REVISTA DE BIOLOGIA E CIÊNCIAS DA TERRA ISSN 1519-5228
Volume 19 - Número 1 - 1º Semestre 2019
LIMNIC MALACOFAUNAL DIVERSITY IN THE STATE OF PARAÍBA, BRAZIL, WITH
EMPHASIS ON THE DISTRIBUTION AND ABUNDANCE OF THE PLANORBIDAE
(MOLLUSCA, GASTROPODA)
Artur Henrique Freitas Florentino de Souza1
, Laura Ney Marcelino Passerat de Silans2
, Martin Lindsey Christoffersen3
ABSTRACT
The phylum Mollusca is well represented in limnic benthic communities, having important roles in ecological,
economic, and health-sanitary issues. Some species transmit diseases to man. The planorbids Biomphalaria
spp. are intermediate hosts for Schistosomiasis. We evaluate the diversity of the limnic malacofauna, with
emphasis on panorbids, in 19 municipalities, as part of the Project “Carta Planorbídica do Estado da Paraíba”.
Samples were obtained from 128 localities within the 19 studied municipalities. Dredgings were made in
water-body sediments and in aquatic macrophyte banks, with a manual collector having a net mesh opening of
1 mm. The collected material was fixed in the field with formalin at 4% and transported to the lab. The material
was rinsed in current water with nets having mesh openings of 1 mm and 500 µm. Molluscs were sorted in
illuminated trays, identified and preserved in alcohol at 70%. Eight species of mollusks were identified,
belonging to five gastropod families (Ampullariidae, Thiaridae, Physidae, Ancylidae, and Planorbidae) and
one species of Bivalvia (family Sphaeriidae). Highest Shannon Diversity and Pilous Equitability indexes were
obtained from the municipality of Serraria (H’= 1.820; J = 0.935), respectively. Largest relative abundances
for genus Biomphalaria were recorded in the municipalities of Pilõezinhos (98.29% for B. glabrata). The later
municipality thus presented the highest index of abundance, the smallest index of Shannon, and smallest
Equitability index (D = 0.966; H’ = 0.086; J = 0.124). Mollusks were absent from samples collected in the
municipality of Marcação.
Key words: Mollusca, Diversity, Biomphalaria spp.
RESUMO
O filo Mollusca é um componente expressivo da comunidade bentônica límnica, desempenhando importante
papel ecológico, econômico e médico-sanitário. Alguns deles são transmissores de doenças para o homem,
como os planorbídeos Biomphalaria spp., que são hospedeiros intermediários da esquistossomose. Objetivou-
se avaliar a diversidade da malacofauna límnica, com ênfase nos planorbídeos, em 19 municípios, dentro do
projeto “Carta Planorbídica do Estado da Paraíba”. Foram realizadas coletas em 128 localidades distribuídas
nos 19 municípios estudados. Realizaram-se arrastos, com um pegador manual de 1 mm de abertura de malha,
no sedimento litorâneo e em macrófitas aquáticas. O material coletado foi fixado em formol 4% no campo e
transportado para o laboratório, onde foi lavado em água corrente com peneiras de malhas 1 mm e 500 µm.
Sua triagem foi feita em bandejas iluminadas. Os moluscos encontrados foram identificados e conservados em
álcool 70%. Registraram-se oito espécies de moluscos, sendo sete destas distribuídas em cinco famílias de
gastrópodes (Ampullariidae, Thiaridae, Physidae, Ancylidae, Planorbidae) e uma espécie de Bivalvia da
família Sphaeriidae. Os maiores índices de diversidades Shannon e de Equitabilidade de Pilous foram obtidas
nos municípios de Serraria (H’= 1,820; J = 0,935), respectivamente, enquanto que as maiores abundâncias
relativas do gênero Biomphalaria foram registradas nos municípios de Pilõezinhos (98,29% de B. glabrata),
o que fez desse município o de maior índice de dominância, além do de menor índice de Shannon e de menor
Equitabilidade (D = 0,966; H’ = 0,086; J = 0,124). De todos os municípios estudados, apenas em Marcação
não houve registro de moluscos.
Palavras-Chaves: Mollusca, Diversidade, Biomphalaria spp.
92
1. INTRODUCTION
Among the eight classes of the phylum
Mollusca, Gastropoda and Bivalvia stand out for
their medical, veterinary, and economic
importance (VIDIGAL et al., 2005).
Limnic mollusks are particularly
important in food webs of aquatic ecosystems
(MALTCHICK et al., 2010), and as intermedite
hosts in the life cycles of digenetic and cestode
parasites, causing medical-veterinary concern
world-wide (ESTEVES, 2011).
In Brazil, authors such as Abílio et al.
(2007), Teles (2005), Suriani et al. (2007), and
Martello et al. (2008) indicated that limnic
mollusks may colonize a great variety of lotic
and lentic habitats.
