- Similares en SciELO
versión On-line ISSN 2007-8706versión impresa ISSN 1870-3453
Rev. Mex. Biodiv. vol.81 no.3 México dic. 2010
Taxonomía y sistemática
First report of nematode parasites of Physalaemus santafecinus (Anura: Leiuperidae) from Corrientes, Argentina
Primer registro de nematodos parásitos de Physalaemus santafecinus (Anura: Leiuperidae) de Corrientes, Argentina
Cynthya Elizabeth González* and Monika Inés Hamann
Centro de Ecología Aplicada del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas. Ruta Provincial Núm. 5, Km 2,5., 3400 Corrientes, Argentina. *Correspondent: email@example.com
Recibido: 26 agosto 2009
Aceptado: 06 febrero 2010
Ciento ochenta y tres nematodos fueron recolectados de 81 adultos del leiupérido Physalaemus santafecinus examinados en Corrientes, Argentina y capturados entre enero del 2002 y diciembre del 2003. Estos nematodos pertenecen a un total de 4 especies, 3 en estado adulto: Cosmocerca podicipinus, Cosmocerca parva, Aplectana hylambatis, y 1 especie en estado larval, Physaloptera sp. Se presentan características morfológicas, información métrica e intervalos de medidas de estas especies de nematodos, comparándolas con ejemplares recolectados de diferentes hospederos de la región neotropical. Éste es el primer registro de nematodos parásitos para P. santafecinus de Argentina.
Palabras clave: anfibios, Cosmocerca, Aplectana, Physaloptera, región neotropical.
One hundred and eightythree nematodes were recovered from 81 adults of leiuperid Physalaemus santafecinus examined from Corrientes, Argentina captured between January 2002 and December 2003. A total of 3 adults nematode species (Cosmocerca podicipinus, Cosmocerca parva, Aplectana hylambatis) and 1 larval species (Physaloptera sp.) were obtained. We present morphological characters, metric information and range for these nematode species and compared these with other specimens collected from different hosts of the Neotropical Realm. This is the first report of nematode parasites of P. santafecinus from Argentina.
Key words: amphibians, Cosmocerca, Aplectana, Physaloptera, Neotropical Realm.
Many studies in nematode parasites of amphibians have been recently conducted in the Neotropical Realm, including a description of new species or genus (González and Hamann, 2004, 2006a, 2007a; Bursey and Goldberg, 2007; MartínezSalazar and LeónRègagnon, 2007; Ramallo et al., 2007, 2008; MartínezSalazar, 2008) as well as, checklists that summarize the diversity of these parasites in these vertebrate hosts (Bursey et al., 2001; González and Hamann, 2006b, 2007b, 2009; Goldberg et al., 2007; Goldberg and Bursey, 2008a, 2008b; Hamann et al., 2009). Despite the fact that many species of parasites are cited in a wide variety of hosts, there are few studies that deal with the morphological and metrical aspects of these nematodes.
The genus Physalaemus Fitzinger, 1826 is distributed in northern and central Argentina, eastern Bolivia, Paraguay, Uruguay, Brazil and the Guianas, the lowlands of southern Venezuela and plains of southeastern Colombia and western Ecuador (Frost, 2009).
Physalaemus santafecinus Barrio, 1965 is found in Argentina in the provinces of Corrientes and Santa Fe. It can survive in both dry and moist substrata, for example near the shore of temporary, semipermanent and permanent ponds, and also in flooded grass. It has a diet with a marked tendency toward the specialization in termites using active foraging as a strategy for prey capturing. It is common in natural environments, but it can also be found in agricultural areas (Duré, 1998; Duré et al., 2008).
The purpose of our study is to report for the first time nematode species that are found in Physalaemus santafecinus from Corrientes, Argentina. Morphometric information and studies of the surface of some of these nematodes is presented using scanning electron microscopy.
Materials and methods
Samples of Physalaemus santafecinus (n= 81) were collected near the city of Corrientes, Province of Corrientes in Argentina (27°28'S, 58°50'W). We examined 28 males and 53 females of this species between January 2002 and December 2003.
