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1 Zootaxa 3666 (4): Copyright 2013 Magnolia Press Article A checklist of cercariae (Trematoda: Digenea) in molluscs from Brazil ISSN (print edition) ZOOTAXA ISSN (online edition) HUDSON ALVES PINTO & ALAN LANE DE MELO Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas da Universidade Federal de Minas Gerais. C.P. 486, , Belo Horizonte, Minas Gerais, Brasil. hudsonalves13@ig.com.br, aldemelo@icb.ufmg.br Abstract A checklist of digenetic trematodes found in molluscs from Brazil is presented based on 127 scientific articles published after a century of studies. To date 23 families, 35 genera and 46 species of trematodes were identified infecting 25 species of molluscs in the country. Another 36 species described in the collective-group Cercaria were found in 15 species of molluscs and have not yet been associated with the respective adult parasites. Larvae found in 20 species of molluscs and grouped into 10 cercarian types are also listed. Key words: trematodes, cercariae, molluscs, parasites, Brazil Introduction The study on the involvement of molluscs in the life cycle of trematodes began in Europe in the eighteenth century (Swammerdam 1737; Müller 1773) and since then a variety of larval trematodes (cercariae) was described and biological life cycles were elucidated by several authors in different parts of the world. Attempts to compilation the diversity of cercariae found in molluscs and life cycles known were performed for some geographic areas or localities (e.g. Nasir & Erasmus 1964; Ito 1964; Yamaguti 1975; Nasir 1984; Scholz et al. 2000; Ostrowski de Núñez & Gil de Pertierra 2004; Bartoli & Gibson 2007; Żbikowska & Nowak 2009; Cichy et al. 2011); some cercarian groups (e.g. Combes et al. 1980; Ostrowski de Núñez 1992); or larvae found in determined species of molluscs (e.g. Nasir 1980; Hechinger 2007, 2012; Esteban et al. 2011; Pinto & Melo 2011). Despite several studies related to the biological interaction between molluscs and trematodes, the diversity of larval stages and life cycles known represent only a small portion in relation to the number of species described from the adult stage recovered in definitive hosts. In fact, although currently the diversity of trematodes described from vertebrate hosts is about 18,000 species (Cribb et al. 2001; Bartoli & Gibson 2007), the number of life cycles known is significantly lower (about 1350), and the larval stages and first intermediate host of several families and genera of these helminths remain unknown (Yamaguti 1975; Cribb et al. 2003). Besides the relevance related to biodiversity, the study of larval trematodes is also justified by their medical and veterinary importance, considering that cercariae are developmental stages involved in the life cycle of several trematode species that cause diseases (e.g. schistosomiasis, paragonimiasis, clonorchiasis, fascioliasis,cercarial dermatitis) in human or domestic animals (e.g Muller & Wakelin 2002; Keiser & Utzinger 2005; Soldánová et al. 2013). Moreover, several species of trematodes are associated with the occurrence of substancial economic losses in the fish (e.g. Hoffman 1999; Lane & Moris 2000; Noga 2010) and oyster (e.g. Lauckner 1983; Bower et al. 1994) farming. In Brazil, the study of larval trematodes began only in the twentieth century with the description of the Cercaria blanchardi by Pirajá da Silva (1912), larva which was subsequently linked to Schistosoma mansoni Sambon, 1907 by Lutz (1919). Since then, a diversity of larval trematodes was reported in molluscs from Brazil in the first decades of the 1900's century exclusively by Adolpho Lutz. Later, other Brazilian and foreign authors devoted to the elucidation of the diversity of larval stages and life cycles of trematodes found in molluscs in Brazil. However these studies are scattered in scientific literature, many of them published in non-english language (Portuguese) and in scientific journal of difficult access outside Brazil. In this regard, a compilation of existing data on cercariae found in molluscs in Brazil is required. Accepted by Norman Dronen: 26 Apr. 2013; published: 4 Jun

2 Material and methods A survey of the scientific literature on larval trematodes found in molluscs from Brazil was conducted between 2009 and 2013 by means of investigations in scientific databases such as Google Scholar, PubMed, Scopus and Web of Science, and by acquisition of the older articles in scientific libraries. The search terms used, both in English and Portuguese (between parentheses), were: larval trematodes (larvas de trematódeos), cercariae (cercárias), molluscs (moluscos) together with the term Brazil (Brasil). The higher taxa of the trematode species found were determined in accordance with Gibson et al. (2002), Jones et al. (2005) and Bray et al. (2008). The taxa of the molluscan hosts were updated according to Rios (1994) to marine species and Simone (2006) to freshwater and land species. The checklist of trematodes species found in molluscs in Brazil is presented in alphabetic order for each taxonomic category, followed by the author and data of description; the molluscan host species followed by author of description, class and family in the first mention; the cercarian group found in each larval trematode, in accordance with the classification originally proposed by Lühe (1909) and supplemented by different authors (Sewell 1922; Miller 1926; Dawes 1946; Schell 1970); the ecosystems where the respectives life cycles of the trematodes occur (freshwater, brackwish water or marine); the class of the potencial definitive hosts (amphibian, birds, fish, mammals and reptile), the Brazilian localities and states where of the molluscs were collected, and the bibliographic references in chronological order. Most records were based on naturally infected molluscs, except the molluscan hosts marked with an asterisk, which proved to be susceptible to experimental infection but have not been found infected in nature. In most of the species of trematodes listed in this study, cercariae emerge from the molluscs in aquatic or terrestrial environment; while in a few species (marked with the abbreviation IM (intramolluscan) in the cercarian type subheading) the cercariae do not emerge and metacercariae develop into their own first intermediate hosts. The trematode species described in the collective group Cercaria Müller, 1773, but not associated with the respective adult parasites are also listed in alphabetic order, with the cercarian group, the molluscan host, localities and states, and the respective references. The studies which cercariae were found in molluscs and have only been characterized as a certain cercarian group are also presented. The following abbreviations were used for Brazilian states: AL, Alagoas; BA, Bahia; CE, Ceará; DF Distrito Federal, GO, Goiás; MT, Mato Grosso; MG, Minas Gerais, PA, Pará; PR, Paraná; PE, Pernambuco; PI, Piauí; RJ, Rio de Janeiro; RS, Rio Grande do Sul; RN, Rio Grande do Norte; SC, Santa Catarina; SP, São Paulo; SE, Sergipe. Results The bibliographic survey results in the analyses of 127 scientific articles published between 1912 and 2013 recording the interaction between trematodes and molluscs in Brazil. In all, 17 families, 24 genera and 39 species of molluscs were evaluated for infection with larval trematodes in 123 localities from 16 Brazilian states and the Federal District. A total of 23 families, 35 genera and 46 species of trematodes were identified infecting 14 families, 18 genera and 25 species of molluscs from Brazil. Most of these trematode species (33) were found in freshwater molluscs, 5 in terrestrial molluscs and 7 are marine species. The experimental susceptibility of different species of molluscs to three trematode species were reported, but the first natural intermediate hosts of these parasites are still unknown. Other 36 species described in the genus Cercaria were reported infecting 8 families, 11 genera and 15 species of molluscs. Furthermore, different morphotypes of unidentified cercariae belonging to 10 cercarian groups were found infecting 8 families, 15 genera and 20 species of molluscs. Cercariae of Digenetic Trematodes Reported in Molluscs from Brazil Phylum Platyhelminthes Gegenbaur, 1859 Sub phylum Neodermata (Ehlers, 1995) 450 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

