Article.

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ZOOTAXA

ISSN 1175-5326 (print edition)

Zootaxa 3666 (4): 449–475 www.mapress.com/zootaxa/

Article

http://dx.doi.org/10.11646/zootaxa.3666.4.3

http://zoobank.org/urn:lsid:zoobank.org:pub:ADFACBA8-2190-4E91-B6B1-E1478B2485B6

A checklist of cercariae (Trematoda: Digenea) in molluscs from Brazil

HUDSON ALVES PINTO & ALAN LANE DE MELO

Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas da Univer-sidade Federal de Minas Gerais. C.P. 486, 30123-970, Belo Horizonte, Minas Gerais, Brasil.

E-mail: [email protected], [email protected]

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 mol-luscs and have not yet been associated with the respective adult parasites. Larvae found in 20 species of molmol-luscs 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

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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)

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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.

Definitive host group: birds.

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.

Habitat: freshwater.

Definitive host group: mammals. Locality: Tremembé, SP.

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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. Habitat: freshwater.

Definitive host group: birds. 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. Locality: Rio de Janeiro, RJ. Reference: Simões et al. (2008).

Cyathocotylidae Mühling, 1898

Mesostephanus odhneri (Travassos, 1924)

Hosts: Bittiolum alternatum (Say) (Gastropoda: Cerithiidae), Potamides sp. (Gastropoda: Potamididae). Cercarian group: strigeid.

Habitat: marine.

Definitive host group: birds. Locality: Rio de Janeiro, RJ.

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).

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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. Cercarian group: strigeid.

Definitive host group: birds. Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2013).

Hysteromorpha triloba (Rudolphi, 1819)

Host: B. peregrina. Cercarian group: strigeid. Habitat: freshwater.

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*. Cercarian group: echinostome.

Localities: Belo Horizonte, MG; Recife, PE. Reference: Lie & Basch (1966).

Echinostoma erraticum Lutz, 1924

Host: Drepanotrema sp. (Gastropoda: Planorbidae). Cercarian group: echinostome.

Definitive host group: birds. Locality: Rio de Janeiro, RJ. Reference: Lutz (1924).

Echinostoma exile Lutz, 1924

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Definitive host group: birds. Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2012b).

Echinostoma luisreyi Maldonado Jr, Vieira & Lanfredi, 2003

Host: P. marmorata.

Cercarian group: echinostome. Habitat: freshwater.

Definitive host group: birds. Locality: Sumidouro, RJ.

Reference: Maldonado Jr et al. (2003).

Echinostoma nephrocystis Lutz, 1924

Host: Physa sp. (Gastropoda: Physidae). Cercarian group: echinostome.

Echinostoma paraensei Lie & Basch, 1967

Hosts: B. glabrata, Lymnaea columella Say* (Gastropoda: Lymnaeidae), P. marmorata*. Cercarian group: echinostome.

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). Cercarian group: echinostome.

Echinostoma revolutum (Froelich, 1802)

Host: Physa sp.

Echinostoma rodriguesi Hsu, Lie & Basch, 1968

Hosts: P. marmorata.

Definitive host groups: birds and mammals. Locality: Belo Horizonte, MG.

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Paryphostomum segregatum Dietz, 1909

Hosts: B. glabrata, B. straminea, B. tenagophila, Biomphalaria sp. Cercarian group: echinostome.

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. Cercarian group: echinostome. Habitat: freshwater.

Locality: Matozinhos, undetermined localities, MG.

References: Milward-de-Andrade & Campos (1969), Pinto et al. (2013a).

Stephanoprora conciliata (Dietz, 1909)

Hosts: Biomphalaria sp., Drepanotrema sp. Cercarian group: echinostome.

Definitive host group: birds. 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.

Definitive host group: birds. 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.

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).

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Haematoloechidae Freitas & Lent, 1939

Haematoloechus sp.

Host: L. columella.

Cercarian group: xiphidiocercaria. Habitat: freshwater.

