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Integrative analysis of new Clinostomum metacercariae (Digenea, Clinostomidae) using COI mtDNA and morphology rises the number of lineages found in South American freshwater fishes

Published online by Cambridge University Press:  10 November 2023

M.M. Montes Open the ORCID record for M.M. Montes [Opens in a new window] ,
I. García Open the ORCID record for I. García [Opens in a new window] ,
J.M. Paredes del Puerto Open the ORCID record for J.M. Paredes del Puerto [Opens in a new window] ,
J.A. Barneche Open the ORCID record for J.A. Barneche [Opens in a new window] ,
M. Ibañez Shimabukuro Open the ORCID record for M. Ibañez Shimabukuro [Opens in a new window] ,
G.F. Reig Cardarella Open the ORCID record for G.F. Reig Cardarella [Opens in a new window] ,
S.R. Martorelli Open the ORCID record for S.R. Martorelli [Opens in a new window]  and
G. Pérez Ponce de León Open the ORCID record for G. Pérez Ponce de León [Opens in a new window]
M.M. Montes*
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), La Plata, Buenos Aires, Argentina
I. García
Affiliation:
Instituto de Limnología “Dr. Raúl A. Ringuelet”, CONICET, La Plata, Argentina
J.M. Paredes del Puerto
Affiliation:
Instituto de Limnología “Dr. Raúl A. Ringuelet”, CONICET, La Plata, Argentina
J.A. Barneche
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), La Plata, Buenos Aires, Argentina
M. Ibañez Shimabukuro
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), La Plata, Buenos Aires, Argentina
G.F. Reig Cardarella
Affiliation:
Escuela de Tecnología Médica y Centro Integrativo de Biología y Química Aplicada (CIBQA). Universidad Bernardo O’ Higgins, Santiago de Chile, Chile
S.R. Martorelli
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), La Plata, Buenos Aires, Argentina
G. Pérez Ponce de León
Affiliation:
Escuela Nacional de Estudios Superiores Unidad Mérida (ENES-Mérida), Universidad Nacional Autónoma de México, Mérida, Yucatán, Mexico
*
Corresponding author: M.M. Montes; Email: martinmiguelmontes@gmail.com
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Abstract

Clinostomidae is a diverse family of digenean parasitizing fish-eating birds as adults and fishes as metacercariae. The species composition, within the genus Clinostomum has been steadily increasing in recent years. In Argentina, four named species of Clinostomum have been documented, accompanied by four metacercariae representing distinct genetic lineages whose adults have not been identified. This study focused on examining clinostomids in three fish species – Australoheros scitulus (ASI), Cichlasoma dimerus (CDIM), and Pimelodella laticeps (PLA) – at various localities in Argentina. We conducted both morphological and molecular characterizations of the Clinostomum metacercariae collected from these fish species. Molecular phylogenetic analyses using COI mtDNA were performed to determine the placement of these metacercariae within the clinostomid phylogenetic tree. Clinostomum ASC represents a distinct lineage, morphologically distinguishable from other sequenced metacercariae due to its body shape (widest anteriorly and becoming slender towards the posterior end); this lineage was found to be closely related to C. caffarae. While Clinostomum CDIM and Clinostomum PLA exhibited morphological differences, they clustered together genetically with metacercariae reported in previous studies as Clinostomum L3 and Clinostomum CVI. This outcome, coupled with a low genetic distance (0 to 3%), suggests that they are conspecific with metacercariae found in fish across Mexico, Costa Rica, and Argentina. In light of the extensive diversity of fish species in Argentine freshwater ecosystems (over 500 species), and considering the relatively constrained extent of prior investigations, the anticipation of unearthing additional Clinostomum species or lineages is plausible.

