A malacological survey in the Manso Power Plant, State of Mato Grosso, Brazil: new records of freshwater snails, including transmitters of schistosomiasis and exotic species

Introduction: Schistosomiasis is a parasitic disease of public health concern in Brazil, and the construction of hydroelectric dams, in addition to increasing permanent human settlement and tourism, has created conditions suitable for the establishment of mollusks that can transmit schistosomiasis. Such areas require a number of actions to prevent the establishment of schistosomiasis. This paper reports on a freshwater malacological survey carried out in the geographical area of the Manso Power Plant. Methods: Mollusks were collected in 18 municipalities in the State of Mato Grosso between February 2002 and February 2004 (qualitative study) and from April 2009 to February 2011 (quantitative study). Results: Thirty-one species of mollusks were collected, including newly recorded species (Antillorbis nordestensis and Burnupia ingae). In addition, the geographic distributions of known species, including Biomphalaria straminea, a snail vector of Schistosoma mansoni, were expanded. A total of 4,507 specimens were collected in the APM Manso reservoir (Usina Hidrelétrica de Aproveitamento Múltiplo de Manso) during the quantitative study, and Biomphalaria amazonica was found in six of the 10 localities analyzed. The Afroasiatic species Melanoides tuberculata, introduced after February 2009, was the dominant species (relative abundance 94.96%). Conclusions: The study area is epidemiologically important due to the occurrence of B. straminea and B. amazonica, which are vectors of schistosomiasis, and M. tuberculata, a snail host of Centrocestus formosanus, which is responsible for centrocestiasis transmission. Observations of M. tuberculata and the exotic freshwater clams Corbicula fluminea and Corbicula largillierti raise concerns about biodiversity.

Schistosomiasis is an important endemic disease associated with environmental changes caused by major economic development projects, such as the construction of hydroelectric power facilities (dams and lakes created by dams) [1][2][3][4] .The difficulty in predicting emerging outbreaks of schistosomiasis associated with these types of projects, and the existence of conditions unique to particular projects, require studies in each particular locality to implement appropriate preventive measures.The energy matrix of Brazil utilizes hydroelectric power 5 , and the increasing number of dams being built throughout the country is problematic because these dams create conditions suitable for the establishment of mollusk vectors of schistosomiasis and lead to increased permanent human settlement and tourism 6,7 .
Environmental changes caused by dams affect water quality, produce eutrophic effects, and alter the hydrological pattern and ecological dynamics of the rivers and basins 8 .Despite the effects of dams on the richness of the fauna, species density, and other aspects of biodiversity, longitudinal studies of invertebrate fauna in dam areas are still scarce in Brazil.In qualitative study carried out between 1997 and 2004 in the geographical area of the Serra da Mesa Power Plant, State of Goiás, Thiengo et al. 9 noted the spread of the schistosomiasis vector Biomphalaria straminea (Dunker, 1848) and the exotic snail Melanoides tuberculata (Müller, 1774), as well as a reduction in the local species Gundlachia ticaga (Marcus & Marcus, 1962) and Aylacostoma tenuilabris (Reeve, 1860).In the Itabapoana River, between the States of Rio de Janeiro and Espírito Santo, an increase in the population of Biomphalaria tenagophila (d'Orbigny, 1835) was observed in the geographical area of the Rosal Power Plant during the construction phase, mainly due to the change from a lotic to a lentic ecosystem and the eutrophication of the water 4 .
Since 1986, Brazilian environmental laws have required the development of preventive measures to minimize the environmental impact of dams and avoid new foci of endemic disease caused by impoundments.The possibility of introducing Between April 2009 and October 2010, the abundance of species in APM Manso was evaluated every two months in 10 sampling stations (quantitative study) distributed in the major rivers of the reservoir (Figure 1) and georeferenced: two locations in the Manso River [(1) = 14 o 49'06"S, 55 o 37'02"W; In the Laboratório de Malacologia of Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, State of Rio de Janeiro, the specimens were placed in aquaria containing dechlorinated tap water with a thin bottom layer of a 2:1 mixture of screened soil and ground oyster shells as a source of mineral nutrients.For species identification, the snails were anesthetized in Hypnol 0.05% solution (Cristália -Produtos Químicos e Farmacêuticos LTDA, Itapira, São Paulo) for five hours, killed using hot water (70°C) and fixed in Railliet-Henry solution 16 .

