Introduction
Parasitism is considered one of the most successful life forms in the animal kingdom due to the number of species that have evolved parasitic adaptations (Self Reference Self1961; Poulin & Morand Reference Poulin and Morand2000; Weinstein & Kuris Reference Weinstein and Kuris2016). Metazoan endoparasites represent the largest proportion of this biological diversity (Zhang Reference Zhang2011). However, the biodiversity in many host groups, including reptiles, is underestimated (Strona & Fattorini Reference Strona and Fattorini2014; Carlson et al. Reference Carlson, Dallas, Alexander, Phelan and Phillips2020a).
Taxonomy is a constantly evolving science that relies on checklists as reference sources, regardless of the taxonomic group or geographic area of interest. The potential value of checklists in various disciplines, such as biogeography, ethology, ecology, or conservation biology, requires regular updates (Poulin et al. Reference Poulin, Besson, Morin and Randhawa2016; Dubois Reference Dubois2017).
A sequence of taxonomic checklists provides useful information on the acknowledged taxa over time. Identifying and categorizing the changes between these checklists can provide valuable insights regarding the rates of name, synonym, and circumscription alterations (Vaidya et al. Reference Vaidya, Lepage and Guralnick2018). The knowledge of endoparasite biodiversity in snakes from most countries in the Neotropical region is scarce, except for Brazil, which has studied helminth parasites of wildlife during the last century (Travassos et al. Reference Travassos, Freitas and Kohn1969; Vicente et al. Reference Vicente, de Oliveira Rodrigues, Correa Gomes and Magalhães Pinto1993; Fernandes & Kohn Reference Fernandes and Kohn2014). Although some studies are available, publications are limited and dispersed, with significant time gaps. For example, the first report of a metazoan parasite in South America was made by Alexander von Humboldt, who described the pentastomid Porocephalus crotali Humboldt, Reference Humboldt, Von Humboldt and Bonpland1812 (as Echinorhynchus crotali) from Crotalus durissus terrificus (Laurenti 1768) in northeastern Venezuela (Humboldt Reference Humboldt, Von Humboldt and Bonpland1812). More than a century later, a pentastome, Cephalobaena tetrapoda Sambon 1922 (Sambon 1922b apud Christoffersen & De Assis Reference Christoffersen and De Assis2013), collected from an unidentified viperid in northeastern Argentina, was the first metazoan parasite of snakes reported in the country.
In recent decades, in Argentina, descriptions of new species, records of distribution or new hosts, and checklists of digeneans and nematodes have been produced (Caubisens Poumarau Reference Caubisens Poumarau1965 Reference Caubisens Poumarau1968; Boero et al. Reference Boero, Led and Brandetti1972, Lunaschi & Sutton Reference Lunaschi and Sutton1985, Lunaschi & Drago Reference Lunaschi and Drago2001 Reference Lunaschi and Drago2007a Reference Lunaschi and Drago2010a; Martínez et al. Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996; Ramallo Reference Ramallo1996 Reference Ramallo2005; Lamas et al. Reference Lamas, Céspedez and Ruíz-García 2016; González et al. Reference González, Schaefer and Duré2018; Castillo et al. Reference Castillo, Acosta, González Rivas and Ramallo2020), showing the country’s growing interest in parasites of reptiles. Nevertheless, reports of other representative endoparasite groups of snakes, such as tongue worms (Arthropoda: Crustacea: Pentastomida), have not been included.
Williams & Vera (Reference William and Vera2023) reported 129 species of snakes in Argentina. This represents nearly 15% of the biodiversity of neotropical snakes (≈880 species, according to Guedes et al. Reference Guedes, Sawaya, Zizka, Laffan, Faurby, Pyron, Bérnils, Jansen, Passos, Prudente, Cisneros-Heredia, Braz, Nogueira and Antonelli2018). Considering the diversity in terms of extension and thermal variations due to the latitudinal gradient, Argentina shows an interesting richness worthy of being explored in depth (Williams & Vera Reference William and Vera2023).
Global climate change, habitat changes, and pollution are among the major drivers of parasite biodiversity loss (Marcogliese Reference Marcogliese2023); as shown through modeling, these drivers represent a constant threat to herpetofauna and associated parasites (e.g., amphibians, Campião et al. Reference Campião, Aquino Ribas, Begon, Cornell and Roland Tavares2015). Moreover, they affect the human-wildlife interface and threaten the well-being encompassed in the One Health concept (MacKenzie & Jeggo Reference Mackenzie and Jeggo2019; Prata et al. Reference Prata, Ribeiro, Rocha-Santos, Prata, Ribeiro and Rocha-Santos 2022).
This research aimed to present a checklist and literature review of metazoan endoparasites of snakes from Argentina, emphasizing the development of this topic in the last century and presenting some interesting aspects and remarks on host and parasite taxonomy.
Materials and methods
A search was carried out using several online engines (PubMed, BioOne, JSTOR, SciELO, Google Scholar, Web of Science and ScienceDirect, researchgate.com, redalyc.com) to find all the available literature on metazoan endoparasite groups in snake species or snake families from 1922 to October 2023. The keywords used for the search were: “parasite”, “metazoan”, “endoparasites”, “helminth”, “nematode”, “cestode”, “trematode”, “digenean”, “acanthocephalan”, “pentastomid”, “tongue worm”, “snake” and their equivalents in French, Spanish, German, and Portuguese.
We excluded reports of metazoan endoparasites not collected from their hosts by necropsies and reports of immature stages with uncertain taxonomic identification (such as eggs and some larvae).
The checklist includes metazoan endoparasite species from the phyla Acanthocephala, Arthropoda (subclass Pentastomida), Nematoda, and Platyhelminthes (subclass Digenea and class Cestoda) found in snakes throughout Argentina. Metazoan endoparasite systematics is based on Amin (Reference Amin1987 Reference Amin2013) for acanthocephalans, Christoffersen & De Assis (Reference Christoffersen and De Assis2013) for pentastomids, Anderson et al. (Reference Anderson, Chabaud and Willmontt2009), and Gibbons (Reference Gibbons2010) for nematodes, Khalil et al. (Reference Khalil, Jones and Bray1994) for cestodes, and Jones et al. (Reference Jones, Bray and Gibson2005), Bray et al. (Reference Bray, Gibson and Jones2008), and Fernandes & Kohn (Reference Fernandes and Kohn2014) for digeneans. Host systematics is based on Williams et al. (Reference Williams, Vera and Di Pietro2021) and Williams & Vera (Reference William and Vera2023).
Abbreviations used in the checklist:
Argentine provinces: Buenos Aires (BAS), Catamarca (CAT), Chaco (CHA), Córdoba (CBA), Corrientes (CTES), Entre Ríos (ENT), Formosa (FOR), Jujuy (JUY), La Rioja (LAR), Misiones (MIS), Salta (SAL), San Luis (SL), Santa Fe (SF), Santiago del Estero (SAN), Tucumán (TUC), undetermined locality (UND).
Museums and collections: The Helminthological Collection of Centro de Ecología Aplicada del Litoral (CECOAL), the Helminthological Collection of Museo de La Plata (MLP), the Helminthological Collection of Fundación Miguel Lillo (CH-FML), and the Zoologisches Museum Berlin (ZMB).
The type of material (holotype and paratype) records and the corresponding catalog numbers are included.
Parasitological descriptors: prevalence (P) as the number of hosts infected with one or more individuals of a particular parasite species (or taxonomic group) divided by the number of hosts examined for that parasite species, and mean intensity (MI) as the total number of parasites of a particular species found in a sample divided by the number of hosts infected with that parasite (sensu Bush et al. Reference Bush, Lafferty, Lotz and Shostak1997). Data from reports that did not specify the location of the collection were excluded.
All maps were created using QGIS 3.22 software (QGIS Development Team 2021).
Results
History of reports
Studies on metazoan endoparasites of snakes from Argentina have increased in number and scope (taxonomic studies, new host or geographic records, veterinary reports) since the first report in 1922 (Fig. 1). However, between 1941 and 1960, no reports on snake infections were published. Chronologically, the first group of metazoan endoparasites reported was the subclass Pentastomida, followed by the subclass Digenea with 22 species. The phylum Nematoda is the second group in terms of richness (8 species) and the most recently studied (Fig. 2). Most of the studies were published from 1991 onwards, and included veterinary reports (Martínez et al. Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996; Reference Martínez, Troiano, Gauna Añasco, Fescina and Jara2000; Peichoto et al. Reference Peichoto, Sánchez, López, Salas, Rivero, Teibler and Tavares2016; Bustos et al. Reference Bustos, Sánchez, Teibler and Peichoto2023), taxonomic descriptions (Lunaschi & Drago Reference Lunaschi and Drago2001 Reference Lunaschi and Drago2002), new geographic or host records (Ramallo Reference Ramallo1996 Reference Ramallo2005; Lunaschi & Drago Reference Lunaschi and Drago2010a; González et al. Reference González, Schaefer and Duré2018), and checklists (Lunaschi & Drago Reference Lunaschi and Drago2007a; Castillo et al. Reference Castillo, Acosta, González Rivas and Ramallo2020). Notably, no ecological studies have been performed on metazoan endoparasites in these hosts in the last century.
Figure 1. Types of research performed in groups of metazoan endoparasites of Argentine snakes from 1921 to 2023. TAX NR: Taxonomic article. New Record, CL: Checklist, VR: Veterinary Report.
Figure 2. Cumulative number of species of representative groups of metazoan parasites in the last 100 years. Asterisk (*) indicates years of publication of checklists.
