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Pathology associated with three new Clinostomum metacercariae from Argentina with morphological and DNA barcode identification

Published online by Cambridge University Press:  04 May 2020

M.M. Montes Open the ORCID record for M.M. Montes [Opens in a new window] ,
S.E. Plaul Open the ORCID record for S.E. Plaul [Opens in a new window] ,
Y. Croci Open the ORCID record for Y. Croci [Opens in a new window] ,
M. Waldbillig ,
W. Ferrari Open the ORCID record for W. Ferrari [Opens in a new window] ,
E. Topa Open the ORCID record for E. Topa [Opens in a new window]  and
S.R. Martorelli Open the ORCID record for S.R. Martorelli [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), calle 120 s/n e/60 y 64, 1900, La Plata, Buenos Aires, Argentina
S.E. Plaul*
Affiliation:
Laboratorio de Histología y Embriología Descriptiva, Experimental y Comparada, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Av. 60 y 118 s/n., La Plata, Buenos Aires, Argentina
Y. Croci
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), calle 120 s/n e/60 y 64, 1900, La Plata, Buenos Aires, Argentina
M. Waldbillig
Affiliation:
Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Av. 60 y 120 s/n, La Plata, Buenos Aires, Argentina
W. Ferrari
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), calle 120 s/n e/60 y 64, 1900, La Plata, Buenos Aires, Argentina
E. Topa
Affiliation:
Centro de Estudios Parasitológicos y Vectores (CEPAVE), Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de La Plata (CCT, CONICET-UNLP), calle 120 s/n e/60 y 64, 1900, La Plata, Buenos Aires, Argentina
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), calle 120 s/n e/60 y 64, 1900, La Plata, Buenos Aires, Argentina
*
Author for correspondence: S.E. Plaul, E-mail: [email protected]
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Abstract

In the Laboratory of Parasites of Fishes, Crustaceans and Mollusks (CEPAVE), we undertook a parasitological study on three species of fish from the Espinal and Esteros del Iberá ecoregions of Argentina. Clinostomid metacercariae were found parasitizing Characidium rachovii, Crenicichla vittata and Gymnogeophagus balzanii. In this study, we analysed the damage that these parasites inflict on their hosts through the evaluation of histological sections. In addition, Clinostomum metacercariae were identified using morphological characters and DNA barcoding. In the pathological analysis, we observed that muscle tissue was the most affected. The inflammatory response showed vascular congestion areas and infiltration of numerous inflammatory cells, mainly lymphocytes. The molecular and morphological approach supports the presence of three new lineages of clinostomid metacercariae in Argentina. This could lead to the discovery of a high number of lineages or species of Clinostomum from South America.

