Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T07:46:33.836Z Has data issue: false hasContentIssue false

Metacercariae of Heterodiplostomum lanceolatum (Trematoda: Proterodiplostomidae) found in Leptodactylus podicipinus (Anura: Leptodactylidae) from Brazil: a morphological, molecular and ecological study

Published online by Cambridge University Press:  23 July 2019

M.S. Queiroz*
Affiliation:
Universidade Estadual Paulista, Instituto de Biociências de Botucatu – IBB/Unesp, 18618-970, Botucatu, São Paulo, Brazil
D. López-Hernández
Affiliation:
Universidade Federal de Mina Gerais – UFMG, Belo Horizonte, Brazil
S.A. Locke
Affiliation:
Department of Biology, University of Puerto Rico at Mayagüez, Call Box 9000, Mayagüez, 00681-9000, Puerto Rico
H.A. Pinto
Affiliation:
Universidade Federal de Mina Gerais – UFMG, Belo Horizonte, Brazil
L.A. Anjos
Affiliation:
Departamento de Biologia e Zootecnia – FEIS/UNESP, Universidade Estadual Paulista, Passeio, CEP 15385000 Ilha Solteira, Brazil
*
Author for correspondence: M.S. Queiroz, E-mail: queiroz51@gmail.com

Abstract

The trematodes from South American reptiles are poorly known, with only one life cycle completely characterized. We used molecular and morphological methods to characterize diplostomoid metacercariae found in 29 of 86 pointedbelly frogs, Leptodactylus podicipinus (Cope, 1862) collected in a marsh pond in Selvíria, in the central-west region of Brazil. The metacercariae were identified as Heterodiplostomum lanceolatum Dubois, 1936 (Proterodiplostomidae), a rarely reported species that matures in snakes. In phylogenetic analysis of partial sequences from 28S rDNA, H. lanceolatum fell within a polytomy with the proterodiplostomid Crocodilicola pseudostoma (molecular divergence of 4.1%) and other members of the superfamily Diplostomoidea. Our collections provide insights into the ecology of this parasite, in that infected frogs were smaller than uninfected frogs, and metacercariae were more numerous in the abdominal cavity and hindlimb muscles than in abdominal muscles, which suggests directions for future research on the transmission and pathology of this proterodiplostomid.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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

