Skip to main content
SpringerLink
Log in

Identification and molecular characterization of digenean trematode parasites of Aylacostoma chloroticum (Gastropoda: Thiaridae) from a Neotropical Basin

  • Research
  • Published:
Parasitology Research Aims and scope Submit manuscript

  • 2 Altmetric

Abstract

Thiarids are pantropical gastropods distributed from South America to Australia and found in lentic and lotic freshwater environments. These gastropods act as intermediate hosts for several species of digeneans. There are difficulties in the correct identification of these digeneans in certain stages of the life cycle as the larvae have a reduced size and few morphological characteristics for diagnosis. Because of this, techniques based on molecular markers have become an extremely useful tool. Our objective was to molecularly characterize the digeneans found in gastropods from the Ivaí River, Paraná, Brazil, using the mitochondrial molecular marker cytochrome c oxidase (COI) and the 28S ribosomal marker. With the molecular marker COI, gastropods showed high genetic similarity with Aylacostoma chloroticum. For the parasites, four different taxa were characterized with both markers. The 28S ribosomal marker proved to be more effective for the identification of Ivaí River parasites, being possible to suggest the identification of two species among the four groups found. Considering that there are no records in the literature of studies involving parasites and gastropods as intermediate hosts in the Ivaí River, this study is the first regarding these relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The datasets generated and analyzed during the study are available in the GenBank repository under the following accession numbers: ON509573–ON509593; ON520658–ON520692; ON524763–ON524797.

Code availability

Not applicable.

References

  • Adams H, Adams A (1854) The genera of Recent Mollusca, 1. London, van Voorst

  • Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao GD (1926) A new species of trematodes from Nycticeius pallidus with a key to the species of Lecithodendrium. Ann Mag Nat Hist 18:299–304. https://doi.org/10.1080/00222932608633511

  • Biazin PC, Santos ML (2008) Características geomórficas do canal e das formas de leito do rio Ivaí em seu curso inferior, Icaraíma PR. Rev Bras Geomorfol 9:43–52. https://doi.org/10.20502/rbg.v9i1.100

    Article  Google Scholar 

  • Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Syst Parasitol 93:295–306. https://doi.org/10.1007/s11230-016-9631-2

    Article  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1995) A molecular phylogeny of the human schistosomes. Mol Phylogenet Evol 4:103–109. https://doi.org/10.1006/mpev.1995.1011

    Article  CAS  PubMed  Google Scholar 

  • Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. PNAS 76:1967–1971. https://doi.org/10.1073/pnas.76.4.1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciccheto JRM, Stabile BHM, Fabrin TMC et al (2021a) The first record of Centrocestus formosanus (Trematoda: Heterophyidae) in southern Brazil supported by molecular data. An Acad Bras Ciênc 93. https://doi.org/10.1590/0001-37652021a20191017

  • Ciccheto JRM, Stabile BHM, Fermino F et al (2021b) Molecular evidence of new freshwater turtle blood flukes (Digenea: Spirorchiidae) in the intermediate snail host Biomphalaria occidentalis Paraense, 1981 in an urban aquatic ecosystem in Brazil. Parasitol Res 120:133–143. https://doi.org/10.1007/s00436-020-06945-4

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dias MLGG, Eiras JC, Machado MH et al (2003) The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná river, Brazil. Parasitol Res 89:506–508. https://doi.org/10.1007/s00436-002-0796-z

    Article  CAS  PubMed  Google Scholar 

  • Fernandez MLA, Santos SB, Miyahira IC et al (2012) Gastrópodes límnicos invasores: morfologia comparada. In: Mansur MCD, Santos CP, Pereira D et al (eds) Moluscos límnicos invasores no Brasil: biologia, prevenção e controle. Porto Alegre, Redes Editora, pp 129–136

  • Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Freitas JFT (1941) Sellacotyle lutzi n.sp., trematodeo parasito de Hoplias malabaricus Bloch. Ann Acad Brasil Sci 13:17–19

  • Freitas JFT (1955) Sobre dois trematódeos parasitos de aves: Philophthalmus lachrymosus Braun, 1902 e Renicola mirandaribeiroi n. sp. Arq Mus Nac 42:585–610

    Google Scholar 

  • Fried B, Graczyk TK, Tamang L (2004) Food-borne intestinal trematodiases in humans. Parasitol Res 93:159–170. https://doi.org/10.1007/s00436-004-1112-x

    Article  PubMed  Google Scholar 

  • Frota A, Deprá GC, Petenucci LM, Graça WJ (2016) Inventory of the fish fauna from Ivaí River basin, Paraná State, Brazil. Biota Neotrop 16. https://doi.org/10.1590/1676-0611-BN-2015-0151

