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Closing the knowledge gap: Helminth parasites of freshwater turtles from the Chaco-Pampa Plain, Southern South America

Published online by Cambridge University Press:  08 April 2024

Ezequiel Oscar Palumbo*
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CEPAVE), FCNyM, UNLP, CONICET, Boulevard 120 s/n e/61 y 62 (1900), La Plata, Buenos Aires, Argentina
Leandro Alcalde
Affiliation:
Instituto de Limnología Dr. R. A. Ringuelet (ILPLA), FCNyM, UNLP, CONICET, Boulevard 120 s/n e/60 y 64 (1900), La Plata, Buenos Aires, Argentina
Marcelo Bonino
Affiliation:
Laboratorio de Ecología, Biología Evolutiva y Comportamiento de Herpetozoos (LEBECH) INIBIOMA (CONICET-UNCo). Centro Regional Universitario Bariloche Quintral 1250 (8400), Bariloche, Río Negro, Argentina
Julián Lescano
Affiliation:
Instituto de diversidad y ecología animal (IDEA), CENTRO CIENTIFICO TECNOLOGICO CONICET – CORDOBA (CCT, CORDOBA) (CONICET), Córdoba, Argentina
Martín Montes
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CEPAVE), FCNyM, UNLP, CONICET, Boulevard 120 s/n e/61 y 62 (1900), La Plata, Buenos Aires, Argentina
Agustín Solari
Affiliation:
Instituto de Biología Subtropical (IBS) (CONICET/UNAM) Av. 3 Fronteras 183, Puerto Iguazú, Misiones, Argentina
Julia Inés Diaz
Affiliation:
Centro de Estudios Parasitológicos y de Vectores (CEPAVE), FCNyM, UNLP, CONICET, Boulevard 120 s/n e/61 y 62 (1900), La Plata, Buenos Aires, Argentina
*
Corresponding author: Ezequiel Palumbo; Email: epalumbo@cepave.edu.ar

Abstract

Six species of freshwater turtles dominate the Chaco-Pampa Plain in southern South America and their parasites have been relatively understudied, with most records concentrated in Brazil. Particularly in Argentina, there are only scattered records of parasites for most of the turtles that inhabit the region, leaving a large knowledge gap. The purpose of the present contribution is to increase the knowledge of the internal parasites of six species of freshwater turtles from Argentina, after 15 years of fieldwork, by providing new hosts and additional geographic records for many host-parasite relationships. Some molecular sequences of the studied parasites were provided as a tool for better species identification. We processed 433 stomach and fecal samples from live individuals and visceral and soft tissue samples from 54 dissected turtles collected from a wide range and different ecoregions. We found 6230 helminths belonging to 18 taxa (one cestode, 11 digeneans and six nematodes). Fourteen new parasite-host associations are reported here, and for the first time parasites are recorded for Phrynops williamsi. This work contributes significantly to the knowledge of the parasitofauna in freshwater turtles in Argentina, providing a detailed list of parasites present in each turtle species and reporting molecular characters for future studies.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Achatz, TJ, Brito, ES, Fecchio, A, and Tkach, VV. (2021) Description and phylogenetic position of a new species of Herpetodiplostomum from Phrynops geoffroanus in Brazil and a reevaluation of Cheloniodiplostomum. Journal of Parasitology 107, 455462. https://doi.org/10.1645/21-18.CrossRefGoogle Scholar