Abdallah, VD, Azevedo, RK and Luque, JL (2006) Ecologia da comunidade parasitária do tamboatá Hoplosternum littorale (Siluriformes: Callichthyidae) do Rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Scientiarum Biological Sciences 28, 413419.Google Scholar
Amato, JFR, Boeger, WA and Amato, SB (1991) Protocolos para Laboratório: Coleta e Processamento de Parasitos de Pescado. p. 81. Seropédica, UFRRJ.Google Scholar
Ayres, M, Ayres Júnior, M, Ayres, DL and Santos, AD (2007) BioEstat: Aplicações estatísticas nas áreas das ciências biomédicas. Belém, PA, Ong Mamiraua.Google Scholar
Blasco-Costa, I and Locke, SA (2017) Life history, systematics and evolution of the Diplostomoidea Poirier, 1886: Progress, promises and challenges emerging from molecular studies. Advances in Parasitology 98, 167225.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.Google Scholar
Costa, HC and Bèrnils, RS (2018) Répteis do Brasil e suas unidades federativas: Lista de espécies. Herpetologia Brasileira 8, 1157.Google Scholar
Dubois, G (1936) Les Diplostomes de reptiles (Trematoda: Proterodiplostomidae nov. fam) du Museé de Vienne. Bulletin de la Société Neuchâteloise des Sciences Naturelles 61, 180.Google Scholar
Dubois, G (1986) Redécouverte d'un Ophiodiplostominé néotropical, Heterodiplostomum lanceolatum Dubois, 1936 (Trematoda: Strigeata: Proterodiplostomidae). Revue Suisse de Zoologie 93, 247248.Google Scholar
Dubois, G (1988) Quelques Strigeoidea (Trematoda) récoltés au Paraguay par les expéditions du Muséum d'Histoire Naturelle de Genève, au cours des années 1979, 1982 et 1985. Revue Suisse de Zoologie 95, 521532.Google Scholar
Fernandes, BMM and Kohn, A (2014) South American trematodes parasites of amphibians and reptiles. p. 228. Rio de Janeiro, Oficina de Livros.Google Scholar
Fernandez, MV and Hamann, MI (2017) Cercariae (Digenea: Strigeidae, Diplostomidae) in Biomphalaria straminea (Planorbidae) from a rice field in Northeastern Argentina. Revista de Biología Tropical 65, 551563.Google Scholar
Ferrari-Hoeinghaus, AP, Takemoto, RM and Pavanelli, GC (2007) Digenetic trematode parasites of Loricariichthys platymetopon (Loricariidae, Siluriformes) of the upper Paraná river floodplain, Brazil. Acta Scientiarum Biological Sciences 29, 327329.Google Scholar
Guidelli, GM, Isaac, A, Takemoto, RM and Pavanelli, GC (2003) Endoparasite infracommunities of Hemisorubim platyrhynchos (Valenciennes, 1840) (Pisces: Pimelodidae) of the Baía River, upper Paraná River floodplain, Brazil: specific composition and ecological aspects. Brazilian Journal of Biology 63, 261268.Google Scholar
Halliday, T (2006) Amphibians. pp. 278293 in Sutherland, WJ (Eds) Ecological census Techniques. New York, University of Cambridge.Google Scholar
Hamann, MI and González, CE (2009) Larval digenetic trematodes in tadpoles of six amphibian species from northeastern Argentina. Journal of Parasitology 95, 623628.Google Scholar
Hamann, MI, Kehr, AI and González, CE (2006) Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis in two contrasting environments from northeastern Argentina. Journal of Parasitology 92, 11711179.Google Scholar
Hernández-Mena, DI, García-Varela, M and Pérez-Ponce de León, G (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 94, 833848.Google Scholar
Kehr, AI and Hamann, MI (2003) Ecological aspects of parasitism in the tadpole of Pseudis paradoxa from Argentina. Herpetological Review 34, 336341.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Locke, SA, Van Dam, A, Caffara, M, Pinto, HA, López-Hernández, D and Blanar, CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal for Parasitology 48, 10431059.Google Scholar
López-Hernández, D, Locke, SA, Melo, AL, Rabelo, ÉML and Pinto, HA (2018) Molecular, morphological and experimental assessment of the life cycle of Posthodiplostomum nanum Dubois, 1937 (Trematoda: Diplostomidae) from Brazil, with phylogenetic evidence of the paraphyly of the genus Posthodiplostomum Dubois, 1936. Infection Genetics and Evolution 63, 95103.Google Scholar
Lunaschi, LI and Drago, FB (2010) Platyhelminthes, Trematoda, Digenea Carus, 1863: Distribution extension in Argentina and new Anura and Ophidia hosts. Check List 6, 447450.Google Scholar
Lunaschi, LI and Sutton, CA (1985) Trematodes de reptiles incorporados a la colección helmintológica del museo de La Plata. Neotropica 31, 6981.Google Scholar
Mañé-Garzón, F and Alonso, A (1976) Em nueva espécie de Digenea Strigeoidea. Heterodiplostomum helicopsis n. sp. del intestino de la culebra de água Helicops carinicaudus (Wied, 1825). Revista de Biologia del Uruguay 4, 8591.Google Scholar
Mañé-Garzón, F and Alonso, A (1979) Descripcion de la metacercaria de Heterodiplostomum lanceolatum Dubois 1936 (Digenea Strigeoidea), parasita de Leptodactylus ocellatus (L.). Revista de Biologia del Uruguay 7, 15.Google Scholar
Niewiadomska, K (2002) Family Proterodiplostomidae Dubois, 1936. pp. 215230 in Gibson, DI, Jones, A and Bray, RA (Eds) Keys to the Trematoda. 1st edn. Wallingford, UK, CABI Publishing and The Natural History Museum.Google 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.Google Scholar
Ostrowski de Núñez, M (1987) Der entwicklungszyklus von Acanthostomum brauni Mañe Garson und Gil, 1961 (Trematoda, Acanthostomatidae). Zoologische Anzeiger 218, 273286.Google Scholar
Pérez-Ponce de León, 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, 260276.Google Scholar
Pérez-Ponce de León, G, Osorio-Sarabia, D and García-Prieto, L (1992) Helmintofauna del ‘juile’ Rhamdia guatemalensis (Pisces: Pimelodidae), del lago de Catemaco, Veracruz. Revista de la Sociedad Mexicana de Historia Natural 43, 2531.Google Scholar
Pinto, HA and Melo, AL (2012) Metacercariae of Renifer heterocoelium (Trematoda: Reniferidae) in tadpoles of Rhinella Schneideri (Anura: Bufonidae) in Brazil. Revista Mexicana de Biodiversidad 83, 553556.Google Scholar
Pinto, HA and Melo, AL (2013) A checklist of cercariae (Trematoda: Digenea) in molluscs from Brazil. Zootaxa 3666, 369386.Google Scholar
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, 377391.Google Scholar
Rambaut, A (2016) FigTree-v1.4.2. 2014. Available at http://tree.bio.ed.ac.uk/software/figtree/ (accessed 6 December 2018).Google Scholar
Ronquist, F, Teslenko, M, Van der Mark, P, et al. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.Google Scholar
Ruiz, JM and Rangel, JM (1954) Estrigêidas de répteis brasileiros. Memórias do Instituto Butantan 26, 257278.Google Scholar
Schaefer, EF, Hamann, MI, Kehr, AI, González, CE and Duré, MI (2006) Trophic, reproductive and parasitological aspects of the ecology of Leptodactylus chaquensis (Anura: Leptodactylidae) in Argentina. Herpetological Journal 16, 387394.Google Scholar
Szidat, L (1969) Structure, development, and behaviour of new Strigeatoid metacercariae from subtropical fishes of South America. Journal of the Fisheries Research Board of Canada 26, 753786.Google Scholar
Tavares-Dias, M, Neves, LR and Fernandes, BMM (2011) First report of metacercariae (Digenea) infecting Astronotus ocellatus (Perciformes: Cichlidae) from the Amazon region. Brazil. Neotropical Helminthology 5, 235240.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, 115.Google Scholar
Travassos, L, Freitas, JFT and Kohn, A (1969) Trematódeos do Brasil. Memórias do Instituto Oswaldo Cruz 67, 1886.Google Scholar
Uetz, P, Freed, P and Hošek, J (2019) The reptile database. Available at http://www.reptile-database.org (accessed 21 January 2019).Google Scholar
Universidade Estadual Paulista – UNESP (2018) Dados climáticos de Ilha Solteira. Departamento de Fitossanidade, Engenharia Rural e Solos/Área de Hidráulica e Irrigação. Available at http://clima.feis.unesp.br/dados_diarios.php (accessed 4 April 2018).Google Scholar
Yamaguti, S (1975) A synoptical review of life histories of digenetic trematodes of vertebrates. 590 pp. Tokyo, Keigaku Publishing Company.Google Scholar
Supplementary material: File

Queiroz et al. supplementary material

Appendix

Download Queiroz et al. supplementary material(File)
File 32.2 KB