Spatial distribution of Lymnaeidae (Mollusca, Basommatophora), intermediate host of Fasciola hepatica Linnaeus, 1758 (Trematoda, Digenea) in Brazil.

Snails of the family Lymnaeidae act as intermediate hosts in the biological cycle of Fasciola hepatica, which is a biological agent of fasciolosis, a parasitic disease of medical importance for humans and animals. The present work aimed to update and map the spatial distribution of the intermediate host snails of F. hepatica in Brazil. Data on the distribution of lymnaeids species were compiled from the Collection of Medical Malacology (Fiocruz-CMM, CPqRR), Collection of Malacology (MZUSP), "SpeciesLink" (CRIA) network and through systematic surveys in the literature. Our maps of the distribution of lymnaeids show that Pseudosuccinea columella is the most common species and it is widespread in the South and Southeast with few records in the Midwest, North and Northeast regions. The distribution of the Galba viatrix, G. cubensis and G. truncatula showed a few records in the South and Southeast regions, they were not reported for the Midwest, North and Northeast. In addition, in the South region there are a few records for G. viatrix and one occurrence of Lymnaea rupestris. Our findings resulted in the first map of the spatial distribution of Lymnaeidae species in Brazil which might be useful to better understand the fasciolosis distribution and delineate priority areas for control interventions.

INTRODUCTION

Snails of the family Lymnaeidae are small Basommatophora hermaphrodites, approximately 10 mm long and 6 mm wide. The lymnaeids species is widely distributed around the tropical and subtropical areas of the Americas, Europe, Asia, Africa, and Oceania[36] and inhabits natural (streams, ponds, swamps) or artificial (irrigation ditches, small dams, floodplain) types of water collections[23].

The importance of the lymnaeids is due to the fact that they act as intermediate hosts in the biological cycle of the digenetic trematode Fasciola hepatica Linnaeus, 1758 (Trematoda, Digenea), biological agent of fasciolosis, which is a parasitic disease of medical importance for both humans and animals.

Based on an increasing number of human cases since 1980, MAS-COMA et al. [50] proposed that fasciolosis should be considered an important parasitic human disease rather than just a secondary zoonotic disease with an estimated number of infected people of more than 2.4 million people worldwide[108]. The economic losses caused by this disease include a significant impact on the livestock industry due to the high costs for therapeutic treatments in cattle, goat, and sheep breeding[24,29,43,49,83]. SMOOKER et al. [84] calculated a global cost of more than two billion dollars a year because of the infection.

In Brazil, the lymnaeids species already recorded are: Pseudosuccinea columella (Say, 1817), Galba viatrix d'Orbigny, 1835, Galba truncatula (Müeller, 1774), Galba cubensis Pfeiffer, 1839 and Lymnaea rupestris Paraense, 1982. Except for L. rupestris, the other species have proved to be susceptible to infection by F. hepatica. Regarding the identification of lymnaeids species, their systematics is confused and there are a lot of difficulties in identifying some species using only morphological characters[28,77], so molecular markers are frequently necessary. Here, we used the taxonomy proposed by BAKER[13] for the species P. columella.

The present work aimed to update and map the spatial distribution of the intermediate host snails of F. hepatica in Brazil.

MATERIAL AND METHODS

Data on the distribution of lymnaeids species were obtained from: i) Collection of Medical Malacology (Fiocruz-CMM) of the Laboratory of Medical Helminthology and Malacology, René Rachou Research Center (Fiocruz/MG); ii) Collection of Malacology of the Museum of Zoology of University of São Paulo (MZUSP); iii) “SpeciesLink” (CRIA) network (http://www.splink.org.br/), by using the keyword Lymnaeidae in the database search; iv) systematic surveys in scientific articles, gray literature, dissertations, theses, and communications, by using the combined keywords: Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + occurrence + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + distribution + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + record + Brazil; Lymnaea/Galba/Pseudosuccinea/Lymnaeidae + collection + Brazil; Fasciola + occurrence + Brazil; Fasciola + distribution + Brazil; Fasciola + record + Brazil; Fasciolosis + occurrence + Brazil; Fasciolosis + distribution + Brazil and Fasciolosis + record + Brazil. According to the type of database (or sites), terms were used in English or Portuguese: Google scholar, Web of Knowledge, Scielo, PubMed, Periódicos Capes (Capes Journals) and Banco Digital de Teses e Dissertações (Theses and Dissertations Digital Database). The data collected had information relative to the occurrence of lymnaeids per state and municipalities of Brazilian regions and if the snails were found naturally infected by F. hepatica.

In the majority of the data used, the identification of the lymnaeids species was made using only morphological characters except when the data are from Fiocruz-CMM, where molecular markers were utilized to confirm the morphological identification. The molecular technique used was the polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP) targeted to the first and second internal transcribed spacers (ITS1 and ITS2) rDNA and to the mitochondrial 16S ribosomal gene (16S rDNAmt)[19,22].

Data management, visualization and mapping were carried out in ArcGIS version 9.3 (ESRI; Redlands, CA, USA).

RESULTS

Reports on five species of Lymnaeidae were found in Brazil. Tables 1 and 2 summarize the distribution per locality of species in the five regions of Brazil (Fig. 1 and 2), South (Fig. 3), Southeast (Fig. 4), Midwest, North and Northeast regions (Fig. 5). In the “SpeciesLink” (CRIA) network, we found data relative to four collections: Collection of Molluscs of Museum of Science and Technology, PUCRS; Collection of Molluscs of National Institute of Research of Amazônia, INPA; Malacological Collection of Biological Science Department, DCBio/UFES and Collection of Malacology of Oswaldo Cruz Institute, Fiocruz-CMIOC. The information about the localities where the specimens occurred was not available from the Collection of Malacology of Oswaldo Cruz Institute, Fiocruz-CMIOC, because of this, we did not add these data to our results. The data from the Collection of Medical Malacology, Fiocruz-CMM, were already available to us.