Keywords

ClinostomidsCOICichlidsCrenuchiidae
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e148
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Acosta, AA, Caffara, M, Fioravanti, ML, Utsunomia, R, Zago, AC, Franceschini, L and da Silva, RJ (2016) Morphological and molecular characterization of Clinostomum detruncatum (Trematoda: Clinostomidae) metacercaria infecting Synbranchus marmoratus. Journal of Parasitology 102, 151–156.CrossRefGoogle ScholarPubMed
Adeyemo, AO and Agbede, SA (2008) Histopathology of tilapia tissues harbouring Clinostomum tilapie parasites. African Journal of Biomedical Research 11, 115–118.Google Scholar
Bastos, RF, Miranda, SF and Garcia, AM (2013) Dieta e estratégia alimentar de Characidium rachovii (Characiformes, Crenuchidae) em riachos de planície costeira do sul do Brasil. Iheringia Serie Zoology 103, 335–341.CrossRefGoogle Scholar
Boero, JJ and Led, JE (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
Bonetto, AA, Roldán, D and Oliver, ME (1978) Estudios limnológicos en la cuenca del Riachuelo (Corrientes, Argentina) I: Poblaciones de peces en ambientes leníticos y lóticos. Ecosur 5, 1–15.Google Scholar
Briosio-Aguilar, R, Pinto, HA, Rodríguez-Santiago, MA, López-García, K, García-Varela, M and 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
Bullard, SA and Overstreet, RM (2008) Chapter 14 Digeneans as enemies of fishes. pp. 815–974in Eiras, J, Segner, H, Wahil, T and Kapoor, BG (Eds) Fish diseases. Enfield, New Hampshire Science Publishers.Google Scholar
Caffara, M, Locke, SA, Gustinelli, A, Marcogliese, DJ and Fioravanti, ML (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, Bruni, G, Paoletti, C, Gustinelli, A and Fioravanti, ML (2014a) Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). Journal of Helminthology 88, 278–285.CrossRefGoogle Scholar
Caffara, M, Davidovich, N, Falk, R, Smirnov, M, Ofek, T, Cummings, D, Gustinelli, A and Fioravanti, ML (2014b) Redescription of Clinostomum phalacrocoracis metacercariae (Digenea: Clinostomidae) in cichlids from Lake Kinneret, Israel. Parasite 21, 1–5.CrossRefGoogle Scholar
Caffara, M, Locke, SA, Echi, PC, Halajian, A, Benini, D, Luus Powell, WJ, Tavakol, S and Fioravanti, ML (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae. Parasitology 144, 1519–1529.CrossRefGoogle ScholarPubMed
Casciotta, J and Gomez, SE (2000) Gymnogephagus che, una nueva especie de la familia Cichlidae de la cuenca del río Paraná (Perciformes, Labroidei). Revista del Museo Argentino de Ciencias Naturales 2, 53–59.CrossRefGoogle Scholar
Casciotta, J, Almirón, A and Bechara, J (2005) Peces del Iberá. Hábitat y diversidad. 1st. Edition. Corrientes, Argentina, Fundación Ecos, pp. 244. ISBN 987-05-0375-6.Google Scholar
Davies, D, Ostrowski de Nuñez, M, Ramallo, G and Nieva, L (2016) Nuevos hospedadores y localidades de colecta de Clinostomum sp. (Strigeida: Clinostomidae). Acta Zoology Liloana 60, 89–94.Google Scholar
Dias, MLGG, Eiras, JC, Machado, MH, Souza, GTR and Pavanelli, GC (2003) The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná River, Brazil. Parasitology Research 89, 506–508.CrossRefGoogle ScholarPubMed
Ferguson, HW (1989) Systemic pathology of fish a text an atlas of comparative tissue reponses in diseases of teleosts. 1st edn.263 pp. Iowa, State University Press.Google Scholar
Gustinelli, A, Caffara, M, Florio, D, Otachi, EO, Wathuta, EM and Fioravanti, ML (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.CrossRefGoogle Scholar
Hara, H, Miyauchi, Y, Tahara, S, Yamashita, H and Nagoya, J (2014) Human laryngitis caused by Clinostomum complanatum. Medical Science 76, 181–185.Google ScholarPubMed
Ibarra-Polesel, MG and Poi, ASG (2016) Alimentacion de Characidium rachovii (Characiformes: Crenuchidae) y Pyrrhulina australis (Characiromes: Lebiasinidae) en lagunas someras de la provincia de Corrientes, Argentina. Revista de Biología Tropical (International Journal of Tropical Biology) 64, 603–615.CrossRefGoogle Scholar
Kalantan, AMN, Arfin, M and Nizami, WA (1987) Seasonal incidence and pathogenicity of the metacercariae of Clinostomum complanatum in Aphanius dispar Jpn. Journal of Parasitology 36, 17–23.Google Scholar
Kanev, I, Radev, V and Fried, B (2002) Family Clinostomidae Lühe, 1901. pp. 113–120in Gibson, DI, Jones, A, and Bray, RA (Eds) Keys to the Trematoda. London, CABI Publishing and The Natural History Museum.CrossRefGoogle Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology Evolution 30, 286–298.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kim, H, Cho, S-W, Oh, H and Byeon, HK (2019) A case of unexpected Clinostomum complanatum infection initially presenting as foreign body in pharynx. Korean Journal of Parasitology 57, 175–177.CrossRefGoogle ScholarPubMed
Kimura, M (1981) Estimation of evolutionary sequences between homologous nucleotide sequences. Proceedings of the National Academic of Science USA 78, 454–458.CrossRefGoogle ScholarPubMed
Lanfear, R, Calcott, B, Ho, S and Guindon, S (2012) Partition finder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology Evolution 29, 1695–1701.CrossRefGoogle Scholar
Lee, GS, Park, SW, Kim, J, Seo, KS, You, KW, Chung, JH, Moon, HC and Hong, GY (2017) A case of endoscopically treated laryngopharyngitis resulting from Clinostomum complanatum infection. Korean Journal of Gastroenterology 69, 177–180.CrossRefGoogle ScholarPubMed
Lemke, LB, Dronen, N, Fox, JG and Nambiar, PR (2008) Infestation of wild-caught American bullfrogs (Rana catesbeiana) by multiple species of metazoan parasites. Journal of the American Association for Laboratory Animal Science 47, 42–46.Google ScholarPubMed
