Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-29T11:08:52.322Z Has data issue: false hasContentIssue false
  • English
  • Français

Exploring Neotropical anuran parasites: a morphological, life cycle and phylogenetic study of Catadiscus marinholutzi (Trematoda: Diplodiscidae)

Published online by Cambridge University Press:  17 February 2021

Murilo S. Queiroz ,
Philippe V. Alves ,
Danimar López-Hernández ,
Luciano A. Anjos  and
Hudson A. Pinto Open the ORCID record for Hudson A. Pinto [Opens in a new window]
Murilo S. Queiroz
Affiliation:
Instituto de Biociências de Botucatu, Universidade Estadual Paulista, Postal Code 18618-970, Botucatu, SP, Brazil
Philippe V. Alves
Affiliation:
Departmento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, Postal Code 31270-901, Belo Horizonte, MG, Brazil
Danimar López-Hernández
Affiliation:
Departmento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, Postal Code 31270-901, Belo Horizonte, MG, Brazil
Luciano A. Anjos
Affiliation:
Departamento de Biologia e Zootecnia, Universidade Estadual Paulista, Passeio Monção 226, Postal Code 15385-000, Ilha Solteira, SP, Brazil
Hudson A. Pinto*
Affiliation:
Departmento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, P.O. Box 486, Postal Code 31270-901, Belo Horizonte, MG, Brazil
*
Author for correspondence: Hudson A. Pinto, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Amphistome species belonging to the genus Catadiscus are poorly studied intestinal trematodes found primarily in Neotropical anurans. Herein, developmental stages of an amphistome species found during herpetological and malacological surveys in a temporary marsh pond from Brazil were subjected to morphological (light and scanning electron microscopy) and molecular analyses. Adult parasites recovered from anurans were identified as Catadiscus marinholutzi. Amphistome cercariae found in the planorbid snails Drepanotrema depressissimum and Drepanotrema lucidum from the same waterbody were used for experimental and molecular studies. Immature parasites, morphologically compatible with members of Catadiscus, were experimentally obtained in laboratory-reared tadpoles. Sequencing of a partial region of 28S rDNA gene of both adult and cercariae revealed 100% similarity between these developmental stages, confirming their conspecificity. Phylogenetic analyses were attempted for the first time to reveal the position of a species of Catadiscus in the superfamily Paramphistomoidea. Catadiscus marinholutzi falls in a virtual polytomy together with other paramphistomoids, which leaves its phylogenetic relationships within the group unclear. Moreover, the high genetic divergence to Diplodiscus spp. (10.06–10.84%) cast doubts on the placement of Catadiscus within Diplodiscidae. Hence the species composition of the Diplodiscidae should be re-evaluated in further studies using a broader spectrum of related taxa.

