AMPHIBIAN DISEASES. Evaluation of Helminths Associated with 14 Amphibian Species from a Neotropical Island Near the Southeast Coast of Brazil

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1 AMPHIBIAN DISEASES 227 AMPHIBIAN DISEASES Herpetological Review, 2014, 45(2), by Society for the Study of Amphibians and Reptiles Evaluation of Helminths Associated with 14 Amphibian Species from a Neotropical Island Near the Southeast Coast of Brazil Brazil harbors a great diversity of amphibians, with approximately 877 species recorded (Segalla et al. 2012). The Atlantic Rain Forest (Mata Atlântica) biome significantly contributes to this high biodiversity, on the Brazilian coast and in fragments inside the country; more amphibian species live here than any other Brazilian biome, including many endemic species (IUCN 2006; SOS Mata Atlântica and INPE 2002). Some islands along the São Paulo State coast are priority areas for Atlantic Forest conservation, with unique biota for scientific investigations. In island environments, information on helminth parasites associated with populations or communities remains scarce. Lent et al. (1946) researched helminth parasites of Rhinella schneideri (Werner, 1894) (syn. Bufo paracnemis) specimens from Isla Valle, Paraguay, and found two species of Digenea (Catadiscus freitaslenti Ruiz, 1943 and Mesocoelium incognitum Travassos, 1921) and one nematode species (Ochoterenella digiticauda Caballero, 1944), increasing the knowledge concerning the helminth fauna of anurans. Torres and Puga (1996) reported for the first time Centrorhynchus sp. (Acanthocephala) associated with Eupsophus roseus (Duméril and Bibron, 1841) from Isla Teja, and Eupsophus calcaratus (Günther, 1881) from Chiloé Island, Chile, increasing to ten the number of helminth species record in anurans of Chile. Ramalho et al. (2009), researching helminth parasites of lizards from the Fernando de Noronha Archipelago, Brazil, discovered three helminth species associated with an ALINE AGUIAR* UNESP Universidade Estadual Paulista, Instituto de Biociências de Botucatu Departamento de Parasitologia, Laboratório de Parasitologia de Animais Silvestres DRAUSIO HONORIO MORAIS UNESP Universidade Estadual Paulista, Instituto de Biociências de Botucatu Departamento de Parasitologia, Laboratório de Parasitologia de Animais Silvestres PAULO JOSÉ PYLES CICCHI UNESP Universidade Estadual Paulista, Instituto de Biociências de Botucatu Departamento de Zoologia REINALDO JOSÉ DA SILVA UNESP Universidade Estadual Paulista, Instituto de Biociências de Botucatu Departamento de Parasitologia, Laboratório de Parasitologia de Animais Silvestres *Corresponding author; aline.aguiarr@gmail.com introduced lizard, Salvator merianae Duméril and Bibron, 1839 (syn. Tupinambis merianae), and seven helminth species associated with endemic lizards, Trachylepis atlantica (Schmidt, 1945) and Amphisbaena ridley Boulenger, 1890, suggesting that introduced lizards can carry other helminths to locations where they had not existed before, and that endemic lizards share parasite species with lizards that have been introduced. Island research is interesting due to geographic isolation and the potential of endemic species (MacArthur and Wilson 1967; Vitousek et al. 1995). However, it is questionable whether Anchieta Island, an island near the north coast of São Paulo, Brazil, is in fact isolated, due to its distance of only 8 km from the continent and receiving visitors of 80,000 people annually to Anchieta Island State Park ( The environment of this island, as well as fragments of Mata Atlântica, has been altered by human development. Unfortunately, there is little information about the endemic fauna of this area. In a herpetofaunal survey of Anchieta Island, Cicchi et al. (2009) reported the following anurans: Fritziana fissilis (Miranda-Ribeiro, 1920) (syn. Flectonotus fissilis) (Hemiphractidae); Haddadus binotatus (Spix, 1824) (Craugastoridae); Ischnocnema bolbodactyla (Lutz, 1925); Ischnocnema parva (Girard, 1853) (Brachycephalidae); Rhinella ornata (Spix, 1824); Dendrophryniscus brevipollicatus Jiménez de la Espada, 1870 (Bufonidae); Hypsiboas albomarginatus (Spix, 1824); Scinax hayii (Barbour, 1909) (Hylidae); Hylodes asper (Müller, 1924); Hylodes phyllodes Heyer and Cocroft, 1986 (Hylodidae); Leptodactylus cf. marmoratus (Steindachner, 1867); Leptodactylus latrans (Steffen, 1815) (Leptodactylidae); Chiasmocleis carvalhoi Cruz, Caramaschi, and Izecksohn, 1997; and Myersiella microps (Duméril and Bibron, 1841) (Microhylidae). It is likely that many other anurans are not yet discovered. The helminth fauna associated with amphibians comprises general parasites (Aho 1990) with a low specificity with their hosts. Therefore, there are frequently new records of hosts harboring parasites that have not previously been related to them. Herein, this study reports the helminth fauna associated to 14 amphibian species, of the Mata Atlântica biome occurring in Anchieta Island Park State an insular environment, of a biome with high endemism and biodiversity in which very little is known. Moreover, we also summarize the known distributions of these helminth parasites in South America to present the state of knowledge about biodiversity of helminthes associated to amphibians from South America. This source will be important for futures studies on this subject.