Alcalde, L, Derocco, NN, and Rosset, SD (2010) Feeding in syntopy: diet of Hydromedusa tectifera and Phrynops hilarii (Chelidae). Chelonian Conservation and Biology 9, 3344. https://doi.org/10.2744/CCB-0794.1.CrossRefGoogle Scholar
Alcalde, L, Derocco, NN, Rosset, SD, and Williams, JD (2012) Southernmost localities of Trachemys dorbigni and first record of Trachemys scripta for Argentina (Cryptodira: Emydidae). Chelonian Conservation and Biology 11, 128133. https://doi.org/10.2744/02k.1.CrossRefGoogle Scholar
Alcalde, L, Sánchez, RM, and Pritchard, P. (2021) Hydromedusa tectifera Cope 1870 – South American Snake-necked Turtle, Argentine Snake-necked Turtle, Tortuga Cuello de Vibora, Cágado Pescoço de Cobra. Chelonian Research Monographs 5, 117.Google Scholar
Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W, and Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 33893402. https://doi.org/10.1093/nar/25.17.3389.CrossRefGoogle ScholarPubMed
Baker, MR (1986) Falcaustra species (Nematoda: Kathlaniidae) parasitic in turtles and frogs in Ontario. Canadian Journal of Zoology 64, 228237.CrossRefGoogle Scholar
Bencke, GA, Chomenko, L, and Sant’Anna, DM (2016) O que é o Pampa? In Chomenko, L, and Bencke, GA (eds), Nosso Pampa Desconhecido. Rio Grande do Sul: Fundação Zoobotânica do Rio Grande do Sul, pp. 243354.Google Scholar
Bonfield, JK, Smith, KF, and Staden, R. (1995) A new DNA sequence assembly program. Nucleic Acids Research 23, 49924999. https://doi.org/10.1093/nar/23.24.4992.CrossRefGoogle ScholarPubMed
Bonino, M, Lescano, J, Haro, J, and Leynaud, G. (2009) Diet of Hydromedusa tectifera (Testudines-Chelidae) in a mountain stream of Córdoba province, Argentina. Amphibia-Reptilia 30, 545554.Google Scholar
Bujes, CS. (2008) Biología e conservacao de quelonios no delta do Rio Jacuí – RS: Aspectos da historia natural de especies em ambientes alterados pelo homem. Universidad Federal do Rio Grande do Sul: Porto Alegre.Google Scholar
Bush, AO, Lafferty, KD, Font, JM, and Shostak, AW (1997) Parasitology meets ecology: definitions, clarifications, examples and Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cabrera, MR, Haro, JG, and Monguillot, JC (1986) Presencia de Hydromedusa tectifera y Phrynops hilarii (Testudines: Chelidae) en la provincia de Córdoba, Argentina. Academia Nacional de Ciencias 73, 110.Google Scholar
Cagle, FR (1939) A system of marking turtles for future identification. Copeia 1939, 170173.CrossRefGoogle Scholar
Campião, KM, Ribas, A, and Tavares, LER (2015) Diversity and patterns of interaction of an anuran–parasite network in a neotropical wetland. Parasitology 142, 17511757. https://doi.org/10.1017/S0031182015001262.CrossRefGoogle Scholar
Carvalho, VT, Vogt, RC, Rojas, RR, Silva Nunes, M, Fraga, R, Ávila, RW, Rhodin, AG, Mittermeier, RA, Hrbek, T, and Farias, IP (2022) Four in one: cryptic diversity in Geoffroy’s Side-Necked Turtle Phrynops geoffroanus (Schweigger, 1812) (Testudines: Pleurodira: Chelidae) in Brazil. Diversity 14, 360.CrossRefGoogle Scholar
Cassano, MJ, and Alcalde, L. (2022) Diet and habitat of the Scorpion Mud Turtle (Kinosternon scorpioides scorpioides) in the southern limit of the species’ distribution (Argentina). Chelonian Conservation and Biology 21, 232245.CrossRefGoogle Scholar
