text new page (beta)
English (pdf)
Article in xml format
Automatic translation
Cited by SciELO 
Cited by Google 
Similars in
SciELO 
Similars in Google 
uBio 
Permalink
1 Introduction
Amphibians are hosts for a wide variety of ecto- and endoparasites. Internal parasites of amphibians include protozoans, as well as a variety of parasitic worms (see Wells, 2007). The latter include tapeworms (Cestoda) (Melo et al., 2011), intestinal round worms (Acanthocephala) (Salgado-Maldonado and Caspeta-Mandujano, 2010), tongue worms (Pentastomida) (Christoffersen and De Assis, 2013), nematodes that infect the lungs and visceral organs (Van Sluys et al., 2006), and monogenean and digenean helminths that infect the lungs, muscles, bladder, and digestive organs (Hamann and González, 2009; Santos and Amato, 2012).
Scinax fuscovarius are medium-sized tree frogs widely distributed in southeastern Brazil, northern Argentina, Paraguay, Bolivia, and Uruguay (Haddad et al., 2008; Almeida-Gomes et al., 2010; Frost, 2013). During the day, it shelters in burrows, crevices, trees, soil, and human construction (Araujo et al., 2009).
Species of the family Naididae (Oligochaeta) can live on a considerable range of substrates, including mollusks (Gorni and Alves, 2006), aquatic macrophytes (Mastrantuono, 1986), sponges (Righi, 1984), mosses, liverworts (Vlckvá et al., 2002), and filamentous algae (Armendáriz, 2000). However, some species are known as endoparasitic from vertebrates (see Harman, 1971).
The subgenus Allodero was erected by Sperber (1948) within the genus Dero (Naididae, Oligochaeta) for parasitic or symbiotic species known from Asia, Africa, and South America (Harman, 1971). Allodero, Aulophorus and Dero are considered subgenera of Dero by some authors (e.g. Milligan, 1997; Kathman and Brikhurst, 1998; Wetzel et al., 2012). However, Cekanovskaya (1962) and Liang (1964) considered Dero and Aulophorus as separate genera, while the latter author also separated Allodero at the generic level. More recently, Aulophorus was listed as a full genus (Timm, 1999). However, we prefer to refer individuals from this study as Dero (Allodero) lutzi until a revision of the subgenus Allodero is effectively conducted.
The subgenus Allodero consists only of one species, D. (Allodero) lutzi Michaelsen, 1926. Dero (Allodero) lutzi is an endoparasitic of the urinary tracts of frogs of the genus Hyla (Maldonado and Oliveira, 1982; Rodrigues and Maldonado Junior, 1982), which also have a free-living stage. Specimens in the parasitic stage lack dorsal setae, branchial fossa, and gills, but when cultured in a free-living form, they developed dorsal setae as well as caudal fossa and gills (Harman and Lawler, 1975). Here we report the occurrence of the endoparasitic Oligochaeta, Dero (Allodero) lutzi in the snouted tree frog, Scinax fuscovarius, from Semi-deciduous Atlantic Rain Forest in southern Brazil.
2 Material and Methods
This study took place in the Caiuá Ecological Station (22° 37’ S and 52° 50’ W, 268 m asl), in the municipality of Diamante do Norte, Paraná, Brazil. The region is inserted in the Semi-deciduous Atlantic Rain Forest. Specimens of Scinax fuscovarius (n = 7, mean SVL = 40.9 mm, ±3.7 SD and mean body weight 4.5 g, ±1.4 SD) were collected in temporary and permanent ponds during visual encounters surveys in February, April, and October 2012. Individuals were taken to the laboratory where they were euthanatized with Lidocaine 5%. Subsequently, the lungs, digestive tract, urinary tract, muscle, skin, spleen, and liver were examined for parasites. The Oligochaeta were identified in semi permanent slides. All anurans are housed at the zoological collection of the Universidade Federal de Goiás (ZUFG), Goiânia, Goiás, central Brazil (ZUFG 7109-7113, 7190, 7208). Voucher parasite specimens are housed at the Helminthological collection of the Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, Rio de Janeiro, Brazil (CHIOC 35863). The current nomenclature of anurans follows Faivovich et al. (2005), Lema and Martins (2011), Frost (2013).
3 Results and Discussion
Seven specimens of Scinax fuscovarius were examined for parasites. Analyses of the treefrogs demonstrated that one specimen (male, SVL = 40.75 mm, weight = 4.53 g) was infected by Dero (Allodero) lutzi (n = 14, mean length = 3.06 mm, ±0.51 SD; Figure 1), which were found in ureters and urinary bladder. These oligochaetes are free-living animals (Rodrigues and Maldonado Junior, 1982), which are adapting to parasitism, since the ecological conditions of the bladder and ureters of amphibians resemble those of the external liquid environment used by the frogs. However, the exact route of transmission of naids to frogs is unknown, but previous studies suggest that frogs are infected during the larval stage (Harman and Lawler, 1975).
