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Morphological and molecular data on Phyllodistomum (Digenea: Gorgoderidae) from Brazil, with the description of a new species parasitizing Hoplias malabaricus (Bloch, 1794) (Osteichthyes, Erythrinidae)

Published online by Cambridge University Press:  24 August 2023

K.G.A. Dias
Affiliation:
Departamento de Parasitologia, Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brazil
G. Pérez-Ponce de León
Affiliation:
Escuela Nacional de Estudios Superiores Unidad Mérida, and Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico
R.J. da Silva
Affiliation:
Departamento de Parasitologia, Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brazil
D.H.M.D. Vieira
Affiliation:
Departamento de Parasitologia, Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brazil
L.A.R. Leite*
Affiliation:
Departamento de Parasitologia, Universidade Estadual Paulista (UNESP), Instituto de Biociências, Botucatu, São Paulo, Brazil
R.K. de Azevedo
Affiliation:
Centro Universitário CESMAC, Maceió, Alagoas, Brazil
V.D. Abdallah
Affiliation:
Setor de Patologia e Parasitologia, Universidade Federal de Alagoas (UFAL), Instituto de Ciências Biológicas e da Saúde, Maceió, Alagoas, Brazil
*
Corresponding author: L.A.R. Leite; Email: lar.leite@unesp.br

Abstract

Phyllodistomum pepirense n. sp. is described from the urinary bladder of Hoplias malabaricus (Bloch, 1794), sampled in the Jacaré-Pepira River in São Paulo state, Brazil. The isolates of the new species were recovered as a monophyletic group in the phylogenetic analysis of the 28S rRNA gene, which showed the new species as the sister taxa of Phyllodistomum virmantasi Pinacho-Pinacho, Sereno-Uribe, Hernández-Orts, García-Varela & Pérez-Ponce de León, 2021, a species sampled from an eleotrid fish in Southeastern Mexico. The new species differs morphologically from P. virmantasi by having a larger body size, slightly lobed testes and ovary, a mostly intercaecal uterus, slightly diverticulated caeca, and vitelline masses irregularly shaped. The new species is also readily distinguished from other species of Phyllodistomum Braun, 1899 reported from freshwater fishes in Brazil – namely, P. rhamdiae Amato & Amato, 1993 and P. spatula Odhner, 1902. The new species is herein described based on morphological characteristics, molecular data from D1–D3 domains of the 28S rRNA gene, host association, and geographical distribution.

