Gastropods potential intermediate hosts of parasites in the region of Lençóis Maranhenses National Park/Brazil, an international tourist destination

Gastrópodes potenciais hospedeiros intermediários de parasitos na região do Parque Nacional dos Lençóis Maranhenses/Brasil, um destino turístico internacional

Abstract

Several aquatic ecosystems present favorable conditions for the establishment of freshwater gastropod populations in Maranhão (Brazil). However, research on these snails in this Brazilian state is more focused on Baixada Maranhense, an endemic area for schistosomiasis in Maranhão. Considering the need to expand information on the occurrence of limnic gastropods in Maranhão, a qualitative study was carried out in the Microregion of Lençóis Maranhenses. The capture of freshwater snails was carried out between June 2016 and November 2019. Were obtained 3,244 specimens of freshwater gastropods: 2,372 specimens of Biomphalaria straminea (Dunker, 1848); 17 specimens of Biomphalaria schrammi (Crosse, 1864); 19 specimens of Drepanotrema lucidum (Pfeiffer, 1939); 115 specimens of (Hydrobiidae; Rissooidea); 24 specimens of Physa marmorata Guilding, 1828; 73 specimens of Pomacea maculata (Perry, 1810); 613 specimens of Pomacea sp. (Perry, 1810). Were also found 11 shells of Biomphalaria glabrata (Say, 1818). The greatest richness of snails was observed in Tutóia. The most abundant species during the study was B. straminea (73,45%). Pomacea sp. was the most representative species with constant frequency (57,15%) in the Lençóis Maranhenses Microregion, present in lentic and lotic ecosystems. The forecast maps indicate the possibility of occurrence and establishment of freshwater gastropods species throughout the investigated region. The presence of gastropods that are hosts of parasites represents a risk to human health, especially in the Lençóis Maranhenses area, which is one of Brazil's tourist destinations. Studies on the occurrence and distribution of limnic gastropods are of great relevance for understanding the conservation status of existing species. Furthermore, they are necessary to monitor snails that act as parasite hosts.

Keywords:  biodiversity; tourism; snails; Rio Preguiças; Delta of the Americas; predictive model

Resumo

Diversos ecossistemas aquáticos apresentam condições propícias para o estabelecimento de populações de gastrópodes de água doce no Maranhão (Brasil). Entretanto, as pesquisas acerca desses moluscos, nesse estado brasileiro, estão mais direcionadas para a Baixada Maranhense, área endêmica da esquistossomose no Maranhão. Considerando a necessidade de ampliar informações sobre a ocorrência de gastrópodes límnicos no Maranhão, realizou-se um estudo qualitativo na Microrregião dos Lençóis Maranhenses. As coletas ocorreram entre junho de 2016 e novembro de 2019. Foram obtidos 3.244 espécimes de gastrópodes de água doce: 2.372 exemplares de Biomphalaria straminea (Dunker, 1848); 17 exemplares de Biomphalaria schrammi (Crosse, 1864); 19 exemplares de Drepanotrema lucidum (Pfeiffer, 1939); 115 exemplares de (Hydrobiidae; Rissooidea); 24 exemplares de Physa marmorata Guilding, 1828; 73 exemplares de Pomacea maculata (Perry, 1810); 613 exemplares de Pomacea sp. (Perry, 1810). Foram encontradas também 11 conchas de Biomphalaria glabrata (Say, 1818). A maior riqueza de moluscos foi observada em Tutóia. A espécies mais abundante durante o estudo foi B. straminea (73,45%). Pomacea sp. foi a espécie mais representativa e com frequência constante (57, 15%) na Microrregião dos Lençóis Maranhenses, presente em ecossistemas lênticos e lóticos. Os mapas de previsão sinalizam a possibilidade de ocorrência e estabelecimento de espécies de gastrópodes de água doce em toda a região investigada. A presença de gastrópodes hospedeiros de parasitos representa um risco para a saúde humana, principalmente na área dos Lençóis Maranhenses que é um dos destinos turísticos do Brasil. Estudos sobre a ocorrência e distribuição de gastópodes límnicos possuem grande relevância para a compreensão do estado de conservação das espécies existentes. Além disso, são necessários para monitorar moluscos que atuam como hospedeiros de parasitos.

Palavras-chave:  biodiversidade; turismo; caramujos; Rio Preguiças; Delta das Americas; modelo pretitivo

1. Introduction

The coast of Northern Brazilian lands presents several different landscapes, such as: mangroves, beaches, restinga forest and dune systems. Due to its morphological characteristics and natural resources, represents one of the most important area to the Brazilian biodiversity conservation and offer great tourist potential (Bezerra et al., 2018). Located in this region, Lençóis Maranhenses National Park is a protected area of 1,550 km² that comprises a mosaic of ecosystems (IBAMA, 2003) and have been visited by more than 100,000 people per year (Souza dos Santos and Santos, 2015; Amaral et al., 2019; ICMBIO, 2020).

Many of the ecosystems from Lençóis Maranhenses favor the establishment of freshwater snails, part of a diverse group of snails, comprising more than one hundred thousand species found in the most diverse environments such as terrestrial, marine and freshwater (Strong et al., 2008; Almeida et al., 2018). These animals stand out in freshwater environments due to the number of species, biomass and participation on various ecological interactions, such as filtering agents, herbivores, predators, ectoparasites (Camargo and Giarrizzo, 2009; Colley et al., 2012; Pombo, 2016). They play a role in the trophic chain, being used as food by fish, amphibians, reptiles, birds and mammals, and even humans (Drügg-Hahn, 1997; Santos and Maia, 2018).

Some freshwater snails, mainly Gastropoda, are of medical and veterinary interest because many species act as intermediate hosts of trematodes and some parasitic nematodes of humans and domestic animals (Fernandez et al., 2008; Agudo-Padrón et al., 2013; Pombo, 2016; Melo, 2018). Despite these, it lacks studies on freshwater snails (Fernandez et al., 2006; Cantanhede, 2015) especially in the north and northeast Brazil (Santos and Maia, 2018).

Studies on the occurrence and distribution of freshwater gastropods are fundamental for several aspects, such as: monitoring of disease-vector species, introduction of exotic species and also for expanding the knowledge on the conservation status of native species (Ohlweiler et al., 2010). However, what is known about the distribution of various species of freshwater snails is limited in the databases. Thus, the use of tools such as predictive modelling of species distribution is effective in estimating the potential geographical distribution of a species and characterizing the environmental conditions that are suitable for occurrence, in addition to providing information of which habitat should be investigated, because through statistical tools it identifies the potential habitat for study (Guisan and Zimmermann, 2000; Ortega-Huerta and Townsend Peterson, 2008; Sarania et al., 2017).

In this sense, the objectives of this study were: i) to investigate the occurrence of freshwater gastropod species in the Lençois Maranhenses Microregion; ii) to record their abundance; iii) and to perform predictive modeling of distribution to identify a complete potential landscape of species occurrences.

2. Material and Methods

2.1. Study area

The Lençois Maranhenses Microregion is located in the Mesoregion North in the state of Maranhão - Brazil. It has a total area of 10,680,089 km² and is divided into six municipalities: Barreirinhas, Humberto de Campos, Paulino Neves, Primeira Cruz, Santo Amaro e Tutóia (IMESC, 2013; Sousa, 2015).

This region has three watersheds: Preguiças, Periá and Parnaíba (IMESC, 2013). It is possible to find in these area environments such as rivers and lakes, restinga, flood fields, dune and mangrove fields. It has a sub-humid climate, with an average annual temperature of 27 °C, while the maximum average temperature varies from 31 to 33 °C (Maranhão, 2003; IBAMA, 2003; Souza dos Santos and Santos, 2015; IMESC, 2020). It has annual relative air humidity between 76% and 82%. In addition, it presents a rainy period that generally extends from January to July, with annual rainfall between 1200 and 2000 mm. Paleodunes and sandbanks vegetation predominate in the region (IMESC, 2020). Given the morphological characteristics and natural resources, on July 2, 1981, part of the area of Lençóis Maranhenses was transformed into Lençóis Maranhenses National Park. The entire area of the Park is part of the Lençóis Maranhenses Microregion (Brasil, 1981; Souza dos Santos and Santos, 2015; Amaral, 2018). The Lençóis Maranhenses National Park territory is distributed by the municipalities of Barreirinhas, Primeira Cruz and Santo Amaro do Maranhão (ICMBio, 2020; Noronha and Araújo, 2017; Araújo, 2015; Salvador et al., 2019; Amaral et al., 2019).