Keywords

AamphibiansBrazilcercariaelife cycleParamphistomoideaphylogenetic relationshipssnailtrematodes
Type
Research Article
Information
Parasitology , Volume 148 , Issue 7 , June 2021 , pp. 798 - 808
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alves, PV, Assis, JCA, López-Hernández, D, Pulido-Murillo, EA, Melo, AL, Locke, SA and Pinto, HA (2020) A phylogenetic study of the cecal amphistome Zygocotyle lunata (Trematoda: Zygocotylidae), with notes on the molecular systematics of Paramphistomoidea. Parasitology Research 119, 2511–2520.10.1007/s00436-020-06749-6CrossRefGoogle Scholar
Amato, JFR, Boeger, WA and Amato, SB (1991) Protocolos para Laboratório: Coleta e Processamento de Parasitos de Pescado. Seropédica, Brazil: Imprensa Universitária da Universidade Federal do Rio de Janeiro.Google Scholar
Assis, JCA, Lopez-Hernández, D, Pulido-Murillo, EA, Melo, AL and Pinto, HA (2019) A morphological, molecular and life cycle study of the capybara parasite Hippocrepis hippocrepis (Trematoda: Notocotylidae). PLoS One 14, e0221662.10.1371/journal.pone.0221662CrossRefGoogle Scholar
Besprozvannykh, VV, Rozhkovan, KV, Ermolenko, AV and Izrailskaya, AV (2018) Diplodiscus mehrai Pande, 1937 and D. japonicus (Yamaguti, 1936): morphology of developmental stages and molecular data. Helminthologia 55, 60–69.10.1515/helm-2017-0049CrossRefGoogle Scholar
Blasco-Costa, I and Poulin, R (2017) Parasite life-cycle studies: a plea to resurrect an old parasitological tradition. Journal of Helminthology 91, 647–656.10.1017/S0022149X16000924CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295–306.10.1007/s11230-016-9631-2CrossRefGoogle ScholarPubMed
Bolek, MG and Janovy, J Jr. (2008) Alternative life cycle strategies of Megalodiscus temperatus in tadpoles and metamorphosed anurans. Parasite 15, 396–401.10.1051/parasite/2008153396CrossRefGoogle ScholarPubMed
Bolek, MG, Stigge, HA and Gustafson, KD (2016) The iron wheel of parasite life cycles: then and now. In Janovy, J Jr. and Esch, GW (eds). A Century of Parasitology: Discoveries, Ideas and Lessons Learned by Scientists who Published in the Journal of Parasitology, 1914–2014. London, UK: Wiley Press, pp. 131–147.10.1002/9781118884799.ch9CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.10.2307/3284227CrossRefGoogle Scholar
Campião, KM, Morais, DH, Dias, OT, Aguiar, A, Toledo, G, Tavares, LER and Silva, RJ (2014) Checklist of helminth parasites of amphibians from South America. Zootaxa 3843, 1–93.10.11646/zootaxa.3843.1.1CrossRefGoogle ScholarPubMed
Dawes, B (1968) The Trematoda. London, UK: Cambridge University Press.Google Scholar
D'Bastiani, E, Campião, KM, Boeger, WA and Araújo, SBL (2020) The role of ecological opportunity in shaping host–parasite networks. Parasitology 147, 1452–1460.10.1017/S003118202000133XCrossRefGoogle ScholarPubMed
Dereeper, A, Guignon, V, Blanc, G, Audic, S, Buffet, S, Chevenet, F, Dufayard, JF, Guindon, S, Lefort, V, Lescot, M, Claverie, JM and Gascuel, O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, W465–W469.10.1093/nar/gkn180CrossRefGoogle ScholarPubMed
Fernandes, BMM and Kohn, A (2014) South American Trematodes Parasites of Amphibians and Reptiles. Rio de Janeiro, Brazil: Fundação Oswaldo Cruz.Google Scholar
Fernandez, MA, Thiengo, SC and Amaral, RS (2008) Técnicas malacológicas. In Amaral, RS, Thiengo, SC and Pieri, OS (orgs). Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas. Brasília, Brazil: Secretaria de Vigilância em Saúde, Ministério da Saúde, pp. 43–70.Google Scholar
Freitas, JFT and Dobbin, JE Jr. (1956) Nôvo parasito de rã: Catadiscus propinquus sp. n. (Trematoda, Paramphistomoidea). Revista Brasileira de Biologia 40, 629–634.Google Scholar