3 Class Trematoda Rudolphi, 1808 Subclass Digenea Carus, 1863 Brachylaimidae Joyeux & Foley, 1930 Postharmostomum gallinum Witenberg, 1923 Host: Bradybaena similaris (Ferussac) (Gastropoda: Bradybaenidae). Cercarian group: cercariaeum IM. Habitat: terrestrial. Localities: Rio de Janeiro, RJ; Pindamonhangaba, Roseira, São José dos Campos, Cachoeira Paulista, SP. References: Duarte (1980), Vianna et al. (1988), Amato & Bezerra (1992). Bucephalidae Poche, 1907 Bucephalopsis haimeana (Lacaze-Duthiers, 1854) Host: Anomalocardia brasiliana (Gmelin) (Bivalvia: Veneridae). Cercarian group: gasterostome. Habitat: marine. Definitive host group: fish. Locality: São Vicente, SP. Reference: Narchi (1966). Bucephalus margaritae Ozaki & Ishibashi, 1934 Host: Perna perna (Linnaeus) (Bivalvia: Mytilidae). Cercarian group: gasterostome. Habitat: marine. Definitive host group: fish. Locality: Florianópolis, SC. Reference: Marchiori et al. (2010). Bucephalus sp. Hosts: Crassostrea rhizophorae (Guilding), Crassostrea brasiliana (Lamarck) (Bivalvia: Mytilidae), Mytella guyanensis (Lamarck) (Bivalvia: Ostridae), P. perna. Cercarian group: gasterostome. Habitat: marine. Definitive host group: fish. Localities: Camamu, Valença, BA; Fortim, CE; Florianópolis, SC; Cananéia, São Sebastião, SP. References: Umiji et al. (1976), Galvão et al. (2000), Silva et al. (2002), Araújo & Rocha-Barreira (2004), Cochôa & Magalhães (2008), Zeidan et al. (2012). Cladorchiidae Fischoeder, 1901 Paraibatrema inesperata Ueta, Deberaldini, Cordeiro & Artigas, 1981 Host: Biomphalaria tenagophila (d'orbigny) (Gastropoda: Planorbidae). Cercarian group: amphistome. Definitive host group: mammals. Locality: Tremembé, SP. Reference: Ueta et al. (1981). CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 451

4 Clinostomidae Lühe, 1901 Clinostomum marginatum (Rudolphi, 1819) Hosts: Biomphalaria sp., Biomphalaria peregrina (d'orbigny) (Gastropoda: Planorbidae). Cercarian group: brevifurcate. Localities: Rio de Janeiro, RJ; Upper Paraná River floodplain, PR. Reference: Lutz (1934, 1935a), Dias et al. (2003). Clinostomum sp. Host: B. tenagophila. Cercarian group: brevifurcate. Locality: Santos, SP. Reference: Ruiz (1953). Cryptogonimidae Ward, 1917 Acanthocollaritrema umbilicatum Travassos et al., 1965 Host: Heleobia australis (d'orbigny) (Gastropoda: Hydrobiidae). Cercarian group: pleurolophocercous. Habitat: brackish water. Definitive hostgroup: fish. Reference: Simões et al. (2008). Cyathocotylidae Mühling, 1898 Mesostephanus odhneri (Travassos, 1924) Hosts: Bittiolum alternatum (Say) (Gastropoda: Cerithiidae), Potamides sp. (Gastropoda: Potamididae). Habitat: marine. References: Lutz (1933, 1935b), Dubois (1970). Derogenidae Nicoll, 1910 Halipegus dubius Klein, 1905 Host: Biomphalaria glabrata (Say) (Gastropoda: Planorbidae). Cercarian group: cystophorous. Definitive host group: amphibians. Locality: Belo Horizonte, MG. Reference: Paraense (1992). 452 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

5 Dicrocoeliidae Looss, 1889 Eurytrema coelomaticum (Giard & Billet, 1892) Host: B. similaris. Cercarian group: microcercous. Habitat: terrestrial. Definitive host group: mammals. Localities: Lorena, Pindamonhangaba, SP; Rio de Janeiro, RJ. References: Ragusa & Campos (1976), Amato & Bezerra (1992), Mattos Jr & Vianna (1994), Pinheiro et al. (2012). Diplostomidae Poirier, 1886 Austrodiplostomum compactum (Lutz, 1928) Hosts: Biomphalaria straminea (Dunker) (Gastropoda: Planorbidae); B. glabrata. Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2013). Hysteromorpha triloba (Rudolphi, 1819) Host: B. peregrina. Locality: Upper Paraná River Floodplain, PR. Reference: Souza et al. (2008). Echinostomatidae Looss, 1899 Echinostoma barbosai Lie & Basch, 1966 Host: B. glabrata, B. tenagophila, B. straminea*. Localities: Belo Horizonte, MG; Recife, PE. Reference: Lie & Basch (1966). Echinostoma erraticum Lutz, 1924 Host: Drepanotrema sp. (Gastropoda: Planorbidae). Reference: Lutz (1924). Echinostoma exile Lutz, 1924 Host: Physa marmorata Guilding (Gastropoda: Physidae). CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 453

