise, D. J. (2012). Genetic sequence data identifies the cercaria of Drepanocephalus spathans (Digenea: Echinostomatidae), a parasite of the double-crested cormorant (Phalacrocorax auritus), with notes on its pathology in juvenile channel catfish (Ictalurus punctatus). Journal of Parasitology, 98, 967–972.

    Article  CAS  Google Scholar 

  • Harrah, E. C. (1922). North American monostomes primarily from freshwater hosts. Illinois Biological Monographs, 7, 225–324.

    Google Scholar 

  • Hernández-Mena, D., García-Varela, M., & García-Prieto, L. (2014). Morphological and molecular differentiation of Parastrigea (Trematoda: Strigeidae) from Mexico, with the description of a new species. Parasitology International, 63, 315–323.

    Article  Google Scholar 

  • Hildebrand, J., Adamczyk, M., Laskowski, Z., & Zaleśny, G. (2015). Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Lühe, 1909 (Digenea, Echinostomatinae) - morphological variation vs. molecular stability. Parasites & Vectors, 8, 481.

  • Howell, S. N. G., & Webb, S. (1995). A guide to the birds of Mexico and northern Central America. New York: Oxford University Press, 851pp.

    Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  CAS  Google Scholar 

  • Kanev, I., Radev, V., & Fried, B. (2002). Family Cyclocoelidae Stossich, 1902. In: Bray, R.A., Gibson, D.I. & Jones, A. (Eds), Keys to the Trematoda, Volume 1. Wallingford: CABI Publishing and the Natural History Museum, pp 131–146.

    Chapter  Google Scholar 

  • Kossack, W. F. K. (1911). Über Monostomiden. Zoologische Jahrbücher Abteilung für Systematik, Geographie und Biologie der Tiere, 31, 491–590.

    Google Scholar 

  • Lamothe-Argumedo, R., & Orozco-Flores, A. (2000). Nota sobre Cyclocoelum obscurum (Trematoda: Cyclocoelidae) registrado por primera vez en Baja California Sur, México. Anales del Instituto de Biología, 71, 89–92.

    Google Scholar 

  • Larios-Rodríguez, I. (1944). Una especie del género Cyclocoelum encontrada en Fulica americana del Lago de Texcoco, México. Anales del Instituto de Biología, 15, 375–378.

    Google Scholar 

  • Literák, I., Heneberg, P., Sitko, J., Wetzel, E. J., Cardenas Callirgos, J. M., Čapek, M., et al. (2013). Eye trematode infection in small passerines in Peru caused by Philophthalmus lucipetus, an agent with a zoonotic potential spread by an invasive freshwater snail. Parasitology International, 62, 390–396.

    Article  Google Scholar 

  • Luton, K., Walker, D., & Blair, D. (1992). Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology, 56, 323–327.

    Article  CAS  Google Scholar 

  • McKindsey, C. W., & McLaughlin, J. D. (1995a). Field studies on the transmission and survival of Cyclocoelum mutabile (Digenea) infections in natural snail populations in southern Manitoba, Canada. Journal of Parasitology, 81, 520–525.

    Article  CAS  Google Scholar 

  • McKindsey, C. W., & McLaughlin, J. D. (1995b). Species- and size-specific infection of snails by Cyclocoelum mutabile (Digenea: Cyclocoelidae). Journal of Parasitology, 81, 513–519.

    Article  CAS  Google Scholar 

  • Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 735–755.

    Article  Google Scholar 

  • Pérez-Ponce de León, G., García-Prieto, L., & Mendoza-Garfias, 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., et al. (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371.

    Article  CAS  Google Scholar 

  • Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.

    Article  CAS  Google Scholar 

  • Rambaut, A. (2006). Tree figure drawing tool version 1.4.0. Edinburgh: Institute of Evolutionary Biology, University of Edinburgh.

  • Sato, H., & Suzuki, K. (2006). Gastrointestinal helminths of feral raccoons (Procyon lotor) in Wakayama Prefecture, Japan. Journal of Veterinary Medical Science, 68, 311–318.

    Article  Google Scholar 

  • Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.