Species belonging to families
Planorbidae, Physidae, Lymnaeidae,
Ampullariidae, and Thiaridae are noteworthy for
their role as intermediate hosts of digenetic
trematodes of medical and veterinalry
importance (SOUZA; LIMA, 1990; REY, 2008).
Among the limnic mollusks, planorbids are the
most intensely studies in Brazil, because of their
role as intermediate hosts in the transmission of
mansonic Schistomiasis (BARBOSA and
BARBOSA, 1994).
According to Barbosa and Barbosa
(1994), the genus Biomphalaria presents a
planospiral shell, with a diameter varying from
7mm to 40 mm, being naturally hay-colored.
This color is modified in contact with dyes
present in the water, such as iron oxide, which
produce darker tones of brown and even black.
This paper aims to evaluate the diversity
of the limnic malacofauna, with emphasis on
planorbids, in 19 municipalities in the State of
Paraíba. The project was conducted by the State
Agency for Public Health of the State of Paraíba
and by the Aquatic Ecology Lab of the Federal
University of Paraíba.
2. MATERIAL AND MÉTHODS
2.1. Study Area
The present study was conducted in 19
municipalities of the State of Paraíba (Figura 01),
nine of which are located in forested areas (Zona
da Mata) (Alhandra, Marcação, Baia da Traição,
Jacaraú, Capim, Cuité de Mamanguape,
Mamanguape, Curral de Cima, and Itapororoca).
Ten municipalities are located in arid regions
(Agreste) (Caiçara, Serraria, Pilõezinhos,
Alagoinha, Lagoa de Dentro, Logradouro, Duas
Estradas, Sertãozinho, Serra da Raiz, and
Pirpirituba).
Figure 1. Location of 19 municipalities in the State of
Paraíba sampled in this paper for the malacofauna in the
years from 2004 to 2006.
2.2. Collecting and Sorting
For the evaluation of the malacological
diversity, three dredgings in the shallow water
sediment – preferably in areas with banks of
aquatic macrophytes – were conducted at each
locality (totalling 128 stations in 19
municipalities) with a dredging net of the Delta
type (35 x 35 x 35 cm), having a net mesh size of
500µm.
Each sample of sediment was previously
washed in the field, conditioned in a labeled
plastic bag, and fixed in formaline at 4%
(neutralized with calcite - chalk). In the lab,
samples were washed with tap water, with nets
measuring 1mm and 0,5mm in mesh size.
Sampling proceeded in strongly illuminated
white trays.
Mollusks were identified under a
binocular stereomicroscope, with the help of
standardized identification keys (PAN
AHO/WHO, 1968; BARBOSA;
BARBOSA,1995). Subsequently, samples were
conserved in flasks containing alcohol at 70%.
Relative abundance of the malacofauna
was estimated. Diversity was evaluated with the
diversity indexes of Shannon-Wiener (H’).
Dominancea (D) and Pilous Equitabilidade (J). All
indexes were analised in the statistical program
PAST (HAMMER et al., 2001).
3. RESULTS AND DISCUSSION
A total of 6931 mollusks were captured in
the studied municipalities. Eight species were
identified, belonging to five gastropod families:
Ampullariidae, Pomacea lineata (Spix, 1827);
Thiaridae, Melanoides tuberculata (Müller,
1774); Physidae, Aplexa marmorata Guilding,
1828; Ancylidae Glundachia sp.; Planorbidae,
Biomphalaria straminea (Dunker, 1848),
Biomphalaria glabrata (Say, 1818);
Drepanotrema sp. Additionally, one species of
Bivalvia, Eupera sp., belonging to family
Sphaeriidae, was sampled.
The highest species richness indexes
were obtained for the municipality of Serraria, in
the arid Agreste Region,, and in Curral de Cima,
in the forested Zona da Mata Region. Both had
seven species, being followed by Baía da Traição
and Itapororoca, with five species.
Regarding total number of individuals
belonging to the malacofauna, the highest
records were obtained for the municipalities of
Jacaraú and of Cuité de Mamanguape, with 1332
and 1227 specimens, respectively (Table 1). In
The municipality of Marcação, differently from
the remaining municipalities, no mollusks were
sampled.
The genus Biomphalaria, and the species
B. straminea, were recorded in 17 of the studied
municipalities, excepting Marcação and
Pilõezinhos. This species was dominant in seven
municipalities, one of which in the forested
region, municipality of Alhandra, with 71.1%.
The other six municipalities with dominant B.
straminea were located in the arid region. The
highest abundance of this species was recorded
for Lagoa de Dentro, with 97.33%, followed by
Duas Estradas, with 82.56% (Figure 2).
Table 1. Mean number of species found in 19 municipalities in years 2004 to 2006.
Figure 2. Mean relative abundance of the malacofauna for 18 municipalities in the State of Paraíba (the municipality of
Marcação is not included because mollusks were not found there) during the years from 2004 to 2006.
