Ithyoclinostomum yamagutii n. sp. (Digenea: Clinostomidae) in the great blue heron Ardea herodias L. (Aves: Ardeidae) from Mississippi, USA

  • Thomas G. RosserEmail author
  • Ethan T. Woodyard
  • Meisha N. Mychajlonka
  • D. Tommy King
  • Matt J. Griffin
  • Mackenzie A. Gunn
  • Adrián López-Porras
Part of the following topical collections:
  1. Digenea


With only six recognised genera, the family Clinostomidae Lühe, 1901 remains a global research interest of parasitologists and ecologists. Recent efforts have focused on providing molecular data to investigate species diversity, elucidate life-cycles, and make inferences on the group’s evolutionary history. Of the clinostomid genera, the monotypic Ithyoclinostomum Witenberg, 1926 has remained more enigmatic compared to the commonly encountered Clinostomum Leidy, 1856. Recent morphological and molecular evidence from metacercariae suggests a second Ithyoclinostomum species may exist in freshwater cichlids in Central America and Mexico. In a recent survey of great blue herons Ardea herodias L. from commercial catfish production farms in Mississippi, USA, two specimens of an abnormally large (> 20 mm) clinostomid were encountered in the oesophagus of a single bird. These specimens were identified as an Ithyoclinostomum sp. morphologically distinct from the only nominal species Ithyoclinostomum dimorphum (Diesing, 1850). Using morphological and molecular data these adult specimens were confirmed as conspecific with the larval metacercariae previously described from Central America and Mexico and represent the novel species, Ithyoclinostomum yamagutii n. sp.



We would like to thank Stephen Clements, Katie Hanson-Dorr, Lanna Durst, and Raleigh Middleton for their assistance in collecting herons for this study.


This work was supported by the Mississippi State University College of Veterinary Medicine, Office of Research and Graduate Studies Internal Grants Programme and United States Department of Agriculture.

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 (IACUC QA 2853).