General data, taxonomy, and diversity
Twenty-eight publications, including 20 taxonomic studies, 5 checklists, and 3 veterinarian reports, contributed 38 records (Fig. 1). Since the first description of a pentastomid in 1922, 34 metazoan endoparasites (and 1 taxa inquirenda) have been reported (Table 1) from five families of snakes in Argentina (Boidae Gray 1825, Colubridae Oppel 1811, Dipsadidae Bonaparte 1838, Elapidae Boie 1827, and Viperidae Oppel 1811) (Fig. 3). Digeneans have been found in all five families. The only family infected with parasites from all groups was Dipsadidae. No metazoan endoparasites have been reported in Anomalepididae Taylor 1939 (2 species), Leptotyphlopidae Stejneger 1892 (7 species), and Typhlopidae Merrem 1820 (1 species).
Table 1. Number of taxonomic levels by group of metazoan endoparasite and available checklists for Argentina
a Including hosts of Argentina only.
b Including hosts worldwide.
c Including South America hosts.
Figure 3. Number of species of metazoan endoparasites grouped by family of snake.
Of the 129 snake species recorded in Argentina (Williams & Vera Reference William and Vera2023), only 40 (31%) have been examined for metazoan endoparasites. Specifically, 20 (22.2%) of the 90 species of the family Dipsadidae in Argentina have been examined for metazoan endoparasites. In contrast, the largest number of specimens examined (n = 343) belong to the family Viperidae (Fig. 4).
Figure 4. Percentage of species by snake family distributed in Argentina surveyed for parasites. The number of individuals by each one is presented with the names of the families of snakes (in parenthesis).
Geographic context
Of the 23 Argentine provinces, 15 have at least one report of a metazoan endoparasite species in one snake species (Fig. 5). The highest number of reports were from the northern provinces, with 3 – 32.5% of their snake species surveyed for metazoan endoparasites. Only one snake species was surveyed in the provinces of Catamarca, Jujuy, La Rioja, Salta, and San Luis (Fig. 6). On the other hand, the highest number of metazoan endoparasite species (15 species) was found in Misiones (Fig. 5).
Figure 5. Number of metazoan endoparasite species by province.
Figure 6. Percentage of host biodiversity evaluated for parasites by province. Number of snake species are cited by Williams & Vera (Reference William and Vera2023).
Specimen and geographic data availability
Of 38 records, 25 have not been deposited in curated biological collections, and 29 lack the corresponding location data. Regarding nematodes, only two reports (Ramallo Reference Ramallo2005; González et al. Reference González, Schaefer and Duré2018) presented the deposit number and geographic coordinates. For digeneans, Lunaschi & Sutton (Reference Lunaschi and Sutton1985) and Lunaschi & Drago (Reference Lunaschi and Drago2001 Reference Lunaschi and Drago2002, Reference Lunaschi and Drago2010a) deposited specimens in biological collections. Still, only Lunaschi & Drago (Reference Lunaschi and Drago2010a) reported the geographic coordinates (Fig. 7). Regardless of the type of study, no associated molecular sequences have been described or deposited in GenBank.
Figure 7. Number of studies by (a): Material deposited in helminthological collections. (b): Geo-referenced site of study. The label on the ‘x’ axis is shared by 7(a) and 7(b).
Annotated check-list:
Phylum Acanthocephala Kohlreuther 1771.
Class Paleacanthocephala Meyer 1931.
Order Polymorphida Petrochenko 1956.
Family Centrorhynchidae Van Cleave 1916.
Centrorhynchus sp.
BAS: Villa Elisa (Partido de La Plata). Paraphimophis rusticus (Cope 1878) (= Clelia rustica) (Dipsadidae). Reference: Vizcaino (1993) apud Hernández-Orts et al. (Reference Hernández–Orts, Kutcha, Semenas, Crespo, González and Aznar2019).
CTES: Corrientes (Departamento Capital) (27°28’01’’S, 58°47’00’W). Leptophis marginatus (Cope 1862) (= Leptophis ahaetulla marginatus) (Colubridae). [P = 100% (1/1); MI = 600]. Material deposited: MLP N° 5874. Reference: Lamas & Lunaschi (Reference Lamas and Lunaschi2009).
Stage: cystacanth.
Site of infection: mesenteries.
Remarks: Centrorhynchus Van Cleave 1916 species are cosmopolitan parasites with a heteroxenous life cycle. They are found in the adult stage in birds of orders Strigiformes and Falconiformes, and occasionally in mammals, their definitive hosts (Amin Reference Amin2013). Insects are usually the intermediate hosts; snakes and amphibians act as paratenic hosts and are parasitized by cystacanths (cystic larvae) (Kennedy Reference Kennedy2006). Eight species in the adult stage have been reported in Neotropical regions. One has been described in Argentina parasitizing Guira guira (Cuculidae) from the province of Formosa (Lunaschi & Drago Reference Lunaschi and Drago2010b).
Phylum Arthropoda von Siebold 1848.
Subphylum Crustacea Brünnich 1772.
Subclass Pentastomida Diesing 1836.
Order Cephalobaenida Heymons 1935.
Family Cephalobaenidae Heymons 1922.
Cephalobaena tetrapoda Heymons 1922.
CTES: Corrientes (Departamento Capital). Pseudablabes patagoniensis (Girard 1858) (= Philodryas patagoniensis) (Dipsadidae). Reference: Bustos et al. (Reference Bustos, Sánchez, Teibler and Peichoto2023).
MIS: Santa Ana (Departamento Loreto). Leptophis marginatus (Cope 1862) (= Leptophis ahaetulla liocercus) (Colubridae). Material deposited: ZMB 48030, 48031, 48032, 48035. Reference: Heymons & Vitzthum (Reference Heymons and Vitzthum1935). Pseudablabes patagoniensis (Girard 1858) (Dipsadidae). Reference: Bustos et al. (Reference Bustos, Sánchez, Teibler and Peichoto2023).
UND: Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Lachesis alternatus) (Viperidae). Reference: Sambon (1922b) apud Christoffersen & De Assis (Reference Christoffersen and De Assis2013), Cavalieri (Reference Cavalieri1970).
Stage: adult.
Site of infection: lungs.
Remarks: data on deposited material published in Heymons (1935) are included in Röhlig et al. (Reference Röhlig, Dunlop, Grau and Friederichs2010). This species is considered the most basal of the order Cephalobaenida and its life cycle is unknown (Fain Reference Fain1966).
Order Porocephalida Sambon 1922.
Family Porocephalidae Heymons 1935.
Porocephalus crotali Humboldt Reference Humboldt, Von Humboldt and Bonpland1812.
CHA: Resistencia (Departamento San Fernando). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae). Reference: Martínez et al. (Reference Martínez, Troiano, Gauna Añasco, Fescina and Jara2000).
Stage: nymphs.
Site of infection: lungs.
Remarks: the life cycle of Porocephalus Humboldt Reference Humboldt, Von Humboldt and Bonpland1812 includes rodents and other mammal species as intermediate hosts. Nymphs and adults have been found in snakes, which serve as definitive hosts (Fain Reference Fain1966). Martínez et al. (Reference Martínez, Troiano, Gauna Añasco, Fescina and Jara2000) mentioned the host as Hydrodinastes in captivity.
Order Raillietiellida Almeida & Christoffersen 1999.
Family Raillietiellidae Sambon 1922.
Railletiella furcocerca Sambon 1922.
CTES: Corrientes (Departamento Capital). Pseudablabes patagoniensis (Girard 1858). Reference: Bustos et al. (Reference Bustos, Sánchez, Teibler and Peichoto2023).
Stage: adult.
Site of infection: lungs.
Remarks: Railletiella Sambon 1910 adults have been reported in lizards and snakes (definitive hosts); while immature stages have been found in lizards and terrestrial arthropods (Fain Reference Fain1966).
Species inquirenda
Family Cephalobaenidae Heymons 1922.
Bothropsiella bicornuta Cavalieri Reference Cavalieri1967.
UND: northeast of Argentina. Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae). Reference: Cavalieri (Reference Cavalieri1967).
Site of infection: lungs.
Remarks: Rego (1984) apud Christoffersen & De Assis (Reference Christoffersen and De Assis2013) considered this species as “taxa inquirenda”. Christoffersen & De Assis (Reference Christoffersen and De Assis2013) indicated that the holotype is deposited in Museo de La Plata, but the only female specimen studied is incomplete.
Phylum Nematoda Potts 1932.
Class Secernentea Chitwood 1950.
Order Rhabditida Chitwood 1933.
Family Rhabdiasidae Railliet 1916.
Acanthorhabdias acanthorhabdias Pereira 1927.
BAS: Los Talas (Partido de Berisso). Erythrolamprus semiaureus (Cope 1862) (= Liophis miliaris semiaureus) (Dipsadidae). Reference: Boero et al. (Reference Boero, Led and Brandetti1972).
Stage: adult.
Site of infection: lungs.
Remarks: the life cycle of Acanthorhabdias Pereira 1927 is unknown. Nevertheless, Tkach et al. (Reference Tkach, Kuzmin and Snyder2014) proposed that, like other parasites of the family Rhabdisidae, the cycle includes homogony and heterogony in parasitic and free-living phases.
Order Ascaridida Skrjabin & Schulz 1940.
Family Ascarididae Baird 1853.
Hexametra boddaerti (Baird 1860).
MIS: Parque Nacional Iguazú (Departamento Iguazú). Oxyrhopus guibei Hoge & Romano 1977 (Dipsadidae) [P = 100% (1/1); MI = 52]. Reference: Peichoto et al. (Reference Peichoto, Sánchez, López, Salas, Rivero, Teibler and Tavares2016). Erythrolamprus aesculapii (Dipsadidae) [P = 100% (1/1); MI = 52]. Reference: Bustos et al. (Reference Bustos, Sánchez, Teibler and Peichoto2023).