  • Gill T (1871) Arrangement of the families of mollusks. Smithsonian Institution, Washington

  • Glaubrecht M, Brinkmann N, Pöppe J (2009) Diversity and disparity “down under”: Systematics, biogeography and reproduction modes of the “marsupial” freshwater Thiaridae (Caenogastropoda, Cerithioidea) in Australia. Zool Reihe 85:199–275. https://doi.org/10.1002/zoos.200900004

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1:95–98

    Google Scholar 

  • Hylton Scott MI (1954) Dos nuevos melánidos del Alto Paraná (Mol. Prosobr.). Neotropica 1:45–48

    Google Scholar 

  • Kanev I, Nollen PM, Vassilev I, Dimitrov V (1993) Redescription of Philophthalmus lucipetus (Rudolphi, 1819) (Trematoda: Philophthalmidae) with a discussion of its identity and characteristics. Ann Nat Mus Wien 94/95B:11–34 (https://www.jstor.org/stable/41766884)

    Google Scholar 

  • Kohn A, Fernandes BMM (1987) Estudo comparativo dos helmintos parasitos de peixes do Rio Mogi Guassu, coletados nas excursões realizadas entre 1927 e 1985. Mem Inst Oswaldo Cruz 82:483–500

    Article  CAS  PubMed  Google Scholar 

  • Kohn A, Moravec F, Cohen SC et al (2011) Helminths of freshwater fishes in the reservoir of the Hydroelectric Power Station of Itaipu, Paraná, Brazil. Check List 7:681–690. https://doi.org/10.15560/7.5.681

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msab120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leite LAR, Filho WRP, Azevedo RKA, 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. Environ Pollut 277. https://doi.org/10.1016/j.envpol.2020.116052

  • Locke SA, Al-Nasiri FS, Caffara M et al (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int J Parasitol 45:841–855. https://doi.org/10.1016/j.ijpara.2015.07.001

    Article  CAS  PubMed  Google Scholar 

  • Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155–171. https://doi.org/10.1046/j.1095-8312.2003.00141.x

    Article  Google Scholar 

  • Looss A (1899) Weitere Beitrage zur Kenntnis der Trematodenfauna Aegyptens, zugleich Verseuch einer natürlichen Gliederung des Genus Distomum Reitzius. Zoologischer Jahrbücher, Abteilung für Systematik 12:521–784

  • Lopes AS, Pulido-Murillo EA, López-Hernández D et al (2021) First report of Melanoides tuberculata (Mollusca: Thiaridae) harboring a xiphidiocercaria in Brazil: A new parasite introduced in the Americas? Parasitol Int 82. https://doi.org/10.1016/j.parint.2021.102284

  • Lühe MFW (1901) Zweie neue Distomen aus indischen Anuren. Zentralblatt für Bakteriologie, Parasitenkunde und Infektionskrankheiten 30:166–177

  • Mathis C, Leger M (1910) Douve oculaire de la poule. Bull Soc Pathol Exot 3:245–251

  • Merlo MJ, Parietti M, Fernández MV, Flores V, Davies D (2022) A checklist of larval Digenea (Platyhelminthes: Trematoda) in molluscs from inland waters of Argentina: one hundred years of research. J Helminthol 96:E32. https://doi.org/10.1017/S0022149X2100081X

    Article  CAS  PubMed  Google Scholar 

  • Miller HM (1923) Notes on some furcocercous larval trematodes. J Parasitol 10:35–46. https://doi.org/10.2307/3270887

  • Miura O, Kuris AM, Torchin ME et al (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35:793–801. https://doi.org/10.1016/j.ijpara.2005.02.014

    Article  CAS  PubMed  Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin JD et al (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:75–82. https://doi.org/10.1111/j.1755-0998.2009.02634.x

    Article  CAS  PubMed  Google Scholar 

  • Muniz-Pereira LC, Amato SB (1993) Philophthalmus gralli (Digenea: Philophthalmidae) parasite of Anas bahamensis and Amazonetta brasiliensis, from lagoons of Maricá county, Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 88:567–569. https://doi.org/10.1590/S0074-02761993000400012

    Article  Google Scholar 

  • Nollen PM, Kanev I (1995) The taxonomy and biology of philophthalmid eyeflukes. Adv Parasitol 36:205–269. https://doi.org/10.1016/S0065-308X(08)60492-3

    Article  Google Scholar 

  • Núñez MO, Quintana MG (2008) The life cycle of Stephanoprora aylacostoma n.sp. (Digenea: Echinostomatidae), parasite of the threatened snail Aylacostoma chloroticum (Prosobranchia, Thiaridae), in Argentina. Parasitol Res 102:647–655. https://doi.org/10.1007/s00436-007-0806-2