  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology,215, 403–410.PubMedCrossRefGoogle Scholar
  2. Aguirre-Macedo, M. L., Scholz, T., González-Solís, D., Vidal-Martínez, V. M., Posel, P., Arjona-Torres, G., et al. (2001). Larval helminths parasitizing freshwater fishes from the Atlantic coast of Nicaragua. Comparative Parasitology,68, 42–51.Google Scholar
  3. Baer, J. G. (1933). Note sur un nouveau trématode, Clinostomum lophophallum sp. nov., avec quelques considerations générales sur la famille des Clinostmoidae. Revue Suisse de Zoologie,40, 317–342.CrossRefGoogle Scholar
  4. Belei, F., Ferreira, S. R., Perin, L. M., Braga, F. R., Sampaio, W. M. S., de Araújo, J. V., et al. (2013). First report of Austrodiplostomum compactum and Ithyoclinostomum dimorphum in trahira (Hoplias malabaricus) from the middle course of the Rio Doce, Minas Gerais, Brazil. Arquivos do Instituto de Biologia,80, 249–252.CrossRefGoogle Scholar
  5. Bengtsson-Palme, J., Ryberg, M., Hartmann, M., Branco, S., Wang, Z., Godhe, A., et al. (2013). Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution,4, 914–919.Google Scholar
  6. Benigno, R. N. M., Knoff, M., Matos, E. R., Gomes, D. C., Pinto, R. M., & Clemente, S. C. S. (2014). Morphological aspects of Clinostomidae metacercariae (Trematoda: Digenea) in Hoplerytrinus unitaeniatus and Hoplias malabaricus (Pisces: Erythrinidae) of the Neotropical region, Brazil. Anais da Academia Brasileira de Ciências,86, 733–744.PubMedCrossRefGoogle Scholar
  7. Braun, M. (1899). Üeber Clinostomum Leidy. Zoologischer Anzeiger,22, 484–493.Google Scholar
  8. Braun, M. (1901). Die Arten der Gattung Clinostomum Leidy. Zoologische Jahrbücher. Abteilung für Systematik Ökologie und Geographie der Tiere,14, 1–48.Google Scholar
  9. Briosio-Aguilar, R., García-Varela, M., Hernández-Mena, D. I., Rubio-Godoy, M., & Pérez-Ponce de León, G. (2018). Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body cavity of freshwater fishes (Cichlidae) across Middle America. Journal of Helminthology,93, 461–474.PubMedCrossRefGoogle Scholar
  10. Caffara, M., Locke, S. A., Cristanini, C., Davidovich, N., Markovich, M. P., & Fioravanti, M. L. (2016). A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). Journal of Parasitology,102, 239–248.PubMedCrossRefGoogle Scholar
  11. Caffara, M., Locke, S. A., Gustinelli, A., Marcogliese, D. J., & Fioravanti, M. L. (2011). Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. Journal of Parasitology,97, 884–891.PubMedCrossRefGoogle Scholar
  12. Caffara, M., Locke, S. A., Halajian, A., Luus-Powell, W. J., Benini, D., Tedesco, P., et al. (2019). Molecular data show Clinostomoides Dollfus, 1950 is a junior synonym of Clinostomum Leidy, 1856, with redescription of metacercariae of Clinostomum brieni n. comb. Parasitology,146, 805–813.PubMedCrossRefGoogle Scholar
  13. Chagas de Souza, D. C., Correa, L. L., & Tavares-Dias, M. (2018). Ithyoclinostomum dimorphum Diesing, 1850 (Digenea, Clinostomidae) in Hoplias malabaricus (Erythrinidae) with the first report of infection of the eyes. Helminthologia,55, 343–349.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Costa, D. P. C., Monteiro, C. M., & Brasil-Sato, M. C. (2015). Digenea of Hoplias intermedius and Hoplias malabaricus (Actinopterygii, Erythrinidae) from upper São Francisco River, Brazil. Revista Brasileira de Parasitología Veterinária,24, 129–135.PubMedCrossRefGoogle Scholar
  15. Delgado, A. E., Tantalean, M. V., Martínez, R. R., & Mondragón, A. M. (2017). Trematodos en Hoplerythrinus unitaeniatus (Erythrinidae) <<Shuyo>> and Pterodoras granulosus (Doradidae) <<Cahuara>> in Yurimaguas, Loreto, Peru. Revista de Investigación Veterinaria Perú,28, 461–467.CrossRefGoogle Scholar
  16. Dias, M. L. G. G., Santos, M. J., Souza, G. T. R., Machado, M. H., & Pavanelli, G. C. (2003). Scanning electron microscopy of Ithyoclinostomum dimorphum (Trematoda: Clinostomidae), a parasite of Ardea cocoi (Aves: Ardeidae). Parasitology Research,90, 355–358.PubMedCrossRefGoogle Scholar
