Fifteen specimens of bufonid toad Rhinella icterica (Spix, 1824), 7 males and 8 females, collected in themunicipality of Botucatu, São Paulo State, Brazil, from March 2002 to January 2003, were examined forhelminth parasites. All toads were infected with at least one parasite species (overall prevalence = 100%). Five helminth species were found, including four nematode species, Rhabdias fuelleborni Travassos, 1926, Oswaldocruzia subauricularis (Rudolphi, 1819), gen. sp. no identified Cosmocercidae Travassos, 1925 and larvae of Physaloptera Rudolphi, 1819, and one acanthocephalan species, Acanthocephalus saopaulensis Smales, 2007. Rhabdias fuelleborni and A. saopaulensis were the most abundant species. Except for Physalopteridae larvae, all helminths occur in high prevalence (&gt; 70%). All helminth species presented a distribution toward to more aggregated pattern in these host samples.Quince ejemplares del sapo bufonido Rhinella icterica (Spix, 1824), 7 machos y 8 hembras, colectados en elmunicipio de Botucatu, Estado de São Paulo, Brasil, desde marzo del 2002 hasta enero del 2003, fueronanalizados en busca de helmintos parásitos. Todos los sapos estaban infectadas con al menos un parásito(prevalencia global = 100%). Cinco especies de helmintos fueron encontradas, entre ellas cuatro especies de nematodos, Rhabdias fuelleborniTravassos, 1926, Oswaldocruzia subauricularis (Rudolphi, 1819), gen. sp. no identificada Cosmocercidae Travassos, 1925 y larvas de Physaloptera Rudolphi, 1819, y una especieacantocéfalo, Acanthocephalus saopaulensis Smales, 2007. Rhabdias fuelleborni y A. saopaulensis fueronlas especies más abundantes. Aexcepción de las larvas de Physalopteridae, todos los helmintos presentaron una alta prevalencia (&gt; 70%). Todas las especies de helmintos presentaron una tendencia hacia un patrón más agregado de distribución en los hospederos muestreados