2 228 AMPHIBIAN DISEASES Table 1. Prevalence of helminths infection in 14 anuran species from Anchieta Island, north coast of São Paulo State, Brazil. Taxon codes: FAMA = Falcaustra mascula; OSSP = Oswaldocruzia sp.; OXOX = Oxyascaris oxyascaris; PHSP = Physaloptera sp.; RHSP = Rhabdias sp.; LARV = Larvae of Nematoda; CYAM = Cylindrotaenia cf. americana; ACAN = Acanthocephala; COSM = Cosmocercidae. Hosts N FAMA OSSP OXOX PHSP RHSP LARV CYAM ACAN COSM Total Bufonidae Dendrophryniscus brevipollicatus Rhinella ornata Brachycephalidae Ischnocnema bolbodactyla Ischnocnema parva Craugastoridae Haddadus binotatus Hemiphractidae Fritziana fissilis Hylidae Scinax hayii Hypsiboas albomarginatus Hylodidae Hylodes asper Hylodes phyllodes Leptodactylidae Leptodactylus latrans Leptodactylus cf. marmoratus Microhylidae Myersiella microps Chiasmocleis carvalhoi TOTAL Anurans were collected from the preserved area of Mata Atlântica, Anchieta Island State Park (23.45 S, W), Ubatuba municipality. The island consists of 828 ha of Dense Rain Forest and Restinga forests (Veloso et al. 1991). Its regional climate is typically tropical humid, with no dry season (Nimer 1989). Anurans were collected monthly from July 2005 to June 2006, using pitfall traps, a visual encounter survey, and opportunistic collection. The specimens were identified, fixed (10% formaldehyde), maintained in alcohol and deposited in the Coleção de Vertebrados Dr. Jorge Jim (CVJJ) of the Universidade Estadual Paulista (UNESP/Botucatu). For parasitological studies, 194 anurans of 14 species were necropsied: F. fissilis (N = 18); H. binotatus (N = 9); I. bolbodactyla (N = 4); I. parva (N = 20); R. ornata (N = 20); D. brevipollicatus (N = 3); H. albomarginatus (N = 18); S. hayii (N = 23); H. asper (N = 2); H. phyllodes (N = 3); L. cf. marmoratus (N = 40); L. latrans (N = 5); C. carvalhoi (N = 26); and M. microps (N = 3). During necropsy, hosts were sexed and the body cavity, digestive tract, accessory organs and musculature were examined for helminth parasites. The helminth parasites were counted and preserved in 70% ethyl alcohol. For identification, the helminths were examined as temporary mounts: nematodes were cleared with lactophenol, whereas acanthocephalans and cestodes were stained with carmine and cleared with eugenol or creosote. The helminths were analyzed using a computerized image analysis system (Qwin Lite 3.1; Leica Microsystems, Wetzlar, Germany). The systematic determination of the helminths was conducted following the methods of Yamaguti (1959, 1961, 1963), Vicente et al. (1991), Anderson et al. (2009), and Gibbons (2010). The infection prevalence, mean abundance (MA) and mean intensity of infection (MII) were calculated for helminths according to Bush et al. (1997). MII and MA are presented as mean values with their standard errors. A total of 2058 helminths were collected from 103 of 195 anuran specimens examined, representing an overall prevalence of 52.82% (Table 1) and an MA of ± The parasitized individuals were infected with an average of ± 9.24 helminth indivuduals per host. In the anuran community, we identified a species of Cestoda, Cylindrotaenia cf. americana Jewell, 1916 (N = 7), a species of Acanthocephala (N = 54) and 12 species of Nematoda including: Falcaustra mascula (Rudolphi, 1819) (N = 2); Oxyascaris oxyascaris Travassos, 1920 (N= 9); Oswaldocruzia sp. (N = 6); Rhabdias sp. (N = 31); and Physaloptera sp. (N = 86), and a total of 1078 cosmocercids. Of the cosmocercids samples that were male, it was possible to identify the following species: Aplectana pintoi Travassos, 1925 (N = 5); Aplectana crucifer Travassos, 1925 (N = 3); Aplectana sp. (N = 13); Cosmocerca brasiliense Travassos, 1925 (N = 11); Cosmocerca parva Travassos, 1925 (N = 1); Cosmocerca travassosi Rodrigues and Fabio, 1970 (N = 11); and Cosmocerca sp. (N = 14). Unidentified nematode larvae (N = 784) parasitized nine of the 14 anuran species examined. Each parasitized individual was infected with an average of 1.56 ± 0.08 helminth species. Overall, cosmocercids were the most common helminth, with a prevalence of 35.38% and an MA of 5.53 ± The next mostcommon helminth was Physaloptera sp., with a prevalence of 11% and an MA of 0.4 ± The other helminth species had low prevalence, MA and MII (see Appendix). Among the analyzed hosts, the L. latrans specimens were highly parasitized (100%), followed by H. binotatus (88.9%) and