  17. Diesing, K. M. (1850). Systema helminthum, Volume 1. Vindobonae: Braumüller, 679 pp.Google Scholar
  18. Edney, J. M. (1950). Productivity in Clinostomum marginatum (Trematoda: Clinostomatidae). Transactions of the American Microscopical Society,69, 186–188.CrossRefGoogle Scholar
  19. Gallio, M., da Silva, A. S., Soares, J. F., da Silva, M. K., Salomão, E. L., & Monteiro, S. G. (2007). Ocorrência de metacercárias de Ithyoclinostomum dimorphum em traíras no Rio Grande do Sul, Brasil: relato de caso. Estudos de Biología,29, 337–339.Google Scholar
  20. Gustinelli, A., Caffara, M., Florio, D., Otachi, E. O., Wathuta, E. M., & Fioravanti, M. L. (2010). First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya. Systematic Parasitology,76, 39–51.PubMedCrossRefGoogle Scholar
  21. Hunter, G. W., & Hunter, W. S. (1934). The life cycle of the yellow grub of fish. Journal of Parasitology,20, 325.Google Scholar
  22. Jhansilakshmibai, K., & Madhavi, R. (1997). Euclinostomum heterostomum (Rudolphi, 1809) (Trematoda): Life-cycle, growth and development of the metacercaria and adult. Systematic Parasitology,38, 51–64.CrossRefGoogle Scholar
  23. Kanev, I., Radev, V., & Fried, B. (2002). Family Clinostomidae Lühe, 1901. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds), Keys to the Trematoda, Vol. 1 (pp. 113–120). Wallingford, UK: CAB International.CrossRefGoogle Scholar
  24. Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research,30, 3059–3066.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution,30, 772–780.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution,33, 1870–1874.PubMedCrossRefGoogle Scholar
  27. Lent, H., & Freitas, J. F. T. (1937). Pesquisas helminológicas realizadas no Estado do Pará. I. Trematoda. Memórias do Instituto Oswaldo Cruz,32, 449–460.CrossRefGoogle Scholar
  28. Locke, S. A., Caffara, M., Marcogliese, D. J., & Fioravanti, M. L. (2015). A large-scale molecular survey of Clinostomum (Digenea, Clinostomidae). Zoologica Scripta,44, 203–217.CrossRefGoogle Scholar
  29. Lunaschi, L. I., & Drago, F. B. (2009). Digenean parasites of six species of birds from Formosa Province, Argentina. Revista Mexicana de Biodiversidad,80, 39–46.CrossRefGoogle Scholar
  30. Machado, M. H., Pavanelli, G. C., & Takemoto, R. M. (1996). Structure and diversity of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Memórias do Instituto Oswaldo Cruz,91, 441–448.PubMedCrossRefGoogle Scholar
  31. Minh, B. Q., Nguyen, M. A. T., & von Haeseler, A. (2013). Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution,30, 1188–1195.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.Google Scholar
  33. Nguyen, L., Schmidt, H. A., von Haesler, A., & Minh, B. Q. (2015). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution,32, 268–274.PubMedCrossRefGoogle Scholar
  34. Overstreet, R. M., & Curran, S. S. (2004). Defeating diplostomoid dangers in USA catfish aquaculture. Folia Parasitologica,51, 153–165.PubMedCrossRefGoogle Scholar
  35. Pérez-Ponce de León, G., García-Varela, M., Pinacho-Pinacho, C. D., Sereno-Uribe, A., & Poulin, R. (2016). Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology,143, 1773–1789.PubMedCrossRefGoogle Scholar
  36. Pinto, R. M., Barros, L. A., Tortelly, L., Teixeira, R. F., & Gomes, D. C. (2004). Prevalence and pathology of helminths of ciconiiform birds from the Brazilian swamplands. Journal of Helminthology, 78, 259–264.PubMedCrossRefGoogle Scholar
  37. Pritchard, M. H., & Kruse, G. O. W. (1982). The collection and preservation of animal parasites. Lincoln: University of Nebraska Press, 141 pp.Google Scholar
  38. Rambaut, A. (2014). FigTree: Tree figure drawing tool v. 1.4.2. Institute of Evolutionary Biology, University of Edinburgh. Retrieved from
  39. Reis, T. S. (2014). Caracterização morfológica e molecular de endoparasitoss de Hoplias affinis malabaricus Bloch, 1794 (Characiformes: Erythrinidae) provenientes do Rio Araguaia, Tocantins, Brasil. PhD dissertation, Universidade Feral do Tocantins, Brazil.Google Scholar