Table 1

Distribution of Pseudosuccinea columella per municipalities and regions of Brazil

Regions/States	Localities	Geographic coordinates	Species	Articles/“SpeciesLink” (CRIA) network
1) South
Rio Grande do Sul	Agudo	29s38/53w15	P. columella	1
	Arroio Grande	32s14/53w05	P. columella	2
	Cachoeira do Sul	30s02/52w53	P. columella	4
	Camaquã	30s51/51w48	P. columella +	4; 5; 6
	Candiota	31s35/53w43	P. columella	MCP-Moluscos
	Capão do Leão	31s46/52w30	P. columella	4; 2
	Dom Pedrito	30s58/54w40	P. columella +	4
	Eldorado do Sul	29s50/51w18	P. columella	81
	Gramado	29s23/50w52	P. columella	Fiocruz-CMM
	Guaíba	30s06/51w19	P. columella	4
	Morro Reuter	29s32/51w04	P. columella	4
	Nova Petrópolis	29s20/51w10	P. columella	4
	Pelotas	31s46/52w20	P. columella	8; 9; Fiocruz-CMM
	Porto Alegre	30s01/51w13	P. columella	11; 4
	Rosário do Sul	30s15/54w55	P. columella +	12
	Santa Maria	29s41/53w48	P. columella	13
	Santa Vitória do Palmar	33s31/53w22	P. columella	4
	Santo Antônio da Patrulha	29s49/50w30	P. columella	84
	São Borja	28s39/55w59	P. columella	15
	São Leopoldo	29s45/51w08	P. columella	MZUSP
	São Martinho da Serra	29s32/53w51	P. columella	13
	Sapucaia do Sul	29s49/51w09	P. columella +	12
	Reserva ecológica do Taim	32s29/52w35	P. columella	4
	Rio Pardo	29s99/52w35	P. columella	MCP-Moluscos
	Taquara	29s38/50w46	P. columella	4; 87
	Tramandaí	29s59/50w07	P. columella	4
	Triunfo	29s56/51w43	P. columella	16; Fiocruz-CMM
	Viamão	30s04/51w01	P. columella	4
Santa Catarina	Araranguá	28s56/49w28	P. columella	4
	Biguaçu	27s29/48w39	P. columella	18; 19; 20
	Blumenau	26s54/49w04	P. columella	18; 19; 20
	Brusque	27s05/48w55	P. columella	18; 19; 20
	Camboriú	27s01/48w39	P. columella	18; 19; 20
	Criciúma	28s41/49w22	P. columella	18; 19; 20
	Florianópolis	27s35/48w33	P. columella	4; 17; 18; 19; 20
	Itá	27s29/52w32	P. columella	MCP-Moluscos
	Joinville	26s17/48w50	P. columella	4
	Lages	27s48/50w19	P. columella	4
	Lauro Müller	28s23/49w24	P. columella	MZUSP
	Nova Trento	27s17/48w55	P. columella	18; 19; 20
	Palhoça	27s38/48w40	P. columella	18; 19; 20
	São João do Sul	29s13/49w48	P. columella	18; 19; 20
	Seara	27s12/52w19	P. columella	4; 24
				Fiocruz-CMM
Santa Catarina	Tubarão	28s28/49w00	P. columella	18; 19; 20
	Urubici	28s00/49w35	P. columella	25
Paraná	Antonina	25s42/48w71	P. columella	91
	Balsa Nova	25s58/49w63	P. columella	91
	Bocaiúva do Sul	25s12/49w06	P. columella	26; 91
	Cambará	23s02/50w04	P. columella	Fiocruz-CMM
	Campina Grande do Sul	25s30/49w05	P. columella	91
	Campo Largo	25s45/49w53	P. columella	91
	Contenda	25s67/49w52	P. columella	91
	Curitiba	25s25/49w16	P. columella	27; 4; 28; 24; 87; 52; 91; Fiocruz-CMM
				MZUSP
	Dionísio Cerqueira (Barracão)	26s15/53w38	P. columella	4
	Morretes	25s28/48w49	P. columella	4; 91
	Paranaguá	25s30/48w30	P. columella	MZUSP
	Quatro Barras	25s36/49w07	P. columella	91
	Rio Branco do Sul	25s19/49w31	P. columella	91
	São José dos Pinhais	25s32/49w12	P. columella	87; 91
	Tunas do Paraná	24s58/49w05	P. columella	26; MZUSP
2) Southeast
São Paulo	Águas de Santa Bárbara	22s52/49w14	P. columella	29
	Altinópolis	21s04/47w22	P. columella	30
	Álvares Machado	22s04/51w28	P. columella	31
	Americana	22s44/47w19	P. columella	80
	Américo Brasiliense	21s43/48w06	P. columella	30
	Angatuba	23s29/48w24	P. columella	29
	Anhembi	22s47/48w07	P. columella	29
	Araçoiaba da Serra	23s30/47w36	P. columella	29
	Aramina	20s05/47w47	P. columella	30
	Arandu	23s08/49w03	P. columella	29
	Araraquara	21s47/48w10	P. columella	30
	Areiópolis	22s40/48w39	P. columella	29
	Atibaia	23s69/46w33	P. columella	80
	Avanhandava	21s27/49w56	P. columella	MZUSP
	Avaré	21s54/49w21	P. columella	29
	Barão de Antonina	23s37/49w33	P. columella	29
	Barra Bonita	22s29/48w33	P. columella	33
	Barretos	20s33/48w34	P. columella	30
	Batatais	20s53/47w35	P. columella	30
	Bebedouro	20s56/48w28	P. columella	30
	Boa Esperança do Sul	21s59/48w23	P. columella	30
	Bofete	23s05/48w15	P. columella	29
	Boituva	23s17/47w40	P. columella	29
	Borborema	21s37/49w04	P. columella	30
	Botucatu	22s53/48w26	P. columella	29
São Paulo	Brodowski	20s59/47w39	P. columella	30
	Brotas	22s17/48w07	P. columella	MZUSP
	Buri	23s47/48w35	P. columella	29
	Cabreúva	23s18/47w07	P. columella	29
	Caçapava	23s05/45w42	P. columella	4; 80
	Caiuá	21s49/51w59	P. columella	31
	Cajurú	21s16/47w18	P. columella	30
	Campinas	22s53/47w05	P. columella	34; 4; 35; 36; 80