3 AMPHIBIAN DISEASES 229 Table 2. Overall Prevalence (P%), number of recovered helminths (RH), mean abundance (MA), mean intensity of infection (MII) followed by standard error (SE), of helminths associated to 14 anuran species from Anchieta Island, São Paulo State, Brazil. Hosts P(%) RH MA ± SE MII ± SE Brachycephalidae Ischnocnema bolbodactyla (N = 4) ± Ischnocnema parva (N = 20) ± ± 0.3 Bufonidae Dendrophryniscus brevipollicatus (N = 3) ± ± 1.0 Rhinella ornata (N = 20) ± ± 4.8 Craugastoridae Haddadus binotatus (N = 9) ± ± 79.4 Hemiphractidae Fritziana fissilis (N = 18) ± ± 0.9 Hylidae Hypsiboas albomarginatus (N = 18) ± ± 2.5 Scinax hayii (N = 23) ± ± Hylodidae Hylodes asper (N = 2) ± Hylodes phyllodes (N = 3) ± ± 0.5 Leptodactylidae Leptodactylus latrans (N = 4) ± ± 3.1 Leptodactylus cf. marmoratus (N = 40) ± ± 1.1 Microhylidae Chiasmocleis carvalhoi (N = 26) ± ± 1.7 Myersiella microps (N = 3) ± Table 3. Countries and localities reported for helminths associated with anurans from South America. Abbreviation of Brazilian States is informed within brackets. Countries Brazil Argentina Chile Colombia Ecuador French Guiana Guyana Paraguay Peru Localities (states, cities or provinces) Amazonas (AM), Bahia (BA), Distrito Federal (DF), Espírito Santo (ES), Goias (GO), Mato Grosso do Sul (MS), Para (PA), Paraná (PR), Rio de Janeiro (RJ), Rio Grande do Sul (RS), Santa Catarina (SC), São Paulo (SP), and Tocantins (TO) Corrientes Locality not reported Central Cordillera Pastaza and Santa Cecilia Comté Rupunini Assuncion, Chaco-I, and Remanso Castillo Cuzco, Lima, Piura, and Ucayali R. ornata (75%). Haddadus binotatus had a high MA of helminths (78.3 ± 70.7) as well as MII (88.1 ± 79.4). Scinax hayii had a high MII due to many nematode larvae parasitizing one individual host (MII = 235 ± 233.5). On the other hand, I. bolbodactyla specimens had both a low MA (0.25 ± 0.25) and MII (1.0) (Table 2). In an Appendix, we list the helminth species of this study with the percentage prevalence and MII per host species, together with the status distribution of these helminths in South American hosts. The localities, as cities or states, are indicated within parentheses followed by the reported host. In all, 27 localities were reported in nine countries from South America (Table 3). The bibliography of helminth species reported for anurans from South American continent were based on information from both online databases (such as BioOne, Isi, Jstor, PubMed, Scielo, Scopus, and Web of Science) and published monographs (Yamaguti 1959, 1961, 1963). We present the first report of helminth fauna from nine anuran species (F. fissilis, I. bolbodactyla, R. ornata, D. brevipollicatus, H. albomarginatus, S. hayii, H. asper, C. carvalhoi, and M. microps). Only five host species (H. binotatus, I. parva, H. phyllodes, L. cf. marmoratus, and L. latrans) have been reported on the continent; however, this study is the only one that has been performed in South America regarding helminths associated with anurans from an insular environment. All helminths found here were previously reported in anurans from the South American continent; however, there were 12 helminth species recorded in new hosts. Only Oxyascaris oxyascaris and Falcaustra mascula have been reported parasitizing Leptodactylus latrans (Stumpf 1982; Baker and Vaucher 1985; Rodrigues et al. 1990; Vicente et al. 1991). Anchieta Island is currently a conservation area, where the parasitic fauna of anurans has never been studied; for some helminthes, we present the parasitism in anurans species for the first time: 