  40. Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics,19, 1571–1574.CrossRefGoogle Scholar
  41. Rosser, T. G., Alberson, N. R., Woodyard, E. T., Cunningham, F. L., Pote, L. M., & Griffin, M. J. (2017). Clinostomum album n. sp. and Clinostomum marginatum (Rudolphi, 1819), parasites of the great egret Ardea alba L. from Mississippi, USA. Systematic Parasitology,94, 35–49.PubMedCrossRefPubMedCentralGoogle Scholar
  42. Rosser, T. G., Baumgartner, W. A., Alberson, N. R., Noto, T. W., Woodyard, E. T., King, D. T., et al. (2018). Clinostomum poteae n. sp. (Digenea: Clinostomidae), in the trachea of a double-crested cormorant Phalacrocorax auritus Lesson, 1831 and molecular data linking the life-cycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Systematic Parasitology,95, 543–566.PubMedCrossRefGoogle Scholar
  43. Sereno-Uribe, A. L., García-Varela, M., Pinacho-Pinacho, C. D., & Pérez-Ponce de León, G. (2018). Three new species of Clinostomum Leidy, 1856 (Trematoda) from Middle American fish-eating birds. Parasitology Research,117, 2171–2185.PubMedCrossRefGoogle Scholar
  44. Sereno-Uribe, A. L., Pinacho-Pinacho, C. D., García-Varela, M., & Pérez-Ponce de León, G. (2013). Using mitochondrial and ribosomal DNA sequences to test the taxonomic validity of Clinostomum complanatum Rudolphi, 1814 in fish-eating birds and freshwater fishes in Mexico, with the description of a new species. Parasitology Research,112, 2855–2870.PubMedCrossRefGoogle Scholar
  45. Skrjabin, K. I. (1947) Family Clinostomatidae Lühe, 1901. In Trematodes of animals and man: Basic trematodology, Volume 1, 1st edn. Moscow: Academy of Sciences of the USSR, pp. 64–97.Google Scholar
  46. Szidat, L. (1969). Structure, development, and behavior of new strigeatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada,26, 753–786.CrossRefGoogle Scholar
  47. Travassos, L., Freitas, J. T., & Kohn, A. (1969). Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz,67, 1–886.PubMedGoogle Scholar
  48. Trifinopoulos, J., Nguyen, L. T., von Haesler, A., & Minh, B. Q. (2016). W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research,44(W1), W232–W235.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Weiblen, A. M., & Brandão, D. A. (1992). Levantamento parasitológico em Hoplias malabaricus Bloch (1794) (traíra) de águas da região de Santa Maria-RS. Ciência Rural,22, 203–208.CrossRefGoogle Scholar
  50. Witenberg, G. G. (1926). Versuch einer Monographie der Trematodenunterfamilie Harmostominae Braun. Zoologische Jahrbücher. Abteilung für Systematic, Ökologie und Geographie der Tiere,51, 167–254.Google Scholar
  51. Woodyard, E. T., Rosser, T. G., & Rush, S. A. (2017). Alligator wrestling: Morphological, molecular, and phylogenetic data on Odhneriotrema incommodum (Leidy, 1856) (Digenea: Clinostomidae) from Alligator mississippiensis Daudin, 1801 in Mississippi, USA. Parasitology Research,116, 2981–2993.PubMedCrossRefGoogle Scholar
  52. Yamaguti, S. (1958). Systema helminthum. Volume I. The digenetic trematodes of vertebrates. New York: Interscience, 1575 pp.Google Scholar
  53. Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Volume 1. Tokyo, Japan: Keigaku Publishing Co, 1074 pp.Google Scholar

Copyright information

© Springer Nature B.V. 2020

Authors and Affiliations

  1. 1.Department of Basic Sciences, College of Veterinary MedicineMississippi State UniversityMississippi StateUSA
  2. 2.Department of Pathobiology and Population Medicine, College of Veterinary MedicineMississippi State UniversityMississippi StateUSA
  3. 3.Mississippi Field Station, National Wildlife Research Center, Wildlife ServicesUnited States Department of AgricultureMississippi StateUSA
  4. 4.Thad Cochran National Warmwater Aquaculture Center, Aquatic Research & Diagnostic Laboratory, College of Veterinary Medicine, Delta Research and Extension CenterMississippi State UniversityStonevilleUSA
  5. 5.Department of Wildlife, Fisheries and Aquaculture, College of Forest ResourcesMississippi State UniversityMississippi StateUSA

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