Current distribution of the exotic freshwater snail Helisoma duryi (Gastropoda: Planorbidae) in Brazil

2010·4.4 MB·English

by  Monica A Fernandez

THE NAUTILUS 124(l):44-50, 2010 Page 44
Current distribution of the exotie freshwater snail Helisoma duryi
(Gastropoda: Planorbidae) in Brazil
MonicaA. Fernandez Fernando S. M. Bezerra Lucia M. S. Alencar
Silvana C. Thiengo DepartamentodeAnalisesClmieas/FFOE Secretariade SaudedoEstadodoCeara
Laboratoriode Malacologia Universidade Federal doCeara RuadosTabajaras 281, Praiade Iracema
Referenda Nacionalem RuaCapitaoFrancisco Pedro 1210 60060-510 Fortaleza, BRAZIL
Malacologia Medica 60430-370 Fortaleza, BRAZIL
Instituto OswaldoCruz- Fiocruz
Av. Brasil4365
21045-900 Rio deJaneiro, BRAZIL
[email protected]
ABSTRACT with exotic species, CBD signed the Decree number
2.519, seeking to protect and manage biodiversity
Thisarticledescribesthecurrentdistributionoftheintroduced (Ministerio do Meio Ambiente, 2009).
gastropod Helisoma duryi in Brazil. The species was recorded
Difficulties in predicting the effects of alien species
faonrdthsienfcierstthteinmeitihnaBsrabzeielninre1p9o72r,teidntFooromcocsuar,insttatheeosftaGtoeisaso,f after introduction were discussed by Meyer et al.
Ceara, Minas Gerais, Paraiba, Rio de Janeiro, and Sao Paulo. (2008), in an investigation on the exotic giant African
Recently, this specieswas found in the state ofCeara, where it snail, Achatina fulica Bowdich, 1822. According to
was introduced through ornamental fish and aquatic plant Ricklefs (2005), every invasion process undergoes lour
trade. The expansion of the species range in Brazil demon- phases: introduction or colonization; settlement, which
strates the need for increased efforts to monitor and con- requires adaptation to local conditions to survive local
trol the introduction of exotic species. Up to now, H. duryi species interactions; geographical expansion; and even-
had been found in 14 municipalities together with spec- tual decay. The period during which every species
iPlmaennosrboifdAamep,ulPlhayrsiiiddaaee,, AanncdyliTdhiaaer,iCdaoer.bieWuelidbaeel,ieLvyemntaheaitdateh,e remains ateach ofthosephases depends oneitherintrin-
bcuerernenptrevaibosuesnlcyecoolfleHc.teddu(r1y9i72inantdhe19l9o8c)alcitoiuelsdwbheerasesoictiahtaedd sriecntolryeexxtpreirniseinccfiancgtotrhseteoxpilt.os(iIvnecipdheanstaelloyf,thBeraiznivlasisiocnuro-f
with environmental changes in those regions and also be- A. fulica, and dense populations ofthat species arewide-
cause selling in H. duryi is not as efficient as it is for other spread in at least 24 out of 26 Brazilian states and the
Planorbidae species. A mapwith the distribution ofH, duryi is Federal District.)
alsoprovided. In Brazil, biological invasions and the pathways of
introduction and spread ofexotic species are notyetwell
Additional keywords: exotic freshwater mollusks, biological
invasions, invasive species, planorbids documented, but a number of instances oftbe spread of
invasive mollusks have been documented in the last
decade: Thiengo et al. (2007a) reportedthe rapid expan-
sion and current distribution of A.fulica since its intro-
INTRODUCTION duction in the state of Parana, in 1988 while Santos et al.
(2002) and Fischer and Colley (2005) reported the
Non-native species, those that have been introduced occurrence ofA.fulica in preservation areas in the states
from another geographic region to an area outside its of Rio de Janeiro (Ilha Grande, Angra dos Reis) and
natural range, have been the focus of several investiga- Parana (Ilha Rasa, municipality of Guaraqueyaba), re-
tions in the past years, mostly because they have been spectively, and Takeda et al. (2003) and Mansur et al.
closely related to problems in human health, in the envi- (2004) reported the occurrence ofthe invasive freshwa-
ronment, and economy. The Convention on Biological ter clams Limnopema fortunei (Drinker, 1857) and
Diversity (CBD), ratified in 188 countries, including Corbicula spp. in Southern Brazil. In addition to envi-
Brazil, is one of the most important international tools ronmental and economical problems related to exotic
conceived to provide environmental conventions, strate- snail species, some of those species have medical and
gies, and agreements in order to promote sustainable veterinary importance as they may be associated with
development. In Brazil, where specialists and environ- zoonotic and parasitic transmission ol diseases (Caldeira
mental public bodies recognize the problems involved et ah, 2007; Thiengo et ah, 2008).