Alves dos Anjos, Luciano

da Silva, Reinaldo José

Pinhão, Rebeca

Wunderlich, Alison Carlos

Spanish

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Forma de citar: Pinhão, R.; Wunderlich, A. C.; Anjos, L. A.; Silva, R. J. 2009. Helminths of toad Rhinella icterica (Bufonidae), from the municipality of Botucatu, São Paulo State, Brazil. Neotropical Helninthology, vol. 3, nº1, pp. 35-40..Resumen Palabras clave: Acanthocephala – Amphibia - Fauna helmíntica - Índice de discrepancia –Nematoda  - Rhinella icterica.Quince ejemplares del sapo bufonido Rhinella icterica (Spix, 1824), 7 machos y 8 hembras, colectados en el municipio de Botucatu, Estado de São Paulo, Brasil, desde marzo del 2002 hasta enero del 2003, fueron analizados en busca de helmintos parásitos. Todos los sapos estaban infectadas con al menos un parásito (prevalencia global = 100%). Cinco especies de helmintos fueron encontradas, entre ellas cuatro especies de nematodos, Rhabdias fuelleborni Travassos, 1926, Oswaldocruzia subauricularis (Rudolphi, 1819), gen. sp. no identificada Cosmocercidae Travassos, 1925 y larvas de Physaloptera Rudolphi, 1819, y una especie acantocéfalo, Acanthocephalus saopaulensis Smales, 2007. Rhabdias fuelleborni y A. saopaulensis fueron las especies más abundantes. A excepción de las larvas de  Physalopteridae, todos los helmintos presentaron una alta prevalencia (> 70%). Todas las especies de helmintos presentaron una tendencia hacia un patrón más agregado de distribución en los hospederos muestreados.Key words: Acanthocephala - Amphibian - Discrepancy index - Helminth fauna - Nematoda - Rhinella icterica.AbstractFifteen specimens of bufonid toad Rhinella icterica (Spix, 1824), 7 males and 8 females, collected in the municipality of Botucatu, São Paulo State, Brazil, from March 2002 to January 2003, were examined for helminth parasites. All toads were infected with at least one parasite species (overall prevalence = 100%). Five helminth species were found, including four nematode species, Rhabdias fuelleborni Travassos, 1926, Oswaldocruzia subauricularis (Rudolphi, 1819), gen. sp. no identified Cosmocercidae Travassos, 1925 and larvae of Physaloptera Rudolphi, 1819, and one acanthocephalan species, Acanthocephalus saopaulensis Smales, 2007. Rhabdias fuelleborni and A. saopaulensis were the most abundant species. Except for Physalopteridae larvae, all helminths occur in high prevalence (> 70%). All helminth species presented a distribution toward to more aggregated pattern in these host samples. Neotrop. Helminthol., 3(1), 20092009 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)35HELMINTHS OF TOAD RHINELLA ICTERICA (BUFONIDAE),FROM THE MUNICIPALITY OF BOTUCATU, SÃO PAULO STATE, BRAZILHELMINTOS DEL SAPO RHINELLA ICTERICA (BUFONIDAE),DE LA MUNICIPALIDAD DE BOTUCATU, ESTADO DE SÃO PAULO, BRAZIL1 1 1 1Rebeca Pinhão , Alison Carlos Wunderlich , Luciano Alves dos Anjos  & Reinaldo José da Silva. *1 UNESP - Univ de Estadual Paulista, Campus de Botucatu,  Instituto de Biociências, Departamento de Parasitologia, Botucatu, São Paulo, Brazil. INTRODUCTIONThe Neotropical region harbors the highest amphibian biodiversity (Frost, 1985; Izecksohn & Carvalho-Silva, 2001) and Brazil has a great number of amphibian species of the world (IUCN, 2009; SBH, 2009). The knowledge of the helminth amphibian parasites is lower and the majority of studies dealing with their parasites are taxonomic descriptions and only few ones have been focused parasite populations and community structure (Goldberg et al., 1995; Linzey et al., 1998; Puga & Torres, 1999; Boquimpani-Freitas et al., 2001; Bursey et al., 2001; Goldberg & Bursey, 2003; Luque et al., 2005; Holmes et al., 2008; Campião et al., 2009).  The Cururu toad, Rhinella icterica (Spix, 1824), is largely distributed in the South American, inhabits forest regions, open vegetal formations and eventuality urban ambient (Izechsohn & Carvalho-Silva, 2001; Silvano et al., 2004). Despite of little knowledge on amphibian parasites, the helminth fauna of this species have been well studied (Kloss, 1971; Faria, 1978; Rodrigues et al., 1978, 1982; Vicente et al., 1990; Martins, 2004, Luque et al., 2005), however, only Luque et al. (2005) focused on the ecological data of helminths of R. icterica from Rio de Janeiro State, Brazil. The aim of this study was to evaluate the helminth fauna of the Cururu toad R. icterica in the municipality of Botucatu, São Paulo State, Brazil.A total of 15 animals comprising 7 males and 8 females were collected from March 2002 to January 2003 in the municipality of Botucatu, São Paulo State, Brazil. The toads were captured in a ruderal field around ponds and streams.  