Another environmental protection territory was created in the Lençóis Maranhenses Microregion, the (APA) of the Parnaíba Delta, was established by Decree s/nº of 28/08/1996, as a federal conservation unit (UC), located on the North Coast, formed by twelve municipalities in the coastal areas of Ceará, Piauí and Maranhão. In Maranhão it includes the municipalities of Araioses, Água Doce, Tutóia and Paulino Neves (ICMBio, 2020; Oliveira et al., 2016; Melo, 2018).

2.2. Sampling and data analysis

The specimens were obtained from different biotopes (rivers, lagoons, ponds in the dunes and streams, rivers, drainage and sewage ditches) in four collections (annual) in the period of June 2016 to November 2019 at the beginning of the rainy season. The snails were collected in Tutóia, Barreirinhas, Santo Amaro and Paulino Neves (Figure 1), using the Olivier and Schneiderman capture method (1956). Three collectors performed 10 minutes of searches in each biotope, and all collection sites were georeferenced using a Garmin eTrex GPS device (Garmin, Olathe, USA). In the Laboratório de Zoologia of Universidade Estadual do Maranhão, specimens were placed in aquaria containing dechlorinated water, substrate and food (fresh lettuce leaves).

Figure 1
Distribution of species collected in the period of June 2016 to November 2019 in the municipalities of the Lençóis Maranhenses Microregion. (A) Barreirinhas: , Physa marmorata and Pomacea sp., Physa marmorata, Pomacea sp.; (B) Santo Amaro: Biomphalaria straminea, Pomacea sp. and Pomacea maculata, Pomacea maculata, Pomacea sp.; (C) Paulino Neves: Biomphalaria straminea and Pomacea sp., Biomphalaria straminea, Biomphalaria straminea and Rissoidea; (D) Tutóia: Biomphalaria straminea and Pomacea sp., Biomphalaria straminea and Drepanotrema lucidum, Biomphalaria straminea, Biomphalaria schrammi, Drepanotrema lucidum and Pomacea sp., Pomacea sp., Biomphalaria straminea.

Ten specimens of each sample were anesthetized in Hypnol 0.05% solution for five hours, killed by hot water (70 °C) and fixed in Railliet-Henry solution for morphological analysis (Fernandez et al., 2008). Ampullarid species were fixed the acording whith Fukuda et al. (2008). Vouchers and snail tissues were deposited in the Tissue and DNA Collection of Maranhenses Fauna (CoFauMA) of the State University of Maranhão, Brazil. The snail collections were authorized by the Brazilian Institute of the Environment and Non- Renewable Natural Resources (SISBIO-Number 53224-1).

The richness of species relative abundance and frequency of occurrence were analyzed. To calculate the frequency of occurrence, the following formula was used FO = p x100 / P, where “p” represents the number of samples in which the taxon occurred and “P” the total of point of collection. The result of FO was classified according to Dajoz (1983), where: FO > 50% frequent or constant; 50% < FO > 25% accessory; FO < 25% accidental or rare.

To obtain the data of relative abundance was %Spi = N x 100 / Na, where “N” is the density of each taxon in the sample and “Na” represents the total density of organisms in the sample. The results are presented in percentage following the Calvacante and Larrazál classification, (2004): very abundant (Spi> 50%), abundant (50% < Spi > 30%), low abundant (30% < Spi > 10%), sporadic (Spi < 10%).

In order to verify the adequacy of the limnic gastropod sampling, a rarefaction curve was elaborated. The curve was produced by the program R version 4.0.2, through the package Vegan and INEXT. The Shannon- Wienner (H') and Simpson (D) indexes were calculated. The analysis of multidimensional scaling (MDS) was used to compare the diversity of the sampling municipalities, through the abundance values of each species, in each locality. An MDS map of Euclidean distances was created.

2.3. Predictive distribution modeling

For the construction of the predictive distribution model, the information on the occurrence of freshwater gastropods species in 38 GPS coordinates points was considered. The shape used was the one made available by the IBGE website for the Lençóis Maranhenses Microregion. The decision to model for all species was supported by the fact that they have very similar habitat conditions, which were observed in the field.

We obtained 19 bioclimatic variables with spatial resolution of 5 arc-min from Wordclim database (http://worldclim.org/) which has 19 bioclimatic variables and we made an evaluation of these environmental variables to avoid redundancy, where a correlation analysis was performed organizing a matrix with the Spearman coefficients values (Guisan and Zimmermann, 2000) for each pair of variables, pairs higher than 0.75 were considered highly correlated (Bueno, 2012) and were discarded from the model (Peterson, 2006; Meyer et al., 2016) making a pre-selection of the bioclimatic variables by means of program R version 4.0.2.

Other environmental data whit the normalized difference vegetation index (NDVI) and enhanced vegetation index (EVI) corresponding to vegetation obtained from NASA's website. In addition to these variables, soil data was also considered (Silt-SLTPPT, Sand-SNDPPT, Clay-AWCh1, Soil PH-PHIHOX) were downloaded from https://soilgrids.org. The vertical distance to the nearest drain was extracted from the algorithm HAND (The Height Above the Nearest Drainage), with a 50 pixels threshold (Rennó et al., 2008), obtained from the site AMBDATA - Instituto Nacional de Pesquisas Espaciais (INPE).

The climate suitability models were developed based on the algorithms: Generalized Linear Models (GLM), Vector and Support Machines (SVM), Environmental Distance (Mahalanobis Bioclimatic Envelope (BIOCLIM), DOMAIN, MaxEnt and Random Forest. We calibrate the models in 70% of the data for training and 30% for testing. Each algorithm performed 10 repetitions. Minimum cut limits were established, 30% and 50%. To evaluate the accuracy of the model we use the area over the curve (Area Under the Curve-AUC), obtained from the ROC (Receiver Operating Characteristics) curve, where AUC varies from zero to one (Elith et al., 2006; Nabout et al., 2009) and through True Skill Statistic (TSS). Only the models indicative of “good” performance with TSS higher than 0.7 and AUC higher than 0.8 were selected.

The bioclimatic data with the species presence records were handled in the R 4.0.2 software to generate potential distribution maps of the species under study, using the ensemble (set of forecasts of potential areas in common between the algorithms) of all algorithms in the construction of the final map of potential distribution of snail, to reduce the uncertainties of the forecasts (Araujo and New, 2007).

3. Results

During the sampling period, 3,244 snails were captured. These animals belong to Gastropoda species: Planorbidae: Biomphalaria straminea (Dunker, 1848) (n=2,372); Biomphalaria schrammi (Crosse, 1864) (n = 17); Drepanotrema lucidum (Pfeiffer, 1939) (n= 19); Hydrobiidae: Rissooidea (n=115); Physidae: Physa marmorata Guilding, 1828 (n=24); Ampullariidae: Pomacea maculata Perry, 1810 (n =73) e Pomacea sp. (n = 613). Including 11 shells of Biomphalaria glabrata (Figure 1 and Supplementary data 1).

Freshwater gastropods were registered in 38 water collections (25 were classified as lentic and 13 as lotic) studied in the municipalities of Santo Amaro, Tutóia, Paulino Neves and Barreirinhas (Supplementary data 2).

The greatest richness of molluscs was observed in Tutóia, with the occurrence of five species: B. straminea, Pomacea sp., B. schrammi, P. maculata, D. lucidum. Biomphalaria straminea was classified as very abundant (73, 45%) during the study and Pomacea sp. was considered as a frequent/constant (57, 15%), (Supplementary data 3 and 4).