, i .
M.A. Fernandez et al., 2010 Page 45
The aquarium trade is a major source ol exotic fresh- measured usinga mereurium thermomether, a pHmeter
water mollusks. In 1972, a population ofHelisoma chinji (Instrutherm pH-1700), and an oxymeter (Lutron
(Wetherby, 1879), autochthonous from the Everglades DO-5510). Samples were maintained under laboratory
LRNM
wetlands in Florida, was first reported in Distrito de conditions at in aquariacontainingdechlorinated
Santa Rosa, municipality of Formosa, state of Goias, tap water and a thin bottom layer of a 2:1 mixture of
Brazil, in natural breedingsites connectedwith the Cana screened soil and ground oyster shells as a source of
Brava River (Paraense, 1975). According to Paraense mineral nutrients.
(1976), these specimens collected in the locality Lagoa For specific identification, the snails were anesthe-
da Pedra, in connection with the Cana Brava River, tized with 0.05% sodium pentobarbital (Hypnol®) for
included a large number of albinos obtained from sym- five hours; killed by immersion in 70'’C water and then
patrie populations of Ampullariidae, Ancylidae, Phys- fixed in Railliet-Henry solution (Fernandez et al. 2008).
idae, and other Planorbidae. Similarly, Thiengo et al. Snail samples were deposited in the Malacologieal Col-
(1998) also reported the presence of albino specimens lection ofInstitute) Oswaldo Cruz (CMIOC).
in fish tanks in the municipality of Guapimirim, state of
Rio de Janeiro, Brazil, in June 1997 and remarked the
importance of aquarium fish trade in the introduction RESULTS
and spread ofexotic snails in new sites.
Recognizing the threat to global biodiversity that in- In the state of Goias (Table 1), eightfreshwatergastropod
species were found: Biomphalaria straminea (Drinker,
vhaasvieverastpieficeidesthpelaCyBBDraziinlains oefnfeortofto18h8elpcoumnatnraiegsetthhaist 1848), Drepanotrema anatimun (Orbigny, 1835), Drepa-
notrema cimex (Morieand, 1839), Drepanotrema depres-
disappearing resource. In 2006 snails were sent from
sissimum (Morieand, 1839), Drepanotrema hicidum
Serra Verde do Saraiva by the Secretaria de Saude of
(Pfeiffer, 1839), Gnndlachia radiata (Guilding, 1828),
the state of Ceara (SESA-CE), to the Centro Nacional
de Referenda em Malacologia Medica (LRNM) for Melanoidestuberculatus (Muller, 1774) andPomacea sp.
identification. These snails were identified as H. clurt/i In the state of Rio de |aneiro, in the municipality of
and prompted surveys ofthe present distribution ofthis Guapimirim (Table 1), no H. duriji specimens were
found but the following species were collected: Bio-
species in Brazil alongwith the occurrence ofsympatric
mphalaria tenagophiJa (d’Orbigny 1835), B. straminea
freshwater snail species were performed andpresented. ,
Hebetancylus morieand (d’Orbigny, 1837), Lymnaea
columella Say, 1817, M.tuberculatus, Physa marmorata
Guilding, 1828, Pomacea diffusa (Reeve, 1856), and
MATERIALS AND METHODS
Pomacea sp. (only juvenile specimens).
In the state of Ceara, specimens of H. dunji were
Information on the distribution of Helisoma dunji in
Brazil since its first recorded introduction was obtained found in the twohabitats, awellandafishtank (Table 1).