Keywords

New speciesintegrative taxonomyCOIArgentinaArdea cocoi
Type
Research Paper
Information
Journal of Helminthology , Volume 97 , 2023 , e85
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Boero, J.J. and Led, J.E. (1971) El parasitismo de la fauna autóctona. V Los parásitos de las aves argentinas. VI Los parásitos de los ofidios argentinos. VII Los parásitos de los murciélagos argentinos [The parasitism of autochthonous fauna. V Parasites of Argentine birds. VI Parasites of Argentine snakes. VII Parasites of Argentine bats]. Analecta Veterinaria 3, 91–103.Google Scholar
Briosio-Aguilar, R., Pinto, H.A., Rodríguez-Santiago, M.A., López-García, K., García-Varela, M. & Pérez Ponce de León, G. (2018) Link between the adult and the metacercaria of Clinostomum heluans Braun, 1899 (Trematoda: Clinostomidae) through DNA sequences, and its phylogenetic position within the genus Clinostomum Leidy, 1856. Journal of Parasitology 104, 292–296.CrossRefGoogle ScholarPubMed
Caffara, M., Bruni, G., Paoletti, C., Gustinelli, A. and Fioravanti, M.L. (2014) Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). Journal of Helminthology 88, 278–285.CrossRefGoogle ScholarPubMed
Caffara, M., Locke, S.A., Cristanini, C., Davidovich, N. & Markovich, M.P. (2016) A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). Journal of Parasitology 102, 239–248.CrossRefGoogle ScholarPubMed
Caffara, M., Locke, S.A., Echi, P.C., Halajian, A., Benini, D., Luus Powell, W.J., Tavakol, S. & Fioravanti, M.L. (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae. Parasitology 144, 1519–1529.CrossRefGoogle ScholarPubMed
Caffara, M., Locke, S.A., Echi, P.C., Halajian, A., Luus-Powell, W.J., Benini, D., Tedesco, P. & Fioravanti, M.L. (2020) A new species of Clinostomum Leidy, 1856 based on molecular and morphological analysis of metacercariae from African siluriform fishes. Parasitology Research 119, 885–892.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Caffara, M., Locke, S.A., Halajian, A., Luus-Powell, W.J., Benini, D., Tedesco, P., Kasembele, G.K. & Fioravanti, M.L. (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, 1–9.CrossRefGoogle Scholar
Cosby, G.T. (1972) Spread of the cattle egret in the western hemisfere. Bird Band 43, 205–211.CrossRefGoogle Scholar
Davies, D., Ostrowski de Nuñez, M., Ramallo, G. & Nieva, L. (2016) Nuevos hospedadores y localidades de colecta de Clinostomum sp (Strigeida: Clinostomidae). Acta Zoologica Liloana 60, 89–94.Google Scholar
Downs, W.G. (1959) Little Egret banded in Spain taken in Trinidad. Auk 76, 241–242.CrossRefGoogle Scholar
Hara, H., Miyauchi, Y., Tahara, S., Yamashita, H. & Nagoya, J. (2014) Human laryngitis caused by Clinostomum complanatum. Nagoya journal of medical science 76, 181–185.Google ScholarPubMed
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. CABI Publising and the Natural History Museum, London, pp 113–120.CrossRefGoogle Scholar
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular biology and evolution 30, 286–298.CrossRefGoogle ScholarPubMed
Kim, H., Cho, S-W, Oh, H. & Byeon, H.K. (2019) A case of unexpected Clinostomum complanatum infection initially presenting as foreign body in pharynx. Korean Journal of Parasitology 57, 175–177.CrossRefGoogle ScholarPubMed
Kifune, T., Ogata, M. & Miyahara, M. (2000) The first case of human infection with Clinostomum (Trematoda: Clinostomidae) in Yamaguchi Prefecture, Japan. Medicine Bulletin of Fukuoka University 27, 101–105 (In Japanese).Google Scholar
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular biology and evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Lanfear, R., Calcott, B., Ho, S. & Guindon, S. (2012) Partition finder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular biology and evolution 29, 1695–1701.CrossRefGoogle Scholar
Lee, G.S., Park, S.W., Kim, J., Seo, K.S., You, K.W., Chung, J.H., Moon, H.C. & Hong, G.Y. (2017) A case of endoscopically treated laryngopharyngitis resulting from Clinostomum complanatum infection. Korean Journal of Gastroenterology 69, 177–180.CrossRefGoogle ScholarPubMed