The rarefaction curve (Supplementary data 5), obtained during the study period, verified in the 38 sampling points, shows an inclination with horizontal tendency, indicating that the number of points analyzed, in relation to the quantity of species, was representative for the freshwater snails of the Lençois Maranhenses Microregion. Evidencing in the extrapolated forecast, find the same species already registered in this study.

The analysis of multidimensional scaling showed similarity among the four municipalities in relation to the distribution of abundance. In relation to the composition of species the municipality of Paulino Neves showed greater divergence (Figure 2).

Figure 2
Analysis of multidimensional scaling scheduling of the abundance (A) and absence and presence of species (B) in the municipalities of the Lençóis Maranhenses Microregion in the period of June 2016 to November 2019.

Based on the occurrence data of freshwater gastropods, we generated a distribution map for potential snail occurrence areas in Lençois Maranhenses Microregion (Figure 3). The map shows areas suitable for the presence of snails. Presenting greater susceptibility of occurrence and establishment of the snail species in the municipality of Paulino Neves, Tutóia and Barreirinhas. Less suitable in Primeira Cruz and Humberto de Campos for the prediction of occurrence in the Lençois Maranhenses Microregion. As for the conservation units, it is possible to predict the occurrence of these species in the APA of Rio Preguiça, in the whole Lençóis Maranhenses National Park, in a part of the APA of the Parnaíba Delta.

Figure 3
Predictive distribution models for snail from the Lençois Maranhenses Microregion. (A) medium consensus; (B) medium consensus with minimum cut-off threshold; (C) medium consensus with 30% cut-off limit; (D) Medium consensus with 50% cut-off limit occurrence.

The predictive distribution modeling has high AUC and TSS for both training and test indicating good model performance for snail species (Supplementary data 6). The models showed the highest AUC values (> 0, 75), while TSS showed only RandomForest showed lower values. While factors such as Height Above the Nearest Drainage (HAND), Average temperature in the hosttes quarter, Physical soil variables, Enhanced vegetation index (EVI), Silt, and Normalized difference vegetation index (NDVI) were also effective contributors to the model, others such as mean temperature of coldest quarter, annual mean temperature, Soil PH, and Clay no contribution to the spatial distribution model (Table 1).

Table 1
Estimate of relative contributions of the environmental variables to distribution the snails in the municipalities of the Lençois Maranhenses Microregion in the period of June 2016 to November 2019.

Variable	Percent contribuition (%)
Heigth Above the Nearest Drainage (HAND)	32.1%
Average temperatura in the hosttes quarter (Bio 10)	26.3%
Physical soil variables	18.1%
Enhanced vegetation index (EVI)	6.9%
Silt-SLTPPT	6.0%
Normalized difference vegetation index (NDVI)	5.2%
Precipitation of Driest Quarter (Bio 17)	3.3%
Mean Diurnal Range (Mean of monthly (max temp)) (Bi2)	1.5%
Sand-SNDPPT	0.6%
Mean temperatura of coldest quarter (Bio 11)	0.0%
Annual mean temperature (Bio 1)	0.0%
Soil PH-PHIHOX	0.0%
Clay-AWCh1	0.0%

4. Discussion

The limnic ecosystems in the Lençóis Maranhenses Microregion present adequate characteristics for the occurrence of freshwater gastropods species, such as the presence of river, lagoons, restinga, flood fields, dune fields (Maranhão, 2003; IBAMA, 2003; IMESC, 2013).

It is common for freshwater gastropods to occur in areas closely related to human activities (Rey, 2001; Tibiriça et al., 2006; Spyra and Cieplok, 2022). Although the municipalities investigated are inserted in conservation units, they suffer from anthropogenic impacts, the limnic ecosystems of the region are used for human supply, animal breeding, domestic services, fishing and the growing tourist activity, in addition to the constant release of organic waste. The sites most impacted by human action tend to have a greater number and diversity of snails (Miranda et al., 2016).

In this sense, it is important to have more attention to vectors snails. In our study, B. straminea was very abundant and present in all investigated municipalities. It was found in lentic environments and considered rare/accidental specie (Supplementary data 3). Although numerous specimens of B. straminea were found during fieldwork, the occurrence of this specie was verified in specific limnic ecosystems (lagoons) suggesting a geographical distribution pattern that is still restricted. Attention is drawn to the need to carefully assess the frequency of occurrence of this species in future monitoring in the Lençóis Maranhenses Microregion, as rain contributes to the formation of lagoons in the region and these aquatics ecosystems are often interconnected (IBAMA, 2003).

Due to the collective effort of researchers and the Ministry of Health, there was already a record of B. straminea in the municipality of Tutóia and Barreirinhas (Carvalho et al., 2008). Similar to our study, this specie also was verificated us the most abundant in Baixada Maranhense Microregion. The difference was that B. straminea was present (constant/frequent species) in more than 50% of the snail breeding sites in that region (Cantanhede, 2015).

The presence of B. glabrata shells is an indication of the probable occurrence of these specie. Additional research in these aquatic environments are necessary in order to find living specimens for specific identification. Studies targeting schistosomiasis in Maranhão reported B. glabrata in Barreirinhas and Tutóia (Carvalho et al., 2008). In the latter municipality, the snails were infected by S. mansoni (Santos and Melo, 2011).

The absence of live specimens of B. glabrata in this region also may be associated with competition between B. glabrata and B. straminea with a probable change in the abundance pattern of the species, as observed by Barbosa et al. (2014a) on the coastal coast of Pernambuco and on the Island of Itamaracá (Barbosa et al., 2014b). One of the probable justifications are the ecological advantages of B. straminea in relation to B. glabrata. Biomphalaria straminea presents a wide geographic distribution, capacity to populate extensive and varied environments, besides being well adapted to the different ecological conditions in Brazil (Barbosa et al., 1993; Souza et al., 2010; Fernandez, 2011; Barbosa et al., 2011; Kotzian and Amaral, 2013; David et al., 2018; Silva et al., 2020).

The other species of the Planorbidae family, B. schrammi and D. lucidum, were found in lentic ecosystems that presented much vegetation with the presence of algae. The occurrence of these two genera, Biomphlaria and Drepanotrema, were associated with an environment with a great amount of aquatic plants and organic matter (Barbosa et al., 1993; Buss et al., 2002; Miranda et al., 2016).

Pomacea sp. was the most representative species and with constant frequency in the Lençois Maranhenses Microregion, present in lentic and lotic ecosystems. Similar results were observed by Miranda et al. (2016) for the metropolitan region of São Luís and Cantanhede (2015) in Baixada Maranhense Microregion. These ampullariid usually live in calm waters and can withstand polluted environments (Hayes et al., 2009).

Ampullariid specimens, including P. maculata have already been verified harboring the nematode Angiostrongylus cantonensis (Chen, 1935) which causes human eosinophilic meningitis (Qvarnstrom et al., 2013; Teem et al., 2013) and therefore the dispersion of Pomacea sp. and P. maculata may represent a threat to public health (Pasquevich et al., 2014). Pinto et al. (2015) reported P. maculata, collected in Baixada Maranhense, as intermediate host of the Stomylotrema gratiosus trematode Travassos 1922, intestinal parasite of birds.

Physa marmorata was found in the municipality of Barreirinhas, verified in the lentic ecosystem. This species often inhabits lentic environments and the water courses of rivers (Perissinotto et al., 2014). In the metropolitan region of São Luís, specimens of the Physa genus were found in lentic and lotic environments adhered to vegetation (Miranda et al., 2016).

Regarding parasitological aspects, P. marmorata was reported as the first natural host of the Echinostoma exile trematode Lutz, 1924 (Pinto and Melo, 2012). The trematodes of the genus Echinostoma Rudolphi, 1809 are intestinal parasites of birds and mammals (Kostadinova and Gibson, 2000; Kostadinova, 2005; Pinto and Melo, 2012). This species was also found naturally infected in Brazil by Trichobilharzia skrjabin Zakharov 1920, the main etiological agent of cercarian dermatitis in humans (Pinto et al., 2014).