In these the water temperatures were 27.3°C and
fromthe literature andfrom dataon specimens collected
27.4°C, environment temperatures were 36.8°C and
bstyattesh,efaruotmhowrsh.icFhietlhde osucrcvueryrsenwceereofpHe.rdfuonrjmiedwaisnptrherveie- 33.7°C, pH was: 7.76 and 6.38, and dissolved oxygen
ously reported by the staff of LRNM: Goias (munici- measured 7.8 mg/L and 7.0 mg/L in the well and the
palities of Formosa and Vila Boa), Rio de Janeiro fish pond, respectively. The other freshwater gastro-
pods found in the state were B.straminea, D. lucidum,
(municipalityofGuapimirim), and Ceara (municipalities
of Acarape, Fortaleza, Guaiuba, and Redenyao). G. radiata, H. dunji, M.tuberculatus, P. marmorata,
perInfotrhmeedstabteetowfeGeonia2s00(3Tabalned1)2,0s0n5ailincowlleetcltainonds awreeraes PPoommaacceeaa slpi.ne(aotnaly(SjpufvxeniinleWaspgenceirm,en1s8)2.7), P. diffusa, and
along federal highway BR-020, and in Lagoa da Pedra,
between the municipalities ofFormosa and Vila Boa. In DISCUSSION
the state ol Rio de Janeiro (municipalityofGuapimirim)
collections were made in 2000, 2003, and2007 (Table 1) According to Paraense (1976) and the data from
in exoticornamental fish (Bettasplendens (Regan. 1910)) CMIOC, in August 1972, in addition to Helisoma dunji,
breeding tanks. Four municipalities were investigated in the following snail species were collected in lakes form-
the state of Ceara (Table 1): three in the region ofSerra ed by the Cana Brava River (in the municipality of
Verde do Saraiva (Acarape, Guaiuba and Redenyao) and Formosa, Goias): B.straminea, Biomphalaria schrammi
one in the Fortaleza municipality (a lake named Lagoa (Crosse, 1864), D. anatinum, D. lucidum, Plesioplysa
de Porangabussu). ornata (Haas, 1938), L. columella, and P. marmorata In
Mollusks were collected from different habitats the present study surveys were performed in seven
(streams, wells, marshyareas, fish tanks and lakes) using ponds formed byCana Brava River flooded areas, in the
collectingsieves. With theaim ofassessingabioticfactors municipalities of Vila Boa and Formosa, but no spec-
in the habitats where IP dunji occurs, variables such imens of H.dunji were found.
as temperature (water and air), pH, and the concen- In the 1990s, manyornamental freshwater fish breed-
tration of dissolved oxygen in the water column were ingfacilities in the state of Rio de Janeirowere located in
Page 46 THE NAUTILUS, Vol. 124, No. 1
Table 1. Study localities and species found.
Geographical Freshwatergastropods (Snailsamples and
State Date Municipality coordinates Biotope respectivetheCMIOC collection number)
Goias March 2003 Vila Boa 1.5°03,54.6"WS, lake D. lucidum (5199), D. cimex (5201), and
47°04'44.8" D. depressissimum (5200)
Formosa 1.5°29'57.5"WS, lake Nofreshwatersnailwas found.
47°06'37.8"
May2005 Vila Boa 15°02T9.9"WS, lake No freshwatersnailwas found.
47°12,04.2"
Vila Boa 15°02'39.1"WS, lake D. anatinum (5191), andM. tuberculatus (5190)
47°12,22.5"
Vila Boa 15°04T0.8"WS, lake B straminea (5193), D anatinum (5192),
47°04'20.9" D. lucidum, G. radiata (5194), andPomacea sp.
August2005 VilaBoa 15°04'09.3"WS, lake B straminea (5195), D. anatinum (5196),
47°05'24.1" D. cimex, andD. lucidum (5198)
Vila Boa 15°04'03.8"WS, lake B straminea, D. anatinum, D. cimex, D. lucidum,
47°05'40.4" G. radiata (5197), andM. tuberculatus
Rio de January2000 Guapimirim 22°38,21.7"WS, fishtank Nofreshwatersnailwas found.
Janeiro 42°58'54.0"
September2003 Guapimirim 22°38,21.7"WS, fishtank B. tenagophila, B. straminea, L. columella.
42°58'54.0" M. tuberculatus andP. marmorata
January2007 Guapimirim 22°38'21.7"WS, tanks B. tenagophila, H. moricandi, M. tuberculatus,
42°58'54.0" P. marmorata, P. bridgesii andPomacea sp.