Type
Research Paper
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Amato, SB and Amato, JF (1993) A new species of Phyllodistomum Braun, 1899 (Digenea: Gorgoderidae) from Rhamdia quelen (Quoy & Gaimard, 1824) (Siluriformes: Pimelodidae). Memórias do Instituto Oswaldo Cruz 88(4), 557559.Google Scholar
Bakke, TA (1988) Morphology of adult Phyllodistomum umblae (Fabricius) (Platyhelminthes, Gorgoderidae): the effect of preparation, killing and fixation proceduresZoologica Scripta 17, 113.CrossRefGoogle Scholar
Baumgartner, G, Pavanelli, CS, Baumgartner, D, Bifi, AG, Debona, T, and Frana, VA (2012) Peixes do Baixo Rio Iguaçu. Eduem, Maringá.CrossRefGoogle Scholar
Bray, RA, Gibson, DI, and Jones, A (2009) Keys to the Trematoda. vol. 3. London, CAB International and Natural History Museum.Google Scholar
Campbell, RA (2008) Family Gorgoderidae Looss, 1899. In Bray, RA, Gibson, DI, Jones, A (Eds), Keys to the Trematoda. vol. 3. London, CAB International and Natural History Museum, 191213.Google Scholar
Choudhury, A, García-Varela, M, and Pérez-Ponce de León, G (2017) Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far? Journal of Helminthology 91, 174196.CrossRefGoogle ScholarPubMed
Costa, DPC, Monteiro, CM, and Brasil-Sato, M (2015) Digenea of Hoplias intermedius and Hoplias malabaricus (Actinopterygii, Erythrinidae) from upper São Francisco River, Brazil. Revista Brasileira de Parasitologia Veterinaria 24, 129135.CrossRefGoogle ScholarPubMed
Cribb, TH, Chisholm, LA, and Bray, RA (2002) Diversity in the Monogenea and Digenea: does lifestyle matter? International Journal for Parasitology 32(3), 321328.CrossRefGoogle ScholarPubMed
Curran, SS, Tkach, VV, and Overstreet, RM (2006) A review of Polylekithum Arnold, 1934 and its familial affinities using morphological and molecular data, with description of Polylekithum catahoulensis sp. nov. Acta Parasitologica 51, 238248.CrossRefGoogle Scholar
Curran, SS, Tkach, VV, and Overstreet, RM (2011) Phylogenetic affinities of Auriculostoma (Digenea: Allocreadiidae), with descriptions of two new species from Peru. Journal of Parasitology 97, 661670.CrossRefGoogle ScholarPubMed
Cutmore, SC, Bennett, MB, and Cribb, TH (2010) Staphylorchis cymatodes (Gorgoderidae: Anaporrhutinae) from carcharhiniform, or ectolobiform and myliobatiform elasmobranchs of Australasia: low host specificity, wide distribution and morphological plasticity. Parasitol Int. 59, 579–86. doi: 10.1016/j.parint.2010.08.003.CrossRefGoogle ScholarPubMed
Cutmore, SC, Miller, TL, Curran, SS, Bennett, MB, and Cribb, TH (2013) Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitology Research 112, 30633074.CrossRefGoogle ScholarPubMed
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
Fernandes, BMM (1984) New host, geographical record and a synonym for Phyllodistomum spatula Odhner, 1902 (Trematoda, Gorgoderidae). Memórias do Instituto Oswaldo Cruz 79, 263265.CrossRefGoogle Scholar
Fernandes, BMM, Justo, MCN, Anjos, CS, Malta, JCO, and Dumbo, JC (2017) Digenea parasites of Acestrorhynchus falcirostris (Osteichthyes, Acestrorhynchidae) in the state of Amazonas, Brazil. Revista Brasileira de Parasitologia Veterinaria 26(4), 439445.CrossRefGoogle ScholarPubMed
Gião, T, Pelegrini, LS, Azevedo, RK, and Abdallah, VD (2020) Biodiversity of parasites found in the trahira, Hoplias malabaricus (Bloch, 1794), collected in the Batalha River, Tietê-Batalha drainage basin, SP, Brazil. Anais da Academia Brasileira de Ciencias 92, 123.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stone-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cppér, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 16471649.CrossRefGoogle ScholarPubMed
Knoff, M and Amato, JFR (1992) Nova espécie do gênero Phyllodistomum Braun, 1899 (Gorgoderidae, Gorgoderinae) parasita de tainha, Mugil platanus Gunther, 1880 da costa do Estado do Rio de Janeiro, Brasil. Revista Brasileira de Biologia 52(1), 5356.Google Scholar
Kohn, A, Fernandes, BMM, Cohen, SC (2007) South American Trematodes Parasites of Fishes. Rio de Janeiro, Imprinta. 318 p.Google Scholar
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, Mcgettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ, and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.CrossRefGoogle ScholarPubMed
