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Centrocestus formosanus (Trematoda: Heterophyidae) in Melanoides tuberculata (Gastropoda: Thiaridae) from Vila do Abraão, Ilha Grande, Rio de Janeiro, Brazil

Centrocestus formosanus (Trematoda: Heterophyidae) em Melanoides tuberculata (Gastropoda, Thiaridae) da Vila do Abraão, Ilha Grande, Rio de Janeiro, Brasil

Abstract

Pleurolophocercous cercariae found in the invasive gastropod Melanoides tuberculata (Müller, 1774) collected in a stream of the Vila do Abraão, Ilha Grande, Angra dos Reis, Rio de Janeiro, Brazil were used for experimental infection that enabled the identification of the heterophyid trematode Centrocestus formosanus (Nishigori, 1924). The parasite has been found in the locality since 2007, after two years of the introduction of M. tuberculata. Recently, from a sample of 483 specimens collected in June 2013, 101 (21%) were found infected with parasite. The potential environmental impacts caused by the parasite occurrence could be underestimated in the country, and actions to monitor and control both the parasite and the mollusk are necessary.

Keywords:
pleurolophocercous cercariae; invasion ecology; exotic freshwater snails

Resumo

Cercárias do tipo pleurolofocerca encontradas no gastrópode invasor Melanoides tuberculata (Müller, 1774) coletados em um riacho da Vila do Abraão em Ilha Grande, Angra dos Reis, Rio de Janeiro, Brasil foram utilizadas em estudos de infecção experimental que possibilitaram a identificação do trematódeo heterofiídeo Centrocestus formosanus (Nishigori, 1924). O parasito vem sendo encontrado na localidade desde 2007, dois anos após a introdução do molusco. Recentemente, de uma amostra de 483 espécimes coletados em junho de 2013, 101 (21%) apresentavam-se infectados pelo parasito. Os potenciais impactos ambientais ocasionados pela ocorrência deste parasito podem estar sendo subestimados no país, sendo necessárias ações visando o monitoramento e controle tanto do parasito quanto do molusco.

Palavras-chave:
pleurolophocercous cercariae; ecologia da invasão; caramujos dulceaquícolas exóticos