Ceara October2006 Aearape 04°11'03.9"WS, lake M. tuberculatus (5147) andPomacea sp. (5202)
38°43'24.9"
Aearape 04°11'45.3"WS, lake B. straminea (5149), D. lucidum (5151),
38°42'55.7" G. radiata (5150), M. tuberculatus (5148) and
P.lineata (5203)
Guaiuba 04°10'32.1"WS, three B. straminea (5153), inoneofthem
38°44'02.2" wells
October2006 Redenyao 04°10'48.9"WS, well Nofreshwatersnailwas found.
38°43'48.0"'
Redenyao 04°10'55.8"WS, well Nofreshwatersnailwas found.
38°43'40.8"
Redenyao 04°10'41.2"WS, well H. duryi (5152)
38043'51.4"
Redenyao 04°10'25.3"WS, well No freshwatersnailwas found.
38°43'52.7"
Redenyao 04°10'50.6"WS, stream Nofreshwatersnailwas found.
38°43'45.3"
Redenyao 04°10'27.2"WS, lake G. radiata (5154) andP. lineata
38°43'49.8"
Redenyao 04°10'46.8"WS, fish tank H. duryi (5157), P. marmorata (5156) and
38°44'02.4" P. diffusa (5204)
Fortaleza 03°44'45.4"WS, lake P. lineata (5146) andB.straminea: onlyshells
38°32'00.0"
August2008 Fortaleza 03°44'37.4"WS, lake P. lineata andB.straminea
38°32'57.8"
the municipality of Guapimirim. This probably favored species occurs naturally throughout the Amazon Basin
the introduction of exotic species. According to the field (Peru, Bolivia and Brazil) but it is widespread nowadays
work registrations in the LRNM, specimens ofH. duryi due to aquarium and fish trade, specially the more
reported by Thiengo et al. (1998) were found in sym- attractive albino specimens known as golden apple
patry with B. straminea, Ferrissia sp., L. columella and snails.
P. bridgesii. The latter is identified as P. diffusa nowa- Our results indicate a reduction in Helisoma duryi
days, according to Hayes et al (2008). Many albino spec- populations in the state of Ceara. In March and May
imens ol H. duryi and P. diffusa were also foundin those 2006, a team from Secretaria de Saude of the state of
fish tanks in September, 1997. Although no PI. duryi Ceara (SESA-CE) collected samples ofH. duryi in five
specimen was found, the present paper confirms the localitiesin the municipalities ofRedenyaoandGuaiuba,
establishment ol P. diffusa, only species reported by and in the present study this species was found in only
Thiengo et al. (1998) and also obtained in 2007. This two ofthese (Table 1). In the lake Porangabussu, in the
M.A. Fernandez et al., 2010 Page 47
municipality of Fortaleza, where H. duryi and M. tuber- Federal, in both lenthicandlothiehabitats,with orwith-
culatus specimens were collected in 1999 by Dr. out anthropic influences (Fernandez et al., 2003).
Fernando Bezerra (Universidade Federal do Ceara) and Melanoides tuberculatus reproduces parthenogeneti-
sent to LRNM for identification, no specimens were eally, which may account for its wider geographic distri-
found in 2006 and 2008. bution when compared to II duryi. The latter may
The introduction ofHelisoma duriji was probably the occasionally utilize selfing as an alternative means of
result of aquaculture activity. Ornamental plants are reproduction, although it is not as efficient as it is for
used in fish tanks chiefly to promote water oxygenation. other Planorbidae species (Paraense and Correa, 1988).
These plants maytransportboth eggs and early stages of According to these authors, H. duryi benefits much less
freshwater gastropods, enabling their spread into new from functional hermaphroditism which, besides other
environments. Correa et al. (1980) inferred the impor- advantages, enables a single virgin individual to found a
tance ofsuch plants asvectors fordispersalol non-native new population. Furthermore, other characteristics of
mollusks, andnotedthattheymayhavebeen particularly M. tuberculatus such as viviparity, iteroparity and high
,
important regarding the spread of schistomsomiasis- survival rate of the young, may also contribute to its
carrying individuals of B. straminea in Sao Paulo state. spread (Santos et al., 2007).