6 Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2012b). Echinostoma luisreyi Maldonado Jr, Vieira & Lanfredi, 2003 Host: P. marmorata. Locality: Sumidouro, RJ. Reference: Maldonado Jr et al. (2003). Echinostoma nephrocystis Lutz, 1924 Host: Physa sp. (Gastropoda: Physidae). Reference: Lutz (1924). Echinostoma paraensei Lie & Basch, 1967 Hosts: B. glabrata, Lymnaea columella Say* (Gastropoda: Lymnaeidae), P. marmorata*. Definitive host group: mammals. Localities: Belo Horizonte, Caratinga, Bambuí, MG; Sumidouro, RJ. References: Lie & Basch (1967), Maldonado Jr et al. (2001). Echinostoma parcespinosum Lutz, 1924 Host: Pomacea sp. (Gastropoda: Ampullariidae). Reference: Lutz (1924). Echinostoma revolutum (Froelich, 1802) Host: Physa sp. Reference: Lutz (1924). Echinostoma rodriguesi Hsu, Lie & Basch, 1968 Hosts: P. marmorata. Definitive host groups: birds and mammals. Locality: Belo Horizonte, MG. Reference: Hsu et al. (1968). 454 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

7 Paryphostomum segregatum Dietz, 1909 Hosts: B. glabrata, B. straminea, B. tenagophila, Biomphalaria sp. Localities: Belo Horizonte, MG; Rio de Janeiro, RJ; Santo André, Santos, SP. References: Lutz (1924), Ruiz (1952a, b), Milward-de-Andrade (1965a, b), Joe & Basch (1967), Eduardo et al. (2012). Petasiger sp. Hosts: B. straminea, B. tenagophila. Locality: Matozinhos, undetermined localities, MG. References: Milward-de-Andrade & Campos (1969), Pinto et al. (2013a). Stephanoprora conciliata (Dietz, 1909) Hosts: Biomphalaria sp., Drepanotrema sp. Locality: Rio de Janeiro, RJ References: Lutz (1924, 1928). Eucotylidae Cohn, 1904 Paratanaisia bragai (Santos, 1934) Hosts: Leptinaria unilamellata (d'orbigny)* (Gastropoda: Subulinidae), Subulina octona (Brugüière)* (Gastropoda: Subulinidae). Cercarian group: cercariaeum IM. Habitat: terrestrial. Locality: undetermined locality, RJ. References: Keller & Araújo (1992), Brandolini et al. (1997), Brandolini & Amato (2006). Fasciolidae Railliet, 1895 Fasciola hepatica Linnaeus, 1758 Hosts: L. columella, Lymnaea viatrix d'orbigny, Lymnaea sp. (Gastropoda: Lymnaeidae). Cercarian group: gymnocephalous. Definitive host group: mammals. Localities: Itajubá, MG; localities from the litoral, PR; Campos dos Goytacazes, Rio de Janeiro, RJ; Rosário do Sul, Santa Vitória do Palmar, Sapucaia do Sul, RS; Eldorado, Miracatu, Piquete, Vale do Paraiba, SP. References: Lutz (1921b, 1922), Rezende et al. (1973), Gonzales et al. (1974), Ueta (1980), Busetti et al. (1983), Müller & Ueno (1984), Carvalho et al. (2001b), Gomes et al. (2002), Oliveira et al. (2002), Coelho & Lima (2003), Lima et al. (2009). CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 455

8 Haematoloechidae Freitas & Lent, 1939 Haematoloechus sp. Host: L. columella. Cercarian group: xiphidiocercaria. Definitive host group: amphibians. Locality: Miracatu, SP. References: Carvalho et al. (2001b, 2002). Heterophyidae Leiper, 1909 Ascocotyle (Phagicola) longa Ransom, 1920 Host: H. australis. Cercarian group: pleurolophocercous. Habitat: brackish water. Definitive host groups: birds and mammals. Reference: Simões et al. (2010). Centrocestus formosanus (Nishigori, 1924) Host: Melanoides tuberculata (Müller) (Gastropoda: Thiaridae). Cercarian group: pleurolophocercous. Definitive host group: birds and mammals. Localities: Brasília, DF; Belo Horizonte, MG; Natal, RN. References: Pinto & Melo (2010a), Paula-Andrade et al. (2012), Pinto & Melo (2012a). Pygidiopsis macrostomum Travassos, 1928 Host: H. australis. Habitat: brackish water. Cercarian group: pleurolophocercous. Definitive host group: mammals. Reference: Simões et al. (2009). Leucochloridiidae Poche, 1907 Leucochloridium flavum Travassos, 1922 Host: Omalonyx sp. (Gastropoda: Succineidae). Habitat: terrestrial. Cercarian group: cercariaeum IM. Locality: Rio de Janeiro, RJ; undetermined locality, MT. References: Lutz (1921a), Travassos (1928b). Leucochloridium sp. Hosts: Omalonyx sp., Succinea meridionalis d'orbigny (Gastropoda: Succineidae). Habitat: terrestrial. Cercarian group: cercariaeum IM. 456 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