Although B. glabrata was recorded in
four municipalities, it predominated only in
Pilõezinhos and Alhandra, with abundances of
98.29% and 71.1%, respectively.
The presence of B. glabrata is recorded in
806 municipalities in the country (BRASIL,
2008). This species is considered to be the most
efficient intermediate host of Schistosomiasis
mansonica in America, being responsible for
active focal areas of infestation (REY, 2008).
The present paper indicates that in the
municipalities with B. straminea there is a low
abundance of B. glabrata. On the other hand,
Mota (2011) found six species of mollusks, B.
straminea being dominant relative to other
species such as Melanoides tuberculata and
Pomacea lineata.
Barbosa (1995) indicates that, although
the two species may overlapp, B. glabrata is
restricted to forested areas, while B. straminea
is a largely distributed species, occurring in both
forested and arid regions. Considering
population interactions between these two
species, it is noteworthy that, during a monitored
experiment during three consecutive years
(Barbosa, 1973), B. straminea, which initially
occurred only occasionally in restricted areas
inhabited exclusively by B. glabrata, ended by
totally replacing the latter species.
Our results are in agreement with Paz
(1997), who indicates that only two of the three
known species of planorbids transmitting
Schistosomiasis occur in the State of Paraíba:
Biomphalaria straminea occurs from the coast to
the arid Sertão, while B. glabrata occurs mainly
in the forested coastal area.
In Brazil, B. glabrata is considered the
main species hosting Schistosoma mansoni.
However, in Northeastern Brazil, B. straminea
becomes the most relevant epidemiological agent
(BARBOSA, 1995), due to its predominance in
aquatic environments. This was also observed by
Abílio et al. (2007). Figure 2 indicates the
relative abundance of mollusks in the studied
municipalities.
The planorbid Drepanotrema is also
representative in four municipalities. In Curral de
Cima, its relative abundance was 86.23%,
followed by Itapororoca, with 59.71%.
The pandemic tiarid mollusk Melanoides
tuberculata was also quite representative, its
highest abundance occurring in the municipality
of Capim, with 93.63%, followed by Cuité de
Mamanguape (86.23%) and Jacaraú (73.62%).
This exotic species of Afro-Asiatic origin was
introduced in the country as a consequence of the
trade of fish and ornamental plants. Melanoides
tuberculatus has dispersed through several
hydrographical basins (SURIANI et al., 2007).
Their reproduction occurs by parthenogenesis,
their young are incubated in a ventral pouch, and
they have both detritivorous and carnivorous
feeding habits.
Their numbers my reach very high levels
(VAZ et al., 1986; VIDIGAL et al., 2005). They
exert profound changes in the colonized benthic
communities (BOGÉA et al., 2005). Their
capacity to colonize several types of habitat tend
to exclude certain pulmonate species, in
particular those related to the transmission of
Schistosomiasis (POINTIER and
MCCULLOUGH, 1989).
According to Pamplim and Rocha (2005),
the record of this species throughout indicates a
strong and rapid dispersal. They have been
introduced into several environments as a
biological regulator against Biomphalaria sp.
Notwithstanding, Souza et al. (2008) recorded
that, in the public dam of Jatobá I, in Patos,
Paraíba, PB, the colonization of artificial
substrates by large numbers of M. tuberculata
directly promoted the installation of large
numbers of Biomphalaria sp., mainly in the
period without rainfall.
The ampullarid Pomacea lineata
dominated in the municipality of Baía da
Traição, representing 93.55% of the malacofauna
of that region.
The municipality of Pilõezinhos
presented the highest value of Dominance (D =
0.966) for the malacofauna, followed by Lagoa
de Dentro (D = 0.947). Serraria and Logradouro
presented the lowest values of dominance for the
malacofauna, with indexes of 0.173 and 0.389,
respectively (Figure 3).
Regarding Pilous Equitability (J),
Serraria was most equitative (J = 0.935),
followed by Logradouro, (J = 0.796). Pilõezinhos
and Lagoa de Dento were the least equitative,
presenting J indexes of 0.124 and 0.126,
respectively (Figure 3).
For the index of alfa diversity of
Shannon-Wiener (H’) for the malacofauna,
Serraria presented the highest indexes
(H’=1.820), followed by Itapororoca (H’= 1.242)
and Logradouro (H’= 1.103), as shown in Figure
3. Pilõezinhos showed the lowest index of
Shannon, with H’= 0,086), followed by Lagoa de
Dentro (H’ = 0.139).
Although the municipality of Curral de
Cima showed a high richness of species in
relation to the remaining studied municipalities,
and a large number of obtained specimens (see
Table 1), this municipality showed a low mean
abundance of Drepanotrema sp. (85.22%),
which resulted in a Dominance index of 0.732,
an Equitability index of 0.321, and a Shannon
index of 0.624.