1) Haddadus binotatus is a new record for Oswaldocruzia sp., Rhabdias sp., Physaloptera sp., A. pintoi and C. brasiliense; 2) H. phyllodes is a new record for Rhabdias sp., C. brasiliense and C. cf. Americana; 3) L. cf. marmoratus is a new record for Rhabdias sp. Of all the helminths reported in this study, acanthocephalans were the least frequent (Smales 2007). This is due to the transmission of acanthocephalans to anurans occurring by ingestion of invertebrates parasitized with cystacants that infect the gastrointestinal tract (Kennedy 2006), making the anuran a definitive or paratenic host (Smales 2007; Pinhão et al. 2009; Santos and Amato 2010b). The cestode Cylindrotaenia cf. americana is a Western-hemisphere species known to infect anurans of the families Bufonidae, Ranidae, Hylidae, Leptodactylidae, and Dendrobatidae (Jones 1987; Bursey et al. 2001). The parasitism of this cestode in H. phyllodes and I. parva adds two anuran families, Hylodidae and Brachycephalidae, to this list. The nematodes of Cosmocercidae family are transmitted directly; the final host is infected by ingestion of eggs containing infective larvae (Aplectana spp.) or by infective larvae that penetrate actively in the host s tegument (Cosmocerca spp.) (Anderson

4 230 AMPHIBIAN DISEASES 2000). These parasites were highly prevalent, and had high MA and MII, corroborating the general pattern of these helminths of amphibians (Aho 1990; Bursey et al. 2001). This is due to the fact that these helminths have to infect their hosts directly, without intermediate hosts to complete their biological cycle (Anderson 2000; Hamann et al. 2006b). The infection by Rhabdias spp. and Oswaldocruzia spp. occurs similarly, transmitted directly by larvae that penetrate actively in the host s tegument. Rhabdias spp. infection occurs only by parthenogenetic females that alternate between free-living and parasitic existence on amphibian lungs (Anderson 2000). About the Kathlaniidae (F. mascula and O. oxyascaris), a nematode family, very little is known concerning their indirect transmission; Anderson (2000) suggests that possibly kathlaniids in the lower vertebrates develop to the third stage outside the host and then invade various invertebrates which serve as paratenic hosts. Physaloptera spp. parasitize mammals and reptiles, and do not complete their life cycle in amphibians. Larvae of Physaloptera sp. are found in the stomach mucosa of amphibians that ingest larvae-infected insects, so the amphibian can be an intermediate or paratenic host (Anderson 2000). We did not find these larvae in five host species: D. brevipollicatus (N = 3), I. bolbodactyla (N = 4), I. parva (N = 20), H. asper (N = 2), and M. microps (N = 3). Excepting for I. parva, this can due to the fact that there were low sample sizes of these anurans. Also, the absence of infection with Physaloptera sp. in these anurans can be explained by their feeding, which may not transmit Physaloptera spp. larvae. The anurans have a generalized diet, eating any arthropods, but some, as those cited above, frequently feed ants and isopods (AmphibiaWeb 2014). Studies concerning the life cycle of Physaloptera spp. indicate the more commum intermediate hosts are cockroaches (Blatella germanica) (Alicata 1937; Hobmaier 1941; Lee 1955). Thus, we may consider that the absence of Physaloptera sp. is related to diet of anurans.we found at least 14 helminth species associated with anurans from Anchieta Island; of these, four species have an indirect life cycle, where an intermediate host is required for completion of the parasite s cycle. The other 10 species are transmitted directly, and do not require an intermediate host. So, in this way, they have success in their life cycle. Digenean trematodes, with two or more intermediate hosts, were not found in anurans from Anchieta Island, possibly due to the absence of the intermediate hosts required for the biological cycle of these helminths. Even though trematodes have been found frequently on the continent in