    Article  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV et al (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755. https://doi.org/10.1016/S0020-7519(03)00049-3

    Article  CAS  PubMed  Google Scholar 

  • Onaca FMT, Graça RJ, Fabrin TMC et al (2019) Molecular characterization and identification of digenean larval stages in Aylacostoma chloroticum (Prosobranchia: Thiaridae) from a neotropical floodplain. J Helminthol 94:1–8. https://doi.org/10.1017/S0022149X19000725

    Article  Google Scholar 

  • Pantoja CS, Hernández-Mena DI, León GP et al (2018) Phylogenetic Position of Pseudosellacotyla lutzi (Freitas, 1941) (Digenea: Cryptogonimidae), A Parasite of Hoplias malabaricus (Bloch) in South America, through 28S rDNA Sequences, and New Observations of the Ultrastructure of Their Tegument. J Parasitol 104:530–538. https://doi.org/10.1645/17-201

    Article  CAS  PubMed  Google Scholar 

  • Pavanelli GC, Eiras JC, Takemoto RM (2002) Doenças de peixes: profilaxia, diagnóstico e tratamento. Maringá, EDUEM

  • Pinto HA, Melo AL (2010) Melanoides tuberculata as intermediate host of Philophthalmus gralli in Brazil. Rev Inst Med Trop S Paulo 52:323–327. https://doi.org/10.1590/S0036-46652010000600007

    Article  PubMed  Google Scholar 

  • Pinto HA, Melo AL (2013a) A checklist of larval trematodes (Platyhelminthes) in molluscs from Brazil. Zootaxa 3666:449–475

    Article  PubMed  Google Scholar 

  • Pinto HA, Melo AL (2013b) Larvas de trematódeos em moluscos do Brasil: panorama e perspectivas após um século de estudos. Rev Patol Trop 42:369–386

    Google Scholar 

  • Pinto HA, Melo AL, Brant SV (2015) Where are the South American freshwater turtle blood flukes (Trematoda: Spirorchiidae)? The first morphological and molecular analysis of spirorchiid cercariae from freshwater snails in Brazil. Parasitol Int 64:553–558. https://doi.org/10.1016/j.parint.2015.08.001

    Article  PubMed  Google Scholar 

  • Pinto RM, Santos LC, Tortelly R et al (2005) Pathology and first report of natural infections of the eye trematode Philophthalmus lachrymosus Braun, 1902 (Digenea, Philophthalmidae) in a non-human mammalian host. Mem Inst Oswaldo Cruz 100:579–583. https://doi.org/10.1590/S0074-02762005000600012

    Article  PubMed  Google Scholar 

  • Pulido-Murillo EA, Tkach VV, Pinto HA (2022) The life cycle of Philophthalmus aylacostoma n. sp. (Trematoda: Philophthalmidae), a new eye fluke species transmitted by Aylacostoma spp. (Gastropoda: Thiaridae) in Brazil. Parasitol Res 121:933–944. https://doi.org/10.1007/s00436-022-07447-1

    Article  PubMed  Google Scholar 

  • Quintana MG, Núñez MO (2014) The Life Cycle of Pseudosellacotyla lutzi (Digenea: Cryptogonimidae), in Aylacostoma chloroticum (Prosobranchia: Thiaridae), and Hoplias malabaricus (Characiformes: Erythrinidae), in Argentina. J Parasitol 100:805–811. https://doi.org/10.1645/13-379.1

    Article  PubMed  Google Scholar 

  • Ramos IP, Franceschini L, Zago AC et al (2013) New host records and a checklist of fishes infected with Austrodiplostomum compactum (Digenea: Diplostomidae) in Brazil. Rev Bras Parasitol Vet 22:511–518. https://doi.org/10.1590/S1984-29612013000400010

    Article  PubMed  Google Scholar 

  • Rosenthal A, Coutelle O, Craxton M (1993) Large-scale production of DNA sequencing templates by microtitre format PCR. Nucleic Acids Res 21:173–174. https://doi.org/10.1093/nar/21.1.173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozas J, Ferrer-Mata A, Sánchez-Delbarrio JC et al (2017) DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  • Santos ML, Stevaux JC, Gasparetto NVL, Souza Filho EE (2008) Geologia e geomorfologia da planície aluvial do rio Ivaí em seu curso inferior. Rev Bras Geomorf 9:23–34. https://doi.org/10.20502/rbg.v9i1.98

    Article  Google Scholar 

  • Scholz T, Aguirre-Macedo ML, Flores Días de Léon ATS, Ditrich O (2000) Larval stages of trematodes in Mexican freshwater mollusc: a review of present state and methodology for future research. In: Salgado-Maldonado G, García-Aldrete AN, Vidal-Martínez VM (ed) Metazoan parasites in the neotropic: a systematic and ecological perspective. México: Instituto de Biología, UNAM 77–100