The toads were euthanatized with sodium thiopental solution and after examined for helminth parasites. In the laboratory, toads were necropsied and body cavity, lungs and the gastrointestinal tract were surveyed for endoparasites. The helminths were fixed in alcohol-formaldehyde-acetic acid (AFA) and stored in 70% ethanol. For identification, acanthocephalans were stained with carmine and cleared with eugenol. Nematodes were cleared with lactophenol. Mean intensity of infection, mean abundance and prevalence was calculated according to Bush et al. (1997).The discrepancy index (D) was calculated as suggested by Poulin (1993). The index has a minimum value of zero (D = 0), when all hosts harbor the same number of parasites. When all parasites are found in a single host, aggregation is maximum (D = 1). This index was calculated with software Quantitative Parasitology 3.0 (Rózsa et al., 2000). Voucher helminth specimens were deposited in the Coleção Helmintológica do Instituto de Biociências de Botucatu (CHIBB) at the Universidade Estadual Paulista, São Paulo State, Brazil.All toads were infected with at least one parasite species (overall prevalence = 100%). Five helminth species were found, including four nematode species, Rhabdias fuelleborni Travassos, 1926, Oswaldocruzia subauricularis (Rudolphi, 1819), Cosmocercidae gen. sp. no identified Travassos, 1925 and larvae of Physaloptera Rudolphi, 1819, a n d  o n e  a c a n t h o c e p h a l a n  s p e c i e s ,  Acanthocephalus saopaulensis Smales, 2007 (Table 1).Regarding the infection sites, lungs harbored only R. fuelleborni, at stomachs only larvae of Physaloptera were found; on the small and large intestines were found A. saopaulensis and O. subauricularis, and further the unidentified Cosmocercidae species were found at large intestine (Table 1). Except for Physaloptera larvae, all helminths occurred in high prevalence (> 70%).Rhabdias fuelleborni and A. saopaulensis were the most abundant species. With relation to intensity of infection, A. saopaulensis and R. fuelleborni presented the higher mean intensities of infection (Table 1).  All helminths species presented a distribution trend to aggregate in this host sample (Table I). The majority of infected amphibian harbored four helminth species (47%, n = 7), with a smaller percentage harboring three (33%, n = 5) or two species (20%, n = 3) (Figure 1).  36MATERIALS AND METHODSRESULTSHelminths of Rhinella Pinhão et al.Nematodes are the main helminth parasites found in the toad R. icterica (Luque et al., 2005), with few record of acanthocephalan infecting this anuran species (Smales, 2007). However, in this study A. saopaulensis was the more prevalent (86.7%) and abundant (723 specimens) parasite species. Acanthocephalus saopaulensis was recently described by Smales (2007) as new species of toad R. icterica, with low prevalence (33.3 %), mean intensity (22), and abundance (7.3). The present study found higher infection pattern than the data presented by Smales (2007) (Table 2), suggesting a different composition in the helminth parasite community associated with geographical variation. Also, the helminth richness found infecting R. icterica in São Paulo State was smaller than from Rio de Janeiro State (Luque et al., 2005), reinforcing the environment component in the establishment of the helminth fauna of this anuran species.Rhabdias fuelleborni and species of the genus Cosmocerca Diesing, 1861 infect several anurans species and occurs in many countries in South America (Baker & Vaucher, 1984; González & Hamann, 2004; Goldberg et al., 2007). Rhabdias fuelleborni was registered in host population from R. icterica (Vicente et al., 1990; Luque et al., 2005), R. marina and R. schneideri (Vicente et al., 1990).  All infection parameters, such as prevalence, mean intensity of infection and mean abundance, were higher on toads from Botucatu municipality (São Paulo State) in contrast to toads from Miguel Pereira municipality (Rio de Janeiro State) which has available data on literature (Luque et al., 2005).Rhabdias fuelleborni has been reported for R. marina, with high prevalence, intensity and abundance means (Ragoo & Omah-Maharaj, 2003). Regarding the genus Cosmocerca, Vicente et al. (1990) reported several helminth parasite species for R. icterica. Oswaldocruzia subauricularis were recorded harboring intestine of two populations of R. icterica, one from Curitiba municipality (Paraná State) (Vicente et al., 1990) and other from Miguel Pereira municipality (Luque et al., 2005).  In comparison with last population, all infection parameters were higher on toads from Botucatu municipality (Table II).  