Amphibians were transported live to the laboratory and sacrificed in a chloroform (CHCL3) solution. At necropsy, hosts were sexed and the alimentary canal, lungs, liver, kidneys, urinary bladder, musculature and integument were examined for parasites by dissection. Nematodes were observed in vivo, counted and killed in hot distilled water and preserved in 70% ethyl alcohol, cleared in glycerine or lactophenol and examined as temporary mounts. Some specimens were studied by scanning electron microscopy (SEM). These specimens were dehydrated in ethanol series, dried using the critical point technique, coated with gold, and examined with a JSM5800 scanning electron microscope. Measurements are given in micrometers (μm) unless otherwise stated, and the mean ± SD followed by range is given in parentheses. Prevalence and mean intensity were calculated according to Bush et al. (1997). The specimens studied were deposited in the Helminthological Collection of the Centro de Ecología Aplicada del Litoral, Corrientes, Argentina (CECOAL).
A total of 183 nematodes were collected from 81 anurans examined. We found 4 species of nematodes from 2 different families: Cosmocercidae: Cosmocerca podicipinus Baker and Vaucher, 1984, Cosmocerca parva Travassos, 1925 and Aplectana hylambatis (Baylis, 1927) Travassos, 1931 and, Physalopteridae: Physaloptera sp.
Cosmocerca podicipinus Baker and Vaucher, 1984 (Fig. 1)
Prevalence, number of parasites, mean intensity: 30.9 % (25 of 81 amphibians infected), 52, 2.07 ± 1.57.
Sites of infection: lung, large intestine and small intestine.
Accession number: CECOAL 02112906 (1 male); 02113219 (1 male, 1 female); 02113215 (1 male); 02123263 (1 male); 02123286 (1 male, 2 females).
The general morphology of these specimens is similar to that referred by González and Hamann (2006b, 2007b, 2008) from amphibian hosts from Corrientes, Argentina. The caudal region of the males of this species was extensively detailed for González and Hamann (2004). The metric characters of both sexes of this nematode species found parasitizing P. santafecinus are presented in Table 1.
One of the most common characters used in the classification of species of the genus Cosmocerca is the number of pairs of plectanes in the caudal region of males (Baker and Vaucher, 1984) (see Table 2). It should be noted that in C. podicipinus the plectanes of each row are fusioned by sclerotized very marked. Within this study are presented details obtained with the scanning electron microscope of the mentioned structures. In lateral view, the plectanes and the sclerotized supports are presented like a row of crests, where the ends are occupied by the plectanes. Each plectane was formed by one interior complete rosette of 1112 punctations and one exterior complete rosette of 1215 punctations. Finally, adanal papillae are presented wider in the base and narrower in the upper limb.
The general metric characteristics of specimens of this species correspond to others specimens of the same species analyzed from others hosts of Corrientes, Argentina. Nevertheless, the body size of the females of this study is greater (4.277.8 mm) than the found ones in other hosts; for example, the maximum body size of females of C. podicipinus from Pseudopaludicola falcipes: 6.0 mm (González and Hamann, 2004); from Rhinella fernandezae: 4.3 mm; from R. bergi: 6.9 mm (González and Hamann, 2007a) and from R. schneideri: 7.35 mm (González and Hamann, 2008). In males, the principal difference is the length of spicules; whereas in this study, the spicules of C. podicipinus are smaller that observed in other hosts: P. falcipes: 98150; R. fernandezae: 7194; R. bergi: 72135; R. schneideri: 108115 (González and Hamann, 2004, 2007a, 2008).
In the Neotropical Realm this species was found in the following families of hosts and countries: Bufonidae, Aromobatidae, Strabomantidae and Leptodactylidae from Peru (Bursey et al., 2001); Leptodactylidae from Paraguay (Baker and Vaucher, 1984); Bufonidae and Dendrobatidae from Colombia (Goldberg and Bursey, 2003); Hylidae and Leptodactylidae from Brazil (Goldberg et al., 2007; 2009); Eleutherodactylidae, Leptodactylidae, Hylidae and Ranidae from Mexico (Goldberg and Bursey, 2002; Goldberg et al., 2002a; CabreraGuzmán et al., 2007); Ranidae, Craugastoridae, Strabomantidae and Hylidae from Costa Rica (Bursey and Goldberg, 2005, 2006, 2007; Goldberg and Bursey, 2008a, 2008b) and, Leiuperidae, Leptodactylidae, Bufonidae and Cycloramphidae from Argentina (González and Hamann, 2004, 2006a, 2006b, 2007a, 2007b, 2008, 2009; Hamann et al., 2006a, 2006b; Schaefer et al., 2006).