Catto, JB, and Amato, JFR (1993) Two new species of Pseudotelorchis (Digenea, Telorchiidae) parasites of the caiman, Caiman crocodilus yacare (Reptilia, Crocodylia) from the Pantanal Mato-Grossense, Brazil. Memorias do Instituto Oswaldo Cruz 88, 561566.CrossRefGoogle Scholar
Chaviel, BM, Mascarenhas, CS, Bernardon, FF, Coimbra, MAA, and Müller, G. (2020) New records of helminths in Chelidae freshwater turtles (Testudines) in South America. Revista Brasileira de Zoociências 21, 111. https://doi.org/10.34019/2596-3325.2020.v21.28232.CrossRefGoogle Scholar
Cope, ED. (1875) Checklist of North American Batrachia and Reptilia. Bulletin of the U.S. National Museum 1, 1104.Google Scholar
Cordero, EH (1946) Ophiotaenia cohospes n. sp. de la tortuga fluvial Hydromedusa tectifera Cope, una larva plerocercoide en el parénquima de Temnocephala brevicornis Mont. y su probable metamorfosis. Comunicaciones Zoologicas del Museo de Historia Natural de Montevideo 2, 115.Google Scholar
Cribb, TH, Adlard, RD, and Bray, RA. (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology 28, 17911795. https://doi.org/10.1016/S0020-7519(98)00127-1.CrossRefGoogle ScholarPubMed
De Sousa, A, Jorge, F, Carretero, MA, Harris, DJ, Roca, V, and Perera, A. (2018) The importance of integrative approaches in nematode taxonomy: the validity of Parapharyngodon and Thelandros as distinct genera. Journal of Helminthology 93, 113. https://doi.org/10.1017/S0022149X1800069X.Google ScholarPubMed
Demkowska-Kutrzepa, M, Szczepaniak, K, Rocze-Karczmarz, M, Palumbo, EO, Studzinska, M, Rózanski, P, and Tomczuk, K. (2021) The first case of Spiroxys contortus in European pond turtle (Emys orbicularis) in the wild in Poland. International Journal for Parasitology Parasites Wildlife 16, 2629. https://doi.org/10.1016/j.ijppaw.2021.07.004.CrossRefGoogle ScholarPubMed
Di Pietro, DO, Alcalde, L, Williams, JW, and Cabrera, MO (2012) Hydromedusa tectifera (South American snake-necked turtle). Herpetological Review 43, 303.Google Scholar
Dollfus, RP. (1935) Sur crocodilicola et autres hemistomes de crocodiliens. Archives du Museum d’HistorieNaturelle, Paris 12, 637646.Google Scholar
Dubois, G. (1936) Les diplostomes de reptiles (Trematoda: Proterodiplostomidae nov. fam.) du Musée de Vienne. Bulletin de la Société Neuchâteloise des Sciences Naturelles 61, 580.Google Scholar
Dubois, G. (1968) Synopsis des strigeidae et des diplostomatidae (Trematoda) . Mémoires de la Société Neuchâteloise des Sciences Naturelles : Vol X. Switzerland: Université de Neuchatel.Google Scholar
Dubois, G. (1982) Répertoire des synonymes récents de genres et d’espèces de la superfamille des Strigeoidea Railliet, 1919 (Trematoda). Bulletin de la Société Neuchâteloise des Sciences Naturelles 105, 163183.Google Scholar
Dubois, G. (1979) Révision et nouvelle clé de determination des Diplostomesde Reptiles (Trematoda: Proterodiplostomidae Dubois, 1936). Bulletin de la Société Neuchâteloise des Sciences Naturalles 102, 3948.Google Scholar
Fernandes, BMM, and Kohn, A. (2014) South American trematodes parasites of amphibians and reptiles. Vol. 1. Rio de Janeiro: Oficina de Livros.Google Scholar
Fischathal, JH, and Kuntz, RE (1975) Some trematodes of amphibians and reptiles from Taiwan. Proceedings of the Helminthological Society of Washington 42, 113.Google Scholar
Floyd, RM, Rogers, AD, Lambshead, JD, and Smith, CR. (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5, 611612.CrossRefGoogle Scholar