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. Locality: Rio de Janeiro, RJ.

Reference: Simões et al. (2010).

Centrocestus formosanus (Nishigori, 1924)

Host: Melanoides tuberculata (Müller) (Gastropoda: Thiaridae). Habitat: freshwater.

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. Locality: Rio de Janeiro, RJ. Reference: Simões et al. (2009).

Leucochloridiidae Poche, 1907

Leucochloridium flavum Travassos, 1922

Host: Omalonyx sp. (Gastropoda: Succineidae). Habitat: terrestrial.

Cercarian group: cercariaeum IM

. Definitive host group: birds.

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

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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.

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. Habitat: freshwater.

Definitive host group: birds. Locality: Belo Horizonte, MG. Reference: Pinto et al. (2013b).

Renicolidae Dollfus, 1939

Renicola sp.

Host: M. tuberculata.

Locality: Belo Horizonte, MG; Natal, RN. Reference: Pinto & Melo (2012a).

Philophthalmidae Looss, 1899

Philophthalmus gralli Mathis & Leger, 1910

Host: M. tuberculata.

Cercarian group: megalurous. Habitat: freshwater.

Definitive host group: birds. Locality: Belo Horizonte, MG. Reference: Pinto & Melo (2010b).

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Schistosomatidae Stiles & Hassall, 1898

Dendritobilharzia pulverulenta (Braun, 1901)

Definitive host group: birds. 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.

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. Habitat: freshwater.

Definitive host group: birds. Locality: Jequitibá, MG. Reference: Leite et al. (1979).

Strigeidae Railliet, 1919

Apharyngostrigea sp.

Hosts: B. peregrina, B. straminea. Cercarian group: strigeid.

Localities: Rio de Janeiro, RJ; Upper Paraná River floodplain, PR. References: Lutz (1931), Dias et al. (2002).

Australapatemon bdellocystis (Lutz, 1921)

Host: B. straminea. Cercarian group: strigeid. Habitat: freshwater.

References: Lutz (1921c, 1933), Dubois (1970).

Cotylurus lutzi Basch, 1969

Host: B. glabrata. Cercarian group: strigeid.

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Definitive host group: birds. Locality: Caetité, BA. Reference: Basch (1969).

Strigea falconis brasiliana Szidat, 1929

Host: Drepanotrema anatinum (d'Orbigny) (Gastropoda: Planorbidae). Cercarian group: strigeid.

References: Lutz (1929), Dubois (1970).

Typhlocoelidae Harrah, 1922

Typhlocoelum cucumerinum (Rudolphi, 1809)

Hosts: B. glabrata*, B. tenagophila*. Cercarian group: cercariaeum IM_.

Definitive host group: birds. Locality: Jequitibá, MG.

Reference: Schafranski et al. (1975).

Zygocotylidae Ward 1917

Zygocotyle lunata (Diesing, 1836)

Cercarian group: amphistome. Habitat: freshwater.

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. Habitat: freshwater.

Localities: Belo Horizonte, Jaboticatubas, MG. Reference: Ruiz (1952b).

Cercaria amplicocecata

Host: B. tenagophila. Cercarian group: strigeid. Habitat: freshwater. Locality: Santos, SP. Reference: Ruiz (1953).

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Cercaria ancylina

Host: Ancylus sp. (Gastropoda: Ancylidae). Cercarian group: strigeid.

Habitat: freshwater. Locality: Niterói, RJ. Reference: Lutz (1933).

Cercaria brevicorpus

Host: L. columella. Cercarian group: strigeid. Habitat: freshwater. Locality: Paravambi, RJ. Reference: Lutz (1933).

Cercaria caratinguensis

Hosts: B. glabrata, B. straminea; B. tenagophila, Biomphalaria sp., Drepanotrema cimex (Moricand) (Gastropoda: Planorbidae).

Cercarian group: strigeid. Habitat: freshwater.

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. Reference: Lutz (1933).