Figure 3. Dominance (D), Shannon-Wiener Diversity
(H’), and Pilous Equatibility (J) indexes for the
malacofauna at 19 municipalities in the State of Paraíba
during the years 2004 to 2006.
4. CONCLUSION
The municipality of Serraria showed the
highest indexes of Shannon and of Equitability
among the 19 investigated municipalities.
With the exception of the municipality of
Marcação, a large occurrence and ample
distribution of species of Biomphalaria was
observed in the studied municipalities. This
indicates the risc of a possible cycle of
Schistosoma mansoni in the places with high
abundance of this snail, pointing to the
importance of continued actions of vigilance and
control of Schistosomiasis.
B. straminea is most important in terms
of epidemiological records of S. mansoni,
because it has the largest distribution relative to
B. glabrata.
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C.B.D.. Responses of freshwater molluscs to
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MARTELLO, A.R.; NUNES, I.G.W.;
BOELTER, R.A.; LEAL, L.A.. Malacofauna
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MOTA, D.J.G.. Levantamento da
malacofauna límnica na área do pesqueiro
Itapecerica, Itapecerica da Serra /São Paulo.
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PAMPLIN, P.A.Z.; O. ROCHA.. Distribuição
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281-305. In: O. ROCHA; E.L.G. ESPÍNDOLA;
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PAZ, R. J. Biologia e Ecologia de Biomphalaria
glabrata (Say, 1818) (Mollusca: Pulmonata:
Planorbidae), na Fazenda Árvore Alta,
Alhandra (Paraíba - Brasil). João Pessoa,
Paraíba, 125p., Dissertação de Mestrado,
Universidade Federal da Paraíba, 1997.
POINTIER, J. P.; MCCULLOUGH, F.
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REY, L.. Parasitologia: Parasitos e doenças
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SOUZA, A.H.F.F.; ABÍLIO, F.J.P.; RIBEIRO,
L.L.. Colonização e Sucessão Ecológica do
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Jatobá I, Patos – PB, Brasil. Revista de
Biologia e Ciências da Terra 8 (2): 125 – 144,
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ALBUQUERQUE, J.O.; BOCANEGRA, S.;
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BARBOSA, C.S. Aspectos ecológicos e
levantamento malacológico para identificação
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Alegre, 100(1):19-24, 2010.
SURIANI, A.L.; FRANÇA, R.S.; ROCHA, O..
A malacofauna bentônica das represas do
médio rio Tietê (São Paulo, Brasil) e uma
avaliação ecológica das espécies exóticas
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TELES, H.M.S.. Distribuição das espécies de
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______________________________________
[1] Federal University of Piaui, Campus
Senador Helvídio Nunes de Barros, 64607-670,
Picos, Piaui, Brazil, ahffs@ufpi.edu.br
[2] Entomology Section, Environmental
Agency, Secretaria de Saúde State of Paraíba,
Brazil, lauraney@uol.com.br
[3] Department of Systematics and Ecology,
Federal University of Paraíba, 58051-900,
Paraíba, Brazil, martinlc.ufpb@gmail.com
98

Artigo bioterra v1_n1_2019_10

  • 1.
    REVISTA DE BIOLOGIAE CIÊNCIAS DA TERRA ISSN 1519-5228 Volume 19 - Número 1 - 1º Semestre 2019 LIMNIC MALACOFAUNAL DIVERSITY IN THE STATE OF PARAÍBA, BRAZIL, WITH EMPHASIS ON THE DISTRIBUTION AND ABUNDANCE OF THE PLANORBIDAE (MOLLUSCA, GASTROPODA) Artur Henrique Freitas Florentino de Souza1 , Laura Ney Marcelino Passerat de Silans2 , Martin Lindsey Christoffersen3 ABSTRACT The phylum Mollusca is well represented in limnic benthic communities, having important roles in ecological, economic, and health-sanitary issues. Some species transmit diseases to man. The planorbids Biomphalaria spp. are intermediate hosts for Schistosomiasis. We evaluate the diversity of the limnic malacofauna, with emphasis on panorbids, in 19 municipalities, as part of the Project “Carta Planorbídica do Estado da Paraíba”. Samples were obtained from 128 localities within the 19 studied municipalities. Dredgings were made in water-body sediments and in aquatic macrophyte banks, with a manual collector having a net mesh opening of 1 mm. The collected material was fixed in the field with formalin at 4% and transported to the lab. The material was rinsed in current water with nets having mesh openings of 1 mm and 500 µm. Molluscs were sorted in illuminated trays, identified and preserved in alcohol at 70%. Eight species of mollusks were identified, belonging to five gastropod families (Ampullariidae, Thiaridae, Physidae, Ancylidae, and Planorbidae) and one species of Bivalvia (family Sphaeriidae). Highest Shannon Diversity and Pilous Equitability indexes were obtained from the municipality of Serraria (H’= 1.820; J = 0.935), respectively. Largest relative abundances for genus Biomphalaria were recorded in the municipalities of Pilõezinhos (98.29% for B. glabrata). The later municipality thus presented the highest index of