Brazilian anurans (Travassos et. al. 1969), it is likely that parasites with heteroxenic cycles have difficulty establishing themselves in insular environments. On the other hand, the composition of anuran helminth fauna of Anchieta Island is similar to the mainland, all helminth species are commonly associated to anurans from continent. Anchieta Island has a continental origin, occurring on the Brazilian continental shelf, and it exists now as an island due to one or more of the several oscillations of sea level during the Pleistocene (Martin et al. 1986), the last of which occurred about 11,000 yrs ago (Souza et al. 2005). The common geological origin and the short distance to the mainland (8 km) have consequences such as the island and mainland having the same vegetation (Atlantic Rain Forest - Mata Atlântica ) and climatic conditions which are similar to littoral coast, allowing the development of the same species. It is expected that continental islands present a similar fauna to the continent, since this isolated portion of land has been directly connected to the continent. Thus, there is still a need for zoological studies in insular environments, allowing observations of the similarity to the continent or to neighboring islands, as well as detection of possible introduced species or local extinctions. The knowledge of parasite communities in amphibian hosts and the patterns and processes underlying their structure has grown, but most of the studies have been performed with species from temperate latitudes (Aho 1990). 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7 AMPHIBIAN DISEASES 233 7: , and E. Santos Fauna helmintológica de Leptodactylus ocellatus de Volta Redonda, Estado do Rio de Janeiro. Atas Sociedade de Biologia do Rio de Janeiro 18: Vitousek, P. M., L. L. Loope, and H. Andersen Islands: Biological Diversity and Ecosystem Function. Springer-Verlag, New York. 238 pp. Yamaguti, S Systema Helminthum - Cestodes. Vol. 2. Interscience Publishers, London. 860 pp Systema Helminthum - Nematodes. Vol. 3 (Part 1 and 2). Interscience Publishers, London pp Systema Heminthum. Vol. 5. The Acantocephala of Vertebrates. Interscience Publishers Inc., New York. 423 pp. Appendix I Nematoda Rhabdiasidae Rhabdias sp. Host, P% and IMI: R. ornata (P= 40%; IMI=2.1 ± 0.4), H. binotatus (P = 22.2%; IMI = 2.5 ± 1.5), S. hayii (P = 4.3%; IMI = 2.0), H. albomarginatus (P = 11.1%; IMI = 2.0 ± 1.0), L. cf. marmoratus (P = 2.4%; IMI= 2.0) and C. carvalhoi (P = 3.8%; IMI = 1.0). Site of infection: lungs. Other reported hosts and locality: Hypsiboas albopunctatus (Spix, 1824) (GO, DF), Leptodactylus chaquensis Cei, 1950 (Corrientes), L. latrans (syn. Leptodactylus ocellatus) (PA, RJ), Leptodactylus podicipinus (Cope, 1862) (MS), Pseudis platensis Gallardo, 1961 (MS), Rhinella bergi (Céspedez, 2000) (Corrientes), Rhinella crucifer (Wied-Neuwied, 1821) (syn. Bufo crucifer) (RJ), Rhinella icterica (Spix, 1824) (syn. Bufo ictericus) (ES) and Rhinella marina (Linnaeus, 1758) (syn. Bufo marinus) (PA). Geographic range: Argentina (González and Hamann 2007b; Hamann et al. 2006b) and Brazil (Campião et al. 2009, 2010; Fabio 1982; Holmes et al. 2008; Rodrigues 1986; Rodrigues et al. 1982, 1990; Travassos et al. 1939; Travassos and Freitas 1964; Vicente et al. 1991; Vicente and Santos 1976). Remarks: R. ornata, H. binotatus, S. hayii, H. albomarginatus, L. cf. marmoratus and C. carvalhoi represent new host records for the genus Rhabdias; Anchieta Island is a new locality record. Molineidae Oswaldocruzia sp. Host, P% and IMI: R. ornata (P = 10%; IMI = 2.0 ± 0) and H. binotatus (P = 22.2%; IMI = 1.0 ± 0). Site of infection: small intestine. Other reported hosts and locality: Hypsiboas boans (Linnaeus, 1758) (syn. Hyla boans) (AM), Hypsiboas sp. (MS), Leptodactylus bufonius Boulenger, 1894 (Corrientes), Leptodactylus fuscus (Schneider, 1799) (syn. Leptodactylus sibilatrix) (ES), L. latrans (syn. L. ocellatus) (PA), Leptodactylus pentadactylus (Laurenti, 1768) (Comté), Lysapsus