The difference observed in the analysis of multidimensional scaling for the municipality of Paulino Neves regarding the species composition, may be related to the farms investigated in the area, predominantly with characteristics of small lakes of muddy sediment and presence of streams. What is different from the other municipalities that presented environments with greater diversity of characteristics: sandy sediment; plenty of vegetation on the banks; swamp and river environments. The diversity of species found is directly related to the effects of interactions that occur in the environment they inhabit, thus the distribution of these species undergo changes of climate and environmental variables (Barbosa et al., 2014b; Cantanhede, 2015).

The present study presents the first predictive map regarding the spatial distribution of freshwater gastropod species for the state of Maranhão. Other studies already carried out in Brazil show distribution modeling of the genus Biomphalaria throughout the Middle Paranapanema river basin, São Paulo (Palasio et al., 2019); in the metropolitan region of Recife, Pernambuco (Barbosa et al., 2016). Regarding global distribution, we can highlight a study that used ecological models to predict the distribution of B. straminea (Yang et al., 2018).

The significant associations in the MaxEnt model of HAND, Average temperature in the hostess quarter, Physical soil variables, EVI, Silt, NDVI with snail occurrence are all compatible with field observations. Our results indicated that HAND is the main factor influencing the distribution of snails in the study area. It is important to remember that HAND is capable of indicating the risk of flooding events that can be caused by high rainfall and increased temperatures due to global climate change (Palasio et al., 2015).

In the Lençóis Maranhenses microregion, water bodies (such as lagoons between the dunes) are formed during the rainy season and this happens due to the ecological characteristics that are peculiar to this region (IBAMA, 2003). Floods in the main rivers and flood events are expected to interfere with the distribution of snails. Considering the occurrence of vector snails in the Lençóis Maranhenses Microregion, it is essential to monitor the area, given the risk of schistosomiasis transmission in this region.

Temperature influence species distribution ins scales global (Tambo et al., 2014) This climatic variable was observed by Scholte et al. (2012) as important Biomphalaria distribution factor in South America. The EVI and NDVI showed adequate environmental conditions for distribution and transmission S. mansoni in many studies with genus Biomphalaria (Guimarães et al., 2013; Stensgaard et al., 2005).

The predictive distribution model demonstrated susceptible areas in the Lençois Maranhenses Micoregion, besides the occurrence of these freshwater gastropod species, in municipalities with increasing tourist activity inserted in environmental protection areas, signaling the need for monitoring in order to know the biodiversity and control probable infectious agents.

The tourist pole of the region involves some of the municipalities investigated in this research. In the Lençois Maranhenses Microregion, the municipalities of Barreirinhas and Santo Amaro exercise a large part of the tourism potential of the region, due to the Lençois National Park and the municipality of Tutóia for being part of the Parnaíba Delta (IMESC, 2013).

These municipalities (Tutóia, Barreirinha, Paulino Neves and Santo Amaro) also make up the Route of Emotions, created to encourage tourism. The Rota das Emoções Maranhense is present in the following protected areas: Preguiças River Environmental Protection Area, Parnaíba Delta Environmental Protection Area, Parnaíba Delta Marine Extractive Reserve and Lençóis Maranhenses National Park (IMESC, 2020). Barreirinhas is the most sought after town by tourists for its easy access, with asphalted road and better infrastructure to receive tourists (Carvalho, 2005).

The search for new forms of leisure, outside urban areas, has led to the practice of tourism in natural areas that promote outdoor activities and exchange experience with nature (Dias, 2003; Muñoz Flores, 2008; Teles, 2001; Santos and Bahl, 2017).

An aggravating factor for these municipalities, given the presence of these snails in water collections, is the lack or inadequate collection of sewage in the region. Santo Amaro and Tutóia have less than 10% of the homes with adequate treatment and Paulino Neves and Barreirinhas less than 20% (IBGE, 2010; IMESC, 2013). The lack of sewage treatment, besides compromising the water quality of the water resources, favors for the cycles of trematodes causing diseases such as and among others, establish yourself in these municipalities.

Considering the few studies directed to the analysis of the biodiversity of freshwater gastropods for the state of Maranhão, the survey conducted in the Lençóis Maranhenses Microregion contributed to the record of the occurrence of the species in the investigated area, besides amplifying the information of the distribution of these gastropods in Brazil.

5. Conclusion

The results obtained in this work showed that the Lençois Maranhenses Microregion presents environmental and climatic characteristics favorable to the establishment and colonization of freshwater gastropods populations and can be characterized as a breeding ground for intermediate hosts of medical-veterinary interest for other water collections.

Considering that B. straminea was the most abundant species in the study with the occurrence in the four municipalities (Tutóia, Barreirinhas, Paulino Neves and Santo Amaro) investigated, added to the precarious sanitary conditions of the Lençois Maranhenses Microregion, they point out the need for measures to prevent schistosomiasis, and monitoring of intermediate hosts.

The prediction map might be used for guide spatial targeting of control interventions in areas with tourist potential susceptible to occurrence of freshwater gastropods species and in direct contact with human activity, emphasizing the need for health surveillance activities, which makes monitoring these areas very important.

Supplementary Material

Supplementary material accompanies this paper.

Supplementary data 1. Limnic gastropods collected in the Lençóis Maranhenses Microregion in the period of June 2016 to November 2019. (A) Biomphalaria glabrata (Say 1818); (B) Biomphalaria schrammi (Crosse, 1864); (C) Biomphalaria straminea (Dunker, 1848); Escala: 5mm; (D) Drepanotrema lucidum (Pfeiffer, 1939); (E) Hydrobiidae: Rissooidea; (F) Physa marmorata Guilding, 1828 Escala: 1mm; (G) Pomacea maculata (Perry, 1810); (H) Pomacea sp. (Perry, 1810) Escala: 10mm.

Supplementary data 2 Data from ecosystems where freshwater gastropods were found in the Lençóis Maranhenses Microregion in the period of June 2016 to November 2019.

Supplementary data 3 Frequency of occurrence of species of the Microregion of Lençóis Maranhenses, categorized according to Dajoz, (1983). Legend: FO > 50% frequent or constant; 50% < FO > 25% accessory; FO < 25% accidental or rare.

Supplementary data 4 Species occurring in the Microregion of Lençóis Maranhenses, categorized according to Cavalcanti and Larrazábal (2004). Legend: very abundant (Spi > 50%), abundant (50% < Spi > 30%), low abundant (30% < Spi > 10%), sporadic (Spi < 10%).

Supplementary data 5 Rarefaction curve for the richness of freshwater snails collected in the Lençóis Maranhenses Microregion in the period of June 2016 to November 2019.

Supplementary data 6 Algorithms performance AUC and TSS.

Acknowledgements

All authors would like to thank the anonymous reviewers for all of their valuable comments and remarks that contributed to the improvement of this manuscript.

The project was suported by CBIOMA-2017 EDITAL FAPEMA Nº 013/2017 - APOIO À COLEÇÕES BIOLÓGICAS E ARQUEOLÓGICAS DO MARANHÃO–COLEÇÕES BIOLÓGICAS of Fundação de Amparo a Pesquisa e ao Desenvolvimento Científico do Maranhão - FAPEMA. M C M Carvalho was supported by a Master's scholarship FAPEMA.

All research pertaining to this article was authorized by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA, License nº 53224.