1 Introduction

Melanoides tuberculata (Müller, 1774) is a limnic invasive gastropod from East Africa and South Asia (Pilsbry and Bequaert, 1927Pilsbry, H.A. and Bequaert, J., 1927. The aquatic mollusks of the Belgian Congo. With a geographical and ecological account of Congo malacology. Bulletin of the American Museum of Natural History, vol. 53, pp. 69-602.), probably introduced to Brazil by aquarium trade (Vaz et al., 1986Vaz, J.F., Teles, H.M.S., Correa, M.A. and Leite, S.P.S., 1986. Ocorrência no Brasil de Thiara (Melanoides) (Muller, 1774) (Gastropoda, Prosobranchia), primeiro hospedeiro intermediário de (Cobbold, 1875) (Trematoda, Plathyhelmintes). tuberculataClonorchis sinensisRevista de Saúde Pública, vol. 20, no. 4, pp. 318-322. http://dx.doi.org/10.1590/S0034-89101986000400008. PMid:3554478.
http://dx.doi.org/10.1590/S0034-89101986...
). To date, it has been reported from 19 states and from the Federal District (Fernandez et al., 2003Fernandez, M.A., Thiengo, S.C. and Simone, L.R.L., 2003. Distribution of the introduced freshwater snail (Gastropoda: Thiaridae) in Brazil. Melanoides tubercultatusThe Nautilus, vol. 117, no. 3, pp. 78-82.; Rocha-Miranda and Martins-Silva, 2006Rocha-Miranda, F. and Martins-Silva, M.J., 2006. First record of the invasive snail . Melanoides tuberculatus (Gastropoda: Prosobranchia: Thiaridae) in the Paranã River basin, GO, BrazilBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 66, no. 4, pp. 1109-1115. http://dx.doi.org/10.1590/S1519-69842006000600018. PMid:17299947.
http://dx.doi.org/10.1590/S1519-69842006...
; Santos et al., 2013Santos, E.G.N., Costa, V.S. and Santos, C.P., 2013. Does the trematode Centrocestus formosanus affect the locomotory activity of the mollusk Melanoides tuberculatus?Parasites & Vectors, vol. 6, no. 1, pp. 92. http://dx.doi.org/10.1186/1756-3305-6-92. PMid:24517106.
http://dx.doi.org/10.1186/1756-3305-6-92...
; Thiengo et al., 2007Thiengo, S.C., Fernandez, M.A. and Mattos, A.C., 2007. Dispersão do molusco introduzido . In: Melanoides tuberculatus (Muller, 1774) (Gastropoda; Thiaridae) no BrasilS.B. SANTOS, A.D. PIMENTA, S.C. THIENGO, M.A. FERNANDEZ and R.S. ABSALÃO. Tópicos em malacologia-Ecos do XVIII EBRAM. Rio de Janeiro: Sociedade Brasileira de Malacologia, pp. 101-106.). The species is associated with ecological problems, such as the modification of the community structure caused by the high population densities that it may reach (Santos and Eskinazi-Sant’Anna, 2010Santos, C.M. and Eskinazi-Sant’Anna, E., 2010. The introduced snail . Melanoides tuberculatus (Muller, 1774) (Mollusca: Thiaridae) in aquatic ecosystems of the Brazilian Semiarid Northeast (Piranhas-Assu River basin, State of Rio Grande do Norte)Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 70, no. 1, pp. 1-7. http://dx.doi.org/10.1590/S1519-69842010000100003. PMid:20231954.
http://dx.doi.org/10.1590/S1519-69842010...
; Santos et al., 2012Santos, S.B., Thiengo, S.C., Fernandez, M.A., Miyahira, I.C., Gonçalves, I.C.B., Ximenes, R.F., Mansur, M.C.D. and Pereira, D., 2012. Espécies de moluscos límnicos invasores no Brasil. In: M.C.D. MANSUR, C.P. SANTOS, D. PEREIRA, I.C.P. PAZ, M.L.L. ZURITA, M.T.R. RODRIGUEZ, M.V. NEHRKE and P.E.A. BERGONCI, eds. Moluscos Límnicos invasores no Brasil: biologia, prevenção, controle. Porto Alegre: Redes Editora, pp. 25-49.). Melanoides tuberculata is also the intermediate host for several parasites of medical and veterinary significance (Pinto and Melo, 2011Pinto, H.A. and Melo, A.L., 2011. A checklist of trematodes (Platyhelminthes) transmitted by (Mollusca: Thiaridae). Melanoides tuberculataZootaxa, vol. 2799, pp. 15-28.; Santos et al., 2012Santos, S.B., Thiengo, S.C., Fernandez, M.A., Miyahira, I.C., Gonçalves, I.C.B., Ximenes, R.F., Mansur, M.C.D. and Pereira, D., 2012. Espécies de moluscos límnicos invasores no Brasil. In: M.C.D. MANSUR, C.P. SANTOS, D. PEREIRA, I.C.P. PAZ, M.L.L. ZURITA, M.T.R. RODRIGUEZ, M.V. NEHRKE and P.E.A. BERGONCI, eds. Moluscos Límnicos invasores no Brasil: biologia, prevenção, controle. Porto Alegre: Redes Editora, pp. 25-49.).