Cosmocerca parva Travassos, 1925 (Fig. 2)
Prevalence, number of parasites, mean intensity: 17.3% (14 of 81 amphibians infected), 60, 4.28 ± 4.15.
Sites of infection: large and small intestine.
Accession number: CECOAL 02032573 (1 male, 2 females); 02032576 (1 male, 5 females); 02032577 (2 males, 4 females); 02103059 (1 male, 1 female).
Table 1 shows the metric characters of the males and females of C. parva. In this study, the number of plectanes varied between 5 and 7 pairs, each one with 2 complete rosettes of punctations directly perpendicular to the body surface and a relatively inconspicuous underlying sclerotized support which is not fused to other plectanes.
In males of C. parva, the number of pairs of plectanes varied considerably between hosts. In the original description, Travassos (1925) established a total of 5 pairs of plectanes. In Paraguayan leptodactylids and bufonids, Baker and Vaucher (1984) described males with 57 pairs of these structures, but in Argentinean amphibians, nematode specimens showed a different number of these structures (Mordeglia and Digiani, 1998; González and Hamann, 2006a, 2006b, 2007b, 2008, 2009). Thus, in bufonids have been registered with 47 pairs of plectanes (Rhinella bergi and R. fernandezae: 5 pairs, R. granulosa: 57 pairs, R. schneideri 45 pairs), in the cycloramphid Odontophrynus americanus 5 pairs, and in hylids (Scinax acuminatus) and leptodactylids (Leptodactylus bufonius), 6 pairs. Males analyzed in this study present a variable number of pairs of plectanes (57 pairs).
Observations with SEM on adanal region of male specimens collected of R. granulosa (Mordeglia and Digiani, 1998) show 2 to 4 pairs of papillae which are surrounded by 1 or 2 small rosettes of punctations and, plectanes with 2 complete rosettes of 1216 punctations. González and Hamann (2008) observed that the plectanes were surrounded by 2 complete rosettes of 1215 punctations. Males of C. parva analyzed in this study presented one interior complete rosette with 1011 punctations and, one exterior complete rosette with 1214 punctations. The sclerotized supports between plectanes is practically nonexistent.
The metric characteristics of males and females of C. parva analyzed in this study correspond with others descriptions of hosts from Corrientes, Argentina (see González and Hamann, 2006a, 2007a, 2008). However, compared with the description of Travassos (1925), the length is smaller in both sexes (females: 6.8 mm; males: 3.5 mm); as well as, the length of gobernaculum is smaller than specimens analyzed by this author (120140).
Similar to the previous one, this is a species with a widely distribution in the Neotropical Realm. In Brazil, it was found in families Leptodactylidae, Leiuperidae and Hylolidae (Travassos, 1925; Fabio, 1982), in Paraguay from Leptodactylidae, Bufonidae and Hylidae (Masi Pallares and Maciel, 1974; Baker and Vaucher, 1984), in Peru from Bufonidae, Aromobatidae, Hylidae, Leiuperidae, Leptodactylidae, Eleutherodactylidae and Microhylidae (Bursey et al., 2001), in Trinidad and Tobago from Leptodactylidae and Eleutherodactylidae (Goldberg et al., 2002b), in Costa Rica from Craugastoridae (Goldberg and Bursey, 2008a), in Mexico from Ranidae (ParedesCalderón et al., 2004) and, in Argentina from Bufonidae, Hylidae, Leptodactylidae and Cycloramphidae (Mordeglia and Digiani, 1998; González and Hamann, 2006a, 2006b, 2007a, 2007b, 2008, 2009; Hamann et al., 2006a, 2006b, 2009, Schaefer et al., 2006).
Prevalence, number of parasites: 1.2% (1 of 81 amphibians infected), 68.