  • Segatto ALA, Goetze M, Turchetto C (2017) Marcadores moleculares baseados na análise de sequências: utilização em filogenia e filogeografia. In: Turchetto-Zolet AC, Turchetto C, Zanella CM et al (org) Marcadores Moleculares na Era genômica: Metodologias e Aplicações. Ribeirão Preto, Sociedade Brasileira de Genética

  • Secretaria de Estado do Meio Ambiente e Recursos Hídricos - SEMA (2010) Bacias Hidrográficas do Paraná. Governo do Estado do Paraná. Curitiba, Série Histórica

  • Simone LRL (2006) Land and Freshwater Molluscs of Brazil: an illustrated inventory on the Brazilian malacofauna, including neighbor regions of the South America, respect to the terrestrial and freshwater ecosystems. Museu de Zoologia, Universidade de São Paulo. São Paulo, EGB/Fapesp

  • Solferini VN, Selivon D (2012) Polimorfismos de isozimas. In: Matioli SR, Fernandes FM (eds) Biologia Molecular e Evolução. Ribeirão Preto, Holos, pp 165–169

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verocai GG, Lopes LN, Burlini L et al (2009) Occurrence of Philophthalmus gralli (Trematoda: Philophthalmidae) in farmed ostriches in Brazil. Trop Anim Health Prod 41:1241–1242. https://doi.org/10.1007/s11250-009-9306-y

    Article  PubMed  Google Scholar 

  • Vogler RE (2012) Aylacostoma chloroticum Hylton Scott, 1954: antecedentes de la especie. Amici Molluscarum 20:43–46

    Google Scholar 

  • Vogler RE, Rumi A, Peso JG, Argüelles CF (2010) Códigos de barra genéticos en Aylacostoma chloroticum (Gastropoda: Thiaridae), especie amenazada de Argentina. In: Libro de Resúmenes del XIV Congreso Latinoamericano de Genética

  • Vogler RE, Beltramino AA, Peso JG, Rumi A (2014) Threatened gastropods under the evolutionary genetic species concept: redescription and new species of the genus Aylacostoma (Gastropoda: Thiaridae) from High Paraná River (Argentina-Paraguay). Zool J Linn Soc 172:501–520. https://doi.org/10.1111/zoj.12179

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia) from the Universidade Estadual de Maringá (UEM), for the logistical support and infrastructure, the Laboratório de Ictioparasitologia (Nupélia/UEM) for the laboratory infrastructure and help for sampling, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES) for the scholarship master’s degree awarded.

Funding

M. D. P. received a master’s scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES).

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais, Centro de Ciências Biológicas, Universidade Estadual de Maringá – UEM, Av. Colombo 5790, Bloco G90, Maringá, Paraná, CEP 87020-900, Brazil

    Mayara Destro Passere, Ricardo Massato Takemoto & Alessandra Valéria de Oliveira

  2. Maringá, Brazil

    Rodrigo Junio da Graça

  3. Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Centro de Ciências Biológicas, Universidade Estadual de Maringá – UEM, Maringá, Paraná, Brazil

    Ricardo Massato Takemoto & Alessandra Valéria de Oliveira

  4. Programa de Pós-Graduação em Biologia Comparada, Centro de Ciências Biológicas, Universidade Estadual de Maringá – UEM, Maringá, Paraná, Brazil

    Ricardo Massato Takemoto

  5. Departamento de Biotecnologia, Genética e Biologia Celular, Centro de Ciências Biológicas, Universidade Estadual de Maringá – UEM, Maringá, Paraná, Brazil

    Alessandra Valéria de Oliveira

Authors
  1. Mayara Destro Passere
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rodrigo Junio da Graça
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo Massato Takemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alessandra Valéria de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of the study. Material preparation and data collection were carried out by Mayara Destro Passere and Rodrigo Junio da Graça. Molecular analyses were performed by Mayara Destro Passere and Alessandra Valéria de Oliveira. The photos were edited by Ricardo Massato Takemoto. All authors contributed to the writing of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mayara Destro Passere.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Handling Editor: Una Ryan

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 22 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Passere, M.D., da Graça, R.J., Takemoto, R.M. et al. Identification and molecular characterization of digenean trematode parasites of Aylacostoma chloroticum (Gastropoda: Thiaridae) from a Neotropical Basin. Parasitol Res 121, 3653–3661 (2022). https://doi.org/10.1007/s00436-022-07692-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07692-4

Keywords

Search

Navigation