Despite the expansion of M. tuberculata in Brazil for some time, the infection records of this thiarid snail with larval trematodes are relatively recent. During the last decade, the trematode transmission by this species was recorded in some localities in Brazil. Pleurolophocercous cercariae were firstly recorded in M. tuberculata in the state of Rio de Janeiro (Boaventura et al., 2002Boaventura, M.F., Fernandez, M.A., Thiengo, S.C., Silva, R.E. and Melo, A.L., 2002. Formas larvais de Trematoda provenientes de gastrópodes límnicos da microrregião Rio de Janeiro, sudeste do Brasil. Lundiana, vol. 3, no. 1, pp. 45-49.; Bogéa et al., 2005Bogéa, T., Cordeiro, F.M. and Gouveia, J.S., 2005. (Gastropoda: Thiaridae) as intermediate host of Heterophyidae (Trematoda: Digenea) in Rio de Janeiro Metropolitan area, Brazil. Melanoides tuberculatusRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 47, no. 2, pp. 87-90. http://dx.doi.org/10.1590/S0036-46652005000200005. PMid:15880219.
http://dx.doi.org/10.1590/S0036-46652005...
; Thiengo et al., 2001Thiengo, S.C., Fernandez, M.A., Boaventura, M.F.F., Grault, C.E., Silva, H.F.R., Mattos, A.M. and Santos, S.B., 2001. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil. I. Metropolitan Mesoregion. Memorias do Instituto Oswaldo Cruz, vol. 96, (suppl.), pp. 177-184. http://dx.doi.org/10.1590/S0074-02762001000900028. PMid:11586447.
http://dx.doi.org/10.1590/S0074-02762001...
) and later, similar larvae were found in Minas Gerais state, which were identified as the heterophyid trematode Centrocestus formosanus (Nishigori, 1924), for the first time in Brazil (Pinto and Melo, 2010Pinto, H.A. and Melo, A.L., 2010. (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Melanoides tuberculataRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 52, no. 4, pp. 207-210. http://dx.doi.org/10.1590/S0036-46652010000400008. PMid:21748229.
http://dx.doi.org/10.1590/S0036-46652010...
). This species was also found parasitizing M. tuberculata in the Federal District (Paula-Andrade et al., 2012Paula-Andrade, C., Pinto, H.A., Coscarelli, D., Vidigal, T.H.D.A. and Melo, A.L., 2012. The natural infection of (Müller, 1774) (Mollusca: Gastropoda) by . Melanoides tuberculataCentrocestus formosanus (Nishigori, 1924) (Platyhelminthes: Trematoda) in Paranoá lake, Brasília, BrazilBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 2, pp. 419-420. http://dx.doi.org/10.1590/S1519-69842012000200026. PMid:22735153.
http://dx.doi.org/10.1590/S1519-69842012...
) and in the states of Rio Grande do Norte (Pinto and Melo, 2012cPinto, H.A. and Melo, A.L., 2012c. Melanoides tuberculata (Mollusca: Thiaridae) harboring renicolid cercariae (Trematoda: Renicolidae) in Brazil. The Journal of Parasitology, vol. 98, no. 4, pp. 784-787. http://dx.doi.org/10.1645/GE-2937.1. PMid:22288437.
http://dx.doi.org/10.1645/GE-2937.1...
) and Rio de Janeiro (Santos et al., 2013Santos, E.G.N., Costa, V.S. and Santos, C.P., 2013. Does the trematode Centrocestus formosanus affect the locomotory activity of the mollusk Melanoides tuberculatus?Parasites & Vectors, vol. 6, no. 1, pp. 92. http://dx.doi.org/10.1186/1756-3305-6-92. PMid:24517106.
http://dx.doi.org/10.1186/1756-3305-6-92...
).