abundance, the smallest index of Shannon, and smallest Equitability index (D = 0.966; H’ = 0.086; J = 0.124). Mollusks were absent from samples collected in the municipality of Marcação. Key words: Mollusca, Diversity, Biomphalaria spp. RESUMO O filo Mollusca é um componente expressivo da comunidade bentônica límnica, desempenhando importante papel ecológico, econômico e médico-sanitário. Alguns deles são transmissores de doenças para o homem, como os planorbídeos Biomphalaria spp., que são hospedeiros intermediários da esquistossomose. Objetivou- se avaliar a diversidade da malacofauna límnica, com ênfase nos planorbídeos, em 19 municípios, dentro do projeto “Carta Planorbídica do Estado da Paraíba”. Foram realizadas coletas em 128 localidades distribuídas nos 19 municípios estudados. Realizaram-se arrastos, com um pegador manual de 1 mm de abertura de malha, no sedimento litorâneo e em macrófitas aquáticas. O material coletado foi fixado em formol 4% no campo e transportado para o laboratório, onde foi lavado em água corrente com peneiras de malhas 1 mm e 500 µm. Sua triagem foi feita em bandejas iluminadas. Os moluscos encontrados foram identificados e conservados em álcool 70%. Registraram-se oito espécies de moluscos, sendo sete destas distribuídas em cinco famílias de gastrópodes (Ampullariidae, Thiaridae, Physidae, Ancylidae, Planorbidae) e uma espécie de Bivalvia da família Sphaeriidae. Os maiores índices de diversidades Shannon e de Equitabilidade de Pilous foram obtidas nos municípios de Serraria (H’= 1,820; J = 0,935), respectivamente, enquanto que as maiores abundâncias relativas do gênero Biomphalaria foram registradas nos municípios de Pilõezinhos (98,29% de B. glabrata), o que fez desse município o de maior índice de dominância, além do de menor índice de Shannon e de menor Equitabilidade (D = 0,966; H’ = 0,086; J = 0,124). De todos os municípios estudados, apenas em Marcação não houve registro de moluscos. Palavras-Chaves: Mollusca, Diversidade, Biomphalaria spp. 92
  • 2.
    1. INTRODUCTION Among theeight classes of the phylum Mollusca, Gastropoda and Bivalvia stand out for their medical, veterinary, and economic importance (VIDIGAL et al., 2005). Limnic mollusks are particularly important in food webs of aquatic ecosystems (MALTCHICK et al., 2010), and as intermedite hosts in the life cycles of digenetic and cestode parasites, causing medical-veterinary concern world-wide (ESTEVES, 2011). In Brazil, authors such as Abílio et al. (2007), Teles (2005), Suriani et al. (2007), and Martello et al. (2008) indicated that limnic mollusks may colonize a great variety of lotic and lentic habitats. Species belonging to families Planorbidae, Physidae, Lymnaeidae, Ampullariidae, and Thiaridae are noteworthy for their role as intermediate hosts of digenetic trematodes of medical and veterinalry importance (SOUZA; LIMA, 1990; REY, 2008). Among the limnic mollusks, planorbids are the most intensely studies in Brazil, because of their role as intermediate hosts in the transmission of mansonic Schistomiasis (BARBOSA and BARBOSA, 1994). According to Barbosa and Barbosa (1994), the genus Biomphalaria presents a planospiral shell, with a diameter varying from 7mm to 40 mm, being naturally hay-colored. This color is modified in contact with dyes present in the water, such as iron oxide, which produce darker tones of brown and even black. This paper aims to evaluate the diversity of the limnic malacofauna, with emphasis on planorbids, in 19 municipalities in the State of Paraíba. The project was conducted by the State Agency for Public Health of the State of Paraíba and by the Aquatic Ecology Lab of the Federal University of Paraíba. 2. MATERIAL AND MÉTHODS 2.1. Study Area The present study was conducted in 19 municipalities of the State of Paraíba (Figura 01), nine of which are located in forested areas (Zona da Mata) (Alhandra, Marcação, Baia da Traição, Jacaraú, Capim, Cuité de Mamanguape, Mamanguape, Curral de Cima, and Itapororoca). Ten municipalities are located in arid regions (Agreste) (Caiçara, Serraria, Pilõezinhos, Alagoinha, Lagoa de Dentro, Logradouro, Duas Estradas, Sertãozinho, Serra da Raiz, and Pirpirituba). Figure 1. Location of 19 municipalities in the State of Paraíba sampled in this paper for the malacofauna in the years from 2004 to 2006. 2.2. Collecting and Sorting For the evaluation of the malacological diversity, three dredgings in the shallow water sediment – preferably in areas with banks of aquatic macrophytes – were conducted at each locality (totalling 128 stations in 19 municipalities) with a dredging net of the Delta type (35 x 35 x 35 cm), having a net mesh size of 500µm. Each sample of sediment was previously washed in the field, conditioned in a labeled plastic bag, and fixed in formaline at 4% (neutralized with calcite - chalk). In the lab, samples were washed with tap water, with nets measuring 1mm and 0,5mm in mesh size. Sampling proceeded in strongly illuminated white trays. Mollusks were identified under a binocular stereomicroscope, with the help of standardized identification keys (PAN AHO/WHO, 1968; BARBOSA;
