Advertisement

Systematic Parasitology

, Volume 95, Issue 4, pp 391–401 | Cite as

Morphological and molecular characterisation of digenean parasites of the Galápagos sheephead Semicossyphus darwini (Jenyns) with the re-description of Labrifer secundus Manter, 1940 (Lepidapedidae) from the Humboldt Current Large Marine Ecosystem

  • Luis A. Ñacari
  • Fabiola A. Sepulveda
  • Rubén Escribano
  • Rodney A. Bray
  • Marcelo E. Oliva
Article
Part of the following topical collections:
  1. Digenea

Abstract

The Humboldt Current Large Marine Ecosystem (HCLME) is recognised as one of the largest and most productive marine ecosystems. The estimated number of teleost fish species for the Chilean coast influenced by the HCLME reaches c.1,030 but digeneans have been reported for 39 teleost species, i.e. less than 4% of the potential hosts. During a survey of parasites of the Galápagos sheephead wrasse Semicossyphus darwini (Jennyns) (Perciformes: Labridae) from off northern Chile, we obtained representatives of three digenean species, Helicometrina nimia Linton, 1910 (Opecoelidae), Proctoeces humboldti George-Nascimento & Quiroga, 1983 (Fellodistomidae) and Labrifer secundus Manter, 1940 (Lepidapedidae). Labrifer secundus, originally described from Semicossyphus pulcher (Ayres, 1854) off the coast of Baja California, Mexico is re-described. Helicometrina nimia is a common parasite from littoral fishes in the HCLME. Semicossyphus darwini is a new host for these three digenean species.

Notes

Acknowledgements

We thank Dr K. Nagasawa, Hiroshima University, Japan for a copy of the article by Yamaguti (1936).

Funding

This research was funded by Grant FONDECYT 1140173 and Grant 5303 “Programa Semilleros de Investigación” DGI—Universidad de Antofagasta. The Millennium Institute of Oceanography (IMO), IC120019 also provided support.

Compliance with ethical standards

Conflict of interest

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.