Long-time malacological studies have been conducted in a human-impacted stream in Vila do Abraão, Ilha Grande, Angra dos Reis city, state of Rio de Janeiro, Brazil (23°08’31”S, 44°10’10”W) (Figure 1), since the first record of M. tuberculata in 2005 (Braga et al., 2014Braga, R.M.R.B., Miyahira, I.C., Lacerda, L.E.M., Gonçalves, I.C.B. and Santos, S.B., 2014. The influence of an invasive gastropod on the population dynamics of Pisidium punctiferum (Sphaeriidae) in an insular impacted stream in Rio de Janeiro, Brazil. In: A.R.T. PIZA, L.F. TALLARICO, G.O. INTROÍNI and S.B. SANTOS, eds. Medical and applied malacology crossing boundaries: integrative approaches to malacology. Newcastle: Cambridge Scholars Publishing, pp. 97-114.; Santos et al., 2007Santos, S.B., Miyahira, I.C. and Lacerda, L.E.M., 2007. First record of Melanoides tuberculata (Müller, 1774) and Biomphalaria tenagophila (d’Orbigny, 1835) on Ilha Grande, Rio de Janeiro, Brazil. Biota Neotropica, vol. 7, no. 3, pp. 361-364. http://dx.doi.org/10.1590/S1676-06032007000300037.
http://dx.doi.org/10.1590/S1676-06032007...
, 2012Santos, S.B., Thiengo, S.C., Fernandez, M.A., Miyahira, I.C., Gonçalves, I.C.B., Ximenes, R.F., Mansur, M.C.D. and Pereira, D., 2012. Espécies de moluscos límnicos invasores no Brasil. In: M.C.D. MANSUR, C.P. SANTOS, D. PEREIRA, I.C.P. PAZ, M.L.L. ZURITA, M.T.R. RODRIGUEZ, M.V. NEHRKE and P.E.A. BERGONCI, eds. Moluscos Límnicos invasores no Brasil: biologia, prevenção, controle. Porto Alegre: Redes Editora, pp. 25-49.). A previous research on helminths associated to M. tuberculata, revealed that pleurolophocercous cercariae have been present in this population since 2007 (personal observations), although the taxonomic identification of the parasite was not performed so far.

Figure 1
Localization of Vila do Abraão, Ilha Grande, Angra dos Reis, RJ, Brazil where specimens of Melanoides tuberculate were found infected with Centrocestus formosanus.

2 Material and Methods

In order to obtain experimentally the respective adult trematodes required for parasite identification, specimens of M. tuberculata were collected in Vila do Abraão (INEA 18/2007 and IBAMA/Sisbio 10812-1 licenses), in June 2013. After artificial photostimulation, cercariae were detected in some specimens of M. tuberculata, of which five specimens were transported to the Laboratório de Taxonomia e Biologia de Invertebrados, Universidade Federal de Minas Gerais (LTBI, UFMG - Belo Horizonte, state of Minas Gerais), where other developmental stages of the parasite were obtained, according to Pinto and Melo (2010)Pinto, H.A. and Melo, A.L., 2010. (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Melanoides tuberculataRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 52, no. 4, pp. 207-210. http://dx.doi.org/10.1590/S0036-46652010000400008. PMid:21748229.
http://dx.doi.org/10.1590/S0036-46652010...
. Briefly, 20 specimens of laboratory-reared Poecilia reticulata Peters, 1859 were individually exposed to a solution containing undetermined number of pleurolophocercous cercariae emerged from naturally infected M. tuberculata. Metacercariae recovered from the gills of fish 30 days after infection were force-fed to mice (50 metacercariae/animal) and adult parasites were recovered from their intestines seven days later. The procedures for experimental infection and euthanasia of vertebrate hosts were performed in accordance to the ethical principles of the Comitê de Ética em Experimentação Animal (CETEA/UFMG - 199/2009).

Adult parasites and cercariae obtained were killed in hot water (70 °C), fixed in 10% formalin, stained with alum acetocarmine, dehydrated using an ascending ethanol gradient, cleared in benchwood and mounted in Canada balsam. The parasites were examined under the microscope and measures were taken with the aid of a micrometer eyepiece. The results obtained were compared to the data provided by other studies (Pinto and Melo, 2010Pinto, H.A. and Melo, A.L., 2010. (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Melanoides tuberculataRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 52, no. 4, pp. 207-210. http://dx.doi.org/10.1590/S0036-46652010000400008. PMid:21748229.
http://dx.doi.org/10.1590/S0036-46652010...
; Scholz and Salgado-Maldonado, 2000Scholz, T. and Salgado-Maldonado, G., 2000. The introduction and dispersal of . Centrocestus formosanus (Nishigori, 1924) (Diginea: Heterophyidae) in Mexico: a reviewAmerican Midland Naturalist, vol. 143, no. 1, pp. 185-200. http://dx.doi.org/10.1674/0003-0031(2000)143[0185:TIADOC]2.0.CO;2.
http://dx.doi.org/10.1674/0003-0031(2000...
), as well as to the samples from other localities in Brazil. Specimens of cercariae and adult parasite were deposited in the collection of LTBI - UFMG, under the access number DPIC 8565-8566. The morphological analyzes performed made it possible to identify the parasite.