Site of infection: large intestine.
Accession number: CECOAL 02103022 (10 males, 15 females).
Table 1 shows the metric characteristics of females and males of this species and, Table 3 shows the distribution of caudal papillae in the posterior end of males compared with specimens found in other hosts. In males of this species we observed that the distal portion of spicules presents an articulation that represents, approximately, 1/8 of its total length. This can be well seen when the spicules are everted.
Baker (1980) emended the diagnosis of genus Aplectana and gave the following characteristics for this genus: tail of male lacking rosettes or plectanes; somatic papillae and lateral alae present; numerous thinshelled, small eggs in uterus; both ovaries anterior to vulva.
The number of caudal papillae on posterior end of males is variable between hosts (see Table 3). The specimens analyzed from P. santafecinus have a higher number of preanals, adanals and postanals papillae compared with those studied from other hosts, although the number of adanals papillae match those found by Baker (1980) in Rhinella achalensis (= B. achalensis) from Córdoba province, Argentina.
In this species the morphology of spicules is controversial; for some authors (Gutierrez, 1945; Masi Pallares and Maciel, 1974) the last portion of these structures corresponded to a fixed articulation, hockey stickshaped, when the spicules are everted. Lent and Freitas (1948) expressed that the body of the spicules ends in fixed articulation, and then there is a membranous portion that relates to sheath the spicules; Baker (1980) wrote, "Distal end of spicules covered by a prominent hookshaped membrane approximately 4050 Î¼m long and usually directed laterally". We agree with the first authors; the spicules of this species are constituted of 2 parts, divided by an articulation. The proximal part representing 1/8 of the total length and the distal part that is bent perpendicularly when this structure is outside the body of the nematode; this can be seen clearly through the scanning electron microscope.
The metric characteristics of these nematodes, in general, were lower than those expressed in other studies (e.g., total length of females and males: Gutierrez, 1945: 4.46.2mm and 44.8mm; MasiPallares and Maciel, 1974: 4.985.84mm and 33.9mm; Baker, 1980: 4.86.3mm and 4.25mm; length of spicules: Gutierrez, 1945: 238349; MasiPallares and Maciel, 1974: 295349; Baker, 1980: 319350; length of gubernaculum: MasiPallares and Maciel, 1974: 119131; Baker, 1980: 109116).
In the Neotropical Realm, A. hylambatis was found in Peru in amphibians of families Bufonidae, Leptodactylidae, Ceratophryidae and Microhylidae (Bursey et al., 2001; Iannacone 2003a, 2003b); in Bufonidae, Mycrohylidae, Leiuperidae, Leptodactylidae and Hylidae from Paraguay (Masi Pallares and Maciel, 1974; Baker and Vaucher, 1986) and in Bufonidae from Uruguay (Lent and Freitas, 1948). In Argentina, this species was found in amphibians of family Bufonidae (Gutierrez, 1945; Sueldo and Ramírez, 1976; Ramírez et al., 1979; Baker, 1980) and Leptodactylidae (González and Hamann, 2006b; Hamann et al., 2006a, 2006b).
Physaloptera sp. (Larvae) (Fig. 6)
Prevalence, number of parasites: 1.2% (1 of 81 amphibian infected), 3.
Site of infection: gastric mucosa.
Accession number: CECOAL 03074252 (3 larvae).
Based on 3 specimens. Body whitish, 3.42±0.28mm (3.133.7) x 162.0±10.4 (150168), with transversely annulated cuticle. Terminus of head with 2 lateral lips and cephalic collar formed by inflated cuticle. On either lip, a sclerotized support and one terminal tooth at upper margin is present. Each lip bearing 2 cephalic papillae and one amphid. Muscular esophagus 211.6±14.0 (195221) x 26.1±2.7 (2328); glandular esophagus 1.06±0.02mm (1.041.08) x 61.7±2.4 (6064). Nerve ring, 171.7±10.4 (161182) from anterior end. Excretory pore near anterior end of glandular esophagus, 188.4±18.5 (168204) from anterior end of body. Tail conical, 89.7±6.9 (8397) long.