References

  1. Arai, H. P. (1971). Helminth parasites of embiotocid fishes II. A new species of Labrifer (Digenea: Lepocreadiidae) from Zalembius rosaceus from California. Journal of the Fisheries Research Board of Canada, 28, 767–769.CrossRefGoogle Scholar
  2. Blair, D., & Barker, S. C. (1993). Affinities of the Gyliauchenidae: utility of the 18S rRNA gene for phylogenetic inference in the Digenea (Platyhelminthes). International Journal for Parasitology, 23, 527–532.CrossRefPubMedGoogle Scholar
  3. Bray, R. A. (2005). Family Lepocreadiidae Odhner, 1905. In D. I. Gibson, A. Jones, & R. A. Bray (Eds) Keys to the Trematoda, Volume 2. Wallingford, UK: CAB International & The Natural History Museum, pp. 545–602.CrossRefGoogle Scholar
  4. Bray, R. A., & Cribb, T. H. (1989). Digeneans of the family Opecoelidae Ozaki, 1925 from the southern Great Barrier Reef, including a new genus and three new species. Journal of Natural History, 23, 429–473.CrossRefGoogle Scholar
  5. Bray, R. A., & Cribb, T. H. (2012). Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Systematic Parasitology, 83, 169–177.CrossRefPubMedGoogle Scholar
  6. Castro, R., & Baeza, H. (1981). Lepeophtheirus dissimulatus Wilson, 1905 and Lepeophtheirus zbigniewi new species (Copepoda: Caligidae) parasites of inshore fishes from the Pacific coast of Chile, South America. Bulletin of Marine Science, 3, 318–328.Google Scholar
  7. Castro, R., & Baeza, H. (1984). Lepeophtheirus frecuens new species and new record of Kroyerina meridionalis Ramírez, 1975 and new host record for Lepeophtheirus chilensis Wilson, 1905 (Copepoda: Siphonostomatoidae) parasitic on fishes of Chile, South America. Bulletin of Marine Science, 34, 197–206.Google Scholar
  8. Cribb, T. H., Bray, R. A., Littlewood, D. T. J., Pichelin, S., & Herniou, E. A. (2001). Relationships of the Digenea - evidence from molecules and morphology. In: Littlewood D. T. J. & R. A. Bray (Eds) Interrelationships of the Platyhelminthes. London: Taylor & Francis, 186–193.Google Scholar
  9. Filatov, D. A. (2002). Proseq : A software for preparation and evolutionary analysis of DNA sequence data sets. Molecular Ecology Notes, 2, 621–624.CrossRefGoogle Scholar
  10. Grove, J. S., & Lavenberg, R. J. (1997). The fishes of the Galápagos islands. Stanford, CA, USA: Stanford University Press, 912 pp.Google Scholar
  11. Hall, K. A., Cribb, T. H., & Barker, S. C. (1999). V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Systematic Parasitology, 43, 81–92.CrossRefPubMedGoogle Scholar
  12. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2. 0. Bioinformatics, 23, 2947–2948.CrossRefPubMedGoogle Scholar
  13. Lumb, S. M., Bray, R. A., & Rollinson, D. (1993). Partial small subunit (18S) rRNA gene sequences from fish parasites of the families Lepocreadiidae and Fellodistomidae (Digenea) and their use in phylogenetic analyses. Systematic Parasitology, 26, 141–149.CrossRefGoogle Scholar
  14. Luque, J. L., Pereira, F. B., Alves, P. V., Oliva, M. E., & Timi, J. T. (2017). Helminth parasites of South American fishes: current status and characterization as a model for studies of biodiversity. Journal of Helminthology, 91, 150–164.CrossRefPubMedGoogle Scholar
  15. Manter, H. W. (1940). Digenetic trematodes of fishes from the Galapagos Islands and the neighboring Pacific. Allan Hancock Pacific Expedition, 2, 329–497.Google Scholar
  16. Markowitz, K. N., Williams, J. D., & Krause, M. K. (2016). Development of quantitative PCR assay for detection of the trematode parasite Proctoeces maculatus in the blue mussel Mytilus edulis. Diseases of Aquatic Organisms, 122, 125–136.CrossRefPubMedGoogle Scholar
  17. Miller, S. A., Dykes, D. D., & Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research, 16, 1215.CrossRefPubMedCentralPubMedGoogle Scholar
  18. Miller, T. L., Bray, R. A., & Cribb, T. H. (2011). Taxonomic approaches to and interpretation of host specificity of trematodes of fishes: lessons from the Great Barrier Reef. Parasitology, 138, 1710–1722.CrossRefPubMedGoogle Scholar
  19. Montgomery, W. R. (1957). Studies on digenetic trematodes from marine fishes of La Jolla California. Transactions of the American Microscopical Society, 76, 3–36.CrossRefGoogle Scholar
  20. Muñoz, G., & Díaz, P. E. (2015). Checklist of parasites of labrid fishes (Pisces: Labridae). Viña del Mar, Chile: Editorial Universidad de Valparaíso, 89 pp.Google Scholar
  21. Muñoz, G., & Olmos, V. (2008). Revisión bibliográfica de especies endoparásitas y hospedadoras de sistemas acuáticos de Chile. Revista de Biologia Marina y Oceanografia, 43, 173–245.Google Scholar
  22. Muñoz, G., López, Z., & Cárdenas, L. (2012). Morphological and molecular analyses of larval trematodes in the intertidal bivalve Perumytilus purpuratus from central Chile. Journal of Helminthology, 87, 356–363.CrossRefPubMedGoogle Scholar
  23. Ñacari, L. A., & Oliva, M. E. (2016). Metazoan parasites of deep-sea fishes from the South Eastern Pacific: Exploring the role of ecology and host phylogeny. Deep Sea Research Part I: Oceanographic Research Papers, 115, 123–130.CrossRefGoogle Scholar
  24. Oliva, M. E., Valdivia, I. M., Chávez, R., Molina, H., & Cardenas, L. (2015). Molecular and morphological evidence demonstrating two species of Helicometrina Linton 1910 (Digenea: Opecoelidae) in northern Chile. Journal of Parasitology, 101, 694–700.CrossRefPubMedGoogle Scholar
  25. Oliva, M. E., Valdivia, I. M., Cárdenas, L., Muñoz, G., Escribano, R., & George-Nascimento, M. (2018). A new species of Proctoeces and reinstatement of Proctoeces humboldti George-Nascimento and Quiroga 1983 (Digenea: Fellodistomidae) based on molecular and morphological evidence. Parasitology International, 67, 159–169.CrossRefPubMedGoogle Scholar
  26. Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.CrossRefPubMedGoogle Scholar
  27. Poulin, R. (2014). Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology, 44, 581–589.CrossRefPubMedGoogle Scholar
  28. Pritchard, M. H. (1960). Preptetos caballeroi n. gen., n. sp. and Labrifer tertius n. sp. (Trematoda: Lepocreadiidae) from fishes of Hawaii. In: Libro Homenaje al Dr. Eduardo Caballero y Caballero, Jubileo 1930–1960. México: Secretaría de Educación Publica, Instituto Politécnico Nacional, pp. 245–251.Google Scholar
  29. Pritchard, M. H. (1970). Neolabrifer bravoae gen. nov. sp. nov. and Labrifer secundus Manter, 1940 (Trematoda: Lepocreadiidae) from the California sheephead in the American Pacific. Anales del Instituto de Biología Universidad Nacional Autónoma de México, Zoologia, 41, 127–134.Google Scholar
  30. Shen, J.-W. (1985). Digenetic trematodes of fishes from the Xisha Islands, II. Studia Marina Sinica, 24, 167–180. (In Chinese).Google Scholar
  31. 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.CrossRefPubMedCentralPubMedGoogle Scholar
  32. Valdivia, I. M., Cárdenas, L., González, K., Jofré, D., George-Nascimento, M., Guiñez, R., et al. (2010). Molecular evidence confirms that Proctoeces humboldti and Proctoeces chilensis (Digenea: Fellodistomidae) are the same species. Journal of Helminthology, 84, 341–347.CrossRefPubMedGoogle Scholar
  33. Wee, N. Q., Cribb, T. H., Bray, R. A., & Cutmore, S. C. (2017). Two known and one new species of Proctoeces from Australian teleosts: Variable host-specificity for closely related species identified through multi-locus molecular data. Parasitology International, 66, 16–26.CrossRefPubMedGoogle Scholar
  34. Yamaguti, S. (1936). Studies on the Helminth Fauna of Japan. Part 16. Trematodes of Fishes, III. Kyoto, Japan: Satyû Yamaguti. 6 pp.Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Programa de Doctorado en Ciencias Aplicadas, Mención Sistemas Marinos CosterosUniversidad de AntofagastaAntofagastaChile
  2. 2.Instituto Milenio de OceanografíaUniversidad de ConcepciónConcepciónChile
  3. 3.Instituto Ciencias Naturales Alexander von HumboldtUniversidad de AntofagastaAntofagastaChile
  4. 4.Life Sciences DivisionNatural History MuseumLondonUK

Personalised recommendations