3 Results

In the present study, 483 specimens of M. tuberculata were collected. Pleurolophocercous cercariae were detected in 101 (21%) specimens of M. tuberculata. Thus, the parasite found in Ilha Grande was identified as Centrocestus formosanus (Figure 2).

Figure 2
Centrocestus formosanus. (a) Cercariae obtained from Melanoides tuberculate collected in Ilha Grande, Brazil. (b) Gills of Poecilia reticulataexperimentally infected with metacercariae. (c) Detail of metacercariae obtained from the gills of Poecilia reticulate experimentally infected. (d) Adult parasite obtained from the intestine of laboratory infected mice. Scales: (a) 50µm; (b) 200 µm; (c) 50µm; (d) 200µm.

4 Discussion

Centrocestus formosanus is a small intestinal parasite of birds and mammals which has also been recorded in humans from Asia (Chai et al., 2013Chai, J.Y., Sohn, W.M., Yong, T.S., Eom, K.S., Min, D.Y., Lee, M.Y., Lim, H., Insisiengmay, B., Phommasack, B. and Rim, H.J., 2013. (Heterophyidae): human infections and the infection source in Lao PDR. Centrocestus formosanusThe Journal of Parasitology, vol. 99, no. 3, pp. 531-536. PMid:23116489.). The species was introduced into American continent in the 1950s (Martin, 1958Martin, W.E., 1958. The life histories of some Hawaiian heterophyid trematodes. The Journal of Parasitology, vol. 44, no. 3, pp. 305-318. http://dx.doi.org/10.2307/3274597. PMid:13550026.
http://dx.doi.org/10.2307/3274597...
) and it may be found in the USA, Mexico, Colombia, Venezuela and Brazil, nowadays (Pinto and Melo, 2011Pinto, H.A. and Melo, A.L., 2011. A checklist of trematodes (Platyhelminthes) transmitted by (Mollusca: Thiaridae). Melanoides tuberculataZootaxa, vol. 2799, pp. 15-28.). Its occurrence is very likely underestimated due the lack of studies. Centrocestus formosanus has a complex life cycle, involving a thiarid snail and fishes as intermediate hosts (Aguilar-Aguilar et al., 2009Aguilar-Aguilar, R., Martínez-Aquino, A., Pérez-Rodriguez, R. and Pérez-Ponce-De-León, G., 2009. Digenea, Heterophyidae, (Nishigori, 1924) metacercarie: distribution extension for Mexico, new state record, and geographic distribution map. Centrocestus formosanusCheck List, vol. 5, no. 2, pp. 357-359.; Scholz and Salgado-Maldonado, 2000Scholz, T. and Salgado-Maldonado, G., 2000. The introduction and dispersal of . Centrocestus formosanus (Nishigori, 1924) (Diginea: Heterophyidae) in Mexico: a reviewAmerican Midland Naturalist, vol. 143, no. 1, pp. 185-200. http://dx.doi.org/10.1674/0003-0031(2000)143[0185:TIADOC]2.0.CO;2.
http://dx.doi.org/10.1674/0003-0031(2000...
). The presence of metacercariae in gills can lead to the death of fishes, resulting in losses for fish-farming (Aguilar-Aguilar et al., 2009Aguilar-Aguilar, R., Martínez-Aquino, A., Pérez-Rodriguez, R. and Pérez-Ponce-De-León, G., 2009. Digenea, Heterophyidae, (Nishigori, 1924) metacercarie: distribution extension for Mexico, new state record, and geographic distribution map. Centrocestus formosanusCheck List, vol. 5, no. 2, pp. 357-359.; Mitchell et al., 2005Mitchell, A.J., Overstreet, R.M., Goodwin, A.E. and Brandt, T.M., 2005. Spread of an exotic fish-gill trematode: a far-reaching and complex problem. Fisheries (Bethesda, Md.), vol. 30, no. 8, pp. 11-16. http://dx.doi.org/10.1577/1548-8446(2005)30[11:SOAEFT]2.0.CO;2.
http://dx.doi.org/10.1577/1548-8446(2005...
; Ortega et al., 2009Ortega, C., Fajardo, R. and Enríquez, R., 2009. Trematode infection and distribution in ornamental fishes in Mexico. Centrocestus formosanusJournal of Aquatic Animal Health, vol. 21, no. 1, pp. 18-22. http://dx.doi.org/10.1577/H07-022.1. PMid:19485122.
http://dx.doi.org/10.1577/H07-022.1...
; Scholz and Salgado-Maldonado, 2000Scholz, T. and Salgado-Maldonado, G., 2000. The introduction and dispersal of . Centrocestus formosanus (Nishigori, 1924) (Diginea: Heterophyidae) in Mexico: a reviewAmerican Midland Naturalist, vol. 143, no. 1, pp. 185-200. http://dx.doi.org/10.1674/0003-0031(2000)143[0185:TIADOC]2.0.CO;2.
http://dx.doi.org/10.1674/0003-0031(2000...
).