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    BARBOSA,1995). Subsequently, sampleswere conserved in flasks containing alcohol at 70%. Relative abundance of the malacofauna was estimated. Diversity was evaluated with the diversity indexes of Shannon-Wiener (H’). Dominancea (D) and Pilous Equitabilidade (J). All indexes were analised in the statistical program PAST (HAMMER et al., 2001). 3. RESULTS AND DISCUSSION A total of 6931 mollusks were captured in the studied municipalities. Eight species were identified, belonging to five gastropod families: Ampullariidae, Pomacea lineata (Spix, 1827); Thiaridae, Melanoides tuberculata (Müller, 1774); Physidae, Aplexa marmorata Guilding, 1828; Ancylidae Glundachia sp.; Planorbidae, Biomphalaria straminea (Dunker, 1848), Biomphalaria glabrata (Say, 1818); Drepanotrema sp. Additionally, one species of Bivalvia, Eupera sp., belonging to family Sphaeriidae, was sampled. The highest species richness indexes were obtained for the municipality of Serraria, in the arid Agreste Region,, and in Curral de Cima, in the forested Zona da Mata Region. Both had seven species, being followed by Baía da Traição and Itapororoca, with five species. Regarding total number of individuals belonging to the malacofauna, the highest records were obtained for the municipalities of Jacaraú and of Cuité de Mamanguape, with 1332 and 1227 specimens, respectively (Table 1). In The municipality of Marcação, differently from the remaining municipalities, no mollusks were sampled. The genus Biomphalaria, and the species B. straminea, were recorded in 17 of the studied municipalities, excepting Marcação and Pilõezinhos. This species was dominant in seven municipalities, one of which in the forested region, municipality of Alhandra, with 71.1%. The other six municipalities with dominant B. straminea were located in the arid region. The highest abundance of this species was recorded for Lagoa de Dentro, with 97.33%, followed by Duas Estradas, with 82.56% (Figure 2). Table 1. Mean number of species found in 19 municipalities in years 2004 to 2006.
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    Figure 2. Meanrelative abundance of the malacofauna for 18 municipalities in the State of Paraíba (the municipality of Marcação is not included because mollusks were not found there) during the years from 2004 to 2006. Although B. glabrata was recorded in four municipalities, it predominated only in Pilõezinhos and Alhandra, with abundances of 98.29% and 71.1%, respectively. The presence of B. glabrata is recorded in 806 municipalities in the country (BRASIL, 2008). This species is considered to be the most efficient intermediate host of Schistosomiasis mansonica in America, being responsible for active focal areas of infestation (REY, 2008). The present paper indicates that in the municipalities with B. straminea there is a low abundance of B. glabrata. On the other hand, Mota (2011) found six species of mollusks, B. straminea being dominant relative to other species such as Melanoides tuberculata and Pomacea lineata. Barbosa (1995) indicates that, although the two species may overlapp, B. glabrata is restricted to forested areas, while B. straminea is a largely distributed species, occurring in both forested and arid regions. Considering population interactions between these two species, it is noteworthy that, during a monitored experiment during three consecutive years (Barbosa, 1973), B. straminea, which initially occurred only occasionally in restricted areas inhabited exclusively by B. glabrata, ended by totally replacing the latter species. Our results are in agreement with Paz (1997), who indicates that only two of the three known species of planorbids transmitting Schistosomiasis occur in the State of Paraíba: Biomphalaria straminea occurs from the coast to the arid Sertão, while B. glabrata occurs mainly in the forested coastal area. In Brazil, B. glabrata is considered the main species hosting Schistosoma mansoni. However, in Northeastern Brazil, B. straminea becomes the most relevant epidemiological agent (BARBOSA, 1995), due to its predominance in aquatic environments. This was also observed by Abílio et al. (2007). Figure 2 indicates the relative abundance of mollusks in the studied municipalities. The planorbid Drepanotrema is also representative in four municipalities. In Curral de Cima, its relative abundance was 86.23%, followed by Itapororoca, with 59.71%. The pandemic tiarid mollusk Melanoides tuberculata was also quite representative, its highest abundance occurring in the municipality of Capim, with 93.63%, followed by Cuité de Mamanguape (86.23%) and Jacaraú (73.62%). This exotic species of Afro-Asiatic origin was introduced in the country as a consequence of the trade of fish and ornamental plants. Melanoides tuberculatus has dispersed through several hydrographical basins (SURIANI et al., 2007).