limellum Cope, 1862 (syn. Pseudis limellum) (PA), Physalaemus albonotatus (Steindachner, 1864) (Corrientes), Rhinella crucifer (syn. B. crucifer) (RJ), Rhinella fernandezae (Gallardo, 1957) (RS), R. icterica (syn. Bufo ictericus and Chaunus ictericus) (ES, RJ, SC), Rhinella granulosa (Spix, 1824) (syn. Bufo granulosus) (PA), R. marina (syn. Bufo marinus) (AM, PA) and Rhinella schneideri (syn. Chaunus schneideri) (MS). Geographic range: Argentina (González and Hamann 2006b, 2012), Brazil (Gonçalves et al. 2002; Luque et al. 2005; Lux Hoppe et al. 2008; Rodrigues et al. 1982; Rodrigues 1986; Santos and Amato 2010a; Travassos et al. 1939, 1964; Travassos and Freitas 1941, 1964; Vicente et al. 1991) and French Guiana (Ben Slimane and Durette-Desset 1996). Remarks: R. ornata and H. binotatus represent new host records for Oswaldocruzia sp.; as species determination was based on male characteristics, it was not possible to assign a species designation for our nematode. Anchieta Island is a new locality record. Physalopteridae Physaloptera sp. Host, P% and IMI: R. ornata (P = 20%; IMI = 2.7 ± 1.2), H. binotatus (P = 33.3%; IMI = 12.0 ± 8.5), F. fissilis (P = 16.7%; IMI = 1.7 ± 0.7), S. hayii (P = 8.7%; IMI = 1.0), H. albomarginatus (P = 22.2%; IMI = 5.7 ± 4.4), H. phyllodes (P = 33.3 %; IMI = 1.0), L. latrans (P = 25%; IMI = 5.0), L. cf. marmoratus (P = 2.4%; IMI = 1.0), C. carvalhoi (P = 7.7%; IMI = 1.0 ± 0) and M. microps (P = 10%; IMI = 2.0 ± 0). Site of infection: stomach. Other reported hosts and locality: Allobates marchesianus (Melin, 1941) (syn. Colostethus marchesianus) (Cuzco), Ctenophryne geayi Mocquard, 1904 (Cuzco), Dendropsophus leali (Bokermann, 1964) (syn. Hyla leali) (Cuzco), Dendropsophus leucophyllatus (Beireis, 1783) (syn. Hyla leucophyllatus) (Cuzco), Dendropsophus marmoratus (Laurenti, 1768) (syn. Hyla marmorata) (Cuzco), Edalorhina perezi Jiménez de la Espada, 1870 (Cuzco), Hamptophryne boliviana (Parker, 1927) (Cuzco), Hypsiboas boans (syn. Hyla boans) (Cuzco), Hypsiboas faber (Wied-Neuwied, 1821) (syn. Hyla faber) (RJ), Hypsiboas cinerascens (Spix, 1824) (syn. Hyla granosa) (Cuzco), Hypsiboas fasciatus (Günther, 1858) (syn. Hyla fasciata) (Cuzco), Leptodactylus bolivianus Boulenger, 1898 (Cuzco), L. bufonius (Corrientes), L. latrans (syn. Leptodactylus caliginosis and L. ocellatus) (RJ, TO), Leptodactylus leptodactyloides (Andersson, 1945) (TO, Cuzco), Leptodactylus lineatus (Schneider, 1799) (syn. Lithodytes lineatus) (Cuzco), L. marmoratus (syn. Adenomera marmorata) (RJ), Leptodactylus mystaceus (Spix, 1824) (RJ, Cuzco), L. pentadactylus (Cuzco), Leptodactylus petersii (Steindachner, 1864) (TO), Leptodactylus rhodonotus (Günther, 1869) (Cuzco), Osteocephalus taurinus Steindachner, 1862 (Cuzco), Oreobates cruralis (Boulenger, 1902) (syn. Eleutherodactylus curalis) (Cuzco), Phyllomedusa tomopterna (Cope, 1868) (Cuzco), P. albonotatus (Corrientes), Physalaemus santafecinus Barrio, 1965 (Corrientes), Physalaemus signifer (Girard, 1853) (RJ), Physalaemus soaresi Izecksohn, 1965 (RJ), Pristimantis fenestratus (Steindachner, 1864) (syn. Eleutherodactylus fenestratus) (Cuzco), Proceratophrys appendiculata (Günther, 1873) (RJ), Proceratophrys boiei (Wied-Neuwied, 1824) (RJ), Pseudis paradoxa (Linnaeus, 1758) (Cuzco), R. fernandezae (Corrientes), R. granulosa (Corrientes), R. icterica (SP), Rhinella margaritifera (Laurenti, 1768) (syn. Bufo typhonius) (Cuzco), R. marina (syn. B. marinus) (AM, PA, Cuzco), R. schneideri (Corrientes), Scinax acuminatus (Cope, 1862) (Corrientes), Scinax ictericus Duellman and Wiens, 1993 (Cuzco), Scinax nasicus (Cope, 1862) (Corrientes), Scinax ruber (Laurenti, 1768) (Cuzco), Trachycephalus coriaceus (Peters, 1867) (syn. Phrynoyas coriacea) (Cuzco) and Trachycephalus typhonius (Linnaeus, 1758) (syn. Phrynohyas venulosa) (Cuzco). Geographic range: Argentina (González and Hamann 2006a, 2006b, 2007a, 2008, 2010, 2012; Hamann et al. 2010), Brazil (Boquimpani-Freitas et al. 2001; Fabio 1982; Goldberg et al. 2009; Gonçalves et al. 2002; Klaion et al. 2011; Pinhão et al. 2009; Travassos 1925; Travassos and Freitas 1964; Vicente et al. 1991) and Peru (Bursey et al. 2001). Remarks: R. ornata, H. binotatus, F. fissilis, S. hayii, H. albomarginatus, H. phyllodes, C. carvalhoi and M. microps represent new host records for larvae of Physaloptera sp., but larval characteristics did not allow a species designation for our nematode. Anchieta Island is a new locality record. Kathlaniidae Falcaustra mascula Host, P% and IMI: L. latrans (P = 25%; IMI = 2.0) Site of infection: large intestine