Compared with larvae that were found in others hosts of the same area, specimens analyzed in this study showed the same morphological characteristics, but in terms of size, were smaller than those found in bufonids (R. granulosa: 4.65.6mm; R. fernandezae: 4.17mm; R. schneideri: 5.9mm) (González and Hamann, 2006b, 2007b, 2008).
Larvae of Physaloptera were found in the following families of amphibians from the Neotropical Realm: Hylidae, Bufonidae, Leptodactylidae, Leiuperidae and Cycloramphidae from Brazil (Vicente et al., 1990; BoquimpaniFreitas et al., 2001; Goldberg et al., 2009); Bufonidae, Aromobatidae, Hylidae, Leiuperidae, Eleutherodactylidae, Leptodactylidae and Microhylidae from Peru (Bursey et al., 2001); Leptodactylidae from Trinidad and Tobago (Goldberg et al., 2002b); Bufonidae, Hylidae and Ranidae fom Mexico (GaliciaGuerrero et al., 2000; Bursey and Goldberg, 2001; Goldberg and Bursey, 2002; Goldberg et al., 2002a; CabreraGuzmán et al., 2007); Craugastoridae and Hylidae from Costa Rica (Goldberg and Bursey, 2008a, 2008b) and, in Argentina from Leiuperidae, Leptodactylidae, Hylidae and Bufonidae (Gutierrez et al., 2005; González and Hamann, 2006a, 2006b, 2007a, 2008).
Four nematode speciesbelonging to genus Cosmocerca have been recorded from different families of Argentinean amphibians. Cosmocerca podicipinus and C. parva were found in leptodactylids, leiuperids, bufonids, hylids and cycloramphids, all of them from Corrientes province (see González and Hamann, 2008, 2009); C. cruzi and C. rara were only found in Corrientes province from L. latinasus (Hamann et al., 2006a).
Also, 5 species of genus Aplectana: A. tarija Ramallo, Bursey and Goldberg, 2007 in Rhinella arenarum; A. adaechevarriae Ramallo, Bursey and Goldberg, 2008 in R. granulosa and R. schneideri from Salta Province (Ramallo et al., 2007; 2008); A. meridionalis Lent and Freitas, 1948 in Pleurodema borellii (Peracca, 1895) from Jujuy Province (Baker, 1980); A. delirae (Fabio, 1971) in R. granulosa from Corrientes Province, and, A. hylambatis in bufonids from Salta, Córdoba, Buenos Aires and Corrientes Provinces and, in leptodactylids from Corrientes Province (Gutierrez, 1945; Sueldo and Ramírez, 1976; Ramírez et al., 1979; González and Hamann, 2006b; Hamann et al., 2006a, 2006b) have been found. In this study, P. santafecinus represents new host record for C. podicipinus, C. parva and A. hylambatis.
Adults of Physaloptera have been found parasitizing the stomach of mammals, snakes, and a few species of lizards which acquire infections from ingesting insects containing infective larvae (Anderson, 2000). In amphibians, only 2 species are known, represented by adults: P. amphibia Linstow, 1899 found in the esophagus and the stomach of Limnonectes macrodon (Duméril and Bibron, 1841) from Philippines Islands and P. tigrinae Ali and Farooqui, 1969 from Hoplobatrachus tigerinus (Daudin, 1802) from India (Baker, 1987). This study adds P. santafecinus to the list of hosts parasitized by larvae of this genus.
This study is the first report of nematodes of P. santafecinus from Argentina and some new morphological data are presented for all the species recorded.
Financial support was provided by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) of Argentina, through grant PIP 2945 to M. I. Hamann.