9 Localities: Rio de Janeiro, RJ; Guaiba, RS. References: Lanzieri (1965), Thomé et al. (2006). Paramphistomidae Fischoeder, 1901 Paramphistomum sp. Hosts: B. tenagophila, Drepanotrema kermatoides (d'orbigny) (Gastropoda: Planorbidae). Cercarian group: amphistome. Definitive host group: mammals. Localities: Guaíba, Pelotas, Rio Grande, Santa Vitória do Palmar, Santo Antônio da Patrulha, RS. References: Santos et al. (1986), Veitenheimer-Mendes & Almeida-Caon (1989), Müller et al. (1992). Psilostomidae Losss, 1900 Ribeiroia sp. Host: B. straminea. Cercarian group: gymnocephalous. Locality: Belo Horizonte, MG. Reference: Pinto et al. (2013b). Renicolidae Dollfus, 1939 Renicola sp. Host: M. tuberculata. Cercarian group: gymnocephalous. Locality: Belo Horizonte, MG; Natal, RN. Reference: Pinto & Melo (2012a). Philophthalmidae Looss, 1899 Philophthalmus gralli Mathis & Leger, 1910 Host: M. tuberculata. Cercarian group: megalurous. Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2010b). CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 457

10 Schistosomatidae Stiles & Hassall, 1898 Dendritobilharzia pulverulenta (Braun, 1901) Host: B. straminea. Cercarian group: brevifurcate. Locality: Jequitibá, MG. Reference: Leite et al. (1982). Schistosoma mansoni Sambon, 1907 Hosts: Biomphalaria amazonica Paraense* (Gastropoda: Planorbidae), Biomphalaria cousini Paraense* (Gastropoda: Planorbidae), B. glabrata, B. peregrina*, B. straminea, B. tenagophila. Cercarian group: brevifurcate. Definitive host group: mammals. Localities: endemic in the Southeast and Northeast from Brazil. References: Pirajá da Silva (1912), Coutinho et al. (1940), Moura (1945), Correa & Paraense (1971), Paraense (1973), Teodoro et al. (2010). Due to the large amount of studies on the occurrence of S. mansoni in several localities from Brazil, only the first record of this parasite to each species of mollusk intermediate host were listed. Trichobilharzia jequitibaensis Leite, Costa & Costa, 1978 Hosts: L. columella*, P. marmorata*. Cercarian group: brevifurcate. Locality: Jequitibá, MG. Reference: Leite et al. (1979). Strigeidae Railliet, 1919 Apharyngostrigea sp. Hosts: B. peregrina, B. straminea. Localities: Rio de Janeiro, RJ; Upper Paraná River floodplain, PR. References: Lutz (1931), Dias et al. (2002). Australapatemon bdellocystis (Lutz, 1921) Host: B. straminea. References: Lutz (1921c, 1933), Dubois (1970). Cotylurus lutzi Basch, 1969 Host: B. glabrata. 458 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

11 Locality: Caetité, BA. Reference: Basch (1969). Strigea falconis brasiliana Szidat, 1929 Host: Drepanotrema anatinum (d'orbigny) (Gastropoda: Planorbidae). References: Lutz (1929), Dubois (1970). Typhlocoelidae Harrah, 1922 Typhlocoelum cucumerinum (Rudolphi, 1809) Hosts: B. glabrata*, B. tenagophila*. Cercarian group: cercariaeum IM. Locality: Jequitibá, MG. Reference: Schafranski et al. (1975). Zygocotylidae Ward 1917 Zygocotyle lunata (Diesing, 1836) Host: B. straminea. Cercarian group: amphistome. Definitive host group: birds and mammals. Locality: Iguatama, MG. Reference: Barbosa et al. (2011). Cercaria Müller, 1773 (species inquirendae) Cercaria acaudata Host: B. glabrata. Cercarian group: cercariaeum. Localities: Belo Horizonte, Jaboticatubas, MG. Reference: Ruiz (1952b). Cercaria amplicocecata Host: B. tenagophila. Locality: Santos, SP. Reference: Ruiz (1953). CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 459

12 Cercaria ancylina Host: Ancylus sp. (Gastropoda: Ancylidae). Locality: Niterói, RJ. Cercaria brevicorpus Host: L. columella. Locality: Paravambi, RJ. Cercaria caratinguensis Hosts: B. glabrata, B. straminea; B. tenagophila, Biomphalaria sp., Drepanotrema cimex (Moricand) (Gastropoda: Planorbidae). Localities: Belo Horizonte; Caratinga, Matozinhos, Uberlândia, MG; Florianópolis, SC; Guarulhos, Itanhaém, Louveira, Santo André, SP. References: Ruiz (1953), Machado & Abreu (1955), Milward-de-Andrade & Campos (1969), Artigas et al. (1970), Espíndola et al. (1992), Coletto et al. (1993), Souza et al. (1981), Souza et al. (1998), Carvalho et al. (2001b), Moraes et al. (2009), Eduardo et al. (2012). Cercaria cernens Host: Pomacea lineata (Spix) (Gastropoda: Ampullariidae). Cercarian group: brevifurcate. Locality: undetermined locality. Cercaria conchicola Host: Unionidae (Bivalvia). Locality: Vargem Pequena, RJ. Cercaria crassipira Host: Bivalvia. Locality: Lassance, MG. Cercaria echinostoma 1 Host: B. peregrina. Locality: Camaquã, RS. Reference: Veitenheimer-Mendes (1982). 460 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

13 Cercaria echinostoma 2 Host: B. peregrina. Locality: Camaquã, RS. Reference: Veitenheimer-Mendes (1982). Cercaria guaibensis 1 Host: B. tenagophila. Locality: Guaíba, RS. Reference: Veitenheimer-Mendes (1981). Cercaria guaibensis 2 Host: B. tenagophila. Cercarian group: xiphidiocercaria. Locality: Guaíba, RS. Reference: Veitenheimer-Mendes (1981). Cercaria guaibensis 3 Host: B. tenagophila. Locality: Guaíba, RS. Reference: Veitenheimer-Mendes (1981). Cercaria guaibensis 4 Host: B. tenagophila. Cercarian group: monostome. Locality: Guaíba, RS. Reference: Veitenheimer-Mendes (1981). Cercaria guaibensis 5 Host: Gundlachia concentrica (d'orbigny) (Gastropoda: Ancylidae) Locality: Porto Alegre, RS. Reference: Veitenheimer-Mendes et al. (1995). Cercaria guaibensis 6 Host: G. concentrica. Cercarian group: gymnocephalous. Locality: Porto Alegre, RS. Reference: Veitenheimer-Mendes et al. (1995). Cercaria guaibensis 7 Hosts: B. peregrina, B. tenagophila. Cercarian group: xiphidiocercaria. CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 461