Freitas, JFT and Lent, H (1939) Revisão do gênero Catadiscus Cohn, 1904 (Trematoda, Paramphistomoidea). Boletim Biologico 4, 305–315.Google Scholar
Galaktionov, KV and Dobrovolskij, AA (2003) The Biology and Evolution of trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic trematodes. Dordrecht, Netherlands: Dordrecht Kluwer Academic Publishers.CrossRefGoogle Scholar
Goldberg, SR, Bursey, CR, Caldwell, JP and Shepard, DB (2009) Gastrointestinal helminths of six sympatric species of Leptodactylus from Tocantins State, Brazil. Comparative Parasitology 76, 258–266.10.1654/4368.1CrossRefGoogle Scholar
Gomes, TFF, Melo, FTV, Giese, EG, Furtado, AP, Gonçalves, EC and Santos, JN (2013) A new species of Mesocoelium (Digenea: Mesocoeliidae) found in Rhinella marina (Amphibia: Bufonidae) from Brazilian Amazonia. Memórias do Instituto Oswaldo Cruz 108, 186–191.10.1590/0074-0276108022013010CrossRefGoogle ScholarPubMed
Gonchar, A, Jouet, D, Skírnisson, K, Krupenko, D and Galaktionov, KV (2019) Transatlantic discovery of Notocotylus atlanticus (Digenea: Notocotylidae) based on life cycle data. Parasitology Research 118, 1445–1456.10.1007/s00436-019-06297-8CrossRefGoogle ScholarPubMed
Grabda-Kazubska, B (1980) Observations on the life cycle of Diplodiscus subclavatus (Pallas, 1760) (Trematoda, Diplodiscidae). Acta Parasitologica Polonica 27, 261–271.Google Scholar
Graça, RJ, Oda, FH, Lima, FS, Guerra, V, Gambale, PG and Takemoto, RM (2017) Metazoan endoparasites of 18 anuran species from the mesophytic semideciduous Atlantic Forest in southern Brazil. Journal of Natural History 51, 705–729.10.1080/00222933.2017.1296197CrossRefGoogle Scholar
Halliday, T (2006) Amphibians. In Sutherland, WJ (ed.), Ecological Census Techniques. New York, USA: University of Cambridge, pp. 278–293.10.1017/CBO9780511790508.008CrossRefGoogle Scholar
Hamann, MI (1992) Catadiscus pomaceae sp. n. (Trematoda, Paramphistomatidae) from Pomacea canaliculata (Lamarck, 1801) (Prosobranchia, Ampullariidae). Memórias do Instituto Oswaldo Cruz 87, 9–14.10.1590/S0074-02761992000100002CrossRefGoogle Scholar
Hamann, MI (2004) Seasonal maturation of Catadiscus propinquus (Digenea: Diplodiscidae) in Lysapsus limellus (Anura: Pseudidae) from an Argentinean subtropical permanent pond. Physis (Buenos Aires) Secc. B 59, 29–36.Google Scholar
Hamann, MI and González, CE (2009) Larval digenetic trematodes in tadpoles of six amphibian species from Northeastern Argentina. Journal of Parasitology 95, 623–628.10.1645/GE-1738.1CrossRefGoogle ScholarPubMed
Hamann, MI, Kehr, AI and González, CE (2013) Helminth communities in the burrowing toad, Rhinella fernandezae, from Northeastern Argentina. Biologia 68, 1155–1162.CrossRefGoogle Scholar
Hamann, MI, Kehr, AI and González, CE (2014) Helminth community structure in the Argentinean bufonid Melanophryniscus klappenbachi: importance of habitat uses and season. Parasitology Research 113, 3639–3649.CrossRefGoogle Scholar
Hamann, MI, Fernández, MV and González, CE (2019) Metacercariae of Strigeidae parasitizing amphibians of the Chaco Region in Argentina. Anais da Academia Brasileira de Ciências 91, e20180044.10.1590/0001-3765201920180044CrossRefGoogle ScholarPubMed
Hamann, MI, González, CE and Fernández, MV (2020 a) Trematode parasites associated with amphibians from a rice field in the northeastern Argentina. Food Webs 22, e00139.10.1016/j.fooweb.2019.e00139CrossRefGoogle Scholar
Hamann, MI, León-Règagnon, V, Fernández, MV and González, CE (2020 b) First record of the genus Choledocystus (Trematoda: Plagiorchiidae) for amphibians of the Chacoan region in Argentina. Anais da Academia Brasileira de Ciências 92, e20180384.10.1590/0001-3765202020180384CrossRefGoogle ScholarPubMed