Anderson, R. C. 2000. Nematode Parasites of Vertebrates: Their Development and Transmission. 2nd Edition. CABI Publishing, Wallingford. 650 p. [ Links ]
Baker, M. R. 1980. Revision of Old World species of the genus Aplectana Raillet and Henry, 1916 (Nematoda, Cosmocercidae). Bulletin du Museum National d'Histoire Naturelle, Paris, Ser. 4, Sect. A 2:955998. [ Links ]
Baker, M. R. 1987. Synopsis of the nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland. Occasional papers in Biology. Number 11. 325p. [ Links ]
Baker, M. R. and C. Vaucher. 1984. Parasitic helminths from Paraguay VI: Cosmocerca Diesing, 1861 (Nematoda: Cosmocercoidea) from frogs. Revue Suisse Zoologie 91:925934. [ Links ]
Baker, M. R. and C. Vaucher. 1986. Parasitic helminths from Paraguay XII: Aplectana Raillet and Henry, 1916 (Nematoda: Cosmocercoidea) from frogs. Revue Suisse Zoologie 93:607616. [ Links ]
BoquimpaniFreitas, L., D. Vrcibradic, J. J. Vicente, C. R. Bursey, C. F. D. Rocha and M. Van Sluys. 2001. Helminths of the horned leaf frog, Proceratophrys appendiculata, from southeastern Brazil. Journal of Helminthology 75:233236. [ Links ]
Bursey, C. R. and S. R. Goldberg. 2001. Falcaustra lowei n. sp. and other helminths from the Tarahumara frog, Rana tarahumarae (Anura: Ranidae), from Sonora, Mexico. Journal of Parasitology 87:340344. [ Links ]
Bursey, C. R. and S. R. Goldberg. 2005. New species of Oswaldocruzia (Nematoda: Molineoidae), new species of Rhabdias (Nematoda: Rhabdiasidae), and other helminths in Rana cf. forreri (Anura: Ranidae) from Costa Rica. Journal of Parasitology 91:600605. [ Links ]
Bursey, C. R. and S. R. Goldberg. 2006. New species of Raillietnema (Nematoda: Cosmocercidae) and other helminths in Rana vibicaria (Ranidae) from Costa Rica. Comparative Parasitology 73:193200. [ Links ]
Bursey, C. R. and S. R. Goldberg. 2007. New Species of Hedruris (Nematoda: Hedruridae), Anuracanthorhynchus lutzi (Hamann, 1891) n. comb. and other Helminths in Lithobates warszewitschii (Anura: Ranidae) from Costa Rica. Caribbean Journal of Science 43:110. [ Links ]
Bursey, C. R., S. R. Goldberg and J. R. Pamarlee. 2001. Gastrointestinal helminths of 51 species of anurans from Reserva Cuzco Amazónico, Peru. Comparative Parasitology 68:2135. [ Links ]
Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575583. [ Links ]
CabreraGuzmán, E., V. LeónRègagnon and L. GarcíaPrieto. 2007. Helminth Parasites of the Leopard Frog Rana cf. forreri (Amphibia: Ranidae) in Acapulco, Guerrero, Mexico. Comparative Parasitology 74:96107. [ Links ]
Duré, M. I. 1998. Alimentación de Physalaemus santafecinus Barrio, 1965 (Anura, Leptodactylidae). Facena 14:4552. [ Links ]
Duré, M. I., A. I. Kehr, E. F. Schaefer and F. Marangoni. 2008. Diversity of amphibians in rice fields from northeastern Argentina. Interciencia 33:523527. [ Links ]
Fabio, S. P. 1982. Helmintos de populações simpátricas de algumas espécies de anfibios anuros da Familia Leptodactylidae. Arquivos da Universidade Federal Rural do Rio de Janeiro 5:6983. [ Links ]
Frost, D. R. 2009. Amphibian Species of the World: an Online Reference. Version 5.3 (12 February, 2009). Electronic Database accessible at http://research.amnh.org/herpetology/amphibia/ American Museum of Natural History, New York. Last access: 09.XII.2009. [ Links ]
GaliciaGuerrero, S., C. R. Bursey, R. S. Goldberg and G. SalgadoMaldonado. 2000. Helminths of two sympatric toad species, Bufo marinus (Linnaeus) and Bufo marmoreus Weigmann, 1833 (Anura: Bufonidae) from Chamela, Jalisco, México. Comparative Parasitology 67:129133. [ Links ]