Stage: adult.
Site of infection: small and large intestines.
Remarks: the life cycle of Hexametra boddaerti has not been determined. However, Bowman (1987) apud Peichoto et al. (Reference Peichoto, Sánchez, López, Salas, Rivero, Teibler and Tavares2016) suggested that its life cycle could be heteroxenic, like that of Toxocara spp. Life history studies of Australian and Asian species of Ophidascaris (ascarids are closely related to the genus Hexametra) demonstrated that L2 or L3 larvae encyst in rodents preyed upon by pythons (Sprent Reference Sprent1963 Reference Sprent1970).
Family Cosmocercidae (Railliet 1916 subfamily) Travassos 1925.
Aplectana travassosi (Gomes & Motta 1967) Baker 1980.
CHA: Colonia Las Mercedes (Departamento San Fernando). Xenodon merremii (Wagler 1824) (= Waglerophis merremi) (Dipsadidae) [P = 5% (1/20); MI = 11]. Material deposited: MLP-He 7250. Reference: Lamas et al. (Reference Lamas, Céspedez and Ruíz-García2016).
Stage: adult.
Site of infection: small and large intestines.
Remarks: Aplectana Railliet & Henry 1916 has been frequently reported as a parasite of amphibians in Argentina (González & Hamann Reference González and Hamman2015). The life cycle of this genus is monoxenic; the host acquires the infection by ingesting larval stages (Anderson Reference Anderson2000). Xenodon merremii feeds exclusively on amphibians (Bellini et al. Reference Bellini, Giraudo, Arzamendia and Etchepare2015).
Order Spirurida Chitwood 1933
Family Camallanidae Railliet & Henry 1915.
Camallanus sp.
CHA: Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (1/1); MI = 19]. Material deposited: CH-FML N° 1609. Reference: Ramallo (Reference Ramallo1996).
Stage: adult.
Site of infection: esophagus.
Remarks: Camallanus Railliet & Henry 1915 is a cosmopolitan genus with a broad host specificity and has been reported in fish, amphibians, and turtles. Immature stages have been found in copepods, which act as intermediate hosts, while fish or amphibians act as paratenic hosts (Anderson Reference Anderson2000). Fish are relevant trophic components in the diet of Hydrodynastes gigas in ecosystems of Argentina (López & Giraudo Reference López and Giraudo2004; Giraudo et al. Reference Giraudo, Arzamendia, Bellini, Bessa and Costanzo 2014).
Family Physalopteridae Railliet 1893.
Physaloptera liophis Vicente & Santos 1974.
CHA: Colonia Las Mercedes (Departamento San Fernando). Xenodon merremii (Wagler 1824) (= Xenodon merremi) (Dipsadidae) [P = 20% (4/20); MI = 23]. Material deposited: MLP-He 7251. Reference: Lamas et al. (Reference Lamas, Céspedez and Ruíz-García2016).
Stage: adult.
Site of infection: stomach.
Remarks: Physaloptera Rudolphi 1819 is a genus with a broad host specificity and has been reported in amphibians, reptiles, and mammals. The life cycle of this genus is heteroxenic. Terrestrial insects are suitable intermediate hosts (Anderson Reference Anderson2000); the larval stage has been recorded in anurans, and the adult stage in lizards in the Chaco region (González et al. Reference González, Hamann and Duré2021a, Reference González, Duré, Palomas, Schaefer, Etchepare and Acostab).
Order Strongylida Chitwood 1937.
Family Diaphanocephalidae Travassos 1920.
Kalicephalus costatus (Rudolphi 1819).
ENT: Ibicuy (Departamento Gualeguaychú) (33°44’ S, 59°10’ W). Erythrolamprus semiaureus (Cope 1862) (= Liophis miliaris semiaureus) (Dipsadidae) [P = 100% (1/1); MI = 115]. Material deposited: CH-FML N° 07428, 07429. Reference: Ramallo (Reference Ramallo2005).
Stage: adult.
Site of infection: small and large intestines.
Remarks: Schad (Reference Schad1962) proposed four subspecies for K. costatus based on geographic distribution: K. costatus parvus (North America), K. costatus micrurus (Africa), K. costatus orientalis (Asia and Oceania), and K. c. costatus (Central and South America). Schad (Reference Schad1956) conducted several experiments using experimental hosts and did not find a suitable host that could cause a successful infection in snakes; for this reason, he suggested that Kalicephalus has a direct life cycle. Ramallo (Reference Ramallo2005) suggested that some specimens found in Entre Rios could be K. c. costatus.
Kalicephalus subulatus Molin 1861.
CTES: Corrientes (Departamento Capital) (27°29’33.89’’ S, 58°45’33.63’’ W). Xenodon merremii (Wagler 1824) (= Xenodon merremi) (Dipsadidae) [P = 20% (1/5); MI = 18]. Material deposited: CECOAL 16061001. Reference: González et al. (Reference González, Schaefer and Duré2018).
Stage: adult.
Site of infection: small and large intestines.
Kalicephalus sp.
CHA: Colonia Las Mercedes (Departamento San Fernando). Xenodon merremii (Wagler 1824) (= Xenodon merremi) (Dipsadidae) [P = 10% (2/20); MI = 2]. Material deposited: MLP-He 7252. Reference: Lamas et al. (Reference Lamas, Céspedez and Ruíz-García2016).
Stage: adult.
Site of infection: small and large intestines.
Phylum Platyhelminthes Gegenbaur 1859.
Class Cestoda Rudolphi 1808.
Order Onchoproteocephalida Caira, Jensen, Waeschenbach, Olson & Littlewood 2014.
Family Proteocephalidae La Rue 1911.
Ophiotaenia racemosa (Rudolphi 1819) La Rué 1911.
BAS: Los Talas (Partido de Berisso). Erythrolamprus semiaureus (Cope 1862) (= Liophis miliaris semiaureus) (Dipsadidae). Reference: Boero et al. (Reference Boero, Led and Brandetti1972).
Stage: adult.
Site of infection: small intestine.
Remarks: the life cycle of this species is unknown, but Scholz & De Chambrier (Reference Scholz and De Chambrier2003) suggested it could be indirect, mediated by a copepod as an intermediate host.
Class Trematoda Rudolphi 1808.
Subclass Digenea Carus 1863.
Order Plagiorchiida La Rue 1957.
Family Diplodiscidae Cohn 1904
Catadiscus dolichocotyle (Cohn 1903) Cohn 1904
FOR: La Marcela farm (Departamento Pirané) (26°17’35’’S, 59°06’67’’W). Philodryas sp. (Dipsadidae) [P = 100% (1/1)]; MI = 4]. Material deposited: MLP N° 5515. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
Stage: adult.
Site of infection: large intestine.
Remarks: species belonging to the genus Philodryas Wagler 1830 have recently been relocated into various genera: Chlorosoma Wagler 1830, Incaspis Donoso Barros 1974, Pseudablabes Boulenger 1896, Tropidodryas (Fitzinger 1843), and Xenoxybelis Machado 1993 by Melo-Sampaio et al. (Reference Melo-Sampaio, Passos, Martis, Moura-Leite, Morato, Venegas, Chávez, Venâncio and De Souza2020). Two genera, Pseudablabes and Philodryas, are present in Argentina (Williams & Vera Reference William and Vera2023). In this context, the host identification provided by Lunaschi & Drago (Reference Lunaschi and Drago2010b), Philodryas sp., does not allow us to know the actual taxonomic position of the host examined. The snail Drepanotrema kermatoides (D’Orbigny 1835) (Gastropoda: Planorbidae) has been mentioned by Lunaschi & Drago (2007) as a possible first intermediate host in the life cycle of Catadiscus species in natural systems in Argentina.
Catadiscus freitaslenti Ruiz 1943.
CBA: Chilibroste (Departamento Unión). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 8]. Jesús María (Departamento Colón). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 7]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CHA: Las Palmas (Departamento Las Palmas). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 3]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Itá Ibaté (Departamento General Paz). Erythrolamprus almadensis (Wagler 1824) (= Liophis almadensis) (Dipsadidae) [P = 100% (1/1); MI = 6]. Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (2/2); MI = 2.5]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
ENT: La Calandria (Departamento Federal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 2]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
MIS: Posadas (Departamento Capital). Bothrops diporus Cope 1862 (= Bothrops neuwiedi meridionalis) (Viperidae) [P=100% (1/1); MI = 3]; Lygophis flavifrenatus Cope 1862 (Dipsadidae) [P = 100% (1/1); MI = 3]. Puerto Esperanza (Departamento Iguazú). Erythrolamprus aesculapii (Linnaeus 1758) (Dipsadidae) [P = 50% (1/2); MI = 6]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SAN: Los Juries (Departamento General Taboada). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 1]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Fortin Olmos (Departamento Vera). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 6]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small and large intestines.
Catadiscus longicoecalis Caubisens Poumarau Reference Caubisens Poumarau1965.
CHA: Las Palmas (Departamento Las Palmas). Bothrops diporus Cope 1862 (= Bothrops neuwiedi meridionalis) [P = 100% (1/1); MI = 4]. References: Caubisens Poumarau (Reference Caubisens Poumarau1965 Reference Caubisens Poumarau1968).
SAL: Padre Lozano (Departamento General José de San Martín). Philodryas olfersii (Lichenstein 1823) (Dipsadidae) [P = 100% (1/1); MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Lucita (?) (Departamento San Cristóbal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 4]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small and large intestines.
Remarks: in Caubisens Poumarau (Reference Caubisens Poumarau1968), “Lucita” could be a misspelling of “La Lucila,” a locality in the province of Santa Fe.
Catadiscus uruguayensis Freitas & Lent 1939.