Theysurveyedaquariumandaquaticplantshopsthrough- In Guapimirim (Rio de Janeiro) and in Lagoa do
out the municipality and found specimens of Physidae, Porangabussu (Ceara), B. straminea appears to have
Lymnaeidae, Ampullariidae, Thiaridae, and Planorbidae, adapted to local conditions, forming colonies, while
including Helisoma sp. In the same state, Franga et al. H. duryi has not. Remarkably, in Guapimirim municipal-
(2007) collected sediment samples in three reservoirs of ity, specimens of B. straminea were found in 1997 and
the Baixo Rio Tiete (Promissao, Nova Avanhandava, and 2003, but not in 2007; whereas B. tenagophila was
Tres Irmaos), in November 2002 and August 2003, in recorded in 2003 and 2007. The disappearance of
order to identify species of benthic mollusks. Specimens B. straminea and the establishment of B. tenagophila
H. duryi were found, including another exotic bivalve, must be confirmed. In contrast, Silva et al. (1997) re-
Corbicula fluminea (Mnller, 1774), and the Afro-asiatie ported the replacementof B.straminea forB.tenagophila
gastropod, M. tuberculatus. Although //. duryi was pre- in the municipalityofParacambi, Rio de Janeiro.
sent in the three reservoirs analyzed, that species had the Tlle introduction ofH. duryi in the state ofCeara may
lowest densityamongthe exoticmollusks. be a result of B. splendens aquaculture (breeding and
Foran exoticspecies tobe regardedas invasive it must trade), similar to that described for Guapimirim (Rio de
have, at least, considerable adaptability to new environ-
ments, rapid sexual maturation, and a large reproductive
capacity (Santos et al. 2007). Ecological and parasitolog-
ical laboratory studies of Helisoma duryi obtained in
Goias in 1972 (Milward-de-Andrade, 1978a, b; Milward-
de-Andrade and Belisario, 1979; Milward-de-Andrade
and Souza, 1979; Milward-de-Andrade et al., 1979) indi-
cate adaptive advantages of that exotic species over
Biomphalaria glabrata (Say, 1818). These include a
higher reproduction rate, lower mortality, higher resis-
tance to environmental desiccation, increased starvation
survival, and increased resistance to infection by
Schistosoma mansoni in that former species.
Other authors reported that Helisoma duryi mayhave
the abilityto control populations ofBiomphalaria spp., a
vector ofschistosomiasis (Frandsen, 1987; Frandsen and
Madsen, 1979), in Puerto Rico, St. Lucia, Egypt, and
Tanzania. In Brazil, Milward-de-Andrade (1979) argued
that the capacity of H.duryi to colonize Neotropical
ecosystems, either directly or indirectly, may play a
key role in the biological control of schistosomiasis
mansoni. However, throughout the last three decades,
such expected interspecific competition has not been
observed (the H. duryi population found in 1972, in
Goias, did not successfully establish itself, and was
not observed in 2003 and 2005). Remarkably, M. tuber-
culatus was found in this habitat after 2005, havingbeen
introduced in Brazil probably by aquarists in Santos in
1967 (Vaz et ah, 1986). Currently, M. tuberculatus may Figure 1. Helisoma duryi from Ceara state, municipality of
be found in seventeen Brazilian states and in the Distrito Redengao (04°10'46.8" S, 38°44'02.4"W).
.
Page 48 THE NAUTILUS, Vol. 124, No. 1
Janeiro). Ornamental and pet fish such as B. splendens difficult to find H. duryi, in contrast to March and May,
originate in Asia andwere introduced to Europe and the the rainfall season in that region. In October 2006, H.
United States in 1874 and 1910, respectively(Fariaetah, duryi specimens (juvenile andeggs) were found in a fish
2006). In the 1960s and 1970s, ornamental fish breeders tank ofornamental fish production in Redengao, as well
in Brazil introduced production techniques and female asothersnailspeciessuchas P. mannorata andP. diffusa.