	Cândido Rodrigues	21s19/48w37	P. columella	30
	Capão Bonito	24s00/48w20	P. columella	29
	Capela do Alto	23s27/47w44	P. columella	29
	Caraguatatuba	23s27/45w24	P. columella	MZUSP
	Cássia dos Coqueiros	21s16/47w10	P. columella	30
	Catiguá	21s03/49w03	P. columella	37
	Cerqueira Cesar	23s01/49w09	P. columella	29
	Cerquilho	23s09/47w44	P. columella	29
	Cesário Lange	23s13/47w57	P. columella	29
	Colina	20s43/48w32	P. columella	30
	Colômbia	20s10/48w41	P. columella	30
	Conchas	23s01/48w00	P. columella	29
	Coronel Macedo	23s38/49w18	P. columella	29
	Cravinhos	21s20/47w43	P. columella	30
	Cristais Paulista	20s23/47w25	P. columella	30
	Descalvado	21s54/47w37	P. columella	30
	Dourado	22s06/48w18	P. columella	30
	Eldorado	24s30/48w05	P. columella +	41
	Estrela do Norte	22s29/51w39	P. columella	31
	Fernando Prestes	21s15/48w41	P. columella	30
	Franca	20s31/47w23	P. columella	30
	Guaíra	20s19/48w19	P. columella	30
	Guapiaçú	20s47/49w13	P. columella	37
	Guapiara	24s10/48w32	P. columella	29
	Guará	20s25/47w49	P. columella	30
	Guaraci	20s29/48w56	P. columella	37
	Guareí	23s22/48w10	P. columella	29
	Guarujá	23s58/46w15	P. columella	MZUSP
	Ibaté	21s57/47w59	P. columella	30
	Ibirá	21s04/49w14	P. columella	37
	Ibitinga	21s45/48w49	P. columella	30
	Ibiúna	23s38/47w13	P. columella	29
	Iepê	22s38/51w06	P. columella	31
	Igarapava	20s02/47w44	P. columella	30; Fiocruz-CMM
	Indiana	22s08/51w15	P. columella	31
	Iperó	23s21/47w42	P. columella	29
São Paulo	Irapuã	21s17/49w24	P. columella	37
	Itaberá	23s51/49208	P. columella	29
	Itaí	23s24/49w05	P. columella	29
	Itapetininga	23s36/48w03	P. columella	29
	Itapeva	23s58/48w52	P. columella	29
	Itápolis	21s35/48w48	P. columella	30
	Itaporanga	23s42/48w29	P. columella	29
	Itararé	24s06/49w20	P. columella	29
	Itariri	24s17/47w03	P. columella	4; 32
	Itatinga	23s06/48w36	P. columella	29
	Itu	23s15/47w17	P. columella	29
	Itupeva	23s08/47w04	P. columella	MZUSP
	Ituverava	20s20/47w47	P. columella	30
	Jaboticabal	21s15/48w18	P. columella	30
	Jaguariúna	22s42/46w59	P. columella	36
	Jardinópolis	21s01/47w45	P. columella	30
	João Ramalho	22s15/50w46	P. columella	31
	Junqueirópolis	21s31/51w26	P. columella	31
	Louveira	23s05/46w58	P. columella	36
	Luis Antônio	21s33/47w42	P. columella	30
	Mairinque	23s32/47w11	P. columella	29
	Marinópolis	20s26/50w49	P. columella	37
	Martinópolis	22s08/51w10	P. columella	31
	Matão	21s36/48w21	P. columella	30
	Miguelópolis	20s10/48w01	P. columella	30
	Miracatu	24s16/47w27	P. columella +	36; 41
	Monte Alto	21s15/48w29	P. columella	30
	Monte Aprazível	20s45/49w42	P. columella	37
	Monte Azul Paulista	20s54/48w38	P. columella	30
	Morro Agudo	20s43/48w03	P. columella	30
	Narandiba	22s24/51w31	P. columella	31
	Nova Europa	21s46/48w33	P. columella	30
	Nova Granada	20s31/49w18	P. columella	37
	Novo Horizonte	21s28/49w13	P. columella	37
	Olímpia	20s44/48w54	P. columella	37
	Orlândia	20s43/47w53	P. columella	30
	Oswaldo Cruz	23s37/46w34	P. columella	31
	Palestina	20s21/49w25	P. columella	37
	Palmital	22s46/50w12	P. columella	Fiocruz-CMM
	Panorama	21s20/51w51	P. columella	31
	Paraíso	20s59/48w46	P. columella	37
	Paranapanema	23s23/48w43	P. columella	29
	Parapuã	21s46/50w47	P. columella	31
	Pardinho	23s04/48w22	P. columella	29
São Paulo	Patrocínio Paulista	20s37/47w16	P. columella	30
	Pedregulho	20s14/47w28	P. columella	30
	Pereiras	23s04/47w58	P. columella	29
	Piedade	23s41/47w25	P. columella	29
	Pilar do Sul	23s48/47w43	P. columella	29
	Piquerobi	21s52/51w43	P. columella	31
	Piquete	22s36/45w10	P. columella +	38; 39; 75; MZUSP
	Piracicaba	22s43/47w39	P. columella	36
	Pirangi	21s09/48w39	P. columella	30
	Pirassununga	21s59/47w25	P. columella	4; 36; 80
	Pitangueiras	20s59/48w12	P. columella	30
	Planalto	21s21/49w55	P. columella	37
	Pontal	20s59/48w02	P. columella	30
	Porangaba	20s54/47w53	P. columella	29
	Porto Feliz	23s12/47w31	P. columella	29
	Pradópolis	21s21/48w03	P. columella	30
	Presidente Bernardes	22s00/51w33	P. columella	31
	Rancharia	22s13/50w53	P. columella	31
	Redenção da Serra	23s13/45w32	P. columella	38
	Regente Feijó	22s13/51w18	P. columella	31
	Registro	24s29/47w51	P. columella	36
	Restinga	20s34/47w29	P. columella	30
	Ribeirão Bonito	20s02/48w10	P. columella	30
	Ribeirão Branco	24s11/48w46	P. columella	29
	Ribeirão Preto	21s10/47w48	P. columella	4; 30; MZUSP
	Rincão	21s34/48w04	P. columella	30
	Rinópolis	21s43/50w43	P. columella	31
	Rio Claro	22s23/47w33	P. columella	4