Locke, SA, Caffara, M, Marcogliese, DJ and Fioravanti, ML (2015) A large-scale molecular survey of Clinostomum (Digenea: Clinostomidae). Zoologica Scripta 44, 203–217.CrossRefGoogle Scholar
Locke, SA, Caffara, M, Barčák, D, Sonko, P, Tedesco, P, Fioravanti, ML and Li, W (2019) A new species of Clinostomum Leidy, 1856 in East Asia based on genomic and morphological data. Parasitology Research 118, 3253–3265.CrossRefGoogle ScholarPubMed
Lucena, CAS and Kullander, SO (1992) The Crenicichla (Teleostei: Cichlidae) species of the Uruguai River drainage in Brazil. Ichthyological Exploration of Freshwater 3, 97–160.Google Scholar
Lunaschi, LI and Drago, FB (2009) Digenean parasites of six species of birds from Formosa Province, Argentina. Revista Mexicana de Biodiversidad 80, 39–46.CrossRefGoogle Scholar
Lunaschi, LI, Cremonte, F and Drago, FB (2007) Checklist of digenean parasites of birds from Argentina. Zootaxa 1403, 1–36.CrossRefGoogle Scholar
Matthews, D and Cribb, TH (1998) Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Systematic Parasitology 39, 199–208.CrossRefGoogle Scholar
McAllister, CT (1990) Metacercaria of Clinostomum complanatum (Rudolphi, 1814) (Trematoda: Digenea) in a Texas Salamander, Eurycea neotenes (Amphibia: Caudata), with Comments on C. marginatum (Rudolphi, 1819). Journal of Helminthological Society of Washington 57, 69–71.Google Scholar
Morais, AM, Varella, AMB, Fernandes, BMM and Malta, JCO (2011) Clinostomum marginatum (Braun, 1899) and Austrodiplostomum compactum (Lutz, 1928) metacercariae with zoonotic potential on Pygocentrus nattereri (Kner, 1858) (Characiformes: Serrasalmidae) from Central Amazon, Brazil. Neotropical Helminthology 5, 8–15.Google Scholar
Nei, M and Kumar, S (2000) Molecular evolution and phylogenetics. 333 pp. New York, Oxford University Press.Google Scholar
Nickum, JG, Bart, HL, Bowser, PR, et al. (2004) Guidelines for the use of fishes in research Bethesda. 48 pp. Kansas, American Fisheries Society.Google Scholar
Novakowski, GC, Cassemiro, FAS and Hahn, NS (2016) Diet an ecomorphological relationship of four cichlid species from Cuaiaba River basin. Neotropical Ichthyology 14, e150151.CrossRefGoogle Scholar
Park, C-W, Kim, J-S, Joo, H-S and 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 Prieto, L and Mendoza-Garfías, B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1–247.CrossRefGoogle Scholar
Pérez-Ponce de León, G, García-Varela, M, Pinacho-Pinacho, CD, Sereno-Uribe, AL and Poulin, R (2016) Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.CrossRefGoogle ScholarPubMed
Pinto, HA, Caffara, M, Fioravanti, ML and Melo, AL (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, MH and Kruse, GOW (1982) The collection and preservation of animal parasites. 141 pp. Nebraska, University of Nebraska Press.Google Scholar
Purivirojkul, W and Sumontha, M (2013) Euclinostomum heterostomum (Rudolphi, 1809) metacercarial infection in three osphronemid fish species. Walailak Journal of Science and Technology 10, 97–102.Google Scholar
Rambaut, A (2014) FigTree v1.4.3 Institute of Evolutionary Biology. Edinburgh, University of Edinburgh. Available at http://tree.bio.ed.ac.uk/software/figtree/ (Accessed April 16 2020).Google Scholar
Roca, FJ, Sepulcre, P, Lopez-Castejon, G, Sarropoulou, E and Kotoulas, G (2007) Fish lymphocytes regulate the inflammatory response via the production of chemokines. Journal of Immunology 178, S175.Google Scholar
Ronquist, F, Teslenkovan, M, van der Mark, P, et al. (2012) MrBayes 32: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology 61, 539–542.CrossRefGoogle Scholar
Rosser, TG, Alberson, NR, Woodyard, ET, Cunningham, FL and Pote, LM (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.CrossRefGoogle Scholar
Rosser, TG, Baumgartner, WA, Alberson, NR, Noto, TW, Woodyard, ET, King, DT, Wise, DJ and Griffin, MJ (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
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle ScholarPubMed
Schwarz, G (1978) Estimating the dimension of a model. The Annals of Statistics 6, 461–464.CrossRefGoogle Scholar
Sereno-Uribe, AL, Pinacho-Pinacho, CD, García-Varela, M and 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
Sereno-Uribe, AL, García-Varela, M, Pinacho-Pinacho, CD and 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
Shamsi, S, Halajian, A, Tavakol, S, Mortazavi, P and Boulton, J (2013) Pathogenicity of Clinostomum complanatum (Digenea: Clinostomidae) in piscivorous birds. Research in Veterinary Science 95, 537–539.CrossRefGoogle Scholar
Sutili, FJ, Tourem Gressler, L and Vilani de Pelegrini, LF (2014) Clinostomum complanatum (Trematoda, Digenea): a parasite of birds and fishes with zoonotic potential in southern Brazil A review. Revista Brasileira de Higiene e Sanidade Animal 8, 99–114.CrossRefGoogle Scholar
Szidat, L (1969) Structure, development, and behaviour of new strigeatoid meatcercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753–786.CrossRefGoogle Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology Evolution 10, 512–526.Google ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 60. Molecular Biology Evolution 30, 2725–2729.CrossRefGoogle Scholar
Teixeira de Mello, F, González-Bergonzoni, I and Loureiro, M (2011) Peces de agua dulce del Uruguay. 1st edn.188 pp. Montevideo, PPR-MGAP.Google Scholar
Van Steenkiste, N, Locke, SA, Castelin, M, Marcogliese, DJ and Abbott, CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Biology Evolution 15, 942–952.Google Scholar
Wantzen, KM, Arruda Machado, F, Voss, M, Boriss, HV and Junk, WJ (2002) Seasonal isotopic shifts in fish of the Pantanal wetland, Brazil. Aquatic Science 64, 239–251.CrossRefGoogle Scholar
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