individuals imported from Europe and the United Recently, Hayes et ah (2008) reported that some
States. Since then, individuals of H. clun/i have been ampullariid species, such as P. diffusa, may have some
recorded in the following Brazilian states: Minas Gerais, characteristics that allow them to become invaders fol-
in the municipalities of Vigosa in 1967, and Uberaba lowing introduction; its occurrence in Guapimirim (Rio
(Vidigal et ah, 2000); Rio de Janeiro, in the municipality de Janeiro), ten years after its first record, supports
ofNova Iguagu in 1975; Paraiba, in the municipalities of Hayes’s remark. Furthermore, the presence ofP. diffusa
Joao Pessoa and Campina Grande (Abilio, 2003); and in Ceara, currently restricted to a fish tank, is reason for
Sao Paulo (Correa et ah, 1980; Franga et ah, 2007). The concern over the potential for future spread and estab-
distribution of the exotic freshwater snail H. duryi in lishmentof newcolonies inotherareas ofSerraVerde do
Brazil is shown in the Figure I Saraiva. This could happen as a result of the rainy sea-
In addition to use of the species in ornamental fish son, a possibility that in itselfmakes evident the urgent
aquaculture, Betta splendens was also released under need for monitoringofthe local malacofauna.
experimental conditions in 2000 as a biological control Todate, thereis no recordofthreatenednative species,
of the mosquito Aedes aegypti Linnaeus, 1758, in the risk of economical loss, or damage to public health that
state of Ceara, municipalities of Fortaleza and Caninde could be triggered by the introduction of Heliosma
(Pamplona et ah, 2004). This mayin partaccount for the duryi in Brazil However, this lack of concern may be
spread ofII. duryi in that state. A temporaryshortage of unwarranted, and preventive measures against the intro-
rainfall in the state of Ceara in October 2006 made it duction and spreadofthe species, aswellas ofothers that
Figure 2. Distributionoftheexoticfreshwatersnail Helisomaduryi in Brazil: 1, Fortaleza; 2, Guaiiiba;3,Acarape; 4, Redengao;5,
CampinaGrande; 6, JoaoPessoa; 7,VilaBoa; 8, Formosa;9, Uberaba; 10,Vigosa; 1 1, Promissao; 12, SaoPaulo; 13, NovaIguagu; 14,
Guapimirim.
.
M.A. Fernandez et al., 2010 Page 49
are associated with environmental damages and public Mansur, M.C.D., C.T. Callil, F.R. Cardoso, and J.A.A. Ibarra.
health problems, should be taken. Accordingly, strict law 2004. Uma retrospectiva e mapeamento da invasao de
enforcementpolicies andprocedures must be established espeeies de Corhicula (Mollusca, Bivalvia, Veneroida,
in the trade ofaquatic plants to fish producers as a pre- Corbiculidae) oriundas do Sudeste Asiatico, na America
ventive measuretopreserveourbiodiversity. do Sul, pp. 39-58. In: Silva, J.S.V. and R.C.C.L. Souza
(Eds.) Agua de Lastro e Bioinvasao. Editora Intercieneia,
Rio de Janeiro, 224pp.
Meyer,W.M., K.A. Hayes and A.I. Meyer. 2008. GiantAfrican
LITERATURE CITED snailAchatinafulica as a predator. American Malacologi-
cal Bulletin 24! 117-119.
Abilio, F.J.P. 2003. Gastropodes e outros invertebrados Milward-de-Andrade, R. 1978a. Fecundidade de Helisoma
bentonieosdosedimentolitoraneoeassociadosamacrofitas duryi e Biomphalaria glahrata criadas em laboratorio.
,
aquaticas em ayudes do semi-aridoparaibano, nordeste do Revista Brasileira de Malariologia e Doenyas Tropicais
Brasil. Available from: http://www.uepb.edu.br/eduep/rbct/ 30: 5-44.
sumarios/pdf/eiehhornia.pdf 13/VIII/2008] Milward-de-Andrade, R. 1978b. Competiyao entre Helisoma
Caldeira, R.L., C.L.G.F. Mend[onya, C.O. Gouveia, H.L. duryi e Biomphalaria glahrata em eondiyoes de labo-
,
Lenzi, C. Graeff-Teixeira, W.S. Lima, E.M. Mota, I.L. ratorio. RevistaBrasileiradeBiologia38: 787-800.
Pecora, A.M.Z. Medeiros, and O.S. Carvalho. 2007. First Milward-de-Andrade, R. 1979. Natalidade comparada de
recordofmolluscsnaturallyinfectedwithAngiostrongijlus Helisoma duryi e Biomphalaria glahrata em laboratorio
,
cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) (Mollusca, Planorbidae). Revista Brasileira de Malari-
in Brazil. Memorias do Instituto Oswaldo Cruz 102: ologiae DoenyasTropicais 31: 35-58.