In Brazil, C. formosanus was first identified in its mollusc intermediate host in 2010 (Pinto and Melo, 2010Pinto, H.A. and Melo, A.L., 2010. (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Melanoides tuberculataRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 52, no. 4, pp. 207-210. http://dx.doi.org/10.1590/S0036-46652010000400008. PMid:21748229.
http://dx.doi.org/10.1590/S0036-46652010...
), although cercariae of the same species have been recognized since 2000’s (Boaventura et al., 2002Boaventura, M.F., Fernandez, M.A., Thiengo, S.C., Silva, R.E. and Melo, A.L., 2002. Formas larvais de Trematoda provenientes de gastrópodes límnicos da microrregião Rio de Janeiro, sudeste do Brasil. Lundiana, vol. 3, no. 1, pp. 45-49.; Bógea et al., 2005Bogéa, T., Cordeiro, F.M. and Gouveia, J.S., 2005. (Gastropoda: Thiaridae) as intermediate host of Heterophyidae (Trematoda: Digenea) in Rio de Janeiro Metropolitan area, Brazil. Melanoides tuberculatusRevista do Instituto de Medicina Tropical de Sao Paulo, vol. 47, no. 2, pp. 87-90. http://dx.doi.org/10.1590/S0036-46652005000200005. PMid:15880219.
http://dx.doi.org/10.1590/S0036-46652005...
; Thiengo et al., 2001Thiengo, S.C., Fernandez, M.A., Boaventura, M.F.F., Grault, C.E., Silva, H.F.R., Mattos, A.M. and Santos, S.B., 2001. Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil. I. Metropolitan Mesoregion. Memorias do Instituto Oswaldo Cruz, vol. 96, (suppl.), pp. 177-184. http://dx.doi.org/10.1590/S0074-02762001000900028. PMid:11586447.
http://dx.doi.org/10.1590/S0074-02762001...
). Recently, the infection of some fish species by C. formosanus was discovered in the state of Minas Gerais (Pinto and Melo, 2012aPinto, H.A. and Melo, A.L., 2012a. Metacercariae of (Trematoda: Heterophyidae) in (Pisces: Cichlidae) in Brazil. Centrocestus formosanusAustraloheros facetusRevista Brasileira de Parasitologia Veterinária, vol. 21, no. 3, pp. 334-337. http://dx.doi.org/10.1590/S1984-29612012000300032. PMid:23070454.
http://dx.doi.org/10.1590/S1984-29612012...
, bPinto, H.A. and Melo, A.L., 2012b. Infecção natural de (Actinopterygii: Poeciliidae) por metacercárias na Represa da Pampulha, Belo Horizonte, Minas Gerais, Brasil. Poecilia reticulataBoletim do Instituto de Pesca, vol. 38, no. 3, pp. 257-264.; Pinto et al., 2014Pinto, H.A., Mati, V.L.T. and Melo, A.L., 2014. Metacercarial Infection of wild Nile tilapia (Oreochromis niloticus) from Brazil. The Scientific World Journal, vol. 2014, pp. 1-7. http://dx.doi.org/10.1155/2014/807492. PMid:25485302.
http://dx.doi.org/10.1155/2014/807492...
). Moreover, there is only one conclusive record of a bird, Butorides striata (L.), harboring this heterophyid in Brazil, (Pinto et al., 2013Pinto, H.A., Mati, V.L.T. and Melo, A.L., 2013. New records and a checklist of trematodes from (Aves: Ardeidae). Butorides striataRevista Mexicana de Biodiversidad, vol. 84, no. 4, pp. 1100-1110. http://dx.doi.org/10.7550/rmb.34431.
http://dx.doi.org/10.7550/rmb.34431...
). However, given the known non-specificity host for the parasite, it probably also occurs in other waterfowl species.