	Riversul	23s48/49w24	P. columella	29
	Rubinéia	20s10/50w59	P. columella	37
	Sales	21s20/49w30	P. columella	37
	Sales Oliveira	20s46/47w56	P. columella	30
	Salesópolis	23s31/45w50	P. columella	78; MZUSP
	Salto	23s11/47w17	P. columella	29
	Salto de Pirapora	23s38/47w34	P. columella	29
	Sandovalina	22s26/51w46	P. columella	31
	Santa Adélia	21s14/48w47	P. columella	37
	Santa Mercedes	21s20/51w45	P. columella	31
	Santa Rita do Passa Quatro	21s42/47w28	P. columella	30
	Santa Rosa do Viterbo	21s28/47w21	P. columella	30
	Santo Anastácio	21s57/51w38	P. columella	31
	Santo Expedito	21s50/51w23	P. columella	31
	São Carlos	21s59/47w53	P. columella	30
	São Joaquim da Barra	20s34/47w52	P. columella	30
São Paulo	São José do Rio Preto	20s40/49w17	P. columella	37
	São José dos Campos	23s11/45w52	P. columella	4
	São Manoel	22s43/47w18	P. columella	29
	São Miguel Arcanjo	23s52/47w59	P. columella	29
	São Paulo	23s32/46w38	P. columella	4; MZUSP
	São Roque	23s31/47w08	P. columella	29
	São Simão	21s28/47w33	P. columella	30
	São Vicente	23s57/46w22	P. columella	MZUSP
	Sarapuí	23s37/47w49	P. columella	29
	Serrana	21s12/47w36	P. columella	30
	Sertãozinho	21s06/47w59	P. columella	30
	Sorocaba	23s28/47w25	P. columella	29
	Tabatinga	21s42/48w40	P. columella	30
	Taiaçu	21s08/48w30	P. columella	30
	Taiuva	21s06/48w26	P. columella	30
	Tapuaí	21s54/49w21	P. columella	29
	Taquaritinga	21s24/48w29	P. columella	30
	Taquarituba	23s31/49w14	P. columella	29
	Tarabaí	22s17/51w33	P. columella	31
	Tatuí	23s21/47w50	P. columella	29
	Taubaté	23s00/45w33	P. columella	4; 80
	Terra Roxa	20s46/48w19	P. columella	30
	Tietê	23s05/47w42	P. columella	29
	Urupês	21s08/49w15	P. columella	37
	Vista Alegre do Alto	21s09/48w38	P. columella	30
	Votorantim	23s32/47w26	P. columella	29
Rio de Janeiro	Angra dos Reis	23s00/44w19	P. columella	42
	Aperibé	21s37/42w06	P. columella	43
	Araruama	22s50/42w20	P. columella	44
	Areal	22s13/43w06	P. columella	45
	Barra do Piraí	22s27/43w48	P. columella	42
	Barra Mansa	22s32/44w10	P. columella	42
	Bom Jardim	22s09/42w25	P. columella	45
	Bom Jesus de Itabapoana	21s07/41w40	P. columella	43
	Cachoeiras de Macacu	22s31/42w42	P. columella +	46; 76
	Cambuci	21s33/41w54	P. columella	43
	Campos dos Goytacazes	21s45/41w20	P. columella +	47; 48; 49
	Cantagalo	21s58/42w22	P. columella	45
	Cardoso Moreira	21s38/41w45	P. columella	49
	Carmo	21s54/42w36	P. columella	45
	Casimiro de Abreu	22s27/42w12	P. columella	44
	Comendador Levy Gasparian	22s00/43w12	P. columella	45
	Conceição de Macabu	22s03/41w51	P. columella	49
	Cordeiro	22s00/42w21	P. columella	45
Rio de Janeiro	Duas Barras	22s02/42w31	P. columella	45
	Engenheiro Paulo de Frontin	22s33/43w41	P. columella	46
	Guapimirim	22s29/42w59	P. columella	50
	Itaboraí	22s43/42w51	P. columella	46
	Itaguaí	22s51/43w46	P. columella +	46; 51; 85
	Italva	21s27/41w40	P. columella	43
	Itaocara	21s38/42w04	P. columella	43
	Itaperuna	21s10/41w53	P. columella	43
	Itatiaia	22s25/44w33	P. columella	42
	Japeri	22s38/43w39	P. columella	46
	Laje do Muriaé	21s11/42w07	P. columella	43
	Macaé	22s21/41w46	P. columella	49
	Magé	22s38/43w02	P. columella	50; 51
	Mangaratiba	22s56/44w02	P. columella	46
	Maricá	22s54/42w49	P. columella	46
	Mendes	22s31/43w44	P. columella	46
	Miguel Pereira	22s26/43w28	P. columella	46
	Miracema	21s22/42w12	P. columella	43
	Natividade	21s01/41w58	P. columella	43
	Niterói	22s52/43w07	P. columella	46; 53
	Nova Friburgo	22s15/42w31	P. columella	45
	Nova Iguaçu	22s44/43w27	P. columella	46
	Paracambi	22s29/43w41	P. columella	46
	Paraíba do Sul	22s08/43w16	P. columella	45
	Parati	23s10/44w43	P. columella	42
	Paty dos Alferes	22s25/43w25	P. columella	46
	Petrópolis	22s21/43w08	P. columella	50
	Pinheiral	22s31/44w00	P. columella	42
	Piraí	22s30/44w00	P. columella	42
	Porciúncula	20s57/42w02	P. columella	43
	Quatis	22s40/44w27	P. columella	42
	Resende	22s27/44w26	P. columella	42
	Rio Bonito	22s40/42w37	P. columella	46
	Rio Claro	22s72/44w13	P. columella	42
	Rio das Flores	22s15/43w58	P. columella	42
	Rio das Ostras	22s29/42w59	P. columella	44
	Rio de Janeiro	22s53/43w12	P. columella	4; 46; 54; 86
	Santa Maria Madalena	21s97/41w99	P. columella	45
	Santo Antônio de Pádua	21s53/42w18	P. columella	43
	São Fidélis	21s37/41w44	P. columella	49
	São Gonçalo	22s83/43w05	P. columella	46; 51
	São João de Meriti	22s80/43w37	P. columella	46
	São José de Ubá	21s36/41w93	P. columella	43