BAS: Laguna Salada Grande (Partido de General Lavalle). Erythrolamprus poecilogyrus (Wied-Neuwied 1825) (= Liophis poecilogyrus) (Dipsadidae) [P = 100% (1/1)]. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2002).
Stage: adult.
Site of infection: small and large intestines.
Remarks: Catadiscus uruguayensis has been previously reported as a parasite of Boana pulchella (Duméril & Bibron 1841) (= Hypsiboas pulchellus) tadpoles, Leptodactylus luctator (Hudson 1892) (= Leptodactylus ocellatus), and Pseudis minuta Günther 1858 in Argentina (Lunaschi & Drago Reference Lunaschi and Drago2007a).
Family Plagiorchiidae Lühe 1901.
Glossidiella ornata Travassos 1927
BAS: Zoológico de La Plata (Partido de La Plata). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (1/1); MI = 2]. Material deposited: MLP N° 1044 D. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
CHA: Las Palmas (Departamento Las Palmas). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 79]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Juan José Castelli (Departamento General Güemes). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
CTES: Bella Vista (Departamento Bella Vista). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 192]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Ituzaingó (Departamento Ituzaingó), Paso de los Libres (Departamento Paso de Los Libres), San Cayetano (Departamento Capital), San Cosme (Departamento San Cosme), San Luis del Palmar (Departamento San Luis del Palmar), Santa Ana (Departamento San Cosme). Hydrodynastes gigas (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
ENT: Estación Federal (Departamento Federal). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 14]. La Paz (Departamento La Paz). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small and large intestines.
Remarks: Travassos (Reference Travassos1927a) described “Glassidiella” as a new genus and established “Glassidiella ornada” as type species. In this work, the type of host was incorrectly named (“Cunectes murinus” instead of “Eunectes murinus”). Strikingly, in another work published the same year, Travassos described “Glassidiella ornata” (Travassos Reference Travassos1927b). The work included measurements but not drawings, which are fundamental for accurate identification. In a third publication the same year, the author changed the spelling of the genus to “Glossidiella” and the spelling of the type species to “Glossidiella ornata” (Travassos Reference Travassos1927c). In addition to the previous measurements (Travassos Reference Travassos1927a; Travassos Reference Travassos1927b), drawings were included. Finally, in 1928, Travassos emended the type of host to Cyclagras gigas (= Hydrodynastes gigas).
Two groups of authors argue the stability of the names “Glassidiella” for the genus and “Glassidiella ornata” for the type species by law of priority (Caubisens Poumarau Reference Caubisens Poumarau1968; Lunaschi & Sutton Reference Lunaschi and Sutton1985; Lunaschi & Drago Reference Lunaschi and Drago2007a). Other authors support the validity of “Glossidiella” and “Glossidiella ornata”, and recently described a new species of this genus and compared it with the type of material deposited in the Helminthological Collection of the Instituto Oswaldo Cruz (Glossidiella peruensis by Huancachoque et al. Reference Huancachoque, Saéz, Cruces, Mendoza, Luque and Chero2020).
Travassos first stated that the new genus was morphologically “very close to Glassidium” (Travassos Reference Travassos1927a Reference Travassos1927b) and later that it was like “Glossidium” (Travassos Reference Travassos1927c). In our opinion, Travassos made an unclear etymological reference based on Glossidium Looss Reference Looss1899 (see Looss Reference Looss1899), because he temporally placed Glossidioides loosi (Travassos Reference Travassos1927a Reference Travassos1927c) and Glossidium ornatum within that genus (nomen in schedula in the online catalog of the Helminthological Collection of the Fundaçao Oswaldo Cruz, 2023). In this regard, Travassos et al. (Reference Travassos, Freitas and Kohn1969) and Fernandes & Kohn (Reference Fernandes and Kohn2014) called it Glossidella based on a single source (Travassos Reference Travassos1927c). This nomenclature confusion should be resolved in an additional paper, where automatic corrections or justified emendations could be clarified, as appropriate in each case.
In Lunaschi & Sutton (Reference Lunaschi and Sutton1985), the host was cited as “Hydrodinastes”. The data supplied by Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) appear to be general and did not differentiate among the seven locations where they reported the presence of this species in the host. The life cycle of this species is unknown.
Glossidioides loosi (Travassos 1927) Yamaguti Reference Yamaguti1958
BAS: Zoológico de La Plata (Partido de La Plata). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (1/1); MI = 37]. Material deposited: MLP N° 1044 D. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
CHA: Las Palmas (Departamento Las Palmas). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (3/3); MI = 132]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Juan José Castelli (Departamento General Güemes). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
CTES: Bella Vista (Departamento Bella Vista). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 111]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Ituzaingó (Departamento Ituzaingó), Paso de Los Libres (Departamento Paso de Los Libres), San Cayetano (Departamento Capital), San Cosme (Departamento San Cosme), San Luis del Palmar (Departamento San Luis del Palmar), Santa Ana (Departamento San Cosme). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
ENT: Estación Federal (Departamento Federal). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 3]. La Paz (Departamento La Paz). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 8]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adults.
Site of infection: trachea, lungs.
Remarks: this species was originally described and named as “Glassidium loosi” (Travassos Reference Travassos1927a), and then as “Glossidium loosi“ (Travassos Reference Travassos1927c). In both descriptions, the author stated the similarity of his material with “Glassidium” (Travassos Reference Travassos1927a) and “Glossidium” (Travassos Reference Travassos1927c). “Glossidium” was the spelling linked to a previously described taxon [Glossidium, described in Looss (Reference Looss1899)]. Later, Yamaguti (Reference Yamaguti1958) created the genus Glossidioides and assigned Glossidioides loosi as type species.
Haplometroides buccicola Odhner 1910.
MIS: Arroyo Cuñá Pirú (Departamento Cainguás) (27°05’14’’ S, 54°57’11’’ W). Micrurus corallinus (Merrem 1820) (Elapidae) [P = 100% (1/1); MI = 1]. Material deposited: MLP N° 5505. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a). Puerto Esperanza (Departamento Iguazú). Micrurus frontalis Duméril, Bibron & Duméril 1854 (Elapidae) [P = 100% (1/1); MI = 2]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adults.
Site of infection: esophagus, lungs.
Remarks: the life cycle of Haplometroides buccicola is unknown.
Plagiorchis luehei Travassos 1927
BAS: La Plata Zoo (Partido de La Plata). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (1/1); MI = 37]. Material deposited: MLP N° 1044 D. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
CHA: Las Palmas (Departamento Las Palmas). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (3/3); MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Juan José Castelli (Departamento General Güemes). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
CTES: Bella Vista (Departamento Bella Vista). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 81]. Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 20]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Ituzaingó (Departamento Ituzaingó), Paso de Los Libres (Departamento Paso de Los Libres), San Cayetano (Departamento Capital), San Cosme (Departamento San Cosme), San Luis del Palmar (Departamento San Luís del Palmar), Santa Ana (Departamento San Cosme), Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
FOR: El Colorado (Departamento Pirané) (26°18’ S, 59° 22’ W). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (1/1); MI = 13]. Material deposited: MLP N° 5501, 5502. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
Stage: adult.
Site of infection: esophagus, lungs.
Remarks: Caubisens Poumarau (Reference Caubisens Poumarau1968), Lunaschi & Sutton (Reference Lunaschi and Sutton1985), and Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) have reported this species as Microderma luhei. In Lunaschi & Sutton (Reference Lunaschi and Sutton1985), the host is cited as Hydrodinastes, possibly due to a typographical error. The prevalence and mean intensity data presented by Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) include the sum of all hosts examined without distinction among localities and only the maximum value reached by the mean intensity of all species of helminths.
Styphlodora condita Faria 1911
CBA: Arroyito (Departamento San Justo). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 30]. Modesto Pizarro (?) (Departamento General Roca). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 30]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CHA: Juan José Castelli (Departamento General Güemes). Micrurus pyrrhocryptus (Cope 1862) (Elapidae) [P = 100% (1/1); MI = 6]. Corzuela (Departamento General Belgrano). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 7]. Km 38, El Zapallar (Departamento Libertador General San Martín). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 7]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Bella Vista (Departamento Bella Vista). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (2/2); MI = 12]. Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (2/2); MI = 20]. Itá Ibaté (Departamento General Paz). Xenodon dorbyngyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbyngyi) (Dipsadidae) [P = 100% (2/2); MI = 14]. Mercedes (Departamento Mercedes). Palusophis bifossatus (Raddi 1820) (= Drymobius bifossatus) (Colubridae) [P = 100% (1/1); MI = 7]. San Roque (Departamento San Roque). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) [P = 100% (1/1); MI = 20]. Santo Tomé (Departamento Santo Tomé). Oxyrhopus rhombifer Duméril, Bibron & Duméril 1854 (Dipsadidae) [P = 100% (1/1); MI = 16]. Yapeyú (Departamento San Martín). Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) [P = 100% (1/1); MI = 8]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
ENT: Gualeguaychú (Departamento Gualeguaychú). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 4]. Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 1/1; MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: Formosa (Departamento Formosa). Micrurus pyrrhocryptus (Cope 1862) (Elapidae) [P = 100% (1/1); MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Clorinda (Departamento Pilcomayo). Eunectes notaeus Cope 1862 (Boidae). Reference: Boero et al. (Reference Boero, Led and Brandetti1972).
SAL: Orán (Departamento Orán). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Malabrigo (Departamento General Obligado). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 15]. Campo Garay (Departamento Nueve de Julio). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (2/2); MI = 15]. Lucita (?) (Departamento San Cristóbal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 17]. Huanqueras (Departamento San Cristóbal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 15] Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CAT: Las Lajas (Departamento Paclín). Pseudablabes patagoniensis (Girard 1858) (= Philodryas schottii) (Dipsadidae) [P = 100% (1/1); MI = 8]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
UND: Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae), Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae), Xenodon merremii (Wagler 1824) (Dipsadidae). Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: ureters, renal canalicles, kidneys.