The first record for M. tuberculata in Ilha Grande dates to 2005 and its infection with pleurolophocercous cercariae, here identified as C. formosanus, was first detected in 2007, indicating a relative short time between the introduction of the intermediate host and its involvement in the transmission of parasites. Other factors concerning the introduction and dispersion of this parasite to previously unaffected areas are still unknown. However, it may be introduced by infected molluscs or fishes; it is more likely that the movement of birds between places with established populations of mollusc hosts is the main form of introduction. Due to the diversity of fishes and birds occurring on Ilha Grande (Alves and Vecchi, 2009Alves, M.A.S. and VECCHI, M.B., 2009. Birds, Ilha Grande, state of Rio de Janeiro, Southeastern Brazil. Check List, vol. 5, no. 2, pp. 300-303.; INEA, 2013INSTITUTO ESTADUAL DO AMBIENTE – INEA, 2013. Parque Estadual da Ilha Grande: plano de manejo (fase 2). Rio de Janeiro: Instituto Estadual do Ambiente.; Rocha et al., 2009Rocha, C.F., Bergallo, H.G., Alves, M.A.S., Van Sluys, M., Mazzoni, R. and Santos, S.B., 2009. Fauna de ambientes interiores. In: M. BASTOS and C.H. CALLADO, eds. O ambiente da Ilha Grande. Rio de Janeiro: Universidade do Estado do Rio de Janeiro, pp. 163-245.), it is likely that the life cycle of C. formosanus is established in Vila do Abraão stream.

Actions to prevent the dispersal of molluscs and parasites are important to control negative effects on the native fauna, as well as to limit the occurrence of future cases of centrocestiasis and other parasite diseases transmitted by M. tuberculata.

Acknowledgements

To Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for research grants to SBS (APQ1 110.430/2007; 410.402/2010; 110.362/2012 e 111.573/2013); Coordenação de Aperfeiçoamento do Pessoal de Ensino Superior (CAPES) for Master scholarships to RFX and ICBG; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Protax 562291/2010-5) for Doctoral scholarship to ICM; Centro de Estudos Ambientais e Desenvolvimento Sustentável (Ceads) for logistic support; Instituto Estadual do Ambiente (INEA) for license 18/2007; IBAMA/Sisbio for license 10812-1 to SBS and Dagmar Frisch of the University of Oklahoma Biological Station for the first review of the English language and Adriena Casini da Silva (Universidade Federal do Rio de Janeiro) for the second review of this paper.

  • (With 2 figures)

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Publication Dates

  • Publication in this collection
    05 Sept 2016
  • Date of issue
    Apr-Jun 2017

History

  • Received
    02 Sept 2015
  • Accepted
    30 Dec 2015
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