	São José do Vale do Rio Preto	22s08/42w55	P. columella	50
Rio de Janeiro	São Sebastião do Alto	21s95/42w14	P. columella	45
	Sapucaia	21s99/42w90	P. columella	45
	Saquarema	22s93/42w49	P. columella	44
	Seropédica	22s51/43w45	P. columella	56; 89; Fiocruz-CMM
	Silva Jardim	22s37/42w23	P. columella	44
	Sumidouro	22s04/42w67	P. columella	45
	Tamoios	22s72/42w01	P. columella	44
	Teresópolis	22s23/42w58	P. columella	50
	Trajano de Morais	22s07/42w06	P. columella	45
	Três Rios	22s05/43w12	P. columella	4; 45
	Valença	22s24/43w70	P. columella	42
	Varre-Sai	20s93/41w87	P. columella	43
	Vassouras	22s40/43w66	P. columella	11; 46
	Volta Redonda	22s52/44w10	P. columella	42
Minas Gerais	Alfenas	21s25/45w56	P. columella	Fiocruz-CMM
	Barbacena	21s13/43w46	P. columella	4
	Belo Horizonte	19s55/43w56	P. columella	11; 4; 58; 59; 23; 24
				Fiocruz-CMM
				INPA-Mollusca
	Betim	19s58/44w04	P. columella	4; 59; 61
				Fiocruz-CMM
	Bicas	21s43/43w04	P. columella	61
	Brasópolis	22s27/45w36	P. columella	61
	Cachoeira de Minas	22s20/45w46	P. columella	61
	Careaçu	22s02/45w41	P. columella	61
	Diamantina	18s13/43w35	P. columella	4
	Ferros	19s12/43w01	P. columella	4
	Igarapé	20s04/44w18	P. columella	61
	Itabirito	20s14/43w47	P. columella	61
	Itajubá	22s25/45w28	P. columella +	9; 61; 62; 24; 8
				Fiocruz-CMM
	Jaboticatubas	19s30/43w44	P. columella	8; 63; Fiocruz-CMM
	Januária	15s26/44w21	P. columella	64
	Juiz de Fora	21s45/43w20	P. columella	4; 65; 61; 83
				Fiocruz-CMM
	Lagoa Santa	19s37/43w53	P. columella	59
	Machado	21s39/45w55	P. columella	Fiocruz-CMM
	Mariana	20s21/43w25	P. columella	66
	Nova Lima	19s58/43w50	P. columella	59
	Ouro Fino	22s16/46w22	P. columella	4
	Passos	20s42/46w36	P. columella	MZUSP
	Pedro Leopoldo	19s36/44w02	P. columella	59
	Perdões	21s09/45w08	P. columella	Fiocruz-CMM
	Piranguinho	22s23/45w32	P. columella	61
	Raposos	19s57/43w48	P. columella	Fiocruz-CMM
Minas Gerais	Ribeirão das Neves	19s45/44w04	P. columella	59
	Rio Acima	20s03/43w47	P. columella	Fiocruz-CMM
	Rio Doce	20s14/42w53	P. columella	8
	Sabinópolis	18s39/43w04	P. columella	4
	Santa Luzia	19s44/43w53	P. columella	59
	Santa Rita do Sapucaí	22s14/45w43	P. columella	61
	São Gonçalo do Sapucaí	22s19/46w19	P. columella	11; 61
	Sete Lagoas	19s26/44w14	P. columella	11
	Timóteo	19s34/42w38	P. columella	Fiocruz-CMM
	Três Pontas	21s21/45w30	P. columella	24; Fiocruz-CMM
	Ubá	21s07/42w56	P. columella	4
	Varginha	21s33/45w26	P. columella	61
	Vespasiano	19s41/43w55	P. columella	59
	Viçosa	20s45/42w52	P. columella	11; 4
Espírito Santo	Alegre	20s45/41w31	P. columella	68
	Atílio Vivacqua	20s53/41w11	P. columella	68
	Cachoeiro do Itapemirim	20s49/41w06	P. columella	68
	Castelo	20s36/41w12	P. columella	68
	Guaçuí	20s45/41w40	P. columella	68
	Guarapari	20s65/40w51	P. columella	UFES-Malacologia
	Jerônimo Monteiro	20s47/41w23	P. columella	68
	Marataízes	21s00/40w49	P. columella	68
	Mimoso do Sul	21s03/41w22	P. columella	68
	Muniz Freire	20s27/41w24	P. columella	68
	Muqui	20s56/41w20	P. columella	68
	Piúma	20s49/40w43	P. columella	68
	Presidente Kennedy	21s04/41w01	P. columella	68
	Serra	20s12/40w30	P. columella	UFES-Malacologia
	Vartem Alta	20s40/41w00	P. columella	68
	Itapemirim	21s00/40w49	P. columella	68
3) Midwest
Goiás	Barro Alto	14s58/48w55	P. columella	69
	Brasília	15s46/47w55	P. columella	4
	Campinaçu	13s44/48w34	P. columella	69
	Campinorte	14s18/49w88	P. columella	69
	Colinas do Sul	14s08/48w04	P. columella	69
	Formosa	15s30/47w20	P. columella	4
	Goiânia	16s41/49w13	P. columella	4; 24; 77
				Fiocruz-CMM
	Minaçu	13s31/48w13	P. columella	69
	Mineiros	17s30/52w32	P. columella	70
	Niquelândia	14s26/48w27	P. columella	69
	Santa Rita do Novo Destino	15s06/49w06	P. columella	69
	Uruaçu	14s29/49w07	P. columella	69
Mato Grosso	Cuiabá	15s35/56w05	P. columella	4
Mato Grosso do Sul	Aquidauana	20s27/55w46	P. columella	4
	Bela Vista	22s04/56w31	P. columella	4
4) Northeast
Bahia	Salvador	12s58/38w32	P. columella	71
Ceará	Fortaleza	3s45/38w32	P. columella	8; Fiocruz-CMM
Paraíba	Campina Grande	7s12/35w53	P. columella	72; 73
5) North
Amazonas	Benjamin Constant	4s22/70w01	P. columella	74
	Careiro	3s81/60w34	P. columella	Fiocruz-CMM
	Coari	4s05/63w08	P. columella	Fiocruz-CMM
	Manaus	3s06/60w03	P. columella	74
	Tefé	3s18/64w42	P. columella	71; Fiocruz-CMM
	Iranduba	3s28/60w18	P. columella	INPA-Mollusca
Acre	Rio Branco	9s58/67w48	P. columella	24; Fiocruz-CMM