Municipalities
The quantitative study carried out in APM Manso revealed the occurrence of mollusks in all the surveyed localities during the dry season (from June to November).M. tuberculata was obtained in all the searches (Table 3).Three species were found only once: Considering the occurrence of species in 18 municipalities, the most frequently found Biomphalaria species was B. occidentalis, occurring in twelve municipalities, followed by B. amazonica and B. straminea.The most frequently found Caenogastropoda species were P. maculata and Pomacea sp., followed by Melanoides tuberculata, which was found in five municipalities.Samples of P. scalaris and Idiopyrgus sp. were found only in the municipalities of Várzea Grande and Rosário Oeste, respectively.
A total of 4,507 specimens were collected in the quantitative study; M. tuberculata was the most common, comprising 94.96% of the overall population.The most representative species was G. radiata, followed by M. tuberculata and B. amazonica, found in six (60%) and seven (70%) sampling stations, respectively (Table 4).In the qualitative study, G. radiata was also the most frequent species, found in 41 out of the 104 surveyed localities in eight municipalities.Among the planorbids, D. anatinum was the most widespread in the study area (36 localities in six municipalities) from 2002 to 2004; in the quantitative study, D. anatinum was only found in two areas (stations 3 and 9).The most common species found at the APM Manso reservoir between 2002 and 2004 was D. anatinum, which was collected from 25 out of the 31 surveyed localities (27 in the Chapada dos Guimarães and four in Nova Brasilândia); the next most common species found was G. radiata (23 localities).

DIsCUssION
The study area is epidemiologically important due to the environmental effects of the APM Manso project and the occurrence of B. straminea and B. amazonica in State of Mato Grosso.Additionally, from a medical standpoint, the abundance of M. tuberculata in the study area is a matter of concern.This exotic species, which is a natural host of Centrocestus formosanus (Nishigori, 1924) in Brazil 17 , is responsible for centrocestiasis transmission.The biological interaction between M. tuberculata and C. formosanus has previously been found in China, Colombia, India, Iran, Japan, Malaysia, Mexico, Taiwan, the United States and Venezuela 18 .Human transmission has already been reported in Asia and occurs through the ingestion of fish that are infected with metacercariae, a larval stage that develops after the fish is exposed to Pleurolophocercous cercaria eliminated by infected snails.This type of cercariae, most likely C. formosanus, has also been obtained in specimens of M. tuberculata collected in the Manso River 19 .6), ( 8), ( 9) and ( 10)]; Quilombo River [ (7)] and in the junction of Casca and Manso Rivers [( 5)].Beside each sampling station is the specific abundance of mollusks (number of individuals) collected in the reservoir, at each sampling station, during the quantitative study.
The present study extends the known distribution of B. straminea in the State of Mato Grosso, as it has previously been reported in the municipalities of Diamantino and Várzea Grande 20 .B. straminea is of great epidemiological importance because it is responsible for areas of active transmission of schistosomiasis in northeastern Brazil, and its occurrence in the Cuiabá River (municipality of Cuiabá) is significant because of the frequent presence of fishermen at this site.Experimental infection studies of B. amazonica populations from the APM Manso reservoir (collected from Chapada dos Guimarães) revealed infection rates of 2.02% and 9.09% with the BH and EC strains of S. mansoni, respectively 21 .Although natural infection of B. amazonica with S. mansoni has never been described, since the 1970s experimental infection studies have raised concerns about the transmission of schistosomiasis in the range of B. amazonica 22 .Considering these studies, in addition to environmental and social factors in the area, the possibility of the introduction of schistosomiasis in this reservoir, although low, cannot be ignored.
Reservoirs have been continually subject to the introduction and establishment of alien species, as reported by Rocha et al. 24 in State of São Paulo.The authors showed that rapid invasion processes were ongoing on the Tietê River basin for three species of mollusks: C. fluminea, Limnoperna fortunei (Dunker, 1857) and M. tuberculata.Similar findings were observed in the APM Manso reservoir for M. tuberculata; (between 2009 and 2010), introduced after February 2009, it became the most abundant species.As well as being an intermediate host of C. formosanus, M. tuberculata destabilizes the course of periphyton colonization, suggesting that it may also disrupt natural food chains 25 .
This study extends the known distribution of A. nordestensis in 11 States (Alagoas, Goiás, Maranhão, Minas Gerais, Pará, Paraná, Pernambuco, Rio Grande do Sul, Rio de Janeiro, Santa Catarina, and São Paulo) and Distrito Federal [26][27][28] to include eight municipalities in the State of Mato Grosso.However, Drepanotrema cimex (Moricand, 1839), previously reported to be present in Cáceres and Cuiabá 23 , was not found in any of the surveyed municipalities.Drepanotrema heloicum (d'Orbigny, 1835) and Drepanotrema kermatoides (d'Orbigny, 1835), which have also previously been found in Mato Grosso 26 , were not found in the study area, confirming the results reported by Paraense in 21 municipalities of the state 23 .