Remarks: metacercariae of Styphlodora Loos 1899 have been found in the liver and kidneys of Odonthophrynus asper (Philippi 1902) (= O. americanus) and Elachistocleis bicolor (Guérin-Méneville 1838) tadpoles in Argentina (Hamman & González Reference Hamann and González2009). Snails are obligate and first intermediate hosts, while tadpoles could be second intermediate hosts in the life cycle of this digenean (Hamman & González Reference Hamann and González2009). “Las Lajas” is a locality in the province of Catamarca, adjacent to the province of Tucumán; probably this is why Las Lajas has been indicated as being part of Tucumán by Caubisens Poumarau (Reference Caubisens Poumarau1968). “Lucita” could be a misspelling of “La Lucila,” a locality in the province of Santa Fe. In Caubisens Poumarau (Reference Caubisens Poumarau1968). Dryophylax hypoconia (= Thamnodynastes hypoconia) has been originally cited as Thamnodynastes pallidus by Caubisens Poumarau (Reference Caubisens Poumarau1968). Thamnodynastes pallidus is found in other South American countries (Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Perú, Suriname, and Venezuela), and does not reach Argentina in its southernmost distribution (Uetz et al. Reference Uetz, Koo, Aguilar, Brings, Catenazzi, Chang, Chaitanya, Freed, Gross, Hammermann, Hosek, Lambert, Sergi, Spencer, Summers, Tarvin, Vredenburg and Wake2021).
Travtrema stenocotyle (Cohn 1902) Goodman 1951.
BAS: Buenos Aires. Erythrolamprus poecilogyrus (Wied-Neuwied 1825) (= Liophis poecilogyrus) (Dipsadidae). Reference: Ostrowski de Nuñez (1979) apud Fernandes & Kohn (Reference Fernandes and Kohn2014). Las Talas (Partido de Berisso). Erythrolamprus semiaureus (Cope 1862) (= Liophis miliaris semiaureus) (Dipsadidae). Reference: Boero et al. (Reference Boero, Led and Brandetti1972). Punta Lara (Partido de Ensenada), Villa Elisa, City Bell (Partido La Plata). Erythrolamprus jaegeri (Günther 1858) (= Liophis jaegeri) (Dipsadidae), Paraphimophis rustica (= Clelia rustica) (Dipsadidae), Pseudablabes patagoniensis (Girard 1858) (= Philodryas patagoniensis) (Dipsadidae) [P = 100% (3/3), MI = 18]. Material deposited: MLP N° 1101 C 1137 C 1142 C. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
CBA: Arroyito (Departamento San Justo), Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 14]. Calamuchita (Departamento Calamuchita), Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 1/1; MI = 20]. Córdoba, Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 5]. Jesús María, Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 33]. Modesto Pizarro (?) (Departamento General Roca), Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (2/2); MI = 43]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CHA: Colonia Benítez (Departamento Primero de Mayo). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 14]. Corzuela (Departamento General Belgrano). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 24]. Las Palmas (Departamento Las Palmas). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 21], Xenodon merremii (Wagler 1824) [P = 100% (1/1); MI = 46]. Km. 38 El Zapallar (Departamento Libertador General San Martín). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 18], Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 59]. Quitilipi (Departamento Quitilipi). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 2]. Río Muerto (Departamento Almirante Brown). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Goya (Departamento Goya). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 38]. Paso de Los Libres (Departamento Paso de Los Libres). Bothrops diporus Cope 1862 (= Bothrops neuwiedii diporus) (Viperidae) [P = 66.7% (10/15), MI = 10]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). San Cosme (Departamento San Cosme), Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 33]. Santa Ana (Departamento San Cosme). Bothrops diporus (= Bothrops neuwiedii diporus) [P = 66.7% (10/15), MI = 10]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). San Roque (Departamento San Roque). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 6]. Sauce (Departamento Sauce). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 20]. Yapeyú. Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) [P = 100% (3/3); MI = 41]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
ENT: La Calandria (Departamento Federal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 215]. La Paz (Departamento La Paz). Xenodon merremii (Wagler 1824) [P = 100% (1/1); MI = 43]. Nogoyá (Departamento Nogoyá). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) [P = 100% (1/1); MI = 13]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
LAR: Chilecito (Departamento Chilecito). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 20]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
MIS: Eldorado (Departamento Eldorado). Dipsas ventrimaculatus (= Sibynomorphus ventrimaculatus) (Dipsadidae) [P = 100% (1/1); MI = 260]. Posadas (Departamento Capital). Lygophis flavifrenatus (Dipsadidae) [P = 100% (1/1), MI = 23]. Santo Pipó (Departamento San Ignacio). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 3]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SAN: Los Jiries (Departamento General Taboada). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 24]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Campo Garay (Departamento Nueve de Julio). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 20]. Fortin Olmos (Departamento Vera). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1); MI = 126]. Huanqueras (Departamento San Cristóbal). Xenodon dorbingyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbingyi) (Dipsadidae) [P = 100% (1/1); MI = 20]. Lucita (?) (Departamento San Cristóbal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1); MI = 20]. Malabrigo (Departamento General Obligado). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (2/2); MI = 86]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SL: El Trapiche (Departamento Coronel Pringles). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 90]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
TUC: La Cocha (Departamento La Cocha). Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae) [P = 100% (1/1); MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
UND: Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae), Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae), Xenodon merremii (Wagler 1824) (Dipsadidae). Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small and large intestines.
Remarks: the prevalence and mean intensity data in Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) are general and do not discriminate among the four localities where the helminth species has been reported to be present in the hosts. Metacercariae of Travtrema aff. stenocotyle have been found in the body cavity, mesentery, pharyngfal region, muscle, liver, and tegument of Scinax nasicus Wagler 1930, Elachistocleis bicolor (Guérin-Méneville 1838), Leptodactylus latinasus (Jiménez de la Espada 1875), Odontophrynus asper (Philippi 1902) (= O. americanus), Physalaemus cristinae Cardozo, Tomatis, Duport-Bru, Kolenc, Borteiro, Pansonato, Confalonieri, Lourenço, Haddad, & Baldo 2023 (= P. albonotatus), and P. santafecinus (Barrio 1965) tadpoles in Argentina (Hamman & González Reference Hamann and González2009). Tadpoles could be second intermediate hosts in the life cycle of this digenean (Hamman & González Reference Hamann and González2009). Adults of this species have been found in Leptodactylus podicipinus (Cope 1862), so anurans could act as definitive hosts too (Campião et al. Reference Campião, da Silva and Ferreira2009). The actual name of the locality mentioned above as “Modesto Pizarro’’ is “Modestino Pizarro.” “Lucita” could be a misspelling of “La Lucila,” a locality in the province of Santa Fe in Caubisens Poumarau (Reference Caubisens Poumarau1968). Dryophylax hypoconia (= Thamnodynastes hypoconia) has been originally cited as Thamnodynastes pallidus by Caubisens Poumarau (Reference Caubisens Poumarau1968), see comments on this species in the remarks on Styphlodora condita.
Family Dicrocoeliidae Odhner 1910
Infidum infidum (Faria 1910) Travassos 1916.
CHA: Colonia Benítez (Departamento Primero de Mayo). Eunectes notaeus (Boidae) [P = 100% (1/1); MI = 20]. Juan José Castelli (Departamento General Güemes). Hydrodynastes gigas [P = 100% (25/25); MI = 80]. Las Palmas (Departamento Las Palmas). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (3/3); MI = 18]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968), Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
CTES: Santa Ana (Departamento San Cosme), Paso de Los Libres (Departamento Paso de Los Libres). Bothrops diporus Cope 1862 (= Bothrops neuwiedi diporus) [P = 66.67% (10/15); MI = 10]. Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Ituzaingó (Departamento Ituzaingó), San Cayetano (Departamento Capital), San Cosme (Departamento San Cosme), San Luis del Palmar (Departamento San Luis del Palmar). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
ENT: La Paz (Departamento La Paz). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1); MI = 20]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: Pozo del Tigre (Departamento Patiño). Philodryas psammophidea Günther 1872 (Dipsadidae) [P = 100% (1/1); MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: gallbladder.
Remarks: the prevalence and mean intensity data in Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) are general and do not discriminate among the seven localities where the helminth species has been reported to be present in the hosts. The life cycle of this digenean is unknown, but adults of this species have been found in Leptodactylus podicipinus (Cope 1862) by Campião et al. (Reference Campião, da Silva and Ferreira2009). Considering that only one sample of each of these species was found in L. podicipinus, these might be cases of accidental parasitism; thus, anurans could also act as definitive hosts.
Infidum similis Travassos 1916.
SAL: Padre Lozano (Departamento General José de San Martín). Philodryas olfersii (Lichenstein 1823) (Dipsadidae) [P = 100% (1/1); MI = 6]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: La Marcela farm (Departamento Pirané) (26°17’35’’ S, 59°06’67’’ W). Philodryas sp. (Dipsadidae) [P = 100% (1/1); MI = 2]. Material deposited: MLP N° 5516. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
Stage: adult.
Site of infection: gallbladder.
Family Mesocoeliidae Dollfus 1929.
Mesocoelium monas (Rudolphi 1819) Freitas 1958.
BAS: General Rodriguez (Partido de General Rodriguez). Tomodon ocellatus Duméril, Bibron & Duméril 1854 (Dipsadidae) [P = 100% (1/1); MI = 115]. San Miguel (Partido de San Miguel). Tomodon ocellatus Duméril, Bibron & Duméril 1854 (Dipsadidae) [P = 100% (2/2); MI = 89]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). La Plata (Partido de La Plata). Tomodon ocellatus Duméril, Bibron & Duméril 1854 (Dipsadidae). Reference: Led & Boero (Reference Led and Boero1973).