14 Locality: Porto Alegre, RS. Reference: Veitenheimer-Mendes et al. (1995). Cercaria guaibensis 8 Host: Drepanotrema depressissimum (Moricand) (Gastropoda: Planorbidae). Cercarian group: gymnocephalous. Locality: Porto Alegre, RS. Reference: Veitenheimer-Mendes et al. (1995). Cercaria gyrinipeta Host: D. anatinum. Localities: undetermined localities, RJ and North region of Brazil. Cercaria hemiura Host: Biomphalaria sp. Cercarian group: cystophorous. Locality: Santos, SP. Reference: Ruiz (1952a). Cercaria lutzi Hosts: B. glabrata, B. tenagophila, Biomphalaria sp. Cercarian group: xiphidiocercaria. Localities: Belo Horizonte, MG; Guarulhos; Santos; São Paulo, SP. References: Ruiz (1943), Ruiz (1952a, b), Souza et al. (1998), Moraes et al. (2009). Cercaria macrogranulosa Hosts: B. glabrata, B. straminea, D. cimex, P. marmorata. Localities: Belo Horizonte, Jaboticatubas, Matozinhos, MG; Florianópolis, SC. References: Ruiz (1952b), Milward-de-Andrade & Campos (1969), Souza et al. (1981), Espíndola et al. (1992), Souza et al. (1998). Cercaria maritima Host: A. brasiliana. Cercarian group: brevifurcate. Habitat: marine. Cercaria mediohyalina Host: Ayalacostoma tuberculata Wagner (Gastropoda: Thiaridae). Locality: Lassance, MG. 462 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

15 Cercaria minense Host: B. glabrata. Cercarian group: xiphidiocercaria. Localities: Belo Horizonte, Jaboticatubas, MG. References: Ruiz (1952b), Souza et al. (1981), Souza et al. (1998). Cercaria molluscipeta Host: Biomphalaria sp. Locality: undetermined locality. Cercaria ocellifera Hosts: Biomphalaria sp., B. glabrata, B. straminea, B. tenagophila. Cercarian group: brevifurcate. Localities: Belo Horizonte, MG; Rio de Janeiro, RJ; Florianópolis, SC; Santos, Guarulhos, SP; Aracajú, SE. References: Lutz (1917, 1919), Lutz (1933), Moura (1945), Paraense (1949), Espíndola et al. (1992), Souza et al. (1981), Souza et al. (1998), Moraes et al. (2009). Cercaria phanerochorde Host: Pomacea sp. Locality: undetermined locality. Cercaria piscipeta Host: B. tenagophila. Cercaria problematica Host: P. marmorata. Locality: Lassance, MG. Cercaria retroocellata Host: A. tuberculata. Cercarian group: brevifurcate. Locality: Salto Grande, SP. Cercaria santense Host: Biomphalaria sp. CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 463

16 Cercarian group: xiphidiocercaria. Locality: Santos, SP. Reference: Ruiz (1952a). Cercaria segmentada Host: P. marmorata. Cercarian group: furcocercous. Cercaria spirochorde Hosts: D. anatinum, Biomphalaria sp. Cercaria stylites Host: Aylacostoma sp. Locality: Lassance, MG. Cercaria zygochorde Host: A. tuberculata. Locality: undetermined locality. Cercarian groups of unidentified species Amphistome Hosts: B. straminea, B. tenagophila. Localities: Goiânia, GO; Itanhaém, SP. References: Artigas et al. (1970), Komma & Alves (1979). Brevifurcate Hosts: B. glabrata, B. straminea, B. tenagophila. Localities: Belo Horizonte, Mariana, Ouro Branco, MG; localities from litoral and fist plateau, PR; Angra dos Reis, Niterói, Piraí, RJ; Miracatu, SP. References: Silva (1992), Luz et al. (1994), Carvalho et al. (2001b), Thiengo et al. (2001), Thiengo et al. (2004a), Souza et al. (2006), Pinto et al. (2012). Cystophorous Host: B. tenagophila. 464 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