Janzen, DH (1985) On ecological fitting. Oikos 45, 308–310.10.2307/3565565CrossRefGoogle Scholar
Jones, A (2005 a) Superfamily Paramphistomoidea Fischoeder, 1901. In Jones, A, Bray, RA and Gibson, DI (eds), Keys to the Trematoda, vol. 2. Wallingford, UK: CAB International & The Natural History Museum, pp. 221–227.10.1079/9780851995878.0221CrossRefGoogle Scholar
Jones, A (2005 b) Family Diplodiscidae Cohn, 1904. In Jones, A, Bray, RA and Gibson, DI (eds). Keys to the Trematoda. vol. 2. Wallingford, UK: CAB International & The Natural History Museum, pp. 319–324.10.1079/9780851995878.0319CrossRefGoogle Scholar
Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A and Jermiin, LS (2017) Modelfinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.10.1038/nmeth.4285CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.10.1093/molbev/msw054CrossRefGoogle ScholarPubMed
Locke, SA, Drago, FB, Núñez, V, Souza, GTRE and Takemoto, RM (2020) Phylogenetic position of Diplostomum spp. from New World herons based on complete mitogenomes, rDNA operons, and DNA barcodes, including a new species with partially elucidated life cycle. Parasitology Research 119, 2129–2137.10.1007/s00436-020-06713-4CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the gateway computing environments workshop (GCE). New Orleans, LA, pp. 1–8.CrossRefGoogle Scholar
Minh, BQ, Nguyen, MAT and Von Haeseler, A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188–1195.10.1093/molbev/mst024CrossRefGoogle ScholarPubMed
Nguyen, LT, Schmidt, HA, Von Haeseler, A and Minh, BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.CrossRefGoogle ScholarPubMed
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal of Parasitology 33, 733–755.10.1016/S0020-7519(03)00049-3CrossRefGoogle Scholar
Ostrowski de Núñez, M (1979) Fauna de agua dulce de la Argentina. IX. Sobre representantes de la Familia Paramphistomatidae (Trematoda). Physis Sección B 38, 55–62.Google Scholar
Ostrowski de Núñez, M and Gil de Pertierra, AA (2004) Ciclos Biológicos dulceacuícolas de Digenea (Trematoda) y Proteocephalidea (Cestoda). In Ranzani-Paiva, MJT, Takemoto, RM and Lizama, MAP (eds), Sanidade de Organismos Aquáticos. São Paulo: Editora Varela, pp. 215–257.Google Scholar
PAHO-Pan American Health Organization (1968) A Guide for the Identification of the Snail Intermediate Hosts of Schistosomiasis in the Americas. Scientific Publication no. 168. Washington, USA: PAHO.Google Scholar
Paraense, WL (1992) Halipegus dubius Klein, 1905 (Trematoda, Hemiuridae): a redescription, with notes on the working of the ovarian complex. Memórias do Instituto Oswaldo Cruz 87, 179–190.10.1590/S0074-02761992000500035CrossRefGoogle Scholar
Paraense, WL and Deslandes, N (1956) The Brazilian species of Drepanotrema. II. D. melleum (Lutz, 1918). Revista Brasileira de Biologia 16, 527–534.Google Scholar
Paraense, WL and Deslandes, N (1957) The Brazilian species of Drepanotrema. III. D. depressissimum (Moricand, 1837). Revista Brasileira de Biologia 17, 339–344.Google Scholar
Paredes-León, R, Garcia-Prieto, L, Guzman-Cornejo, C, Leon-Regagnon, V and Perez, TM (2008) Metazoan parasites of Mexican amphibians and reptiles. Zootaxa 1904, 1–166.10.11646/zootaxa.1904.1.1CrossRefGoogle Scholar
Pérez-Ponce de Léon, G and Hernández-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. Journal of Helminthology 93, 260–276.10.1017/S0022149X19000191CrossRefGoogle ScholarPubMed
Provete, DB, Garey, MV, Silva, FR and Rossa-feres, DC (2011) Anurofauna do noroeste paulista: Lista de espécies e chave de identificação para adultos. Biota Neotropica 11, 377–391.CrossRefGoogle Scholar