8 234 AMPHIBIAN DISEASES Other reported hosts and locality: Crossodactylus gaudichaudii Duméril and Bibron, 1841 (RJ), Hylodes nasus (Lichtenstein, 1823) (Brazil), Hypsiboas albopunctatus (DF), H. faber (syn. H. faber) (Brazil), Ischnocnema guentheri (Steindachner, 1864) (syn. Eleutherodactylus guentheri) (RJ), I. parva (syn. Eleutherodactylus parvus) (RJ), Leptodactylus vastus A. Lutz, 1930 (syn. Leptodactylus labyrinthicus) (BA), Leptodactylus labyrinthicus (Spix, 1824) (BA, RJ), L. latrans (syn. L. ocellatus) (PR, RJ, Assuncion, Chaco-I, Remanso Castillo), Leptodactylus rhodomystax Boulenger, 1884 (PA), Rhinella granulosa (syn. B. marinus) (RJ), Rhinella icterica (syn. Bufo marinus ictericus and Bufo ictericus) (RJ) and R. schneideri (Corrientes, Assuncion, Chaco-I, Remanso Castillo). Geographic range: Argentina (González and Hamann 2008), Brazil (Fabio 1982; Fahel 1952; Freitas and Lent 1941; Goldberg et al. 2007; Holmes et al. 2008; Luque et al. 2005; Martins and Fabio 2005; Rodrigues et al. 1982; Stumpf 1982; Travassos 1925; Vicente and Santos 1976; Vicente et al. 1991,) and Paraguay (Lent et al. 1946, McAllister et al. 2010b). Remarks: Three species of Falcaustra have been reported from South America. Anchieta Island is a new locality record for F. mascula. Oxyascaris oxyascaris Host, P% and IMI: L. latrans (P = 50%; IMI = 4.5 ± 0.5). Site of infection: large and small intestines. Other reported hosts and locality: I. guentheri (syn. E. guentheri) (RJ), Leptodactylus fuscus (MS), Leptodactylus macrosternum Miranda-Ribeiro, 1926 (Paraguay), L. mystaceus (RJ), Leptodactylus mystacinus (Burmeister, 1861) (MS), L. latrans (syn. L. ocellatus) (PR, SP), Physalaemus signifer (RJ), P. soaresi (RJ), Pleurodema diplolister (Peters, 1870) (BA), Proceratophrys boiei (RJ) and Rhinella schneideri (Paraguay). Geographic range: Brazil (Fabio 1980, 1982; Klaion et al. 2011; Martins and Fabio 2005; Rodrigues 1986; Rodrigues et al. 1990; Travassos 1920, 1925; Vicente and Santos 1976; Vicente et al. 1991) and Paraguay (Baker and Vaucher 1985). Remarks: Anchieta Island is a new locality record for O. oxyascaris. Cosmocercidae Cosmocercidae gen. sp. Host, P% and IMI: S. hayii (P = 4.3%; IMI = 1.0), C. carvalhoi (P = 88.5%; IMI = 7.5 ± 1.6), H. asper (P = 50%; IMI = 17.0), H. phyllodes (P = 66.7%; IMI = 3.5 ± 0.5), L. cf. marmoratus (P = 9.5%; IMI = 5.0 ± 2.2), L. latrans (P = 50%; IMI = 10.0 ± 9.0), R. ornata (P = 65%; IMI = 11.6 ± 5.2), D. brevipollicatus (P = 66.7%; IMI = 3.0 ± 1.0), I. parva (P = 70%; IMI = 1.7 ± 0.2) and H. binotatus (P = 77.8%; 94.1 ± IMI = 89.9). Site of infection: stomach, large and small intestines. Other reported hosts and locality: Dermatonotus muelleri (Boettger, 1885) (MS), Eupemphix nattereri Steindachner, 1863 (MS), Hypsiboas prasinus (Burmeister, 1856) (SP), Leptodactylus latrans (syn. Leptodactylus ocellatus) (MS, RJ), L. pentadactylus (RJ), L. podicipinus (MS), Phyllomedusa azurea Cope, 1862 (MS), Rhinella crucifer (syn. Bufo crucifer) (RJ), R. granulosa (MS) R. icterica (SP and RJ), R. marina (MS), R. schneideri (syn. Bufo marinus) (MS) and Stereocyclops incrassatus Cope, 1870 (syn. Hypopachus incrassatus) (MS). Geographic range: Brazil (Campião et al. 2012, 2014; Chabaud 1978; Madelaire et al. 2012; Pinhão et al. 2009; Rodrigues et al. 1982, 1990; Travassos and Freitas 1942; Vicente et al. 1991). Remarks: This nematode is a very common parasite of amphibians, but