Goldberg, S. R. and C. R. Bursey. 2002. Helminth Parasites of seven anuran species from Northwestern Mexico. Western North American Naturalist 62:160169. [ Links ]
Goldberg, S. R. and C. R. Bursey. 2003. Helminths of two anuran species; Atelopus spurrelli (Bufonidae) and Dendrobates histrionicus (Dendrobatidae), from Colombia, South America. Parasitology Internacional 52:251253. [ Links ]
Goldberg, S. R. and C. R. Bursey. 2008a. Helminths from 10 Species of Brachycephalid Frogs (Anura: Brachycephalidae) from Costa Rica. Comparative Parasitology 75:255262. [ Links ]
Goldberg, S. R. and C. R. Bursey. 2008b. Helminths from fifteen species of frogs (Anura, Hylidae) from Costa Rica. Phyllomedusa 7:2533. [ Links ]
Goldberg, S. R., C. R. Bursey, J. P. Caldwell, L. J. Vitt and G. C. Costa. 2007. Gastrointestinal helminths from six species of frogs and three species of lizards, sympatric in Pará State, Brazil. Comparative Parasitology 74:327342. [ Links ]
Goldberg, S. R., C. R. Bursey, J. P. Caldwell and D. B. Shepard. 2009. Gastrointestinal helminths of six sympatric species of Leptodactylus from Tocantins State, Brazil. Comparative Parasitology 76:258266. [ Links ]
Goldberg, S. R, C. R. Bursey, G. SalgadoMaldonado, R. Báez and C. Cañeda 2002a. Helminth parasites of six species of anurans from Los Tuxtlas and Catemaco Lake, Veracruz, Mexico. Southwestern Naturalist 47:293299. [ Links ]
Goldberg, S.R., C. R. Bursey, J. D. Trujillo and H. Kaiser. 2002b. Intestinal helminths of seven frog species from Trinidad and Tobago. Caribbean Journal of Science 38:147150. [ Links ]
González, C. E. and M. I. Hamann. 2004. Primer registro de Cosmocerca podicipinus Baker y Vaucher, 1984 (Nematoda: Cosmocercidae) en Pseudopaludicola falcipes (Hensel, 1867) (Amphibia: Leptodactylidae) en Corrientes, Argentina. Facena 20:6572. [ Links ]
González, C. E. and M. I. Hamann. 2006a. Nematodes parásitos de Chaunus granulosus major (Müller & Hellmich, 1936) (Anura: Bufonidae) en Corrientes, Argentina. Cuadernos de Herpetología 20:4349. [ Links ]
González, C. E. and M. I. Hamann. 2006b. Helmintos parásitos de Leptodactylus bufonius Boulenger, 1894 (Anura: Leptodactylidae) de Corrientes, Argentina. Revista Española de Herpetología 20:3946. [ Links ]
González, C. E. and M. I. Hamann. 2007a. Nematode parasites of two species of Chaunus (Anura: Bufonidae) from Corrientes, Argentina. Zootaxa 1393:2734. [ Links ]
González, C. E. and M. I. Hamann. 2007b. Chaunus bergi (NCN) Endoparasites. Herpetological Review 38:181. [ Links ]
González, C. E. and M. I. Hamann. 2008. Nematode parasites of two anurans species, Rhinella schneideri (Bufonidae) and Scinax acuminatus (Hylidae), from Corrientes, Argentina. Revista de Biología Tropical 56:21472161. [ Links ]
González, C. E. and M. I. Hamann. 2009. First Report of Nematodes in the Common Lesser Escuerzo Odontophrynus americanus (Duméril and Bibron, 1841) (Amphibia: Cycloramphidae) from Corrientes, Argentina. Comparative Parasitology 76:122126. [ Links ]
Gutierrez, R. O. 1945. Contribución al conocimiento de los nematodes parásitos de anfibios argentinos. Thesis, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata. La Plata, Argentina. 45 p. [ Links ]
Gutierrez, C., A. Attademo, S. Guerrero, P. Peltzer and R. Lajmanovich. 2005. Physalaemus biligonigerus (Falseeyed Frog). Endoparasites. Herpetological Review 36:161162. [ Links ]