Font, WF, and Lotz, JM (2009) Family Telorchiidae Looss, 1899. In Bray, RA, Gibson, DI, and Jones, A. (eds), Keys to the Trematoda. Volume 3. London: CAB International.Google Scholar
Freiberg, MA. (1945) Una nueva especie de Tortuga del genero Platemys Wagler. Physis 20, 1923.Google Scholar
Freitas, JF, and Lent, H. (1938) Pesquisas helminthologicas realisadas no Estado do Pará: II. dois novos trematodeos de Caiman sclerops Gray. Memórias do Instituto Oswaldo Cruz 33, 5356.CrossRefGoogle Scholar
Freitas, JFT, and Dobbin, JE. Jr. (1959) Telorchis diaphanus sp. n. trematódeo parasito de quelônio. Anais da Sociedade de Biologia de Pernambuco 16, 191199.Google Scholar
Freitas, JFT, and Dobbin, JE. Jr. (1967) Sobre um novo trematódeo Echinostomatidae parasito de quelônio. Memorias do Instituto Oswaldo Cruz 65, 3739.CrossRefGoogle Scholar
Gray, JE. (1831) A synopsis of the species of the class Reptilia. In Griffith, E, and Pidgeon, E. (eds), The Animal Kingdom Arranged in Conformity with its Organization, by the Baron Cuvier. Vol. 9. London: The Class Reptilia Arranged by the Baron Cuvier, with Specific Descriptions, Whittaker, Treacher & Co.Google Scholar
Hedrick, LR (1935) The life history and morphology of Spiroxys contortus (Rudolphi); Nematoda: Spiruridae. Transactions of the American Microscopical 54, 307335.CrossRefGoogle Scholar
Hudson, PJ (2002) Parasites, diversity and the ecosystem. In Thomas, F, Renaud, F, and Guégan, JF (eds), Parasitism & Ecosystems Vol. 1. New York: Oxford University Press.Google Scholar
Hudson, PJ, Dobson, AP, and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381385.CrossRefGoogle Scholar
Kimura, MA. (1980) Simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120. https://doi.org/10.1007/BF01731581.CrossRefGoogle ScholarPubMed
Larkin, MA, Blackshields, G, Brown, NP et al. (2007) Clustal Wand Clustal X version 2.0. Bioinformatics 23, 29472948. https://doi.org/10.1093/bioinformatics/btm404.CrossRefGoogle Scholar
Legler, JM (1977) Stomach flushing: a technique for Chelonian dietary studies. Herpetologica 33, 281284.Google Scholar
Littlewood, DTJ. (1994) Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution 3, 221229. https://doi.org/10.1006/mpev.1994.1024.CrossRefGoogle ScholarPubMed
Littlewood, DTJ, Curini-Galletti, M, and Herniou, EA. (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449466. https://doi.org/10.1006/mpev.2000.0802.CrossRefGoogle ScholarPubMed
Lombardero, OJ, and Moriena, A. (1977) Nuevos trematodos para la Argentina en Phrynops hilarii (Duméril y Bibron). Revista de Medicina Veterinaria 58, 6468.Google Scholar
MacCallum, M. (1921) Studies in helminthology. New York: Zoopathologica.Google Scholar
Mañé-Garzón, F, and Gil, O. (1961a) Trematodos de las tortugas del Uruguay II. Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo 97, 113.Google Scholar
Mañé-Garzón, F, and Gil, O. (1961b) Trematodos de las tortugas del Uruguay IV: Tres nuevas especies del género Telorchis Luhe, 1900. Comunicaciones Zoológicas del Museo de Historia Natural de Montevideo 90, 114.Google Scholar
Mañé-Garzón, F, and Holcman-Spector, B. (1968) Trematodos de las tortugas del Uruguay VII: Una nueva especie del género Telorchis (Lühe, 1900) del intestino de Pseudemys dorbigni (Dum. & Bib.). Comunicaciones zoológicas del museo de historia natural de Montevideo 9, 14.Google Scholar