S. hayii, C. carvalhoi, H. asper, H. phyllodes, R. ornata and D. brevipollicatus represent new host records for cosmocercids, and this study is the first report regarding helminth fauna of these anurans; only H. phyllodes has an acanthocephalan species reported: Anuracanthorhyncus tritaxisentis Bursey, Vrcibradic, Hatano and Rocha Specimens reported here as Cosmocercidae gen. sp., as well as prevalence and MII correspond to females and males of this helminth family. Congeneric females are very similar and specific identification was not possible based on morphological characteristics. Only males were identified based on morphology and size of taxonomic characteristics; these species identified are listed as follows. This segregated view between males and females for the present study is due to uncertainty of whether females belong to the same species as males, as well as the scarce research descriptions of female specimens. Aplectana crucifer Host: R. ornata Site of infection: large intestine Other reported hosts and locality: R. crucifer (syn. Bufo crucifer) (RJ). Geographic range: Brazil (Travassos 1925, 1931; Vicente et al. 1991) and Paraguay (McAllister et al. 2010b). Remarks: R. ornata represents the second host record for Aplectana crucifer in South America, and this study is the first report concerning helminth fauna of this anuran. Aplectana pintoi Host: I. parva and H. binotatus Site of infection: small and large intestines. Other reported hosts and locality: Craugastor gollmeri (Peters, 1863) (syn. Eleutherodactylus gollmeri) (RJ) and Ischnocnema guentheri (syn. Hylodes guentheri) (RJ). Geographic range: Brazil (Travassos 1925, 1931; Vicente et al. 1991). Remarks: I. parva and H. binotatus represent the third and fourth host records for Aplectana pintoi in South America. Anchieta Island is a new locality record for A. pintoi. Aplectana sp. Host: C. carvalhoi Site of infection: large intestine Other reported hosts and locality: Ceratophrys cranwelli Barrio, 1980 (MS), Dendropsophus microps (Peters, 1872) (syn. Hyla microps) (Brazil), Dermatonotus muelleri (MS), Haddadus binotatus (syn. Hylodes binotatus) (Brazil), Hypsiboas albopunctatus (DF), Hypsiboas pardalis (Spix, 1824) (syn. Hyla pardalis) (Brazil), Leptodactylus bufonius (Corrientes), L. chaquensis (Corrientes), Leptodactylus elenae Heyer, 1978 (MS), L. fuscus (MS), L. marmoratus (syn. Adenomera marmorata) (RJ), L. mystacinus (MS), L. podicipinus (MS), Leptodactylus syphax Bokermann, 1969 (MS), Physalaemus signifier (RJ), Rhinella granulosa (syn. Bufo granulosus) (PA), R. icterica (syn. Bufo ictericus) (ES, RJ), and R. marina (syn. Bufo marinus) (PA), Scinax acuminatus (syn. Hyla phrynoderma) (MS), Thoropa miliaris (Spix, 1824) (Brazil) and Trachycephalus mesophaeus (Hensel, 1867) (syn. Hyla mesophaea) (Brazil). Geographic range: Argentina (González and Hamann 2006b, Schaefer et al. 2006), Brazil (Chabaud 1978; Fabio 1982; Holmes et al. 2008; Luque et al. 2005; Rodrigues et al. 1990; Travassos 1925; Travassos et al. 1939, 1964; Travassos and Freitas 1964; Vicente and Pinto 1981; Vicente et al. 1991;) and Paraguay (Baker and Vaucher 1986). Remarks: C. carvalhoi represents a new host record for Aplectana sp., and this study is the first report concerning helminth fauna of this anuran. There are 23 Neotropical species of Aplectana, but characteristics did not allow a species designation for our nematode. Anchieta Island is a new locality record for Aplectana sp. Cosmocerca brasiliense Host: R. ornata, H. binotatus and H. phyllodes. Site of infection: small and large intestines. Other reported hosts and locality: Ameerega parvula (Boulenger, 1882) (syn. Dendrobates parvulus) (Santa Cecilia), Dendropsophus brevifrons (Duellman and Crump, 1974) (syn. Hyla brevifrons) (Cuzco), Dendropsophus cachimbo (Napoli and Caramaschi, 1999) (PA), Dendropsophus koechlini (Duellman and Trueb, 1989) (syn. Hyla koechlini) (Cuzco), D. leali (syn. Hyla leali) (Cuzco), D. leucophyllatus (syn. Hyla leucophyllata) (Cuzco),