Cercaria conchicola

Host: Unionidae (Bivalvia). Cercarian group: strigeid. Habitat: freshwater.

Locality: Vargem Pequena, RJ. Reference: Lutz (1933).

Cercaria crassipira

Host: Bivalvia.

Cercarian group: strigeid. Habitat: freshwater. Locality: Lassance, MG. Reference: Lutz (1933).

Cercaria echinostoma 1

Host: B. peregrina.

Locality: Camaquã, RS.

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Cercaria echinostoma 2

Host: B. peregrina.

Locality: Camaquã, RS.

Reference: Veitenheimer-Mendes (1982).

Cercaria guaibensis 1

Host: B. tenagophila. Cercarian group: strigeid. Habitat: freshwater. Locality: Guaíba, RS.

Locality: Guaíba, RS.

Cercarian group: monostome. Habitat: freshwater.

Host: Gundlachia concentrica (d'Orbigny) (Gastropoda: Ancylidae) Cercarian group: strigeid.

Locality: Porto Alegre, RS.

Reference: Veitenheimer-Mendes et al. (1995).

Host: G. concentrica.

Locality: Porto Alegre, RS.

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Habitat: freshwater. Locality: Porto Alegre, RS.

Host: Drepanotrema depressissimum (Moricand) (Gastropoda: Planorbidae). Cercarian group: gymnocephalous.

Habitat: freshwater. Locality: Porto Alegre, RS.

Cercaria gyrinipeta

Host: D. anatinum. Cercarian group: strigeid. Habitat: freshwater.

Localities: undetermined localities, RJ and North region of Brazil. Reference: Lutz (1933).

Cercaria hemiura

Host: Biomphalaria sp.

Cercarian group: cystophorous. Habitat: freshwater.

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. Cercarian group: echinostome.

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.

Locality: Rio de Janeiro, RJ. Reference: Lutz (1933).

Cercaria mediohyalina

Host: Ayalacostoma tuberculata Wagner (Gastropoda: Thiaridae). Cercarian group: strigeid.

Habitat: freshwater. Locality: Lassance, MG. Reference: Lutz (1933).

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Cercaria minense

Host: B. glabrata.

Localities: Belo Horizonte, Jaboticatubas, MG.

References: Ruiz (1952b), Souza et al. (1981), Souza et al. (1998).

Cercaria molluscipeta

Host: Biomphalaria sp. Cercarian group: strigeid. Habitat: freshwater.

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. Cercarian group: strigeid. Habitat: freshwater.

Cercaria piscipeta

Host: B. tenagophila. Cercarian group: strigeid. Habitat: freshwater.

Cercaria problematica

Host: P. marmorata. Cercarian group: strigeid. Habitat: freshwater. Locality: Lassance, MG. Reference: Lutz (1933).

Cercaria retroocellata

Host: A. tuberculata.

Locality: Salto Grande, SP. Reference: Lutz (1933).

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Locality: Santos, SP. Reference: Ruiz (1952a).

Cercaria segmentada

Host: P. marmorata.

Cercarian group: furcocercous. Habitat: freshwater.

Cercaria spirochorde

Hosts: D. anatinum, Biomphalaria sp. Cercarian group: strigeid.

Cercaria stylites

Host: Aylacostoma sp.

Locality: Lassance, MG. Reference: Lutz (1933).

Cercaria zygochorde

Host: A. tuberculata. Cercarian group: strigeid. Habitat: freshwater.

Cercarian groups of unidentified species

Amphistome

Hosts: B. straminea, B. tenagophila. Habitat: freshwater.

Localities: Goiânia, GO; Itanhaém, SP.

References: Artigas et al. (1970), Komma & Alves (1979). Brevifurcate

Hosts: B. glabrata, B. straminea, B. tenagophila. Habitat: freshwater.

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

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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. Habitat: freshwater.

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. Habitat: freshwater.

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. Habitat: freshwater.

Strigeid

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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

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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.

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