Queiroz, MS, López-Hernández, D, Locke, SA, Pinto, HA and Anjos, LA (2019) Metacercariae of Heterodiplostomum lanceolatum (Trematoda: Proterodiplostomidae) found in Leptodactylus podicipinus (Anura: Leptodactylidae) from Brazil: a morphological, molecular and ecological study. Journal of Helminthology 94, e66.10.1017/S0022149X19000646CrossRefGoogle ScholarPubMed
Queiroz, MS, Pontes, MR, Neto, MC, Campião, KM and Anjo, LA (2020) Helminths of 8 anuran species from a remnant riparian forest in the Cerrado biome, Brazil. Herpetology Notes 13, 463–478.Google Scholar
Rambaut, A (2012) FigTree v1.4. Available from http://tree.bio.ed.ac.uk/software/figtree/ (Accessed February 2020).Google Scholar
Rambaut, A, Suchard, MA, Xie, D and Drummond, AJ (2014) Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.10.1093/sysbio/sys029CrossRefGoogle ScholarPubMed
Schell, SC (1985) Handbook of Trematodes of North America, North of Mexico. Moscow, Russia: University Press Idaho.Google Scholar
Sela, I, Ashkenazy, H, Katoh, K and Pupko, T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43, W7–W14.10.1093/nar/gkv318CrossRefGoogle ScholarPubMed
Sewell, RBS (1922) Cercariae indicae. Indian Journal of Medical Research 10(Suppl. 1), 1–370.Google Scholar
Sey, O (1983) Reconstruction of the systematics of the family Diplodiscidae Skrjabin, 1949 (Trematoda: Paramphistomata). Parasitologia Hungarica 16, 63–89.Google Scholar
Sey, O (1991) CRC Handbook of the Zoology of Amphistomes. Boca Raton, USA: CRC Press.Google Scholar
Skryabin, KI (1949) Trematodes of Animals and Men, vol. 3. Moscow, Russia: Publishing House of the USSR Academic Science.Google Scholar
Thatcher, VE (1964) Estudios sobre los tremátodos de reptiles de Tabasco, México: Lista de huéspedes y sus parásitos. Anales de la Escuela Nacional de Ciencias Biológicas 13, 91–96.Google Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.10.1023/A:1025546001611CrossRefGoogle Scholar
Travassos, L (1940) Relatório da terceira excursão a zona da Estrada de Ferro Noroeste do Brasil realizada em fevereiro e março de 1940: I – Introdução. Memórias do Instituto Oswaldo Cruz 35, 607–696.10.1590/S0074-02761940000300013CrossRefGoogle Scholar
Travassos, LP, Freitas, JFT and Kohn, A (1969) Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz 67, 1–886.Google Scholar
Veitenheimer-Mendes, IL and Almeida-Caon, JEM (1989) Drepanotrema kermatoides (Orbigny, 1835) (Mollusca, Planorbidae), hospedeiro de um paramfistomídeo (Trematoda), no Rio Grande do Sul. Memórias do Instituto Oswaldo Cruz 84, 107–111.CrossRefGoogle Scholar
Vettorazzi, RI, Norbis, WA and Martorelli, SR (2020) Novel host report for Catadiscus uruguayensis Freitas & Lent, 1939 (Trematoda, Diplodiscidae) infecting Austrolebias Costa, 1998 species from Uruguay. Check List 16, 1277–1282.CrossRefGoogle Scholar
Yamaguti, S (1971) Synopsis of Digenetic Trematodes of Vertebrates, vol. 1. Tokyo, Japan: Keigaku Publishing Company.Google Scholar
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates with Special Reference to the Morphology of Their Larval Forms. Tokyo, Japan: Keigaku Publishing Company.Google Scholar
Supplementary material: Image

Queiroz et al. supplementary material

Queiroz et al. supplementary material 1

Download Queiroz et al. supplementary material(Image)
Image 547.6 KB
Supplementary material: Image

Queiroz et al. supplementary material

Queiroz et al. supplementary material 2

Download Queiroz et al. supplementary material(Image)
Image 514.3 KB
Supplementary material: File

Queiroz et al. supplementary material

Queiroz et al. supplementary material 3

Download Queiroz et al. supplementary material(File)
File 24.8 KB
Supplementary material: File

Queiroz et al. supplementary material

Queiroz et al. supplementary material 4

Download Queiroz et al. supplementary material(File)
File 43.1 KB