Leite, LAR, Pedreira Filho, WR, Azevedo, RK, and Abdallah, VD (2021) Patterns of distribution and accumulation of trace metals in Hysterothylacium sp. (Nematoda), Phyllodistomum sp. (Digenea) and in its fish host Hoplias malabaricus, from two neotropical rivers in southeastern Brazil. Environmental Pollution 277, 112.Google Scholar
Mendoza-Garfias, B and de León G, Pérez-Ponce (2005) Phyllodistomum centropomi sp. n. (Digenea: Gorgoderidae), a parasite of the fat snook, Centropomus parallelus (Osteichthyes: Centropomidae), in the Papaloapan River at Tlacotalpan, Veracruz state, Mexico. Zootaxa 1056, 4351.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W, and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8 in 2010 Gateway Computing Environments Workshop (GCE 2010).CrossRefGoogle Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA, and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733755.CrossRefGoogle ScholarPubMed
Oyakawa, OT (2003) Family Erythrinidae (Trahiras). In Reis, RE, Kullander, SO, and Ferraris, CJ (Eds), Check list of the freshwater fishes of South and Central America. Porto Alegre, EDIPUCRS, 238340.Google Scholar
Pérez-Ponce de León, G, García Prieto, L, and Mendoza-Garfías, B (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1247.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Razo-Mendivil, U, Mendoza-Garfias, B, Rubio-Godoy, M, and Choudhury, A (2015) A new species of Wallinia Pearse, 1920 (Digenea: Allocreadiidae) in Astyanax mexicanus (Characidae) from Mexico revealed by morphology and sequences of the 28S ribosomal RNA gene. Folia Parasitology 62, 16.Google Scholar
Petkevičiūtė, R, Stunžėnas, V, and Stanevičiūtė, G (2004) Cytogenetic and sequence comparison of adult Phyllodistomum (Digenea: Gorgoderidae) from the three-spined sticklebackwith larvae from two bivalves. Parasitology 129, 771778.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R, Stunzenas, V, Stanevicite, G, and Zhokhov, AE (2014) European Phyllodistomum (Digenea, Gorgoderidae) and phylogenetic affinities of cercaria duplicata based on rDNA and karyotype. Zoologica Scripta 44, 191202.CrossRefGoogle Scholar
Petkevičiūtė, R, Zhokhov, AE, Stunžėnas, V, Poddubnaya, LG, and Stanevičiūte, G (2020) Phyllodistomum kupermani n. sp. from the European perch, Perca fluviatilis L. (Perciformes: Percidae), and redescription of Phyllodistomum macrocotyle (Lühe, 1909) with notes on the species diversity and host specificity in the European Phyllodistomum spp. (Trematoda: Gorgoderidae). Parasites & Vectors 13, 561.CrossRefGoogle Scholar
Pinacho-Pinacho, CD, Sereno-Uribe, AL, Hernández-Orts, JS, Gárcia-Varela, M, and Peréz-Ponce de León, G (2021) Integrative taxonomy reveals an even greater diversity within the speciose genus Phyllodistomum (Platyhelminthes: Trematoda: Gorgoderidae), parasitic in the urinary bladder of Middle American freshwater fishes, with descriptions of five new species. Invertebrate Systematics 35, 754775.CrossRefGoogle Scholar
Razo-Mendivil, U, Pérez-Ponce de León, G, and Rubio-Godoy, M (2013) Integrative taxonomy identifies a new species of Phyllodistomum (Digenea: Gorgoderidae) from the twospot livebearer, Heterandria bimaculata (Teleostei: Poeciliidae), in Central Veracruz, Mexico. Parasitol Res. 112, 4137–50.CrossRefGoogle ScholarPubMed
Rosas-Valdez, R, Choudhury, A, and Pérez-Ponce de León, G (2011) Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zoologica Scripta 40, 296305.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 13121313.CrossRefGoogle ScholarPubMed
Stunzenas, V, Cryan, JR, and Molloy, DP (2004) Comparison of rDNA sequences from colchicine treated and untreated sporocysts of Phyllodistomum folium and Bucephalus polymorphus (Digenea). Parasitol Int. 53, 223–8. doi: 10.1016/j.parint.2003.12.003.CrossRefGoogle ScholarPubMed
Tkach, VV, Pawlowski, J, and Mariaux, J (2000) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology 30, 8393.CrossRefGoogle ScholarPubMed
Tkach, VV, 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. and Bray, R.A. (Eds), Interrelationships of the Platyhelminthes. Taylor & Francis, London, 186193.Google Scholar
Tkach, VV, DTJ, Littlewood, Olson, PD, Kinsella, JM, and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 115.CrossRefGoogle ScholarPubMed
Xia, X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30, 17201728.CrossRefGoogle ScholarPubMed