CHA: Gancedo (Departamento Doce de Octubre). Dipsas ventrimaculatus (Boulenger 1885) (= Sibynomorphus ventrimaculatus) (Dipsadidae) [P = 100% (1/1); MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Arroyo El Sombrerito (Departamento Capital) (27°38’ S, 58°44’ W). Dipsas sp. (= Sibynomorphus sp.) (Dipsadidae) [P = 100% (1/1); MI = 13]. Material deposited: MLP N° 5512. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
ENT: La Paz (Departamento La Paz). Dipsas turgida Cope 1868 (= Sibynomorphus turgidus) (Dipsadidae) [P = 100% (2/2); MI = 33]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
MIS: Eldorado (Departamento Eldorado). Dipsas ventrimaculatus (Boulenger 1885) (= Sibynomorphus ventrimaculatus) (Dipsadidae) [P = 100% (2/2); MI = 166]. Posadas (Departamento Capital). Dipsas turgida Cope 1868 (= Sibynomorphus turgidus) (Dipsadidae) [P = 100% (1/1); MI = 10]. Puerto Esperanza (Departamento Iguazú). Dipsas ventrimaculatus (Boulenger 1885) (= Sibynomorphus ventrimaculatus) (Dipsadidae) [P = 100% (2/2); MI = 38]. Puerto Leoni (Departamento Libertador General San Martín). Dipsas turgida Cope 1868 (= Sibynomorphus turgidus) (Dipsadidae) [P = 100% (2/2); MI = 110]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small intestine.
Remarks: Mesocoelium monas has been reported as a parasite of Rhinella diptycha (Cope 1862) (= Rhinella schneideri) in Argentina (Lunaschi & Drago Reference Lunaschi and Drago2010a). Thomas (Reference Thomas1965) described the life history of Mesocoelium monodi, determining that a terrestrial gastropod is the first intermediate host and metacercariae could be found encysted in two species of ants.
Mesocoelium sibynomorphi Ruiz & Leão 1949
MIS: Posadas (Departamento Capital). Dipsas turgida Cope 1868 (= Sibynomorphus turgidus) (Dipsadidae) [P = 100% (1/1); MI=19]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small intestine.
Family Opisthogonimidae Travassos Reference Travassos1928.
Opisthogonimus artigasi Ruiz & Leão 1942
CBA: Deán Funes (Departamento Ischilín). Philodryas psammophidea (Dipsadidae) [P = 100% (1/1); MI = 1]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CHA: Las Palmas (Departamento Las Palmas). Palusophis bifossatus (Raddi 1820) (= Drymobius bifossatus) (Colubridae) [P = 100% (1/1); MI = 34]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Yapeyú (Departamento General San Martín). Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) (Dipsadidae) [P = 100% (2/2); MI = 20]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: Pozo del Tigre (Departamento Patiño). Philodryas psammophidea (Dipsadidae) [P = 100% (1/1); MI = 4]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
MIS: Posadas (Departamento Capital). Erythrolamprus poecilogyrus schotti (Schlegel 1837) (= Leimadophis typhlus) [P = 100% (1/1); MI = 3]. Eldorado (Departamento Eldorado). Dryophylax hypoconia (Cope 1860) (=Thamnodynastes hypoconia) [P = 100% (1/1); MI = 17.] Puerto Esperanza (Departamento Iguazú). Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) [P = 100% (1/1); MI = 24]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SAN: Santiago del Estero (Departamento Juan Francisco Borges). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbinyi) (Dipsadidae) [P = 1/1; MI = 8]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
UND: Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia), Bothrops jararaca (Wied-Neuwied 1824) (Viperidae). Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: mouth.
Remarks: metacercariae of Opisthogonimus Lühe 1900 have been found parasitizing the body cavity, muscle, pharyngeal region, and tegument of Odontophrynus asper (Philippi 1902) (= O. americanus) and Physalaemus santafecinus (Barrio 1965) tadpoles (Hamman & González Reference Hamann and González2009), and adults of Scinax nasicus Wagler 1930 (Hamman et al. Reference Hamann, Kehr, González, Duré and Schaefer2009). Dryophylax hypoconia (= Thamnodynastes hypoconia) has been originally cited as Thamnodynastes pallidus by Caubisens Poumarau (Reference Caubisens Poumarau1968), see comments on this species in the remarks on Styphlodora condita. The life cycle of Opisthogonimus species is unknown.
Opisthogonimus fonsecai Ruiz & Leão 1942
BAS: Los Talas (Partido de Berisso). Erythrolamprus semiaureus (= Liophis miliaris semiaureus) (Dipsadidae). Reference: Boero et al. (Reference Boero, Led and Brandetti1972).
MIS: Aristóbulo del Valle (Departamento Cainguás). Xenodon merremii (Wagler 1824) (Dipsadidae) (= Waglerophis merremii). [P = 100% (1/1); MI = 41]. Material deposited: MLP N° 4589. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2001).
Stage: adult.
Site of infection: esophagus, small and large intestines.
Opisthogonimus interrogativus (Nicoll) Pereira 1928
MIS: Aristóbulo del Valle (Departamento Cainguás). Xenodon merremii (Wagler 1824) (= Waglerophis merremii) (Dipsadidae) [P = 100% (1/1); MI = 2]. Material deposited: MLP N° 4589. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2001).
Stage: adult.
Site of infection: small and large intestines.
Opisthogonimus lecithonotus Lühe 1900
BAS: Coronel Pringles (Partido de General Pringles). Bothrops alternatus (= Bothrops alternata) Duméril, Bibron & Duméril 1854 [P = 100% (1/1), MI = 3]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CBA: Arroyito (Departamento San Justo). Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 14]. Córdoba (Departamento Capital). Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 17]. Cruz del Eje (Departamento Cruz del Eje). Lygophis anomalus (Günther 1858) (= Liophis anomalus) [P = 100% (1/1), MI = 15]. Jesús María (Departamento Colón). Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 15]. Yacasto de Calamuchita (Departamento Calamuchita). Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 13]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CHA: Colonia Benítez (Departamento Primero de Mayo). Erytrhrolamprus poecilogyrus caesius (Cope 1862) (= Leimadophis typhlus) [P = 100% (1/1), MI = 10]. Corzuela (Departamento General Belgrano). Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 1]. El Zapallar (Departamento Libertador General San Martín). Bothrops diporus (= Bothrops neuwiedii meridionalis) [P = 100% (1/1), MI = 15]. Juan José Castelli (Departamento General Güemes). Hydrodynastes gigas [P = 100% (25/25), MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). Las Palmas (Departamento Las Palmas). Bothrops diporus (= Bothrops neuwiedii meridionalis) [P = 100% (1/1), MI = 21]. Xenodon merremii (Wagler 1824) [P = 100% (1/1), MI = 61]. Machagai (Departamento Veinticinco de Mayo). Bothrops alternatus Duméril, Bibron & Duméril 1854 (Viperidae) [P = 50% (10/20), MI = 20]. Bothrops moojeni Hoge 1966 (Viperidae) [P = 100% (5/5), MI = 10]. Quitilipi (Departamento Quitilipi). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1), MI = 6]. Resistencia (Departamento San Fernando). Micrurus pyrrhocryptus (Cope 1862) (Elapidae) [P = 100% (2/2), MI = 5]. Roque Saenz Peña (Departamento Comandante Fernández). Bothrops moojeni Hoge 1966 [P = 100% (5/5), MI = 10], Erytrholamprus poecilogyrus caesius (Cope 1862) (= Leimadophis typhlus) [P = 100% (1/1), MI = 4]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Alvear (Departamento General Alvear). Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) [P = 100% (1/1), MI = 1]. Bella Vista (Departamento Bella Vista). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1), MI = 1]. Corrientes (Departamento Capital). Helicops leopardinus (Schlegel 1837) (= Helicops leopardina) (Dipsadidae) [P = 100% (1/1), MI = 23]. Itá Ibaté (Departamento General Paz). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1), MI = 10]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968). Ituzaingó (Departamento Ituzaingó). Bothrops alternatus Duméril, Bibron & Duméril 1854 (Viperidae) [P = 50% (10/20), MI = 20], Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25), MI = 80]. Mesotes strigatus (Günther 1858) (= Thamnodynastes strigatus) [P = 100% (20/20), MI = 20]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). Mercedes (Departamento Mercedes). Palusophis bifossatus (Raddi 1820) (= Drymobius bifossatus) (Colubridae) [P = 100% (1/1), MI = 38]. Santa Ana (Departamento San Cosme). Helicops infrataeniatus Jan 1865 (= Helicops carinicauda) (Dipsadidae) [P = 100% (10/10), MI = 20]. Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) [P = 100% (25/25), MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). San Cayetano (Departamento Capital). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25), MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). San Cosme (Departamento San Cosme). Helicops infrataeniatus Jan 1865 (= Helicops carinicauda) (Dipsadidae) [P = 100% (10/10), MI = 20]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). San Luis del Palmar (Departamento San Luis del Palmar). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25), MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996). Paso de Los Libres (Departamento Paso de Los Libres). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25), MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996), Yapeyú (Departamento General San Martín). Dryophylax hypoconia (Cope 1860) (= Thamnodynastes hypoconia) [P = 100% (1/1), MI = 1]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
ENT: Gualeguaychú (Departamento Gualeguaychú). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1), MI = 8]. La Paz (Departamento La Paz). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (1/1), MI = 4]. Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1), MI = 36]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: Formosa (Departamento Formosa). Micrurus pyrrhocryptus (Cope 1862) (Elapidae) [P = 100% (1/1), MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
JUY: Xenodon merremii (Wagler 1824) (Dipsadidae). Reference: Cordero & Vogelsang (1928) apud Fernandes & Kohn (Reference Fernandes and Kohn2014).