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
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
Montes, M.M., Plaul, S.E., Croci, Y., Waldbillig, M., Ferrari, W., Topa, E. & Martorelli, S.R. (2020) Pathology associated with three new Clinostomum metacercariae from Argentina with morphological and DNA barcode identification. Journal of Helminthology 94, e148:1–11.CrossRefGoogle ScholarPubMed
Montes, M.M., Barneche, J., Pagano, L., Ferrari, W., Martorelli, S.R. & Pérez Ponce de León, G. (2021) Molecular data reveal hidden diversity of the genus Clinostomum (Digenea, Clinostomidae) in Argentina, with the description of a new species from Ardea cocoi (Ardeidae). Parasitology Research 120, 2779–2791.CrossRefGoogle ScholarPubMed
Mirande, J.M. & Koerber, S. (2020) Checklist of the Freshwater fishes of Argentina 2nd edition (CLOFFAR-2). Ichtyological Contribution of Peces Criollos 72, 1–81.Google Scholar
Murrieta-Morey, G.A., Tuesta Rojas, C.A., Echevarria-Matos, A.M. & Chuquipiondo-Guardia, C.T. (2022) Metacercaria de Clinostomum sp. (trematoda: clinostomidae) infestando a cíclidos cultivados ornamentales en la amazonía peruana. Neotropical Helminthology 16, 49–56.Google Scholar
Park, C-W, Kim, J-S, Joo, H-S & Kim, J. (2009) A human case of Clinostomum complanatum infection in Korea. Korean Journal of Parasitology 47, 401–404.CrossRefGoogle ScholarPubMed
Pérez Ponce de León, G., García-Varela, M., Pinacho-Pinacho, C.D., Sereno-Uribe, A.L. & Poulin, R. (2016) Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.CrossRefGoogle ScholarPubMed
Pinto, H.A., Caffara, M., Fioravanti, M.L. & Melo, A.L. (2015) Experimental and molecular study of cercariae of Clinostomum sp. (Trematoda: Clinostomidae) from Biomphalaria spp (Mollusca: Planorbidae) in Brazil. Journal of Parasitology 101, 108–113.CrossRefGoogle ScholarPubMed
Pritchard, M.H. & Kruse, G.O.W. (1982) The collection and preservation of animal parasites. University of Nebraska Press, Nebraska.Google Scholar
Ronquist, F., Teslenkovan, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 32: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rosser, T.G., Baumgartner, W.A., Alberson, N.R., Noto, T.W., Woodyard, E.T., King, D.T., Wise, D.J. & Griffin, M.J. (2018) Clinostomum poteae n. sp. (Digenea: Clinostomidae), in the trachea of a double-crested cormorant Phalacrocorax auritus Lesson, 1831 and molecular data linking the lifecycle stages of Clinostomum album Rosser, Alberson, Woodyard, Cunningham, Pote & Griffin, 2017 in Mississippi, USA. Systematic Parasitology 95, 543–566.CrossRefGoogle Scholar
Rosser, T.G., Woodyard, E.T., Mychajlonka, M.N., King, D.T., Griffin, M.J., Gunn, M.A. & López-Porras, A. (2020). Ithyoclinostomum yamagutii n. sp. (Digenea: Clinostomidae) in the great blue heron Ardea herodias L. (Aves: Ardeidae) from Mississippi, USA. Systematic parasitology 97, 69–82.CrossRefGoogle Scholar
Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle ScholarPubMed
Sereno-Uribe, A.L., Garcia-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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sutton, C.A. & Damborenea, M.C. (2000) Colección Helmintológica del Museo de La Plata: I. Catálogo de preparaciones microscópicas, material tipo y no tipo. Serie Técnica y Didáctica del Museo de La Plata 35, 1–20.Google Scholar
Szidat, L. (1969) Structure, development, and behavior of new strigeatoid meatcercariae from subtropical fishes of South America. Journal of Fisheries Research 26, 753–786.Google Scholar
Van Steenkiste, N., Locke, S.A., Castelin, M., Marcogliese, D.J. & Abbott, C.L. (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular biology and evolution 15, 942–952.Google ScholarPubMed
Weyenbergh, H. (1878). Description détaillée d’une nouvelle espèce de la Famille des Distomides, savoir Distoma pulcherrimum. Periodico Zoologico 3, 31–38.Google Scholar
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.CrossRefGoogle ScholarPubMed
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