17 Localities: Rio de Janeiro, RJ; Itanhaém, SP. References: Lutz (1922), Artigas et al. (1970). Echinostome Hosts: Ancylidae sp. (Gastropoda), Ayalacostoma sp., Biomphalaria sp., B. glabrata, B. peregrina, B. straminea, B. tenagophila, Drepanotrema sp.; D. anatinum, D. cimex, D. depressissimum, Drepanotrema lucidum (Pfeiffer) (Gastropoda: Planordidae), Gundlachia ticaga (Marcus & Marcus) (Gastropoda: Ancylidae), Heleobia sp., Lymnaea sp., L. columella, P. marmorata, Pomacea sp. Localities: Salvador, BA; Goiânia, GO; Lassance, Mariana, Ouro Branco, MG; Parnaíba, PI; Bocaiúva do Sul, localities from litoral and first plateau, Tunas do Paraná, PR; Angra dos Reis, Aperibé, Araruama, Barra Mansa, Cambuci, Campos, Itaguaí, Italva, Itaocara, Itaperuna, Itatiaia, Laje do Muriaé, Macaé, Maricá, Nova Friburgo, Parati, Pinheral, Piraí, Quatis, Rio de Janeiro, Santo Antônio de Pádua, São Fidélis, São Francisco de Itabapoana, São João da Barra, São Pedro da Aldeia, Trajano de Morais, Três Rios, Vassouras, RJ; Campinas, Louveira, Miracatu, Santo André, SP. References: Lutz (1922, 1924, 1933), Coutinho (1950), Komma & Alves (1979), Paraense & Araújo (1984), Machado et al. (1987, 1988), Silva (1992), Balan et al. (1993), Luz et al. (1994), Carvalho et al. (2001b), Thiengo et al. (2001), Boaventura et al. (2002), Queiroz et al. (2002), Thiengo et al. (2002a, b), Thiengo et al. (2004a, b), Souza et al. (2006), Thiengo et al. (2006) Souza & Melo (2012), Eduardo et al. (2012). Gymnocephalous Hosts: B. glabrata, B. tenagophila, D. lucidum. Localities: Louveira, SP; Mariana, Ouro Branco, MG; Cambuci, RJ. References: Machado et al. (1987), Silva (1992), Souza et al. (2006), Souza & Melo (2012), Thiengo et al. (2006). Parapleurolophocercous Hosts: Heleobia davisi Silva & Thomé (Gastropoda: Hydrobiidae); Heleobia sp. Habitat: freshwater and brackwish water. Localities: Itaperuna, Maricá, RJ; undetermined locality, RS. References: Thiengo et al. (2001), Coimbra et al. (2005), Thiengo et al. (2006). Pleurolophocercous Hosts: Heleobia parchappei (d'orbigny) (Gastropoda: Hydrobiidae), Heleobia sp. (Gastropoda: Hydrobiidae), Idiopyrgus souleyetianus Pilsbry (Gastropoda: Pomatiopsidae), Littoridina piscium (d'orbigny) (Gastropoda: Hydrobiidae), M. tuberculata. Habitat: freshwater and brackwish water. Localities: Arraial do Cabo, Guapimirim, Maricá, Miracema, Porciúncula, Rio de Janeiro, São Fidélis, São Francisco de Itabapoana, RJ; Viamão, RS. References: (Silva & Thomé (1981), Thiengo et al. (2001), Boaventura et al. (2002), Thiengo et al. (2002b, 2004b), Bogéa et al. (2005), Thiengo et al. (2006). Rhopalocercous Hosts: Ayalacostoma sp., Biomphalaria sp. Locality: undetermined locality. Reference: Lutz (1922). Strigeid Hosts: Biomphalaria sp., B. glabrata, B. peregrina, B. straminea, B. tenagophila, Drepanotrema pfeifferi (Strobel) (Gastropoda: Planorbidae), D. cimex, D. lucidum, Ferrissia sp., L. columella, P. marmorata. CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 465

18 Localities: Penedo, AL; Salvador, BA; Goiânia, GO; Mariana, Ouro Branco, MG; Belém, PA; Upper Paraná River floodplain, Bocaiúva do Sul, localities from litoral and fist plateau, Tunas do Paraná, PR; Angra dos Reis, Araruama, Barra Mansa, Campos, Duque de Caxias, Italva, Itaocara, Macaé, Niterói, Piraí, Porciúncula, Quissamã, Resende, Santa Maria Madalena, Santo Antônio de Pádua, São João da Barra, São Sebastião do Alto, Três Rios, Vassouras, RJ; Camaquã, RS; Florianópolis, SC; Campinas, Itanhaém, Louveira, Santos SP. References: Lucena (1947), Coutinho (1949, 1950), Artigas et al. (1970), Komma & Alves (1979), Veitenheimer-Mendes (1982), Paraense et al. (1984), Machado et al. (1987, 1988), Espíndola et al. (1992), Silva (1992), Balan et al. (1993), Luz et al. (1994), Thiengo et al. (2001), Boaventura et al. (2002), Dias et al. (2002), Queiroz et al. (2002), Thiengo et al. (2002a, 2002b, 2006), Souza et al. (2006), Souza & Melo (2012). Xiphidiocercaria Hosts: Ayalacostoma sp., Biomphalaria sp., B. straminea, B. tenagophila, Drepanotrema sp., D. cimex, D. depressissimum, D. kermatoides, D. lucidum, D. pfeifferi, G. ticaga, H. davisi, Lymnaea sp., L. columella, Physa sp., P. marmorata, Pomacea sp., P. lineata, Pomacea sordida (Swainson) (Gastropoda: Ampullaridae). Localities: Goiânia, GO; Jaboticatubas, Juiz de Fora, Mariana, Ouro Branco, MG; Bocaiúva do Sul, localities from litoral and first plateau, Tunas do Paraná PR; Angra dos Reis, Araruama, Arraial do Cabo, Belford Roxo, Barra Mansa, Barra do Piraí, Bom Jesus de Itabapoana, Cambuci, Campos, Cantagalo, Comendador Levy Gasparian, Conceição de Macabu, Cordeiro, Duque de Caxias, Engenheiro Paulo de Frontin, Itaboraí, Itaguaí, Italva, Itaocara, Itaperuna, Laje do Muriaé, Macaé, Maricá, Miracema, Niterói, Nova Friburgo, Parati, Piraí, Rio Claro, Rio das Ostras, Rio de Janeiro, Santo Antônio de Pádua, São Francisco de Itabapoana, São Fidélis, São João da Barra, São João de Meriti, São José de Ubá, São Sebastião do Alto, Sapucaia, Saquarema, Silva Jardim, Trajano de Morais, Três Rios, Valença, Vassouras, RJ; Camaquã, RS; Campinas, Itanhaém, Louveira, Miracatu, Piquete, Santo André, São Paulo, SP. References: Lutz (1922), Ruiz (1957), Artigas et al. (1970), Komma & Alves (1979), Ueta (1980), Veitenheimer-Mendes (1982), Melo & Pereira (1985), Machado et al. (1987, 1988), Silva (1992), Balan et al. (1993), Luz et al. (1994), Carvalho et al. (2001b, c), Thiengo et al. (2001), Boaventura et al. (2002), Medeiros et al. (2002), Queiroz et al. (2002), Thiengo et al. (2002a, b, 2004a, b, 2006), Carmo et al. (2006), Souza et al. (2006), Souza & Melo (2012), Eduardo et al. (2012). Discussion According to the bibliographic survey presented, a diversity of larval trematodes was reported in different species of molluscs in Brazil during one hundred years of parasitological studies. However, the number of trematode identified at generic or specific level (46) is relatively small, considering that more than 500 species of these flukes were reported as adult parasites in vertebrate hosts in Brazil (Travassos et al. 1969; Thatcher 1993). So, most Brazilian trematode species reported in vertebrate definitive hosts remains with the first intermediate host and larval stages unknown. Similarly, few species of molluscs (38) were evaluated for the natural infection with larval trematodes in the country, however the Brazilian malacofauna presents more than 2,600 species known (about 1,000 freshwater and terrestrial and 1,600 marine) (Rios 1994; Simone 2006). It was also verified a significant number of interactions between molluscs and trematodes in Brazil reported under provisional species names, which will remain until the elucidation of life cycles and association with adult parasites. Many of these unidentified larval species require additional studies including detailed morphological characterization and comparison to closely related species, which may reveal cospecificity with some species already known. Moreover, with few exceptions (S. mansoni, F. hepatica, E. paraensei), the Brazilian larval trematodes still require a molecular study, which may help in the identification of species in the future. Despite the diversity of species of trematodes and molluscs in Brazil, the study of biological interaction between these organisms can be considered neglected in the country. In fact, most of the malacological studies carried out in Brazil were related to molluscs transmitters of schistosomiasis. It was also verified that the distribution of the records on involvement of molluscs in the life cycle of trematodes are not uniform throughout 466 Zootaxa 3666 (4) 2013 Magnolia Press PINTO & MELO