    Article  CAS  Google Scholar 

  • Stock, S. P., Campbell, J. F., & Nadler, S. A. (2001). Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology, 87, 877–889.

    Article  CAS  Google Scholar 

  • Stossich, M. (1902). Monostomum mutabile Zeder e le sue forme affini. Bollettino della Societa Adriatica di Scienze, Trieste, 21, 1–40.

    Google Scholar 

  • Tajrine, D. D., Kapoor, N. N., & McLaughlin, J. D. (1999). Scanning electron microscopy of newly excysted juvenile and adult Cyclocoelum mutabile (Digenea). Canadian Journal of Zoology, 77, 1111–1116.

    Article  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.

    Article  CAS  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., & Jeanmougin, F. (1997). The clustal windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.

    Article  CAS  Google Scholar 

  • Tkach, V. V., Kudlai, O., & Kostadinova, A. (2016). Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology, 46, 171–185.

    Article  Google Scholar 

  • Tkach, V. V., Pawlowski, J., Mariaux, J., & Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood, D. T. J. & Bray, R. A. (Eds), Interrelationships of the platyhelminthes. London: Taylor & Francis, pp 186–193.

    Google Scholar 

  • Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates, Volume. I. Tokyo: Keigaku Publishing Company, 1,074 pp.

  • Zamparo, D., Brooks, D. R., Causey, D., & Rodriguez, B. (2003). Neohaematotrephus arayae n. sp. (Digenea: Echinostomiformes: Cyclocoelidae) in Jacana spinosa (Aves: Charadriiformes: Jacanidae) from the Area de Conservación Guanacaste, Costa Rica. Journal of Parasitology, 89, 829–831.

    Article  Google Scholar 

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Acknowledgements

We are indebted to Drs Norman Dronen and Aneta Kostadinova for their review, comments and suggestions to improve our manuscript. The authors are grateful to Carlos Mendoza Palmero, Ulises Razo and Mirza Ortega Olivares for their help during the field work. Our special thanks are due to Carlos D. Pinacho-Pinacho for his technical assistance collecting the birds and in the molecular analyses. Thanks are also due to Luis García Prieto for providing specimens from the CNHE, and to Susana Guzmán Gómez for her advice on the use of the stereomicroscope.

Funding

This study was supported by the Programa de Apoyo a Proyectos de Investigación e Inovación Tecnológica (PAPIIT No IN206716), the Consejo Nacional de Ciencia y Tecnología (CONACYT) (No. 179048) and the Czech Science Foundation (project ECIP P505/12/G112). A.L.J. benefited from a Master student grant from the Programa de Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México (scholarship number 308181829) and from the CONACYT of the Mexican Government (scholarship number 706116).

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Author notes

  1. Alejandra López-Jiménez and Jesús S. Hernández-Orts contributed equally to this work.

Authors and Affiliations

  1. Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Avenida Universidad 3000, Ciudad Universitaria, 04510, Mexico City, Mexico

    Alejandra López-Jiménez & Martín García-Varela

  2. Posgrado en Ciencias Biológicas, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Avenida Universidad 3000, Ciudad Universitaria, 04510, Mexico City, Mexico

    Alejandra López-Jiménez

  3. Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos Almirante Storni (CIMAS – CCT CONICET – CENPAT), Güemes 1030, 8520, San Antonio Oeste, Río Negro, Argentina

    Jesús S. Hernández-Orts

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  1. Alejandra López-Jiménez
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  2. Martín García-Varela
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  3. Jesús S. Hernández-Orts
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Correspondence to Jesús S. Hernández-Orts.

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The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed. Birds were collected under the collecting permit FAUT 0202 issued by the Mexican government through the Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT) to MGV.

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This article is part of the Topical Collection Digenea.

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López-Jiménez, A., García-Varela, M. & Hernández-Orts, J.S. Review of five species of cyclocoelids (Digenea: Cyclocoelidae) from aquatic birds in Mexico with notes on their interspecific variation. Syst Parasitol 95, 921–942 (2018). https://doi.org/10.1007/s11230-018-9825-x

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