887-889. Milward-de-Andrade, R. and R.F. Belisario. 1979. Tipo
Correa, L.L., M.O.A. Correa, J.F. Vaz, M.I.P.G. Silva, de substrato e natalidade comparada de Helisoma duryi
R.M. Silva, and M.T. Yamanaka. 1980. Importancia das e Biomphalaria glahrata. Ciencia e Cultura 31 (Suppl.):
plantas ornamentals dos aquarios como veiculos de 412.
propagayao de vetores de Schistosoma rnansoni. Revista Milward-de-Andrade, R., S. Oliveira, and A.A. Ramos. 1979.
do InstitutoAdolfo Lutz40: 89-96. Observayao preliminar sobre liberayao de eerearias de
Faria, P.M.C., D.V. Crepaldi, E.A. Teixeira, L.P Ribeiro, S. rnansoni por Biomphalaria glahrata associadas a
A.B. Souza, D.C. Carvalho, D.C. Melo, and E.O.S. Helisomaduryi. CienciaeCultura31 (Suppl.): 532.
Saliba. 2006. Criayao, manejoereproduyaodopeixeBetta Milward-de-Andrade, R. and C.R Souza. 1979. Infecyao
splendens (Regan 1910). RevistaBrasileirade Reproduyao experimental de Biomphalaria glahrata com Schisto-
Animal30: 134-149. soma rnansoni na presenya de Helisoma duryi. Revista
,
Fernandez, M.A., S.C. Thiengo, and R.S. Amaral. 2008. Brasileira de Malariologia e Doenyas Tropicais 31
Teenicas Malacologicas, pp. 47-81. IN Thiengo, S.C., (Suppl.): 185-186.
O.S. Pieri, and R.S. Amaral (Orgs) Vigilancia e eontrole Ministerio do Meio Ambiente. 2009. Convenyao sobre
de moluscos de importancia epidemiologica: diretrizes Diversidade Biologica. Available from: http:// www.mma.
teenicas. Programa de Vigilancia e Controle da gov.br/port/sbf/chm/cdb/decreto.html [03/111/2009].
Esquistossomose (PCE), Ministerio da Saude, Secretaria Pamplona, L.G.C., J.W.O. Lima, J.C.L. Cunha, and
de Vigilancia em Saude, Departamento de Vigilancia W.R Santana. 2004. Avaliayao do impacto na infestayao
Epidemiologica, 2a Ediyao, Brasilia, 177pp. por Aedes aegypty em tanques de cimento do Municipio
Fernandez, M.A., S.C. Thiengo, and L.R. Simone. 2003. Dis- deCaninde, Ceara, Brasil, apos autilizayaodopeixe Betta
tribution of the introduced freshwater snail Melanoides splendens como alternativa de controle biologico. Revista
tuberculatus (Gastropoda: Thiaridae) in Brazil. The Nau- da Sociedade Brasileira de Medicina Tropical 37:
tilus 117: 78-82 400-104.
Fischer, M.L. and E. Colley. 2005. Especie invasora em Paraense, W.L. 1975. Estado atual da sistematica dos pla-
Reservas Naturais: earaeterizayao da populayao de norbfdeos brasileiros. Arquivos do Museu Nacional 55:
Achatina fulica Bowdich, 1822 (Mollusca - Achatinidae) 105-128.
na Ilha Rasa, Guaraqueyaba, Parana, Brasil. Biota Paraense, W.L. 1976. A natural population of Helisoma duryi
Neotropica5: 1-18. in Brazil. Malacologia 15: 369-376
Franya, R.S., A.L. Sudani, and O. Rocha. 2007. Composiyao Paraense, W.L. and L.R. Correa. 1988. Self-fertilization in the
das espeeies de moluscos bentonieos nos reservatorios do freshwater snails Helisoma duryi and Helisoma trivolvis.
baixo rio Tiete (Sao Paulo, Brasil) com uma avaliayao do Memorias do Instituto OswaldoCruz83: 405-409.
impactocausadopelas espeeies exoticasinvasoras. Revista Ricklefs, R.E. 2005. Taxon cycles: insights from invasive
BrasileiradeZoologia24: 41-51. species, pp. 165-199. In: Sax, D.F., J.J. Stachowicz, and
Frandsen, F. 1987. Control ofschistosomiasis byuse ofbiolog- S.D. Gaines (Eds.) Speciesinvasions:insightsintoecology,
ical control ofsnailhostswith specialreference tocompe- evolution, and biogeography. Sinauer Associates, Sunder-
tition. Memorias do Instituto Oswaldo Cruz 82 (Suppl. land, 495pp.