References

• AGUDO-PADRÓN, A.I., AD-VÍNCULA VEADO, R.W. and SAALFELD, K., 2013. Moluscos e saúde pública em Santa Catarina: subsídios para a formulação estadual de políticas preventivas sanitaristas. 1ª ed. Duque de Caxias: Espaço Científico Livre Projetos Editoriais, 132 p.
• ALMEIDA, P.R.S., NASCIMENTO FILHO, S.L. and VIANA, G.F.S., 2018. Effects of invasive species snails in continental aquatic bodies of Pernambucano semiarid. Acta Limnologica Brasiliensia, vol. 30, no. 573, pp. 1-10. http://doi.org/10.1590/s2179-975x10616
  » http://doi.org/10.1590/s2179-975x10616
• AMARAL, Y.T., SANTOS, E.M., RIBEIRO, M.C. and BARRETO, L., 2019. Landscape structural analysis of the Lençóis Maranhenses national park: implications for conservation. Journal for Nature Conservation, vol. 51, pp. 125725. http://doi.org/10.1016/j.jnc.2019.125725
  » http://doi.org/10.1016/j.jnc.2019.125725
• AMARAL, Y.T., 2018. Avaliação dos impactos antropogênicos sobre a estrutura da paisagem do Parque Nacional dos Lençóis Maranhenses. São Luís: Universidade Federal do Maranhão, 95 p. Dissertação de Mestrado em Biodiversidade Conservação.
• ARAÚJO, T.D., 2015. Análise espaço-temporal dos Lençóis Maranhenses com o uso de imagens de satélite para o planejamento ambiental. Porto Alegre: Universidade Federal do Rio Grande do Sul, 105 p. Dissertação de Mestrado em Sensoriamento Remoto.
• ARAUJO, M. and NEW, M., 2007. New M. Ensemble forecasting of species distributions. Trends in Ecology and Evolution, vol. 22, no. 1, pp. 42-47. https://doi.org/10.1016/j.tree.2006.09.010
  » https://doi.org/10.1016/j.tree.2006.09.010
• BARBOSA, C.S., SANTOS, R.S., GOMES, E.S., ARAÚJO, K., ALBUQUERQUE, J., MELO, F., SEVILHA, M.A., BRASILEIRO, D., BARRETO, M.I., LEAL NETO, O.B., BARBOSA, V., CORREIA, W. and GUIMARÃES, R.J.P.S., 2014a. Epidemiologia da Esquistossomose no litoral de Pernambuco. Revista de Patologia Tropical, vol. 43, no. 4, pp. 436-445. http://doi.org/10.5216/rpt.v43i4.33607
  » http://doi.org/10.5216/rpt.v43i4.33607
• BARBOSA, C.S., BARBOSA, F.S. and ARRUDA, F., 1993. Long-term controlled field experiment on the competition between two species of Biomphalaria (Mollusca, Basommatophora), the snail vectors of Schistosoma mansoni in Northeastern Brazil. Cadernos de Saude Publica, vol. 9, no. 2, pp. 170-176. http://doi.org/10.1590/S0102-311X1993000200008 PMid:15448838.
  » http://doi.org/10.1590/S0102-311X1993000200008
• BARBOSA, C.S., BARBOSA, V.S., NASCIMENTO, W.C., PIERI, O.S. and ARAÚJO, K.C.G.M., 2014b. Spatial displacement of Biomphalaria glabrata by Biomphalaria straminea, snail hosts of Schistosoma mansoni, in Itamaracá Island north east Brazil. Geospatial Health, vol. 8, no. 2, pp. 345-351. http://doi.org/10.4081/gh.2014.24 PMid:24893012.
  » http://doi.org/10.4081/gh.2014.24
• BARBOSA, F.S., PINTO, H.A. and MELO, A.L., 2011. Biomphalaria straminea (Mollusca: Planorbidae) como hospedeiro intermediário de Zygocotyle lunata (Trematoda: Zygocotylidae) no Brasil. Neotropical Helminthology, vol. 5, no. 2, pp. 241-246. http://doi.org/10.24039/rnh2011521081
  » http://doi.org/10.24039/rnh2011521081
• BARBOSA, V.S., GUIMARÃES, R.J.P.S., LOYO, R.M. and BARBOSA, C.S., 2016. Modelling of the distribution of Biomphalaria glabrata and Biomphalaria straminea in the metropolitan region of Recife, Pernambuco, Brazil. Geospatial Health, vol. 11, no. 3, pp. 490. http://doi.org/10.4081/gh.2016.490 PMid:27903064.
  » http://doi.org/10.4081/gh.2016.490
• BEZERRA, D.S.B., DIAS, B.C.C., RODRIGUES, L.H.S., TOMAZ, R.B. and SANTOS, A.L.S., 2018. Análise dos focos de queimadas e seus impactos no Maranhão durante eventos de estiagem no período de 1988 à 2016. Revista Brasileira de Climatologia, vol. 22, pp. 446-462. http://doi.org/10.5380/abclima.v22i0.57337
  » http://doi.org/10.5380/abclima.v22i0.57337
• BRASIL, 1981. Decreto nº 86.080, de 2 de junho de 1981. Cria, no Estado do Maranhão, o Parque Nacional dos Lençóis Maranhenses, com os limites que especifica e dá outras providências Diário Oficial da União, Brasília, 4 jun.
• BUENO, B.A.A., 2012. Ecological niche modeling applied to the conservation of Brazilian Merganser (Mergus octosetaceus, Vieillot, 1817) in Brazil. Uberlândia: Universidade Federal de Uberlândia, 113 p. Dissertação de Mestrado em Ciências Biológicas.
• BUSS, D.F., BAPTISTA, D.F.M.P., NESSIMIAN, J.L. and DORVILLÉ, L.F.M., 2002. Influence of water chemistry and environmental degradation on macroinvertebrate assemblage in a stream basin in Southeast Brazil. Hydrobiologia, vol. 481, no. 82, pp. 299-305.
• CAMARGO, M. and GIARRIZZO, T., 2009. Biological parameters. In: M. CAMARGO and R. GHILARDI JUNIOR, eds. Entre a terra, as águas, e os pescadores do médio Rio Xingu: uma abordagem ecológica. Belém: Eletronorte, pp. 215-231.
• CANTANHEDE, S.P.D., 2015. Gastrópodes límnicos e helmintofauna associada da Microrregião da Baixada Maranhense, MA, com ênfase nos transmissores da esquistossomose Rio de Janeiro: Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 211 p. Tese de Doutorado em Biodiversidade e Saúde.
• CARVALHO, J.C.A., 2005. Desenvolvimento Sustentável e Turismo: o caso dos Lençóis Maranhenses. Rio de Janeiro: Fundação Getúlio Vargas, 168 p. Dissertação de Mestrado em Administração Pública.
• CARVALHO, O.S., AMARAL, R.S., DUTRA, L.V., SCHOLTE, R.G.C. and GUERRA, M.A.M., 2008. Distribuição espacial de Biomphalaria glabrata, B. straminea e B. tenagophila, hospedeiros intermediários do Schistosoma mansoni no Brasil. In: O.S. CARVALHO, P.M.Z. COELHO and H. LENZI, eds. Schistosoma mansoni & Esquistossomose: uma visão multidisciplinar. Rio de Janeiro: Editora Fiocruz, pp. 393-418. http://doi.org/10.7476/9788575413708
  » http://doi.org/10.7476/9788575413708
• CAVALCANTI, E.A.H. and LARRAZÁBAL, M.E.L., 2004. Macrozzoplâncton da zona econômica exclusiva do Nordeste do Brasil (segunda expedição oceanográfica – REVIZEE/NE II) com ênfase em Copepoda (Crustacea). Revista Brasileira de Zoologia, vol. 21, no. 3, pp. 467-475. http://doi.org/10.1590/S0101-81752004000300008
  » http://doi.org/10.1590/S0101-81752004000300008
• COLLEY, E., SIMONE, L.R.L. and SILVA, J.L., 2012. Uma viagem pela história da Malacologia. Revista Estudos de Biologia: Ambiente e Diversidade, vol. 34, no. 83, pp. 175-190. http://doi.org/10.7213/estud.biol.7331
  » http://doi.org/10.7213/estud.biol.7331
• DAJOZ, R., 1983. Ecologia geral 4ª ed. Petrópolis: Vozes, 472 p.