Figure 1 Dero (Allodero) lutzi found in an adult male of Scinax fuscovarius: a) general aspect (Bar = 500 μm); b) ventral setae (Bar = 50 μm); c) rudimentary caudal fossa (Bar = 150 μm).
Only Dero is known to use frogs for transport and as hosts among the Brazilian freshwater genera of naidids (Righi, 1984; Lopez et al., 1999). As example, Dero superterrenus Michaelsen, 1912 are free-living inhabitants of tank bromeliads and tree holes and can use amphibians to disperse (Lopez et al., 1999). Laboratory experiments support the hypothesis that the phoretic behaviour presented by D. superterrenus is stimulated by chemical substances released by amphibian skins (Lopez et al., 2005). Lopez et al. (2005) suggest that if D. (A.) lutzi use the same chemical substances used by D. superterrenus to find their amphibian vectors, it will strengthen the hypothesis that parasitic and phoretic behaviours using frogs are evolutionarily linked in the annelid Dero group. Thereby, D. superterrenus and D. (A.) lutzi might have shared a close common ancestor with parasitic or phoretic behavior (Lopez et al., 2005).
Reports on Dero (A.) lutzi are scarce and restricted to a few anuran species. The first record was made on Trachycephalus cf. typhonius, Hypsiboas albomarginatus, Scinax gr. ruber and Dendropsophus minutus (Lutz, 1926). Lutz (1927) found the species in Hypsiboas faber (Brazil) and Osteopilus septentrionalis from Cuba. Righi (1972) also found D. (A.) lutzi in Scinax strigilatus and considered Schmardaella hylae Goodchild 1951, parasite of Hyla squirella, a synonym of D. (A.) lutzi. More recently, oligochaetes were expelled along with eggs of Trachycephalus mesophaeus during oviposition (Prado et al., 2003). The current taxonomy of hosts is presented in Table 1. The reported of S. fuscovarius as host of D. (A.) lutzi represents a new host record for this Oligochaeta endoparasite.
Table 1 Checklist of anuran species host of Dero (Allodero) lutzi.
| Host | Locality / Countrya | Current taxonomy (Host) | Source |
|---|---|---|---|
| BUFONIDAE Bufo crucifer |
Nova Iguaçú, RJ (BRA) | Rhinella ornata | Rodrigues and Maldonado Junior (1982) |
| HYLIDAE Hyla misera |
Rio de Janeiro, RJ (BRA) | Dendropsophus cf. meridianus | Rodrigues and Maldonado Junior (1982) |
| Maracay (VEN) | Dendropsophus microcephalus | ||
| Hyla bilineata c | São Paulo, SP (BRA) | Dendropsophus minutus | Rodrigues and Maldonado Junior (1982) |
| Hyla albomarginata | Rio de Janeiro, RJ (BRA) | Hypsiboas albomarginatus | Rodrigues and Maldonado Junior (1982) |
| Hyla faber | (BRA) | Hypsiboas faber | Rodrigues and Maldonado Junior (1982) |
| Diamante do Norte, PR (BRA) | Scinax fuscovarius b | ||
| Hyla strigilata | Lauro Müller, SC (BRA) | Scinax gr. catharinae | Rodrigues and Maldonado Junior (1982) |
| Hyla rubra | Belo Horizonte, MG (BRA) | Scinax gr. ruber | Rodrigues and Maldonado Junior (1982) |
| São Paulo, SP (BRA) | |||
| Hyla venulosa | Rio de Janeiro, RJ (BRA) | Trachycephalus cf. typhonius | Rodrigues and Maldonado Junior (1982) |
| Phrynohyas mesophaea | Ubatuba, SP (BRA) Maracay (VEN) |
Trachycephalus mesophaeus | Prado et al. (2003) |
| Hyla septentrionalis | (CUB) | Osteopilus septentrionalis | Rodrigues and Maldonado Junior (1982) |
| Hyla squirella | Dade County, Florida (USA) | Hyla squirella | Rodrigues and Maldonado Junior (1982) |
a BRA, Brazil: MG, Minas Gerais; PR, Paraná; RJ, Rio de Janeiro; SC, Santa Catarina; SP, São Paulo; CUB, Cuba; VEN, Venezuela; USA, United States of America;
b This study;
c name unknown (possible confusion with Hyla bivittata).
Previous records of Dero (A.) lutzi include the Brazilian States of Santa Catarina, São Paulo, Rio de Janeiro, and Minas Gerais, as well as Cuba and North America (Righi, 1984; Christoffersen, 2007). Therefore, our record in Paraná represents a new locality for D. (A.) lutzi.
Reports of Dero (A.) lutzi are rare, due to difficulty of observation. Such events are restricted to fortuitous cases. In this context, it is important to emphasize the need for future studies to the understanding of biological and ecological aspects of D. (A.) lutzi.