Table 2

Distribution of Galba viatrix, G. rupestris, G. cubensis, Lymnaea truncatula and Lymnaea sp. per municipalities and regions of Brazil

Regions/States	Localities	Geographic coordinates	Species	Articles/“SpeciesLink” (CRIA) network
1) South
Rio Grande do Sul	Bagé	31s19/54w06	G. viatrix	3
	Bom Jesus	28s66/50w43	Lymnaea sp.	MCP-Moluscos
	Cambará do Sul	28s97/50w31	Lymnaea sp.	MCP-Moluscos
	Dom Pedrito	30s58/54w40	G. viatrix +	4; 3; 7; 82
	Erval Grande	27s38/52w57	Lymnaea sp.	MCP-Moluscos
	Estrela	28s86/51w17	Lymnaea sp.	MCP-Moluscos
	Ibirubá	28s54/53w09	Lymnaea sp.	MCP-Moluscos
	Jaguarão	32s33/53w22	G. viatrix +	4; 3
	Lavras do Sul	30s48/53w53	G. viatrix	3
	Pelotas	31s46/52w20	G. viatrix	10
	Porto Alegre	30s01/51w13	Lymnaea sp.	MCP-Moluscos
	Santa Vitória do Palmar	33s31/53w22	G. viatrix +	4; 14; 3; 89
				Fiocruz-CMM
	São Borja	28s39/55w59	Lymnaea sp.	MCP-Moluscos
	São Francisco de Paula	29s26/50w35	Lymnaea sp.	MCP-Moluscos
	Selbach	28s37/52w56	Lymnaea sp.	MCP-Moluscos
	Três Coroas	29s30/50w46	Lymnaea sp.	MCP-Moluscos
	Vacaria	28s48/50w92	Lymnaea sp.	MCP-Moluscos
	Viamão	30s04/51w01	Lymnaea sp.	MCP-Moluscos
Santa Catarina	Campos Novos	27s40/51w22	Lymnaea sp.	MCP-Moluscos
	Florianópolis	27s35/48w33	G. viatrix	21
Santa Catarina	Seara	27s12/52w19	G. viatrix	22; 4
			L. rupestris	23
Paraná	Curitiba	25s25/49w16	Lymnaea sp.	MZUSP
2) Southeast
São Paulo	Piracicaba	22s43/47w39	Lymnaea sp.	MZUSP
	Presidente Prudente	22s07/51w23	Lymnaea sp.	40
	São Paulo	23s32/46w38	Lymnaea sp.	MZUSP
	Ubatuba	23s25/45w04	Lymnaea sp.	MZUSP
Rio de Janeiro	Nova Friburgo	22s15/42w31	Lymnaea sp.	45
			G. truncatula	Fiocruz-CMM
	Paraíba do Sul	22s08/43w16	G. cubensis	51
	Petrópolis	22s21/43w08	G. cubensis	51
	Rio de Janeiro	22s53/43w12	G. cubensis	55
			Lymnaea sp.	MZUSP
	Teresópolis	22s23/42w58	Lymnaea sp.	50
			G. cubensis	51
			G. truncatula	Fiocruz-CMM
	Três Rios	22s05/43w12	G. cubensis	51; 90
	Vassouras	22s40/43w66	Lymnaea sp.	57
Minas Gerais	Belo Horizonte	19s55/43w56	G. cubensis	60; Fiocruz-CMM
			G. viatrix	4
	Careaçu	22s02/45w41	Lymnaea sp.+	79
	Ouro Branco	20s30/43w41	Lymnaea sp.	67
	Rio Acima	20s03/43w47	G. viatrix	63
			G. truncatula	60; Fiocruz-CMM
3) North
Pará	Belém	1s26/48w29	Lymnaea sp.	MZUSP