MIS: Posadas (Departamento Capital). Bothrops jararaca (Wied-Neuwied 1824) (Viperidae) [P = 100% (10/10), MI = 30], Lygophis flavifrenatus [P = 100% (1/1), MI = 25], Mesotes strigatus (Günther 1858) (= Thamnodynastes strigatus) (Dipsadidae) [P = 100% (20/20), MI = 20]. Santa Ana (Departamento Candelaria). Palusophis bifossatus (Raddi 1820) (= Drymobius bifossatus) (Colubridae) [P = 100% (1/1), MI = 5]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Fortín Olmos (Departamento Vera). Xenodon merremii (Wagler 1824) (Dipsadidae) [P = 100% (1/1), MI = 23]. Lucita (?) (Departamento San Cristobal). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1), MI = 5]. Malabrigo (Departamento General Obligado). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1), MI = 14]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SAL: Padre Lozano (Departamento General José de San Martín). Clelia (Daudin 1803) (= Cloelia cloelia) (Dipsadidae) [P = 100% (2/2), MI = 19]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SAN: Santiago del Estero (Departamento Juan Francisco Borges). Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae) [P = 100% (1/1), MI = 15]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
TUC: San Miguel de Tucumán (Departamento Capital). Pseudablabes patagoniensis (Girard 1858) (= Philodryas schotti) (Dipsadidae) [P = 100% (1/1), MI = 40]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
UND: Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae), Bothrops diporus Cope 1862 (= Bothrops neuwiedii meridionalis) (Viperidae), Xenodon dorbignyi (Duméril, Bibron & Duméril 1854) (= Lystrophis dorbignyi) (Dipsadidae), Xenodon merremii (Wagler 1824) (Dipsadidae). Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: mouth and esophagus.
Remarks: Distomun xenodontis (Cordero & Vogelsang 1928) has been synonymized with Opisthogonimus lecithonotus (Kohn & Fernándes 2014). The prevalence and mean intensity data in Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996) are general and do not discriminate among the nine localities where the helminth species has been reported to be present in the hosts. “Lucita” could be a misspelling of “La Lucila,” a locality in the province of Santa Fe in Caubisens Poumarau (Reference Caubisens Poumarau1968). Dryophylax hypoconia (= Thamnodynastes hypoconia) was originally cited as T. pallidus by Caubisens Poumarau (Reference Caubisens Poumarau1968); see comments on this species in the remarks on Styphlodora condita.
Opisthogonimus megabothrium Pereira 1928.
BAS: Punta Lara (Partido de Ensenada). Erythrolamprus jaegeri (= Liophis jaegeri) (Dipsadidae) [P = 100% (1/1); MI = 10]. Material deposited: MLP N° 1011. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
MIS: Aristóbulo del Valle (Departamento Cainguás). Xenodon merremii (Wagler 1824) (= Waglerophis merremii) (Dipsadidae) [P = 100% (1/1); MI = 2]. Material deposited: MLP N° 4587. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2001).
Stage: adult.
Site of infection: small and large intestines.
Opisthogonimus misionensis Lunaschi & Drago Reference Lunaschi and Drago2001.
MIS: Aristóbulo del Valle (Departamento Cainguás). Xenodon merremii (Wagler 1824) (= Waglerophis merremii) [P = 100% (1/1); MI = 15]. Material deposited: MLP N° 4590/1 (holotype), 4590/2 (paratype). Reference: Lunaschi & Drago (Reference Lunaschi and Drago2001).
Stage: adult.
Site of infection: small and large intestines.
Opisthogonimus serpentis Artigas, Ruiz & Leão 1943.
BAS: Punta Lara (Partido de Ensenada). Helicops infrataeniatus Jan 1865 (= Helicops carinicaudus) (Dipsadidae) [P = 100% (1/1); MI = 6]. Material deposited: MLP N° 1090. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
Stage: adult.
Site of infection: mouth.
Remarks: Lunaschi & Sutton (Reference Lunaschi and Sutton1985) cited this species as Opisthogonimus (Westella) serpentis.
Family Telorchiidae Looss Reference Looss1899.
Telorchis clava (Diesing 1850)
CHA: Colonia Benítez (Departamento Primero de Mayo). Eunectes notaeus Cope 1862 (Boidae) [P = 100% (1/1); MI = 36]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Ituzaingó (Departamento Ituzaingó), Paso de Los Libres (Departamento Paso de Los Libres), Ramada Paso (Departamento Itatí), San Cayetano (Departamento Capital), San Cosme (Departamento San Cosme), San Luis del Palmar (Departamento San Luis del Palmar), Santa Ana (Departamento San Cosme). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (Dipsadidae) [P = 100% (25/25); MI = 80]. Reference: Martínez et al. (Reference Martínez, Troiano, Binda, Selles, Jara and Fescina1996).
FOR: La Marcela farm (Departamento Pirané) (26°17’35’’ S, 59°06’67’’ W). Eunectes notaeus Cope 1862 (Boidae) [P = 100% (1/1); MI = 7]. Material deposited: MLP N° 5511. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
Stage: adult.
Site of infection: small intestine.
Remarks: Telorchis Lühe 1899 has been reported as a parasite of freshwater turtles such as Phrynops hilarii (Duméril & Bibron 1835) in Argentina (Lunaschi & Drago Reference Lunaschi and Drago2007a). The life cycle of Telorchis species is unknown.
Order Diplostomida Olson, Cribb, Tkach, Bray & Littlewood 2003
Family Proterodiplostomidae Dubois 1936.
Heterodiplostomum lanceolatum Dubois 1936
BAS: Punta Lara (Partido de Ensenada). Helicops infrataeniatus Jan 1865 (= Helicops carinicaudus) (Dipsadidae) [P = 100% (1/1), MI = 4]. Material deposited: MLP N° 1091 C. Reference: Lunaschi & Sutton (Reference Lunaschi and Sutton1985).
CHA: Las Palmas (Departamento Las Palmas). Helicops leopardinus (Schlegel 1837) (= Helicops leopardina) (Dipsadidae) [P = 100% (1/1); MI = 1]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
CTES: Bella Vista (Departamento Bella Vista). Helicops leopardinus (Schlegel 1837) (= Helicops leopardina) (Dipsadidae) [P = 100% (1/1); MI = 3]. Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% (2/2); MI = 18]. Goya (Departamento Goya). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 2]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
FOR: El Colorado (Departamento Pirané) (26°18’ S, 59°22’ W). Hydrodynastes gigas (Duméril, Bibron & Duméril 1854) (= Cyclagras gigas) (Dipsadidae) [P = 100% 1/1; MI = 2]. Material deposited: MLP N° 5504. Reference: Lunaschi & Drago (Reference Lunaschi and Drago2010a).
SAN: Río Hondo (Departamento Río Hondo). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 2]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
SFE: Malabrigo (Departamento General Obligado). Bothrops alternatus Duméril, Bibron & Duméril 1854 (= Bothrops alternata) (Viperidae) [P = 100% (1/1); MI = 2]. Reference: Caubisens Poumarau (Reference Caubisens Poumarau1968).
Stage: adult.
Site of infection: small and large intestines.
Remarks: larvae of this species have been reported in Leptodactylus latinasus (Jiménez de la Espada 1875) and L. macrosternum (Miranda-Ribeiro 1926) from agricultural and non-agricultural landscapes in the province of Corrientes (Hamman et al. Reference Hamann, González and Fernandez2020 Reference Hamann, Fernández and González2023) and in Leptodactylus podicipinus (Cope 1862) in Brazil (Queiroz et al. Reference Queiroz, López Hernández, Locke, Pinto and Anjos2020). The life cycle of this species is unknown; however, it has been inferred that cercariae penetrate the skin of tadpoles and develop into metacercariae in the body cavity. Snakes become infected as definitive hosts when they ingest parasitized tadpoles or adult amphibians (Yamaguti Reference Yamaguti1975).
Discussion
This study compiles the largest number of published data on metazoan endoparasites of snakes in Argentina over the last century.
Despite the existence of parasite checklists of digeneans (Lunaschi & Drago Reference Lunaschi and Drago2007a Reference Lunaschi and Drago2010a), acanthocephalans (Hernández-Ortz et al. Reference Hernández–Orts, Kutcha, Semenas, Crespo, González and Aznar2019), and nematodes (Castillo et al. Reference Castillo, Acosta, González Rivas and Ramallo2020) in amphibians, reptiles, and other vertebrates, this work presents the only parasite checklist devoted exclusively to snakes as hosts in the country.
Several checklists of helminth parasites of different groups of vertebrates in Argentina have been published during the last 16 years, i.e., nematodes and digeneans of freshwater fishes (Ostrowski de Núñez et al. Reference Ostrowski de Nuñez, Arredondo and Gil de Pertierra2017; Ramallo & Ailán-Choke Reference Ramallo and Ailán Choke2022); nematodes of amphibians (González & Hamann Reference González and Hamman2015); digeneans, nematodes and cestodes of wild birds (Lunaschi et al. Reference Lunaschi, Cremonte and Drago 2007b; Drago et al. Reference Drago, Nuñez and Dueñas Diaz 2020 Reference Drago, Dueñas Diaz, Draghi and Nuñez 2021), and acanthocephalans, cestodes, digeneans, and nematodes of Patagonian wild mammals (Fugassa Reference Fugassa2015; Reference Fugassa2020). Due to the limited number of studies on parasites of snakes in Argentina, this host group has been included in checklists along with other hosts related to evolutionary history (Lunaschi & Drago Reference Lunaschi and Drago2007a; Castillo et al. Reference Castillo, Acosta, González Rivas and Ramallo2020).