Mañé-Garzón, F, and Holcman-Spector, B. (1969) Trematodos de las tortugas del Uruguay IX: Tres nuevas especies del género Herpetodiplostomum Dubois, 1936. Comunicaciones zoológicas del museo de historia natural de Montevideo 126, 14.Google Scholar
Mascarenhas, CS, Bernardon, FF, and Müller, G. (2016) Intestinal digeneans of freshwater turtles Phrynops hilarii and Acanthochelys spixii (Testudines: Chelidae) from southern Brazil. Revista Mexicana de Biodiversidad 87, 3541. https://doi.org/10.1016/j.rmb.2016.01.010.CrossRefGoogle Scholar
Mascarenhas, CS, and Müller, G. (2015) Spiroxys contortus (Gnathostomatidae) and Falcaustra affinis (Kathlaniidae) from Trachemys dorbigni (Emydidae) in Southern Brazil. Comparative Parasitology 82, 129136. https://doi.org/10.1654/4726.1.CrossRefGoogle Scholar
Mascarenhas, CS, and Müller, G. (2017) Camallanus emydidius n. sp. (Nematoda: Camallanidae) in Trachemys dorbigni (Dumeril & Bibron, 1835) (Testudines: Emydidae) from Southern Brazil. International Journal for Parasitology: Parasites Wildlife 6, 108114. https://doi.org/10.1016/j.ijppaw.2017.04.004.Google Scholar
Mascarenhas, CS, and Müller, G. (2021) Checklist of helminths associated with continental Testudines from South América. Neotropical Helminthology 15, 97126. https://doi.org/10.24039/rnh20211511047.CrossRefGoogle Scholar
Mascarenhas, CS, Chaviel, BM, Bernardon, FF, Wolter, JH, Coimbra, MAA, and Müller, G. (2022) Gastrointestinal helminths associated with three species of freshwater turtles in the Pampa biome, Southern Brazil. Parasitology Research 11, 19. https://doi.org/10.1007/s00436-021-07361-y.Google Scholar
McAllister, CT, Bursey, CR, and Freed, PS (2010) Helminth parasites (Cestoidea: Nematoda) of select Herpetofauna from Paraguay. Journal of Parasitology 96, 222224. https://doi.org/10.1645/GE-2191.1.CrossRefGoogle ScholarPubMed
Mereles, F, Céspedes, G, Egea-Elsam, J, and Spichger, R. (2020) Estudios fitosociológicos en el gran chaco: estructura, composición florística y variabilidad del bosque de Schinopsis balansae en el chaco húmedo boreal, Paraguay. Bonplandia 29, 3955.CrossRefGoogle Scholar
Morello, JH, Matteucci, SD, Rodríguez, AF, and Silva, ME (2012) Ecorregiones y Complejos Ecosistémicos Argentinos. Vol 1. Orientación Gráfica Editora: Buenos Aires.Google Scholar
Morgan, JAT, and Blair, D. (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111, 609615. https://doi.org/10.1017/S003118200007709X.CrossRefGoogle ScholarPubMed
Narain, D. (1930) Neodiplostomum gavialis n. sp. from the crocodile. Journal of Parasitology 16, 154157.CrossRefGoogle Scholar
Niewiadomska, K. (2002) Family Diplostomidae Poirier, 1886. In Gibson, DI, Jones, A, and Bray, RA. (eds), Keys to the Trematoda Vol. I. London: CAB International and Natural History Museum.Google Scholar
Ostrowski de Núñez, VM (1987) The life history of Acanthostomum brauni Mañé-Garzón and Gil, 1961 (Trematoda, Acanthostomatidae). Zoologischer Anzeiger 218, 273286.Google Scholar
Palumbo, EO, and Diaz, JI (2018) New species and new record of the genus Cheloniodiplostomum (Trematoda, Proterodiplostomidae, Polycotylinae), parasites of freshwater turtles from Argentina. Parasitology Research 117, 767773. https://doi.org/10.1007/s00436-018-5750-9.CrossRefGoogle ScholarPubMed