Legends for the tables 1 and 2: The numbers at the column Articles of the tables 1 and 2 are references to the authors that record the occurrence of specimens of Lymnaeidae. 1: Simões (2002); 2: Amaral et al. (2007); 3: Ueno et al. (1982); 4: Paraense (1982a); 5: Mattos et al. (1997); 6: Pereira et al. (2000a); 7: Mattos & Ueno (1985); 8: Coelho (2007); 9: Coelho et al. (2009); 10: Rey (1957); 11: Dacal et al. (1988); 12: Gonzales et al. (1974); 13: Indrusiak (1983); 14: Müller et al. (1998); 15: Martello et al. (2008); 16: Pereira et al. (2000b); 17: Agudo (2004) apud Agudo-Padrón (2008); 18: Agudo (2005); 19: Agudo (2007); 20: Agudo (2006); 21: Agudo-Padrón (2008); 22: Hubendick (1951); 23: Paraense (1982b); 24: Cardoso et al. (2006); 25: Bellato et al. (1996); 26: Queiroz et al. (2002); 27: Amaral & Busetti (1979) apud Buseti (1982); 28: Busetti (1982); 29: Vaz et al. (1987); 30: Vaz et al. (1986); 31: Vaz et al. (1983); 32: Muniz (2007); 33: Gouveia & Henry (1990); 34: Ueta (1976); 35: Magalhães et al. (1991); 36: Carvalho et al. (2001); 37: Vaz et al. (1992); 38: Maure et al. (1998); 39: Ueta (1980); 40: Tostes et al. (2004); 41: Oliveira et al. (2002); 42: Thiengo et al. (2004a); 43: Thiengo et al. (2006); 44: Thiengo et al. (2002b); 45: Thiengo et al. (2002a); 46: Thiengo et al. (2001); 47: Gomes et al. (2002); 48: Fiuza et al. (2006); 49: Thiengo et al. (2004b); 50: Thiengo et al. (1998); 51: Rezende et al. (1973); 52: Andrade Neto et al. (1999); 53: Medeiros et al. (2002); 54: Fernandez et al. (2001); 55: Nuernberg (1978); 56: Pinheiro & Amato (1996); 57: Lutz (1921); 58: Souza et al. (2002); 59: Souza et al. (1998); 60: Cardoso (2004); 61: Lima et al. (2009); 62: Coelho & Lima (2003); 63: Carvalho et al. (2004); 64: Vianna et al. (2007); 65: Martins & Alves (2008); 66: Souza et al. (2006); 67: Silva et al. (1994); 68: Almeida (2010); 69: Thiengo et al. (2005); 70: Teles et al. (1991); 71: Paraense (1986); 72: Abílio & Watanabe (1998); 73: Abílio et al. (2006); 74: Paraense (1983); 75: Amato et al. (1986); 76: Bruno et al. (1995); 77: Araújo et al. (1995); 78: Silva (2010); 79: Oliveira (2008); 80: Ueta (1977); 81: Silva-Santos et al. (1994); 82: Silva-Santos et al. (1987); 83: Martins & Alves (2010); 84: Veitenheimer-Mendes (1992); 85: Pile et al. (1999); 86: Braun (2005); 87: Morretes (1949); 88: Pinheiro et al. (2009); 89: Lara et al. 1988; 90: Nuernberg et al. 1983; 91: Luz et al. (1994). Fiocruz-CMM represents data obtained from the Collection of Medical Malacology, CPqRR, Fiocruz/MG. MCP-Moluscos represents data obtained from the Collection of Molluscs of Museum of Science and Technology, PUCRS. INPA-Mollusca represents data obtained from the Collection of Molluscs of National Institute of Research of Amazônia, INPA. UFES-Malacologia represents data obtained from the Malacological Collection of Biological Science Department, DCBio/UFES. MZUSP represents data obtained from the Malacological Collection of Zoology Museum of University of São Paulo. The symbol + represents snails found naturally infected with Fasciola hepatica.

Fig. 1

Spatial distribution of Pseudosuccinea columella in Brazil.

Fig. 2

Spatial distribution of Galba viatrix, G. cubensis, G. truncatula, Lymnaea rupestris, and Lymnaea sp. in Brazil.

Fig. 3

Spatial distribution of Lymnaeidae in the South region of Brazil.

Fig. 4

Spatial distribution of Lymnaeidae in the Southeast region of Brazil.

Fig. 5

Spatial distribution of Lymnaeidae in the Midwest, North and Northeast regions of Brazil.

Lymnaeids snails were reported in 417 municipalities and one ecological reserve (Taim) of 16 states, which corresponds to 7.5% of all municipalities in Brazil. Pseudosuccinea columella was reported in 400 (95.7%) localities while G. viatrix in 10 (2.4%), G. cubensis in six (1.4%), G. truncatula in three (0.7%) and L. rupestris in one (0.2%). In 25 (6%) municipalities: Bom Jesus, Cambará do Sul, Erval Grande, Estrela, Ibirubá, Porto Alegre, São Borja, São Francisco de Paula, Selbach, Três Coroas, Vacaria and Viamão of Rio Grande do Sul State; Piracicaba, Presidente Prudente, São Paulo and Ubatuba of São Paulo State; Rio de Janeiro, Nova Friburgo, Teresópolis and Vassouras of Rio de Janeiro State; Ouro Branco and Careaçu of Minas Gerais State; Campos Novos/SC; Curitiba/PR and Belém/PA, it was not possible to accomplish a complete identification of the specimens collected. Occurrence of more than one species was reported in 13 municipalities (3.1%): Dom Pedrito, Pelotas and Santa Vitória do Palmar in the state of Rio Grande do Sul; Florianópolis (P. columella and G. viatrix) and Seara (L. rupestris, P. columella and G. viatrix) in the state of Santa Catarina; Teresópolis (P. columella; G. cubensis and G. truncatula), Nova Friburgo (P. columella and G. truncatula), Paraíba do Sul, Petrópolis, Rio de Janeiro and Três Rios (P. columella and G. cubensis) in the state of Rio de Janeiro; Belo Horizonte (P. columella, G. viatrix and G. cubensis) and Rio Acima (P. columella, G. viatrix and G. truncatula) in the state of Minas Gerais.