19 the country. Most studies were developed especially in localities from the Southeastern and Southern regions of the country, where more of the main research centers and specialists in trematodes and molluscs are located. Interestingly, studies on the diversity of larval trematodes in the molluscan fauna of Amazon region, Northeast and Center-West regions of the country, as well as in potencial marine intermediate hosts remain virtually unknown. Thus, additional studies on larval trematodes in molluscs in Brazil are required and may contribute to a better understanding of aspects of parasite-host interaction, elucidation of the life cycle, taxonomy and ecology of these parasites. References Amato, S.B. & Bezerra, J.C.B. (1992) Concurrent infection of Postharmostomum gallinum (Digenea, Brachylaimidae) and Eurytrema coelomaticum (Digenea, Dicrocoeliidae) in Bradybaena similaris (Stylommatophora, Xanthonichidae). Memórias do Instituto Oswaldo Cruz, 87 (2), Araújo, M.L.R. & Rocha-Barreira, C.A. (2004) Occurrence of Bucephalus sp. (Trematoda: Bucephalidae) in Anomalocardia brasiliana (Gmelin, 1791) (Mollusca: Veneriidae) at Canto da Barra Beach, Fortim, Ceará State, Brazil. Arquivos de Ciências do Mar, 37, Artigas, P.T., Perez, M.D., Otsuko, J.M. & Nishimori, G. (1970) Levantamentos parasitológicos, em particular a esquistossomose mansônica, nas cidades de Itanhaém e Mongaguá (Litoral Sul do Estado de São Paulo). Revista de Saúde Pública, 4 (1), Balan, D.S.L., Magalhães, L.A., Piedrabuena, A.E. (1993) Aspectos imunológicos e parasitológicos em Biomphalaria tenagophila infectadas por Schistosoma mansoni e outros Digenea. Revista de Saúde Pública, 27 (6), Barbosa, F.S., Pinto, H.A. & Melo, A.L. (2011) Biomphalaria straminea (Mollusca: Planorbidae) como hospedeiro intermediário de Zygocotyle lunata (Trematoda: Zygocotylidae) no Brasil. Neotropical Helminthology, 5 (2), Bartoli, P. & Gibson, D.I. (2007) Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History, 41 (25/28), Basch, P.F. (1969) Cotylurus lutzi sp. n (Trematoda: Strigeidae) and its life cycle. Journal of Parasitology, 55 (3), Boaventura, M.F., Fernandez, M.A., Thiengo, S.C., Silva, R.E. & Melo, A.L. (2002) Formas larvais de Trematoda provenientes de gastrópodes límnicos da microrregião Rio de Janeiro, sudeste do Brasil. Lundiana, 3 (1), Bogéa, T., Cordeiro, F.M. & Gouveia, J.S. (2005) Melanoides tuberculatus (Gastropoda: Thiaridae) as intermediate host of Heterophyidae (Trematoda: Digenea) in Rio de Janeiro metropolitan area, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 47 (2), Bower, S.M., McGladdery, S.E., Price, I.M. (1994) Synopsis of infection diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases, 4, Brandolini, S.V.P.B. & Amato, S.B. (2006) Desenvolvimento larval de Paratanaisia bragai (Santos) (Digenea, Eucotylidae) sob condições experimentais. Revista Brasileira de Zoologia, 23 (4), Brandolini, S.V.P.B., Amato, S.B. & Pereira, A.A. (1997) Relacionamanto de Tanaisia bragai (Digenea Eucotylidae) e seu hospedeiro intermediario, Subulina octona (Gastropoda, Subulinidae) sob condições experimentais. Parasitología al Día, 21 (3/4), Braun, M.V. (1901) Zur revision der Trematoden der Vogel. II. Zentralblatt für Bakteriologie, 29, Bray, R.A., Gibson, D.I. & Jones, A. (Eds.) (2008) Keys to the Trematoda. Vol. 3. CAB International, Wallingford, and The Natural History Museum, London, 824 pp. Bussetti, E.T., Paske, A., Ruis, M.C.E., Tomaz, V. & Colinelli, A. (1983) Helmintos parasitos de Bubalus bubalis no Estado do Paraná. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 35 (3), Carmo, V.L.E., Lima, S.S. & Bessa, E.C.A. (2006) Morfologia e aspectos da ecologia comportamental de cercárias parasitos de Pomacea lineata (Spix, 1827) (Mollusca, Ampullariidae). Revista Brasileira de Zoociências, 8 (2), 220. Carus, J.V. (1863) Raderthiere, Wormer, Echinodermen, Coelenterated und Protozoen. In: Carus, J.V., Peters W.C.H. & Gerstacker, K.E.A. (Eds.), Handbuch der Zoologie. Vol. 2. Wilhelm Engelman, Leipzig, pp Carvalho, G.A., Andrade, C.F.S. & Ueta, M.T. (2002) Experimental infection of Aedes albopictus (Diptera: Culicidae) larvae with the xiphidiocercariae of a hematolechid. Memórias do Instituto Oswaldo Cruz, 97 (4), CERCARIAE IN MOLLUSCS FROM BRAZIL Zootaxa 3666 (4) 2013 Magnolia Press 467