Palumbo, EO, Werneck, MR, and Diaz, JI (2019) Is Amphiorchis (Digenea: Spirorchiidae) an exclusive parasite of sea turtles? Helminthologia 6, 7580. https://doi.org/10.2478/helm-2018-0045.CrossRefGoogle Scholar
Palumbo, EO, Capasso, SC, Cassano, MJ, Alcalde, L, and Diaz, JI (2016) Spiroxys contortus (Rudolphi, 1819) and Hedruris orestiae (Moniez, 1889) in Argentine turtles. Checklist 12, 1993. https://doi.org/10.15560/12.6.1993.CrossRefGoogle Scholar
Palumbo, EO, Servián, A, Sánchez, R, and Diaz, JI (2020) A new species of Hedruris (Nematoda: Hedruridae) from freshwater turtles, its life cycle and biogeographic distribution of the genus. Journal of Helminthology 94, e93. https://doi.org/10.1017/S0022149X19000877.CrossRefGoogle Scholar
Palumbo, EO, Cassano, MJ, Alcalde, L, and Diaz, JI (2021) Seasonal variation of Hedruris dratini (Nematoda) parasitizing Hydromedusa tectifera (Chelidae), with focus on host’s torpor state. BMC Zoology 6, 10. https://doi.org/10.1186/s40850-021-00078-6.CrossRefGoogle ScholarPubMed
Palumbo, EO, Servián, A, Cassano, MJ, and Diaz, JI (2024) Camallaninae nematodes parasitizing endangered freshwater turtles from South America with the description of two new species. South America Journal of Herpetology 30, 2839. https://doi.org/10.2994/SAJH-D-21-00051.1.Google Scholar
Rodrigues, JFM, Soares, DO, and Silva, JRF (2014) Sexing freshwater turtles: penile eversion in Phrynops tuberosus (Testudines: Chelidae). Acta Herpetologica 9, 259263. https://doi.org/10.13128/Acta_Herpetol-14736.Google Scholar
Semeñiuk, MB, Alcalde, L, Sánchez, RM, and Cassano, MJ (2017) An easy, cheap, and versatile method to trap turtles, with calibrated sampling effort. South American Journal of Herpetology 12, 107116. https://doi.org/10.2994/SAJH-D-16-00048.1.CrossRefGoogle Scholar
Silva, LAF (2014) Helmintofauna associada a répteis provenientes da Reserva Particular do Patrimônio Natural Foz do Rio Aguapeí, Estado de São Paulo. Vol 1. São Paulo: Universidade Estadual Paulista.Google Scholar
Snyder, SD, and Tkach, VV. (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology 87, 14331440. https://doi.org/10.1645/0022-3395(2001)087 [1433:PABRAS]2.0.CO;2CrossRefGoogle ScholarPubMed
Sudarikov, VE (1960) Order Strigeata La Rue, 1926. Part 3. Superfamily Diplostomatoidea Nicoll, 1937. Families Alariidae Tubangui, 1922 and Bolbocephaloidea Strand, 1935. Superfamily Proterodiplostomatoidea Sudarikov, 1960. Trematodes of animals and man. Osnovy Trematodologii 18, 451694.Google Scholar
Thatcher, VE (1963) Trematodes of turtles from Tabasco, Mexico, with a description of a new species of Dadaytrema (Trematoda: Paramphistomidae). The American Midland Naturalist 70, 347355.CrossRefGoogle Scholar
Thatcher, VE (1964) Estudio sobre los trematodos de reptiles de Tabasco, Mexico: lista de huespedes y sus parasites. Anales de la Escuela Nacional de Ciencias Biológicas 13, 9196.Google Scholar
Wood, CL, and Johnson, PT (2015) A world without parasites: exploring the hidden ecology of infection. Frontiers in Ecology Environment 13, 425434.CrossRefGoogle ScholarPubMed
Zerecero, MC. (1947) Posición sistemática de Diplostomum brevis y D. cinosterni MacCallum, 1921, y descripción de un nuevo tremátodo parásito de Chelydra serpentina L. Anales del Instituto de Biología, Universidad Nacional Autónoma de México 18, 507516.Google Scholar