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    Their reproduction occursby parthenogenesis, their young are incubated in a ventral pouch, and they have both detritivorous and carnivorous feeding habits. Their numbers my reach very high levels (VAZ et al., 1986; VIDIGAL et al., 2005). They exert profound changes in the colonized benthic communities (BOGÉA et al., 2005). Their capacity to colonize several types of habitat tend to exclude certain pulmonate species, in particular those related to the transmission of Schistosomiasis (POINTIER and MCCULLOUGH, 1989). According to Pamplim and Rocha (2005), the record of this species throughout indicates a strong and rapid dispersal. They have been introduced into several environments as a biological regulator against Biomphalaria sp. Notwithstanding, Souza et al. (2008) recorded that, in the public dam of Jatobá I, in Patos, Paraíba, PB, the colonization of artificial substrates by large numbers of M. tuberculata directly promoted the installation of large numbers of Biomphalaria sp., mainly in the period without rainfall. The ampullarid Pomacea lineata dominated in the municipality of Baía da Traição, representing 93.55% of the malacofauna of that region. The municipality of Pilõezinhos presented the highest value of Dominance (D = 0.966) for the malacofauna, followed by Lagoa de Dentro (D = 0.947). Serraria and Logradouro presented the lowest values of dominance for the malacofauna, with indexes of 0.173 and 0.389, respectively (Figure 3). Regarding Pilous Equitability (J), Serraria was most equitative (J = 0.935), followed by Logradouro, (J = 0.796). Pilõezinhos and Lagoa de Dento were the least equitative, presenting J indexes of 0.124 and 0.126, respectively (Figure 3). For the index of alfa diversity of Shannon-Wiener (H’) for the malacofauna, Serraria presented the highest indexes (H’=1.820), followed by Itapororoca (H’= 1.242) and Logradouro (H’= 1.103), as shown in Figure 3. Pilõezinhos showed the lowest index of Shannon, with H’= 0,086), followed by Lagoa de Dentro (H’ = 0.139). Although the municipality of Curral de Cima showed a high richness of species in relation to the remaining studied municipalities, and a large number of obtained specimens (see Table 1), this municipality showed a low mean abundance of Drepanotrema sp. (85.22%), which resulted in a Dominance index of 0.732, an Equitability index of 0.321, and a Shannon index of 0.624. Figure 3. Dominance (D), Shannon-Wiener Diversity (H’), and Pilous Equatibility (J) indexes for the malacofauna at 19 municipalities in the State of Paraíba during the years 2004 to 2006. 4. CONCLUSION The municipality of Serraria showed the highest indexes of Shannon and of Equitability among the 19 investigated municipalities. With the exception of the municipality of Marcação, a large occurrence and ample distribution of species of Biomphalaria was observed in the studied municipalities. This indicates the risc of a possible cycle of
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    Schistosoma mansoni inthe places with high abundance of this snail, pointing to the importance of continued actions of vigilance and control of Schistosomiasis. B. straminea is most important in terms of epidemiological records of S. mansoni, because it has the largest distribution relative to B. glabrata. REFERÊNCIAS BIBLIOGRÁFICAS ABÍLIO, F.J.P.; RUFFO, T.L.M.; SOUZA, A.H.F.F.; FLORENTINO, H.S.; OLIVEIRA- JUNIOR, E.T.; MEIRELES, B.N.; SANTANA, A.C.D. Macroinvertebrados Bentônicos como Bioindicadores de Qualidade Ambiental de Corpos Aquáticos da Caatinga Oecologia Brasiliense, 11 (3): 397-409, 2007. BARBOSA, F. S.. Possible competitive displacement and evidence of hybridization between two brazilian species of planorbid snails. Malacologia, 14: 401-408, 1973. BARBOSA, F.S. (Org.). Tópicos em Malacologia Médica. Rio de Janeiro: FIOCRUZ, 314p. 1995. BARBOSA, F.S.; BARBOSA, C.S.. The bioecology of snail vectors for schistosomiasis in Brazil. Cadernos de Saúde Pública, 10(2): 200-209, 1994. BOGÉA T, CORDEIRO FM, GOUVEIA JS. Melanoides tuberculatus (Gastropoda: Thiaridae) as intermediate host of Heterophidae (Trematoda: Digenea) In Rio de Janeiro Metropolitan área, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 47(2): 87- 90, 2005. BRASIL. Ministério da Saúde. Vigilância e Controle de Moluscos de Importância Epidemiológica - Diretrizes Técnicas: Programa de Vigilância e Controle da Esquistossomose (PCE) - 2. ed. Brasília, 178 p. 2008. ESTEVES, F. A. (coord.) Fundamentos em Limnologia. Rio de Janeiro: Interciência, 3ª Ed, 2011. HAMMER, O.; HARPER, D.A.T.; RYAN, P.D.. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4(1): 9. 2001. MALTCHIK, L.; STENERT, C.; KOTZIAN, C.B.D.. Responses of freshwater molluscs to environmental factors in Southern Brazil wetlands. Brazilian Journal of Biology, 70 (3): 473 – 482, 2010. MARTELLO, A.R.; NUNES, I.G.W.; BOELTER, R.A.; LEAL, L.A.. Malacofauna límnica associada à macrófitas do rio Iguariaçá, São Borja, RS, Brasil. Ciência e Natura, UFSM. 2008; 30(1): 27-41. MOTA, D.J.G.. Levantamento da malacofauna límnica na área do pesqueiro Itapecerica, Itapecerica da Serra /São Paulo. Dissertação apresentada ao programa de pós- graduação em ciências da coordenadoria de controle de doenças da Secretaria de Estado da Saúde de São Paulo, 2011. PAMPLIN, P.A.Z.; O. ROCHA.. Distribuição batimétrica e sazonal de moluscos na represa de Bariri, com ênfase nas espécies exóticas, Melanoides tuberculata (Gastropoda: Thiaridae) e Corbicula fluminea (Bivalvia: Corbiculidae), p. 281-305. In: O. ROCHA; E.L.G. ESPÍNDOLA; N. FENERICH-VERANI; J.R. VERANI & A.C. RIETZLER (Eds). Espécies invasoras em águas doces. Estudos de caso e propostas de manejo. São Carlos, Editora Universidade Federal de São Carlos, 416p, 2005. PAN AHO/WHO. 1968. A Guide for the Identification of the Snail Intermediate Hosts of Schistosomiasis in the Americas. Scientific Publication No. 168, p: 5-122. PAZ, R. J. Biologia e Ecologia de Biomphalaria glabrata (Say, 1818) (Mollusca: Pulmonata: Planorbidae), na Fazenda Árvore Alta, Alhandra (Paraíba - Brasil). João Pessoa, Paraíba, 125p., Dissertação de Mestrado, Universidade Federal da Paraíba, 1997. POINTIER, J. P.; MCCULLOUGH, F. Biological control of the snail hosts of Schistosoma mansoni in the Caribbean area
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    using Thiara sp.Acta Tropica 46(3):147-155, 1989. REY, L.. Parasitologia: Parasitos e doenças parasitárias do homem nos trópicos ocidentais - 4ª ed, Rio de Janeiro: Guanabara Koogan, 883 p., 2008. SOUZA, A.H.F.F.; ABÍLIO, F.J.P.; RIBEIRO, L.L.. Colonização e Sucessão Ecológica do Zoobentos em Substratos Artificiais no Açude Jatobá I, Patos – PB, Brasil. Revista de Biologia e Ciências da Terra 8 (2): 125 – 144, 2008. SOUZA, C. P.; LIMA, L. C. Moluscos de Interesse Parasitológico do Brasil. FIOCRUZ/CPqRR, Belo Horizonte-MG, 76p. 1990. SOUZA, M.A.A.; BARBOSA, V.S.; ALBUQUERQUE, J.O.; BOCANEGRA, S.; SOUZA-SANTOS, R.; PAREDES, H.; BARBOSA, C.S. Aspectos ecológicos e levantamento malacológico para identificação de áreas de risco para transmissão da esquistossomose mansoni no litoral norte de Pernambuco, Brasil. Iheringia, Sér. Zool., Porto Alegre, 100(1):19-24, 2010. SURIANI, A.L.; FRANÇA, R.S.; ROCHA, O.. A malacofauna bentônica das represas do médio rio Tietê (São Paulo, Brasil) e uma avaliação ecológica das espécies exóticas invasoras, Melanoides tuberculata (Müller) e Corbicula flumínea (Müller). Revista. Brasileira de Zoologia; 24(1): 21-32, 2007. TELES, H.M.S.. Distribuição das espécies de caramujos transmissores de Schistosoma mansoni no Estado de São Paulo. Revista da Sociedade Brasileira de Medicina Tropical, 38(5): 426- 432, 2005. VIDIGAL, T.H.D.A.; MARQUES, M.M.G.S.; LIMA, H.P.; BARBOSA, FAR. Gastrópodes e bivalves límnicos do trecho médio da bacia do Rio Doce, Minas Gerais, Brasil. Lundiana (6): 67-76, 2005. ______________________________________ [1] Federal University of Piaui, Campus Senador Helvídio Nunes de Barros, 64607-670, Picos, Piaui, Brazil, ahffs@ufpi.edu.br [2] Entomology Section, Environmental Agency, Secretaria de Saúde State of Paraíba, Brazil, lauraney@uol.com.br [3] Department of Systematics and Ecology, Federal University of Paraíba, 58051-900, Paraíba, Brazil, martinlc.ufpb@gmail.com 98