20 Carvalho, G.A., Andrade, C.F.S. & Ueta, M.T. (2001a) Suscetibilidade de três espécies de mosquitos (Diptera, Culicidae) ao parasitismo por xifidiocercárias (Trematoda). Entomología y Vectores, 8 (1), Carvalho, G.A., Ueta, M.T. & Andrade, C.F.S. (2001b) Búsqueda de xifidiocercarias (Trematoda) en moluscos de agua dulce recolectados en nueve municipios del estado de São Paulo, Brasil. Boletin Chileno de Parasitología, 56 (1/2), Carvalho, G.A., Ueta, M.T. & Andrade, C.F.S. (2001c) Estudios morfométricos y biológicos de xifidiocercarias (Trematoda) provenientes de la infección natural de Lymnaea columella Say, 1817 (Basommatophora, Lymaenidae) y Biomphalaria tenagophila Orbigny, 1835 (Basommatophora, Planorbidae) recolectados en Miracatu, estado São Paulo, Brasil. Boletin Chileno de Parasitología, 56 (3/4), Cichy, A., Faltýnková, A. & Żbikowska, E. (2011) Cercariae (Trematoda, Digenea) in European freshwater snails a checklist of records from over one hundred years. Folia Malacologica, 19 (3), Cochôa, A.R. & Magalhães, A.R.M. (2008) Perdas de sementes de mexilhões Perna perna (L., 1758), cultivados na baía norte Ilha de Santa Catarina/SC. Boletim do Instituto de Pesca, 34 (1), Coelho, L.H.L. & Lima, W.S. (2003) Population dynamics of Lymnaea columella and its natural infection by Fasciola hepatica in the state of Minas Gerais, Brazil. Journal of Helminthology, 77 (1), Cohn, L (1904) Helminthologische Mitteilungen. 2. Archiv für Naturgeschichte, 70 (3), Coimbra, H.S., Schuch, L.F.D., Veitenheimer-Mendes, I.L. & Meireles, M.C.A. (2005) Neorickettsia (Ehrlichia) risticii in Southern Brazil: Heliobia spp. (Mollusca: Hydrobilidae) and parapleurolophocercous cercariae (Trematoda: Digenea) as possible vectors. Arquivos do Instituto Biológico, 72 (3), Coletto, F.A., Cambraia, D.J., Silveira, E.P. & Machado, M.I. (1993) Sobre criadouros urbanos de Biomphalaria straminea na cidade de Uberlândia, Minas Gerais. Revista do Centro de Ciências Biomédicas, Universidade Federal de Uberlândia, 9 (1), Combes, C., Albaret, J.L., Arvy, L., Bartoli, P., Bayssade-Dufour, C., Deblock, S., Durette-Desset, M.C., Gabrion, C., Jourdane, J., Lambert, A., Leger, N., Maillard, C., Matricon, M., Nassi, H., Prevot, G., Richard, J. & Theron, A. (1980) Atlas mondial des cercaires. Mémoires du Muséum National d Histoire Naturelle, Paris, Nouvelle serie, Serie A, Zoologie, 235 pp. Correa, L.R. & Paraense, W.L. (1971) Susceptibility of Biomphalaria amazonica to infection with two strains of Schistosoma mansoni. Revista do Instituto de Medicina Tropical de São Paulo, 13 (6), Coutinho, J.O. (1949) Contribuição para o estudo do hospedador intermediário do Schistosoma mansoni em Santos - São Paulo. Revista Clínica de São Paulo, 25 (1), Coutinho, J.O. (1950) Índices de infestação natural dos planorbídeos pelas cercárias do Schistosoma mansoni na cidade do Salvador Bahia. Anais da Faculdade de Medicina da Universidade de São Paulo, 25 (1), Coutinho, A.B., Gouveia, L. & Lucena, D.T. (1940) Investigação em torno da epidemiologia da esquistossomose mansonica em Pontezinha e Vitória, Estado de Pernambuco, Brasil. Memórias do Instituto Oswaldo Cruz, 35 (1), Cribb, T.H., Bray, R.A., Littlewood, D.T.J., Pichelin, S.P. & Herniou, E.A. (2001) The Digenea. In: Littlewood, D.T.J. & Bray, R.A. (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp Cribb, T.H., Bray, R.A., Olson, D.P. & Littlewood, D.T.J. (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology, 54, Dawes, B. (1946) The Trematoda, with Special Reference to British and Europeans forms. Cambridge University Press, London, reprinted with corrections 1956, reissued, 1968, 644 pp. Dias, M.L.G.G., Eiras, J.C., Machado, M.H., Souza, G.T.R. & Pavanelli, G.C. (2002) Cercariae infection in Planorbidae molluscs from the floodplain of the high Paraná river, Brazil. Arquivos do Instituto Biológico, 69 (4), Dias, M.L.G.G., Eiras, J.C., Machado, M.H., Souza, G.T.R. & Pavanelli, G.C. (2003) The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná River, Brazil. Parasitology Research, 89 (6), Diesing, C.M. (1836) Monographie der Gattungen Amphistoma und Diplodiscus. Annalen des Wiener Museums der Naturgeschichte Wien, 1, Dietz, E. (1909) Die Echinostomiden der Vogel. Zoologischer Anzeiger, 34, Dollfus, R.P. (1939) Distome d un abcès palpebro-orbitire chez une panthère. Possibilité d affinités lointaines entre ce distome et les Paragonimidae. Annales de Parasitologie Humaine et Comparée, 17, Duarte, M.J.F. (1980) O ciclo evolutivo de Postharmostomum gallinum Witenberg, 1923, no estado do Rio de Janeiro, Brasil. (Trematoda, Brachylaemidae). 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