IV): 129-133. Santos, S.B., D.P Monteiro, and S.C. Thiengo. 2002.Achatina
Frandsen, F. and PI. Madsen. 1979.AreviewofHelisomaduryi ftdica (Mollusca, Achatinidae) na Ilha Grande, Angra dos
in biological control. ActaTropica36: 67-84. Reis, Rio de Janeiro: implieayoes para saude ambiental.
Hayes, K.A., R.C. Joshi, S.C. Thiengo and R.H. Cowie. 2008. Biociencias 10: 159-152.
Out of South America: multiple origins of non-native Santos, S.B., I.C. Miyahira, and L.E.M. Lacerda. 2007. First
apple snails in Asia. Diversity and Distributions 14: record of Melanoides tuberculatus (Muller, 1774) and
701-712. Biomphalaria tenagophila (d’Orbigny, 1835) on Ilha
Page 50 THE NAUTILUS, Vol. 124, No. 1
Grande, Rio de Janeiro, Brazil. Biota Neotropica 7: Melanoides tuherculatus (Muller, 1774) (Gastropoda;
361-364. Thiaridae) no Brasil, p. 101-106. In: Barbosa, S.B., A.D.
Silva, C.L.P.A.C., M.S. Soares, and M.G.M. Barreto. 1997. Pimenta, S.C. Thiengo, M.A. Fernandez, and R.S.Absalao
Occurrence of Biomphalaria tenagophila and disap- (Eds.) Topicos em Malacologia- Eeos do XVIII Encontro
pearance of Biomphalaria straminea in Paracambi, Brasileiro de Malacologia. Sociedade Brasileira de
RJ. Memorias do Instituto OswaldoCruz92: 37-38. Malacologia, RiodeJaneiro,365pp.
Takeda,A M., M.C.D. Mansur, D.S. Fujita, and J.P.R. Bibian. Thiengo, S.C., M.A. Fernandez, E.J.L. Torres, P.M. Coelho,
2003. Ocorreneia da especie invasora de mexilhao and R.M. Lanfredi. 2008. First record of a nematode
dourado, Limnopemafortunei (Dunker, 1857), em dois Metastrongyloidea (Aelurostrongylus abstmsus larvae) in
pequenos reservatorios proximos a Curitiba, PR. Acta Achatina (Lissachatina)fulica (Mollusca, Achatinidae) in
BiologicaLeopoldensia25: 251-254. Brazil. JournalofInvertebrate Pathology98: 34-39.
Thiengo, S.C., F.A. Faraco, N.C. Salgado, R.H. Cowie, and Vaz, J.F., II.M.S. Telles, M.A. Correa, and S.P.S. Leite. 1986.
M.A. Fernandez. 2007a. Rapid spreadofan invasive snail Ocorreneia no Brasil de Thiara (Melanoicles) tuberculata
in South America: the giantAfrican snail,Achatinafulica, (Muller, 1774) (Gastropoda; Prosobranc-hia), primeiro
in Brasil. Biological Invasions9: 693-702. hospedeiro intermediario de Clonorchis sinensis
Thiengo, S.C., M.A. Fernandez, M.F. Boaventura, and (Cobbold, 1875) (Trematoda, Plathyhelmintes). Revista
M.A. Stortti. 1998. A survey of freshwater gastropods in de Saude Publica20: 318-322.
the Microrregiao Serrana ofthe State ol Rio de Janeiro, Vidigal,T.H.D.A., J.C. Kissinger, R.L. Caldeira, E.C.R. Piles,
Brazil. Memoriasdo InstitutoOswaldoCruz93 (Suppl. I): E. Monteiro, A.|.G. Simpson, and O.S. Carvalho. 2000.
233-234. Phylogenetic relationships among Brazilian Biomphalaria
Thiengo, S.C., M.A. Fernandez, A.C. Mattos, and A.F. species (Mollusca: Planorbidae) based upon analysis of
Barbosa. 2007b. Dispersao do molusco introduzido ribosomal ITS2sequences. Parasitology 121: 611-620.