• DAVID, N.F., CANTANHEDE, S.P.D., MONROE, N.B., PEREIRA, L.P.L.A., SILVA-SOUZA, N., ABREU-SILVA, A.L., OLIVEIRA, V.M. and TCHAICKA, L., 2018. Spatial distribution and seasonality of Biomphalaria spp. in São Luís (Maranhão, Brazil). Parasitology Research, vol. 117, no. 5, pp. 1495-1502. http://doi.org/10.1007/s00436-018-5810-1 PMid:29551000.
  » http://doi.org/10.1007/s00436-018-5810-1
• DIAS, R., 2003. Turismo sustentável e meio ambiente São Paulo: Atlas, 208 p.
• SANTOS, S.R. and BAHL, M., 2017 [viewed 17 January 2023]. Percepção e intervenções turísticas na paisagem natural do Parque Nacional dos Lençóis Maranhenses (Maranhão, Brasil). Ateliê do Turismo [online], vol. 1, no. 1, pp. 1-23. Available from: https://periodicos.ufms.br/index.php/adturismo/article/view/5336
  » https://periodicos.ufms.br/index.php/adturismo/article/view/5336
• DRÜGG-HAHN, S., 1997. Potencial de atuação de Heleobia piscium (Orbigny, 1835) (Molusco, Hydrobiidae) como hospedeiro intermediário de Nocotylidaem (Platyhelminthes, Trematoda), no RS. Porto Alegre: Universidade Federal do Rio Grande do Sul, 78 p. Dissertação de Mestrado em Biologia Animal.
• ELITH, J., GRAHAM, H., ANDERSON, R., DUDÍK, M., FERRIER, S., GUISAN, A., HIJMANS, R., HUETTMANN, F., LEATHWICK, J., LEHMANN, A., LI, J., LOHMANN, L., LOISELLE, B., MANION, G., MORITZ, C., NAKAMURA, M., NAKAZAWA, Y., OVERTON, J., PHILLIPS, S., RICHARDSON, K., SCACHETTI-PEREIRA, R., SCHAPIRE, R., SOBERÓN, J., WILLIAMS, S., WISZ, M. and ZIMMERMANN, N., 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography, vol. 29, pp. 129-151. http://doi.org/10.1111/j.2006.0906-7590.04596.x
  » http://doi.org/10.1111/j.2006.0906-7590.04596.x
• FERNANDEZ, M.A., 2011. Variação espaço-temporal da malacofauna límnica em dois reservatórios no rio Tocantins, com ênfase na transmissão da esquistossomose, no período entre junho de 2004 e outubro de 2010 Rio de Janeiro: Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 184 p. Tese de Doutorado em Biologia Parasitária.
• FERNANDEZ, M.A., THIENGO, S.C. and AMARAL, R.S., 2008. Técnicas malacológicas. In: R.S. AMARAL, S.C. THIENGO and O.S. PIERI, eds. Vigilância e controle de moluscos de moluscos de importância médica: diretrizes técnicas Brasília: Secretaria de Vigilância em Saúde, Ministério da Saúde, pp. 43-70.
• FERNANDEZ, M.A., THIENGO, S.C. and PARAENSE, W.L., 2006. Primeiro registro de Plesiophysa guadeloupensis ("Fischer" Mazé) no Estado do Rio de Janeiro, Brasil. Revista Brasileira de Zoologia, vol. 23, no. 3, pp. 883-885. https://doi.org/10.1590/S0101-81752006000300037
  » https://doi.org/10.1590/S0101-81752006000300037
• FUKUDA, H., HAGA, T. and TATARA, Y., 2008. Niku-nuki: a useful method for anatomical and DNA studies on shell-bearing molluscs. Zoosymposia, vol. 1, pp. 15-38. http://doi.org/10.11646/zoosymposia.1.1.5
  » http://doi.org/10.11646/zoosymposia.1.1.5
• GUIMARÃES, R.J., FREITAS, C.C., OLIVEIRA, G., DUTRA, L.V. and CARVALHO, O.S., 2013. Multiple regression for the schistosomiasis positivity index estimates in the Minas Gerais State-Brazil at small communities and cities levels. In: R. EL RIDI, ed. Parasitic diseases: Schistosomiasis. Crotia: InTech, pp. 3-26. http://doi.org/10.5772/53500
  » http://doi.org/10.5772/53500
• GUISAN, A. and ZIMMERMANN, N.E., 2000. Predictive habitat distribution models in ecology. Ecological Modelling, vol. 135, no. 2, pp. 147-186. http://doi.org/10.1016/S0304-3800(00)00354-9
  » http://doi.org/10.1016/S0304-3800(00)00354-9
• HAYES, K.A., COWIE, R.H. and THIENGO, S.C., 2009. A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biological Journal of the Linnean Society. Linnean Society of London, vol. 98, no. 1, pp. 61-76. http://doi.org/10.1111/j.1095-8312.2009.01246.x
  » http://doi.org/10.1111/j.1095-8312.2009.01246.x
• INSTITUTO BRASILEIRO DO MEIO AMBIENTE E DOS RECURSOS NATURAIS RENOVÁVEIS – IBAMA, 2003 [viewed 17 January 2023]. Plano de manejo do Parque Nacional dos Lençóis Maranhense [online]. Available from: https://www.icmbio.gov.br/parnalencoismaranhenses/planos-de-manejo.html
  » https://www.icmbio.gov.br/parnalencoismaranhenses/planos-de-manejo.html
• INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA – IBGE, 2010 [viewed 17 January 2023]. Síntese de indicadores sociais: uma análise das condições de vida da população brasileira [online]. Available from: https://censo2010.ibge.gov.br/resultados.html
  » https://censo2010.ibge.gov.br/resultados.html
• INSTITUTO INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE – ICMBIO, 2020 [viewed 17 January 2023]. National Parks of Brazil [online]. Available from: https://dados.gov.br/organization/a144dc5c-3a194630a65f8484dc46e844?tags=Parque+Nacional
  » https://dados.gov.br/organization/a144dc5c-3a194630a65f8484dc46e844?tags=Parque+Nacional
• INSTITUTO MARANHENSE DE ESTUDOS SOCIOECONÔMICOS E CARTOGRÁFICOS – IMESC, 2013 [viewed 20 January 2023]. Situação ambiental da Região dos Lençóis Maranhenses [online]. São Luís. Available from: https://imesc.ma.gov.br/portal/Post/show/situacao-ambiental
  » https://imesc.ma.gov.br/portal/Post/show/situacao-ambiental
• INSTITUTO MARANHENSE DE ESTUDOS SOCIOECONÔMICOS E CARTOGRÁFICOS – IMESC, 2020 [viewed 20 January 2023]. Enciclopédia dos Municípios Maranhenses: Lençóis Maranhenses [online]. São Luís: IMESC, vol. 5. Available from: https://imesc.ma.gov.br/portal/Post/show/enciclopedia-dos-municipios
  » https://imesc.ma.gov.br/portal/Post/show/enciclopedia-dos-municipios
• KOSTADINOVA, A. and GIBSON, D.I., 2000. The systematics of the echinostomes. In: B. FRIED and T.K. GRACZYK, eds. Echinostomes as experimental models for biological research Dordreched: Kluwer, pp. 31-57. http://doi.org/10.1007/978-94-015-9606-0_2
  » http://doi.org/10.1007/978-94-015-9606-0_2
• KOSTADINOVA, A., 2005. Familia Echinostomatidae Looss, 1899. In: A. JONES, R.A. BRAY and D.I. GIBSON, eds. Keys to the Trematoda. London: CBI Publishing and The Natural History Museum, vol. 2, pp. 9-64.
• KOTZIAN, C.B. and AMARAL, A.M.B., 2013. Diversity and distribution of mollusks along the Contas River in a tropical semiarid region (Caatinga), Northeastern Brazil. Biota Neotropica, vol. 13, no. 4, pp. 299-314. http://doi.org/10.1590/S1676-06032013000400027
  » http://doi.org/10.1590/S1676-06032013000400027
• MARANHÃO, 2003. Zoneamento Costeiro do Estado do Maranhão São Luís: Fundação Sousândrade de Apoio e Desenvolvimento, Universidade Federal do Maranhão/IICA/GEAGRO/LABOHIDRO, 242 p.