With regard to the Ancylidae, the distribution of the genus Anisancylus Pilsbry, 1924 was extended to the Central-West Region.Anisancylus dutrae Santos, 1994 occurs in northeastern Brazil, from Pernambuco to Bahia 29,30 ; Anisancylus obliquus (Broderip & Sowerby, 1832) has been recorded from southern Brazil to Uruguay, Argentina and Chile 30,31 .These species occur in shallow lotic waters, especially over stones, and seldom occur on the abaxial surface of leaves.Burnupia ingae was observed for the first time in three municipalities (Chapada dos Guimarães, Cuiabá and Nobres) in the State of Mato Grosso.This finding of B. ingae in Mato Grosso extends its known range, as it was previously found only in southern Brazil, in the States of Santa Catarina and Rio Grande do Sul [30][31][32] .Lacerda and Santos 33 reviewed samples housed in the Malacological Collections, including the CMIOC, and a literature search estimating the current distribution of B. ingae in Brazil showed that it was present in 20 municipalities in seven states.The genus Laevapex Walker, 1903 was also recorded for the first time in the State of Mato Grosso, in the municipalities of Chapada dos Guimarães, Cuiabá, Jangada and Rosário Oeste; it was previously cited as present in the Serra da Mesa dam 9 as well as other scattered locations in Brazil 30,31 .
The diversity of lentic habitats provided by dam construction seems to favor the expansion and establishment of G. radiata, which has a wide distribution, from the southern United States, Central America and Caribbean, to northern and northeastern Brazil 30,31 .Recently, this species has been found in the State of Rio de Janeiro, extending its known distribution to southeastern Brazil 34 .The results of this quantitative study were similar to previous studies performed in the Serra da Mesa dam 9 in central Brazil, where an intense colonization by G. radiata and the disappearance of G. ticaga was reported a few years after the creation of the reservoir.
High densities of the macrophytes P. stratiotes and S. auriculata were found in the Manso and Casca Rivers, respectively, which form the APM Manso reservoir, between 2002 and 2003 3 .Takeda et al. 35 noted 25 groups of invertebrates associated with five different macrophytes in the floodplain of the high Parana River, with P. stratiotes having the largest invertebrate density, followed by Salvinia sp.The present study confirmed the importance of these macrophytes in the establishment and colonization of mollusks in the APM Manso reservoir, as it was common to find snails attached to macrophyte roots that were floating on the lake far from the edge of the reservoir.
The present study extends the distribution of some species of the Ampullariidae and Corbiculidae, including P. lineata, which occurs from northeastern to southeastern Brazil but generally in the coastal region and P. maculata, which is among the largest of the freshwater snails and, together with P. scalaris, occurs frequently in the basins of the Prata, Paraguay and Uruguay Rivers 36 .
In the Manso Power Plant area, the discovery of two Corbiculidae species, C. largillierti and C. fluminea, is a major problem, mainly because of the ecological and economic impact on local fauna and hydroelectric power.These Asiatic species were introduced in the State of Rio Grande do Sul in the 1980s, and, in 1998, they were reported in the flooded area of Pantanal Mato-Grossense near Cuiabá 37,38 .The present paper reports both species in Cuiabá, confirming previous reports, and adds C. fluminea to three municipalities, including the reservoir area.Recently, Pereira et al. 39 listed the freshwater bivalve species of South America, including the families Corbiculidae, Mycetopodidae and Sphaeriidae, and commented that changes from lotic to lentic ecosystems interfere in the life cycle of these mollusks, which depend on fish for their dispersal.
Mollusks are particularly common in the dry season; in an analysis of the diversity of mollusks in a reservoir in Thailand, Tesana 40 reported that many species increased in population during the cold season.These species appear to hatch during the rainy season and grow large enough to be detected by the dry season 40 .Furthermore, Paraense 41 commented that populations decrease substantially at the peak of the rainy season, due to the effects of floods and other environmental disturbances.
Cercarial dermatitis 42 , which is considered an emerging disease, may be occurring in the study area because Ampullariidae and Planorbidae specimens have been found harboring Brevifurcate apharyngeate cercaria in the municipalities of Alto Paraguai, Poconé and Nobres 43 .According to Horák and Kolárová 44 , the dispersal of bird schistosomes to new regions and an increased availability of snail hosts, together with the use of new water reservoirs for recreational purposes, may contribute to a higher number of outbreaks of cercarial dermatitis.In the State of Espirito Santo, Brevifurcate apharyngeate cercariae were found in naturally infected P. marmorata and identified by morphological and molecular methods as Trichobilharzia sp., the main etiological agents of cercarial dermatitis in humans 45 .This observation suggests an increased possibility of the existence of unknown cases of avian cercarial dermatitis in Brazil, including the Central-West Region, due to the presence of well-established populations of P. marmorata in areas affected by hydroelectric plants in the Tocantins 9,46 and Araguaia 47 Rivers, in addition to those found in this study.Given the increasing number of dams in the middle-west region of the country over the past few years, malacological surveys should be performed in such areas.Those studies are an important strategy to prevent new foci of schistosomiasis and other zoonoses and will provide data on the effect of dams on freshwater mollusk populations.

FIGURE 1 -
FIGURE 1 -Location of study area.A: Map of South America showing Brazil and the State of Mato Grosso.B: Municipalities that were surveyed for the presence of snails.C: APM Manso reservoir showing the sampling station of the quantitative study: 1 and 4: Manso River; 2 and 3: Palmeiras River; 5: Stream in the junction of the Casca and Manso Rivers near the dam; 6, 8, 9 and 10: Casca River; and 7: Quilombo River.APM Manso: Usina Hidrelétrica de Aproveitamento Múltiplo de Manso.

TABLE 4 -Number of specimens of mollusks collected in each sampling station in the APM reservoir during the quantitative study carried out between April 2009 and October 2010.
APM Manso: Usina Hidrelétrica de Aproveitamento Múltiplo de Manso.