Specimens of P. columella and G. viatrix were reported in 403 localities (96.4%). P. columella was reported naturally infected with F. hepatica in 11 municipalities of the states of Rio Grande do Sul, São Paulo, Minas Gerais and Rio de Janeiro, G. viatrix was found naturally infected in three municipalities of Rio Grande do Sul while Lymnaea sp. was found in one municipality of Minas Gerais. In Dom Pedrito/RS, both species were found naturally infected.

DISCUSSION

Our study resulted in the first map of the spatial distribution of Lymnaeidae species, intermediate host snails of F. hepatica in Brazil. The presence of host snails could reflect the disease distribution, and these data are essential for describing the risk areas of fasciolosis since there is an increase of the association between the global number of human cases and the presence of the intermediate host snail[50].

PARAENSE[65] showed that G. viatrix had few records in the South and P. columella was distributed mainly in the South and Southeast, where a high number of fasciolosis cases occurs[36], with few records in the Midwest region. After that, the same author reported two new localities of P. columella for the states of Amazonas and Bahia[67] in the North and Northeast respectively. This agrees with our study where we also reported a low presence of this species in these regions. Our final maps about spatial distribution of lymnaeids snails show that P. columella is the most common species and it is widespread in the South and Southeast with few records in the Midwest, North and Northeast regions. Galba viatrix is predominantly distributed in the South (eight records) with only two records for the Southeast region (Belo Horizonte and Rio Acima, Minas Gerais State). The distribution of G. viatrix, G. cubensis and G. truncatula comprises few records in Southeast and South regions. They were not reported for the Midwest, North and Northeast. For the South region, the species L. rupestris was only described and found in the Nova Teutônia district in Seara municipality at Santa Catarina State[64].

Despite the few records showed by G. viatrix in our study, according to MATTOS & UENO[52] this intermediate host is considered the most efficient species in the transmission of F. hepatica due to its high susceptibility when compared with P. columella [52]. However, P. columella showed to be the most distributed species (Fig. 1; 95.7%) and is certainly the most important intermediate host in Brazil. This is probably due to its biological aspects, such as its high capacity for self-fertilization, favorable condition in dispersion and colonization of new habitats[20,35]. Pseudosuccinea columella is commonly found in most human or animal fasciolosis outbreaks while the occurrence of G. viatrix is, currently, restricted to the state of Rio Grande do Sul[24,33,63,76,101] and in Minas Gerais[22].

In relation to the others susceptible species, G. cubensis occurs only in the Southeast, mainly in Rio de Janeiro State[19,60,76]. There was a gap of 30 years in its record and until now its presence in other regions was not reported. Galba truncatula is also susceptible to F. hepatica, however with few records (0.7%) it has never been found naturally infected in Brazil. Lymnaea rupestris was only described and found in one locality and there is no information about its susceptibility. Due to these facts, the role in the transmission of fasciolosis of the species above mentioned remains unknown.

In the present study, it was possible to observe the occurrence of P. columella in several localities of the South (four municipalities) and Southeast (seven municipalities) and of G. viatrix in the South (three municipalities) naturally infected by F. hepatica (Table 1 and 2). In the South region, the presence of extensive endemic areas of fasciolosis is frequent, while in the Southeast and Midwest regions there are only small endemic areas[41]. Some environmental and climatic factors in the South region provide favorable habitats for the intermediate host snails of F. hepatica, such as low elevation (where there are numerous rice fields), clay soil, humid areas, and a temperate climate. These habitats, as shown by UENO et al. [98], contribute to the maintenance of the snails' life cycle in this region.

Despite the great efforts made by research groups, some important issues related to the nature and precision of the presence of lymnaeid species in Brazil need to be considered when interpreting our findings. The complete distribution of intermediate host snails of F. hepatica in Brazil remains unknown, especially due to the large areas that need to be surveyed mainly in the North and Midwest regions. Other restraining factors include the insufficient number of researchers involved in the taxonomy area, which may cause difficulties in identifying the snails at a species level due to the confusing taxonomic situation of the Lymnaeidae family. It was confirmed by our study that in several localities (25 municipalities; 6%) the specific identification was not possible to be done. The identification of specimens is important since knowing the species that act as intermediate hosts in a particular area, we can define priority strategies regarding intermediate hosts biology to control fasciolosis. In Careaçu, MG, the occurrence of naturally-infected specimens without specific identification was reported (Table 2).

Another important point concerns the validity of the species identification used from the literature data and malacological collections due to systematics confusion of lymnaeids snails. This identification is essential in order to justify the distribution of lymnaeid species in Brazil. Regarding L. rupestris and P. columella, there is no problem because these two species can be easily identified using a set of reliable morphological characters and the literature data can be used with a reasonable confidence. However, this is not the case regarding the three other remaining species, G. viatrix, G. cubensis and G. truncatula, because these small species cannot be separated morphologically and only molecular markers allow a clear separation[14,27,28,56,73,77]. In our literature search we identified only 19 localities where the specific identification might be a concern (10 localities with G. viatrix, six localities with G. cubensis and three localities with G. truncatula). Only in the occurrence of G. cubensis for Belo Horizonte, MG[19], G. truncatula for Rio Acima, MG[22] and the data from Fiocruz-CMM have the authors already carried out molecular identification.

Studies on the lymnaeid fauna should be increased all over Brazil, mainly where the information is scarce or nonexistent, with the objective to learn more about the spatial distribution of the intermediate host snail of F. hepatica. The methodology used and the intermediate host snail final maps could be useful in identifying priority areas for control interventions of fasciolosis, so that limited resources could be allocated most effectively.