• MELO, I.F.L., 2018. Levantamento da malacofauna límnica e helmintofauna associada aos moluscos dulcícolas do município de Nossa Senhora de Lourdes, Sergipe. Sergipe: Universidade Federal de Sergipe, 88 p. Dissertação de Mestrado em Biologia Parasitária.
• MEYER, C., WEIGELT, P. and KREFT, H., 2016. Multidimensional biases, gaps and uncertainties in global plant occurrence information. Ecology Letters, vol. 19, no. 8, pp. 992-1006. http://doi.org/10.1111/ele.12624 PMid:27250865.
  » http://doi.org/10.1111/ele.12624
• MIRANDA, G.S., RODRIGUES, J.G.M., LIRA, M.G.S., NOGUEIRA, R.A., GOMES, G.C.C., MIRANDA, B.S., ARAÚJO, A.D. and SILVA-SOUZA, N., 2016. Moluscos límnicos como hospedeiros de trematódeos digenéticos de uma região metropolitana da ilha do Maranhão, Brasil. Scientia Plena, vol. 12, no. 9, pp. 1-11. http://doi.org/10.14808/sci.plena.2016.091004
  » http://doi.org/10.14808/sci.plena.2016.091004
• MUÑOZ FLORES, J.C., 2008 [viewed 9 February 2024]. El turismo en los espacios naturales protegidos españoles, algo más que una moda reciente. Boletín de la Asociación de Geógrafos Españoles [online], vol. 46, pp. 291-304. Available from: https://www.researchgate.net/publication/40669967_El_turismo_en_los_espacios_naturales_protegidos_espanoles_algo_mas_que_una_moda_reciente
  » https://www.researchgate.net/publication/40669967_El_turismo_en_los_espacios_naturales_protegidos_espanoles_algo_mas_que_una_moda_reciente
• NABOUT, J.C., MARCO JÚNIOR, P., BINI, L.M. and DINIZ-FILHO, J.A.F., 2009. Distribuição geográfica potencial de espécies americanas do caranguejo” violinista” (Uca spp.) (Crustacea, Decapoda) com base em modelagem de nicho ecológico. Iheringia. Série Zoologia, vol. 99, no. 1, pp. 92-98. http://doi.org/10.1590/S0073-47212009000100013
  » http://doi.org/10.1590/S0073-47212009000100013
• NORONHA, G.S. and ARAÚJO, J.L.L., 2017. Gestão ambiental das hospedagens domiciliares de Santo Amaro do Maranhão-Parque Nacional dos Lençóis Maranhenses. Caderno Virtual de Turismo, vol. 17, no. 2, pp. 64-79. http://doi.org/10.18472/cvt.17n2.2017.1089
  » http://doi.org/10.18472/cvt.17n2.2017.1089
• OHLWEILER, F.P., TAKAHASHI, F.Y., GUIMARÃES, M.C.A., GOMES, S.R. and KAWANO, T., 2010. Manual de gastrópodes límnicos e terrestres do Estado de São Paulo associados às helmintoses Porto Alegre: Redes, 224 p.
• OLIVEIRA, F.S., RIBEIRO, M.H.M., NUNEZ, C.V. and ALBUQUERQUE, P.M.C., 2016. Flowering phenology of Mouriri guianensis (Melastomataceae) and its interaction with the crepuscular bee Megalopta amoena (Halictidae) in the restinga of Lençóis Maranhenses National Park, Brazil. Acta Amazonica, vol. 46, no. 3, pp. 281-290. http://doi.org/10.1590/1809-4392201504853
  » http://doi.org/10.1590/1809-4392201504853
• ORTEGA-HUERTA, M.A. and TOWNSEND PETERSON, A., 2008. Modeling ecological niches and predicting geographic distributions: a test of six presence-only methods. Revista Mexicana de Biodiversidad, vol. 79, no. 1, pp. 205-216.
• PALASIO, R.G.S., CASOTTI, M.O., RODRIGUES, T.C., MENEZES, R.M.T., ZANOTTI-MAGALHAES, E.M. and TUAN, R., 2015. The current distribution pattern of Biomphalaria tenagophila and Biomphalaria straminea in the northern and southern regions of the coastal fluvial plain in the state of São Paulo. Biota Neotropica, vol. 15, no. 3, e20140153. http://doi.org/10.1590/1676-06032015015314
  » http://doi.org/10.1590/1676-06032015015314
• PALASIO, R.G.S., XAVIER, I.G., CHIARAVALOTTI-NETO, F. and TUAN, R., 2019. Diversity of Biomphalaria spp. freshwater snails and associated mollusks in areas with schistosomiasis risk, using molecular and spatial analysis tools. Biota Neotropica, vol. 19, no. 4, e20190746. http://doi.org/10.1590/1676-0611-bn-2019-0746
  » http://doi.org/10.1590/1676-0611-bn-2019-0746
• PASQUEVICH, M.Y., DREON, M.S. and HERAS, H., 2014. The major egg reserve protein from the invasive apple snail Pomacea maculata is a complex carotenoprotein related to those of Pomacea canaliculata and Pomacea scalaris Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, vol. 169, pp. 63-71. http://doi.org/10.1016/j.cbpb.2013.11.008 PMid:24291422.
  » http://doi.org/10.1016/j.cbpb.2013.11.008
• PERISSINOTTO, R., MIRANDA, N.A., RAW, J.L. and PEER, N., 2014. Biodiversity census of lake St Lucia, iSimangaliso Wetland Park (South Africa): gastropod molluscs. ZooKeys, vol. 43, no. 440, pp. 1-43. http://doi.org/10.3897/zookeys.440.7803 PMid:25317060.
  » http://doi.org/10.3897/zookeys.440.7803
• PETERSON, A.T., 2006. Uses and requirements of ecological niche models and related distributional models. Biodiversity Informatics, vol. 3, pp. 59-72. http://doi.org/10.17161/bi.v3i0.29
  » http://doi.org/10.17161/bi.v3i0.29
• PINTO, H.A., BRANT, S.V. and DE MELO, A.L., 2014. Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Tropica, vol. 138, pp. 38-43. http://doi.org/10.1016/j.actatropica.2014.06.002 PMid:24931284.
  » http://doi.org/10.1016/j.actatropica.2014.06.002
• PINTO, H.A., CANTANHEDE, S.P.D., THIENGO, S.C., MELO, A.L. and FERNANDEZ, M.A., 2015. The apple snail Pomacea maculata (Caenogastropoda: Ampullariidae) as the intermediate host of Stomylotrema gratiosus (Trematoda: Stomylotrematidae) in Brazil: the first report of a mollusc host of a stomylotrematid trematode. The Journal of Parasitology, vol. 101, no. 2, pp. 134-139. http://doi.org/10.1645/14-659.1 PMid:25559320.
  » http://doi.org/10.1645/14-659.1
• PINTO, H.A. and MELO, A.L., 2012. Physa marmorata (Molusca: Physidae) as intermediate host of Echinostoma exile (Trematoda: Echinostomatidae) in Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 291-299. http://doi.org/10.24039/rnh2012621020 PMid:24931284.
  » http://doi.org/10.24039/rnh2012621020
• POMBO, V.B. 2016. Moluscos límnicos. In: A.O. LATINI, D.C. RESENDE, V.B. POMBO and L. CORADIN, eds. Espécies exóticas invasoras de águas continentais no Brasil Brasília: Ministério do Meio Ambiente, pp. 123-231.
• QVARNSTROM, Y., BISHOP, H.S. and DA SILVA, A.J., 2013. Detection of rat lungworm in intermediate, definitive, and paratenic hosts obtained from environmental sources. Hawai’i Journal of Medicine & Public Health: a Journal of Asia Pacific Medicine & Public Health, vol. 72, no. 6, suppl. 2, pp. 63-69. PMid:23901387.