According Aho (1990), the higher richness helminth fauna in amphibians host are related to time that hosts spend in water during larval stages and breeding season. In this period the anurans are exposed to acanthocephalans and other helminths that are typically transmitted through the ingestion of aquatic invertebrates. Further, during terrestrial life-cycle hosts are exposed to transcutaneous penetration by nematode larvae (e.g. Rhabdias spp. and some Cosmocercidae) and ingestion of eggs of nematodes (such as Trichostrongylidae Leiper, 1912 and Cosmocercidae) (Aho, 1990). Moreover, this toad species presents a wide feeding spectrum that include 27 food items (Sabagh & Carvalho-e-Silva, 2008), increasing the possibility of infection by a large number of species of parasites.The higher prevalence, mean intensity of infection and abundance, mainly for A. saopaulensis, found in this R. icterica population could be related to differences in local composition of helminth species (component community, sensu Bush et al., 1997) or host ecological characteristics such as aggregation of the host population and differential consumption of dietary items. However, additional studies on other R. icterica population in a wide geographical distribution could improve the knowledge of this host-parasites relationship.A high infection rate by cosmocercid nematodes (prevalence = 80%; mean intensity of infection = 16 ± 5.5, range 1-68) was observed in the studied sample, however, the species was not identified because only females were found in all anuran hosts. The absence of males and the high number of eggs containing larvae may suggest a parthenogenetic reproduction mechanism in this helminth population, similar to other nematodes such as Strongyloides spp. and Rhabdias spp. (Anderson, 2000). We have no information on the occurrence of parthenogenesis in Cosmocercidae and so future studies will be conducted to better understanding this curious case.DISCUSSIONNeotrop. Helminthol., 3(1), 20093738Helminths of Rhinella Pinhão et al.Helminth Prevalence (%)  MA ± SE  MII ± SE (range)  D  Site of infection  Nematoda      Cosmocercidae CHIBB 289, 293, 297, 301, 303, 309, 314, 321, 326, 330, 334, 344, 350 80  12.8 ±  4.7  (0-68)  16 ±  5.5  (1-68)  0.595  Large intestine  Rhabdias fuelleborni  CHIBB 286, 290, 294, 298, 310, 315, 318, 322, 327, 331, 335, 338, 341  80  30.3 ± 10.1  (0-105)   37.8 ± 11.6  (3-105)  0.596  Lung  Oswaldocruzia subauricularis  CHIBB 288, 292, 296, 300, 304, 305, 306, 313, 324, 325, 333, 336, 337, 339, 343, 345, 348 73.3  5.6 ± 1.4  (0-20)  7.6 ± 1.5  (2-20)  0.476  Small and large intestine  Physalopteridae larvae  CHIBB 332 6.7  0.4  6  -  stomach  Acanthocephala      Acanthocephalus saopaulensis  CHIBB 287, 291, 295, 299, 302, 307, 308, 311, 312, 316, 317, 319, 320, 323, 328, 329, 340, 342, 346, 347, 349  86.7  48,2 ± 12,8  55,6 ± 13,6  (1-190)  0.471  Small and large intestine   Table 1. Prevalence, mean abundance (± standard error), mean intensity (± standard error), discrepancy index (D), and site of infection of helminths from Rhinella icterica (n = 15) from Botucatu, São Paulo State, Brazil. MA - mean abundance. MII - mean intensity of infection. CHIBB - Coleção Helmintológica do Instituto de Biociências de Botucatu.  PARASITE  Prevalence  (%)NºsampledRangeMean Intensity± SEMean Abundance± SEInfectionSiteReference33.386.7 315  2255.6 ± 13.6 7.348.2 ± 12.8ISI, LI Smales (2007)present studyAcanthocephalussaopaulensis   1-190       12.573.3  3215 1 - 9 4.5 ± 0.77.6 ± 1.5 0.5 ± 0,35.6 ± 1.4SISI, LILuque et al. (2005)present studyOswaldocruziasubauricularis  2 - 20     53.180.032151  - 31 8 ± 1.637.8 ± 11.6 4.2 ± 1.330.3 ± 10.1L Luque et al. (2005)present studyRhabdiasfuelleborni 3 - 105 LTable 2. Comparison between prevalence, mean intensity (± standard error), mean abundance (± standard error) and infection site of three population of toad Rhinella icterica.  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Percentage of Rhinella icterica (n = 15) infecting with two, three or four helminth species in the municipality of Botucatu, São Paulo State, Brazil.0 5 10 15 20 25 30 35 40 45 50 2 3 4Infected hosts (%) Richness of helminth speciesInfected hosts (%) *Correspondence to author/Autor para correspondencia:Reinaldo José da Silva,Departamento de Parasitologia, Instituto de Biociências,Universidade Estadual Paulista, Botucatu, São Paulo, Brazil. Correo electrónico/E-mail: reinaldo@ibb.unesp.brNeotrop. Helminthol., 3(1), 200940

HELMINTOS DEL SAPO RHINELLA ICTERICA (BUFONIDAE), DE LA MUNICIPALIDAD DE BOTUCATU, ESTADO DE SÃO PAULO, BRAZIL

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HELMINTOS DEL SAPO RHINELLA ICTERICA (BUFONIDAE), DE LA MUNICIPALIDAD DE BOTUCATU, ESTADO DE SÃO PAULO, BRAZIL

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