History of reports
The contribution to the knowledge of metazoan endoparasites of snakes from Argentina has been very irregular over time. Of all known metazoan endoparasite species included here, 58.8% were reported before 1968. The amount of studies increased between 1960 and 1999 and the first two decades of the 21st century, with a special focus on digenean biodiversity. Specifically, studies on nematode parasites of Argentine snakes have increased notably since the 1990s (Ramallo Reference Ramallo1996 Reference Ramallo2005; González et al. Reference González, Schaefer and Duré2018; Lamas et al. Reference Lamas, Céspedez and Ruíz-García2016; Peichoto et al. Reference Peichoto, Sánchez, López, Salas, Rivero, Teibler and Tavares 2016; Castillo et al. Reference Castillo, Acosta, González Rivas and Ramallo 2020; Bustos et al. Reference Bustos, Sánchez, Teibler and Peichoto 2023).
According to Poulin & Jorge (Reference Poulin and Jorge2019), descriptions of new species of any helminth taxon reached the highest number of publications during different decades, regardless of the region in which the studies were conducted. The authors also stated that active researchers could disproportionately impact the survey of new species in their study regions, which would end with their retirement. The contributions of Dr. Emma Caubisens Poumarau to the field, which ended with her sudden death, are proof of this.
General data, taxonomy, and diversity
Caubisens Poumarau (Reference Caubisens Poumarau1968) reported the largest number of records in this work and a previous publication listing digeneans of snakes in Argentina. Caubisens Poumarau also included the geographic distribution and abundance of taxa, covering most regions of the country. Along with the adult digeneans described, concomitant infections of numerous larval stages (metacercariae and mesocercariae) were observed in the mesentery of the hosts. Nevertheless, as a precise taxonomic identification of said stages was not achieved, the actual richness of this endoparasitic fauna was underestimated.
Larval stages of heteroxenous parasites (i.e., acanthocephalans, digeneans, nematodes, and pentastomids) could be important for understanding food webs in different environments and the position of the hosts in these webs (Marcogliese & Cone Reference Marcogliese and Cone1997; Lafferty et al. Reference Lafferty, Dobson and Kuris2006 Reference Lafferty, Allesina, Arim, Briggs, De Leo, Dobson, Dunne, Johnson, Kuris, Marcogliese, Martínez, Memmott, Marquet, McLaughlin, Mordecai, Pascual, Poulin and Thieltges2008; Sukhdeo Reference Sukhdeo2012; Michalska-Smith et al. Reference Michalska-Smith, Sander, Pascual and Allesina 2018). Many larval forms are difficult to identify properly. Thus, molecular studies of metacercariae, mesocercariae, cystacanths, nymphs, and larvae of the parasitizing nematodes are essential.
Nematodes were the most frequently recorded species in checklists of metazoan parasites and helminths in reptiles in Peru and northeastern Brazil (Cuellar et al. Reference Cuellar, Sáez, Cantú, Sánchez, Mendoza, Conga, Cruces, Luque and Chero2022; Lacerda et al. Reference Lacerda, Santana, de Araújo, Filho and Ribeiro2023). In contrast, in this study, the subclass Digenea (phylum Platyhelminthes) was comparatively the group of metazoans with the highest richness. From an exhaustive analysis that used three approaches to evaluate the completeness of 25 checklists of parasites in vertebrate hosts from various geographic regions, Poulin et al. (Reference Poulin, Besson, Morin and Randhawa2016) concluded that the checklists, although a useful synthesis of regional host–parasite associations, could not be used as reliable sources of data for comparative analyses. Therefore, caution should be taken when using this as a method of comparing parasite richness between host species or specificity.
Geographic context
Studies have focused on the northeastern provinces (Chaco, Corrientes, Formosa, Misiones, and Entre Rios) and have shown a high richness and abundance of metazoan groups.
The high diversity, phylogenetic composition, and functional groups of snake assemblages in northeastern Argentina could be driven by a latitudinal and thermal gradient, where tropical and temperate fauna from different biogeographic regions (e.g. Chaco, Pampa, The Espinal, and The Atlantic Rainforest) converge (Arzamendia & Giraudo Reference Arzamendia and Giraudo2009). Additionally, the large rivers of La Plata basin, with their dynamics of flood pulses and the complexity of the associated riparian forest vegetation, offer a spatio-temporal heterogeneity of conditions and resources that can be used by several snake species, providing them with numerous microhabitats and ecological niches to exploit (Junk et al. Reference Junk, Brown, Campbell, Max Finlayson, Gopal, Ramberg and Warner 2006; Arzamendia & Giraudo Reference Arzamendia and Giraudo2009 Reference Arzamendia and Giraudo2012; Piatti et al. Reference Piatti, Rosauer, Nogueira, Strussmann, Ferreira and Martins2019; Rincón-Aranguri et al. Reference Rincón-Aranguri, Toro-Cardona, Galeano, Roa-Fuentes and Urbina-Cardona2023).
This is evinced by the higher number of snake species reported in the northern provinces compared to the southern ones (Williams & Vera Reference William and Vera2023), consistent with the number of parasitological studies on this host group.
Specimen and geographic data availability
Most of the works produced in Argentina were descriptive, and the group that received the most attention and interest was the digenean. Although the digeneans described by Caubisens Poumarau (Reference Caubisens Poumarau1968) are the most numerous, the current location of all the material collected by this author is unknown. Of 16 species reported by Caubisens Poumarau (Reference Caubisens Poumarau1968), only two of them (Nos. 118 and 240 for O. lecithonotus and No. 190 for G. loosi) are available in the Helminthological Collection of Museo de La Plata. In addition, the formal deposit numbers in the collection catalog are unavailable (Brusa, F. pers. comm.). Since this was a pioneering work, with abundant material of the largest number of helminths and the widest coverage of the country’s regions and host range, we consider it important to include these specimens in a helminthological collection formally.
Of all the metazoan endoparasites of snakes from Argentina compiled here, those available in zoological collections are deposited in only four collections (three in Argentina and one in Germany). In agreement with Tyler et al. (Reference Tyler, Fucsko and Roberts2023), we consider it essential to allocate type material to different natural history museums to avoid possible losses due to natural disasters or anthropogenic factors.
The geographic coordinates of the study site became mandatory for depositing in zoological collections only in the 21st century, so geographic data are not available for all the records in this study. These data are important to better understand the current biodiversity and elaborate a comprehensive parasite conservation plan (Carlson et al. Reference Carlson, Hopkins, Bell, Doña, Godfrey, Mackenzie, Lafferty, Moir, Speer, Strona, Torchin and Wood2020b; Lymbery & Smit Reference Lymbery and Smit2023). In addition, this information could allow us to know the past state of parasitic fauna and evaluate its current state under conditions of anthropogenic intervention (Harmon et al. Reference Harmon, Littlewood and Wood2019; Thompson et al. Reference Thompson, Phelps, Allard, Cook, Dunnum, Ferguson, Gelang, Khan, Paul, Reeder, Simmons, Vanhove, Webala, Weksler and Kilpatrick2021; Wood & Vanhove Reference Wood and Vanhove2022; Wood et al. Reference Wood, Leslie, Claar, Mastick, Preisser, Vanhove and Welicky2023).
It should be noted that the prevalence reported for nematodes is lower than that reported for digeneans. This may be because the studies on snake nematodes included more specimens per host species. Margolis et al. (Reference Margolis, Esch, Holmes, Kuris and Schad1982) and Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997) made the first efforts to unify criteria on the terminology associated with the quantitative structure of parasite communities (prevalence, mean abundance, mean intensity); this is probably the reason why publications before 1960 do not include abundant data.
Poulin (Reference Poulin2019) highlighted the relevance of presenting prevalence and abundance measurements (mean abundance or mean intensity) of each parasite population in studies of parasite community ecology. In taxonomic research, those values are not essential items, but data are often included in new species descriptions in sections such as “Taxonomy Summary” or “Comments” on new geographic/new host records or checklists with corresponding mean abundance and intensity values. These infection parameters are easy to calculate and could be useful in future studies to compare species collected from the same or different geographic areas or host species, which have not been previously evaluated for parasites. Therefore, it is desirable to include these descriptors in taxonomic studies whenever possible.
Finally, we consider that studies on metazoan parasites of reptiles in general, and of snakes in particular, should be carried out in Argentina to (a) expand knowledge of the existing parasite biodiversity in the vertebrates in the country, (b) diagnose the existing information gaps on the subject and the prospects for progress in this field, (c) describe the patterns and processes that allow the structuring of parasite communities in these hosts to measure the anthropogenic influence on their modification, and (d) determine which of these parasite species could cause pathologies in snakes and other hosts, including humans.
Acknowledgements
J.C. deeply thanks to Dr. Israel Cañizales for their useful observations and suggestions to initial versions of this manuscript. To BSc. José Antonio Gouveia de Jesús, Dr. Gilberto Payares-Trujillo for their comments and helping with translation to English of drafts. To Dr. Francisco Brusa, curator of the Helminthological Collection of Museo de La Plata, for providing the information required about Dr. Caubisens Poumarau’s material. We acknowledge two anonymous reviewers whose comments contributed to improving the manuscript significantly.
Financial support
Financial support was received from Universidad Nacional del Nordeste (Grant number PI 21Q001 to C.E.G.), from CONICET (PIP 11220200101582CO to C.E.G.), from CONICET (PUE 22920180100001CO to O.F. Gallego), from Universidad Nacional del Litoral (CAID- UNL 2020 to V.A.), and Agencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (PICT-2020-SERIEA-01341 to V.A.).