• RENNÓ, C.D., NOBRE, A.D., CUARTAS, L.A., SOARES, J.V., HODNETT, M.G., TOMASELLA, J. and WATERLOO, M.J., 2008. HAND, a new terrain descriptor using SRTM-DEM: mapping terra-firme rainforest environments in Amazonia. Remote Sensing of Environment, vol. 112, no. 9, pp. 3469-3481. http://doi.org/10.1016/j.rse.2008.03.018
  » http://doi.org/10.1016/j.rse.2008.03.018
• REY, L., 2001. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na África. In: L. REY, ed. Parasitologia: parasitos e doenças parasitárias do homem nas Américas e na África. Rio de Janeiro: Guanabara Koogan, 856 p.
• SALVADOR, G.N., GARCIA RISTAU, N., SANCHES DA SILVA, I. and NUNES, A.V., 2019. First record of Wild Boar (Sus scrofa Linnaeus, 1758) in Lençóis Maranhenses National Park, Maranhão state, northern Brazil. Check List, vol. 15, no. 5, pp. 915-919. http://doi.org/10.15560/15.5.915
  » http://doi.org/10.15560/15.5.915
• SANTOS, A.M. and MELO, A.C.F.L., 2011. Prevalência da esquistossomose num povoado do Município de Tutóia, Estado do Maranhão. Revista da Sociedade Brasileira de Medicina Tropical, vol. 44, no. 1, pp. 97-99. http://doi.org/10.1590/S0037-86822011000100021 PMid:21340417.
  » http://doi.org/10.1590/S0037-86822011000100021
• SANTOS, M.R. and MAIA, R.C., 2018. Padrões de distribuição e abundância de gastrópodes límnicos no município de Acaraú, Ceará: avaliando aspectos da Teoria da Biogeografia de Ilhas. Biotemas, vol. 31, no. 4, pp. 35-46. http://doi.org/10.5007/2175-7925.2018v31n4p35
  » http://doi.org/10.5007/2175-7925.2018v31n4p35
• SARANIA, B., DEVI, A., KUMAR, A., SARMA, K. and GUPTA, A.K., 2017. Predictive distribution modeling and population status of the endangered Macaca munzalain Arunachal Pradesh, India. American Journal of Primatology, vol. 79, no. 2, e22592. http://doi.org/10.1002/ajp.22592 PMid:27643565.
  » http://doi.org/10.1002/ajp.22592
• SCHOLTE, R.G., CARVALHO, O.S., MALONE, J.B., UTZINGER, J. and VOUNATSOU, P., 2012. Spatial distribution of Biomphalaria spp., the intermediate host snails of Schistosoma mansoni in Brazil. Geospatial Health, vol. 6, no. 3, pp. 95-101. http://doi.org/10.4081/gh.2012.127 PMid:23032289.
  » http://doi.org/10.4081/gh.2012.127
• SILVA, E.L., ROCHA, A.J., LEAL, M.F., SANTOS, O., SOUSA, J.H., SILVA, A.R.V., DANTAS, K.K.S., RULIM, E.M.M., CASTRO, E.S., PACHECO, A.C.L. and PINHEIRO, T.G., 2020. Freshwater mollusks from three reservoirs of Piauí, northeastern Brazil. Biota Neotropica, vol. 20, no. 1, e20190868. http://doi.org/10.1590/1676-0611-bn-2019-0868
  » http://doi.org/10.1590/1676-0611-bn-2019-0868
• SOUSA, K.R., 2015. Economia extrativa da fibra de buriti (Mauritia flexuosa) para o desenvolvimento sustentável da microrregião dos Lençóis Maranhenses, MA na atualidade. São Luís: Universidade Federal do Maranhão, 99 p. Dissertação de Mestrado em Desenvolvimento Socioeconômico.
• SOUZA DOS SANTOS, J.H. and SANTOS, N.F.B. 2015. The Lençóis Maranhenses: a paradise of dunes and ponds. In: B. VIEIRA, A. SALGADO and L. SANTOS, eds. Landscapes and Landforms of Brazil. Dordrecht: Springer, pp. 79-90. World Geomorphological Landscapes. http://doi.org/10.1007/978-94-017-8023-0_8
  » http://doi.org/10.1007/978-94-017-8023-0_8
• SOUZA, M.A.A., BARBOSA, V.S., ALBUQUERQUE, J.O., BOCANEGRA, S., SOUZA-SANTOS, R., PAREDES, H. and BARBOSA, C.S., 2010. Aspectos ecológicos e levantamento malacológico para identificação de áreas de risco para transmissão da esquistossomose mansoni no litoral norte de Pernambuco, Brasil. Iheringia. Série Zoologia, vol. 100, no. 1, pp. 19-24. http://doi.org/10.1590/S0073-47212010000100003
  » http://doi.org/10.1590/S0073-47212010000100003
• SPYRA, A. and CIEPLOK, A., 2022. Structure and dynamics of gastropod communities in highly transformed aquatic environments colonized and uncolonized by globally invasive Potamopyrgus antipodarum (Gray, 1843). Aquatic Invasions, vol. 17, no. 3, pp. 431-452. http://doi.org/10.3391/ai.2022.17.3.07
  » http://doi.org/10.3391/ai.2022.17.3.07
• STENSGAARD, A., JØRGENSEN, A., KABATAREINE, N., MALONE, J.B. and KRISTENSEN, T.K., 2005. Modeling the distribution of Schistosoma mansoni and host snails in Uganda using satellite sensor data and geographical information systems. Parassitologia, vol. 47, no. 1, pp. 115-125. PMid:16044680.
• STRONG, E.E., GARGOMINY, O., PONDER, W.F. and BOUCHET, P., 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 149-166. http://doi.org/10.1007/s10750-007-9012-6
  » http://doi.org/10.1007/s10750-007-9012-6
• TAMBO, E., AI, L., ZHOU, X., CHEN, J.-H., HU, W., BERGQUIST, R., GUO, J.-G., UTZINGER, J., TANNER, M. and ZHOU, X.-N., 2014. Surveillance-response systems: the key to elimination of tropical diseases. Infectious Diseases of Poverty, vol. 3, no. 1, pp. 1-11. http://doi.org/10.1186/2049-9957-3-17 PMid:24401663.
  » http://doi.org/10.1186/2049-9957-3-17
• TEEM, J.L., QVARNSTROM, Y., BISHOP, H.S., DA SILVA, A.J., CARTER, J., WHITE-MCLEAN, J. and SMITH, T., 2013. The occurrence of the rat lungworm, Angiostrongylus cantonensis, innonindigenous snails in the Gulf of Mexico region of the United States. Hawai’i Journal of Medicine & Public Health : a Journal of Asia Pacific Medicine & Public Health, vol. 72, no. 6, suppl. 2, pp. 11-14. PMid:23901374.
• TELES, R.M.S., 2001. Turismo e meio ambiente ou turismo de natureza? Alguns apontamentos para organização. In: R.M.S. TELES, ed. Turismo e meio ambiente Rio de Janeiro: Elsevier.
• TIBIRIÇA, S.H.C., BESSA, E.C.A., MITTHEROFHE, A., CASTRO, M.F.D., CARVALHO, O.D.S., CALDEIRA, R.L., PASSOS, L.K., MATTOS, A.M.M., PINHEIRO, L.S., SILVA, D.S., BASTOS, F.O., ANDREOLI, G.Q., BONATO, G.R. and COIMBRA, E.S., 2006. Biomphalaria spp. (Preston, 1910) snails in the municipality of Juiz de Fora, Zona da Mata Mineira mesoregion, ate of Minas Gerais, Brazil. Memorias do Instituto Oswaldo Cruz, vol. 101, no. 1, suppl. 1, pp. 179-184. http://doi.org/10.1590/S0074-02762006000900028 PMid:17308767.
  » http://doi.org/10.1590/S0074-02762006000900028
• YANG, Y., CHENG, W., WU, X., HUANG, S., DENG, Z., ZENG, X., YUAN, D., YANG, Y., WU, Z., CHEN, Y., ZHOU, Y. and JIANG, Q., 2018. Prediction of the potential global distribution for Biomphalaria straminea, an intermediate host for Schistosoma mansoni PLoS Neglected Tropical Diseases, vol. 12, no. 5, e0006548. http://doi.org/10.1371/journal.pntd.0006548 PMid:29813073.
  » http://doi.org/10.1371/journal.pntd.0006548

Publication Dates

• Publication in this collection
  14 Oct 2024
• Date of issue
  2024

History

• Received
  09 Feb 2024
• Accepted
  24 June 2024