Hamann, M. I., C. E. González and A. I. Kehr. 2006a. Helminth community structure of the oven frog Leptodactylus latinasus (Anura, Leptodactylidae) from Corrientes, Argentina. Acta Parasitologica 51:294299. [ Links ]
Hamann, M. I., A. I. Kehr and C. E. González. 2006b. Species affinity and infracommunity ordination of helminths of Leptodactylus chaquensis (Anura: Leptodactylidae) in two contrasting environments from Northeastern Argentina. Journal of Parasitology 92:11711179. [ Links ]
Hamann, M. I., A. I. Kehr, C. E. González, M. I. Duré and E. F. Schaefer. 2009. Parasite and reproductive features of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Interciencia 34:214218. [ Links ]
Iannacone, J. 2003a. Helmintos parásitos de Atelopus bomolochus Peters, 1973 (Anura: Bufonidae) de Piura, Perú. Gayana (Concepción) 67:915. [ Links ]
Iannacone, J. 2003b. Helmintos parásitos de Telmatobius jelskii (Peters) (Anura, Leptodactylidae) de Lima, Perú. Revista Brasilera de Zoologia 20:131134. [ Links ]
Lent, H. and J. F. T. Freitas. 1948. Uma coleçao de nematodeos, parasitos de vertebrados, do Museu de Historia Natural de Montevideo. Memorias do Instituto Oswaldo Cruz 46:171. [ Links ]
MartínezSalazar, E. A. 2008. A new rhabdiasid species from Craugastor occidentalis (Anura: Brahcycephalidae) from Sierra de Manantlán, Jalisco, Mexico. Revista Mexicana de Biodiversidad 79:8189. [ Links ]
MartínezSalazar, E. A and V. LeónRègagnon. 2007. New species of Rhabdias (Nematoda: Rhabdiasidae) from Bufo occidentalis (Anura: Bufonidae) from Sierra Madre del Sur, Mexico. Journal of Parasitology 93:11711177. [ Links ]
Masi Pallares, R. and S. Maciel. 1974. Helminthes en batracios del Paraguay (1ra. Parte), con descripción de una nueva especie Aplectana pudenda (Oxyuridae: Cosmocercinae). Revista Paraguaya de Microbiología 9:5560. [ Links ]
Mordeglia, C. and M. C. Digiani. 1998. Cosmocerca parva Travassos, 1925 (Nematoda: Cosmocercidae) in Toads from Argentina. Memorias do Instituto Oswaldo Cruz. 93:737738. [ Links ]
ParedesCalderón, L., V. LeónRègagnon and L. GarcíaPrieto. 2004. Helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. Journal of Parasitology 90:692696. [ Links ]
Ramallo, G., C. R. Bursey and S. R. Goldberg. 2007. Two new species of Cosmocercids (Ascaridida) in the toad Chaunus arenarum (Anura: Bufonidae) from Argentina. Journal of Parasitology 93:910916. [ Links ]
Ramallo, G., C. R. Bursey and S. R. Goldberg. 2008. New species of Aplectana (Ascaridida: Cosmocercidae) in the toads Rhinella granulosa and R. schneideri (Anura: Bufonidae) from Northem Argentina. Journal of Parasitology 94:13571360. [ Links ]
Ramírez, V. G, C. Sueldo and R. V. Mesones. 1979. Aportes sobre parásitos de Bufo arenarum de la Provincia de Salta. II. (Nematoda). Neotropica 25:90. [ Links ]
Schaefer, E. F., M. I. Hamann, A. I. Kehr, C. E. González and M. I. Duré 2006. Trophic, reproductive and parasitological aspects of the ecology of Leptodactylus chaquensis (Anura: Leptodactylidae) in Argentina. Herpetological Journal 16:387394. [ Links ]
Sueldo, C. and V. G. Ramírez. 1976. Aportes sobre parásitos de Bufo arenarum en la provincia de Salta (Nematoda). Neotropica 22:105106. [ Links ]
Travassos, L. 1925. Contribução ao conhecimento da fauna helmintolojica dos batráchios do Brasil. Nematódeos intestinais. Sciencia Medica 3:673687. [ Links ]
Vicente, J. J., H. O. Rodríguez, D. C. Gomes and M. R. Pinto. 1990. Nematóides do Brasil. Parte II: Nematóides de anfíbios. Revista Brasilera de Zoologia 7:549626. [ Links ]