Sampling collections and metadata of planorbidae (Mollusca: Gastropoda) in Brazil: a comprehensive analysis of the Oswaldo Cruz Institute’s Mollusk Collection from 1948 to 2023

Silvana Carvalho Thiengo; Mariana Gomes Lima; Alexandre Bonfim Pinheiro da Silva; Raiany Thuler Nogueira; Flávia Cristina dos Santos Rangel; Suzete Rodrigues Gomes

doi:10.46471/gigabyte.102

Gigabyte

2709-4715

GigaScience Press

Sha Tin, New Territories, Hong Kong SAR

DRR-202307-02

102

10.46471/gigabyte.102

https://doi.org/10.5281/zenodo.10213911

Data Release

Ecology

Biodiversity

Taxonomy

Sampling collections and metadata of planorbidae (Mollusca: Gastropoda) in Brazil: a comprehensive analysis of the Oswaldo Cruz Institute’s Mollusk Collection from 1948 to 2023

S. C. Thiengo et al.

Sampling collections and metadata of planorbidae (Mollusca: Gastropoda) in Brazil: a comprehensive analysis of the Oswaldo Cruz Institute’s Mollusk Collection from 1948 to 2023

https://orcid.org/0000-0002-5547-206X

ThiengoSilvana Carvalho

Conceptualization

Supervision

Writing - review editing

https://orcid.org/0000-0002-6127-0624

LimaMariana Gomes

Writing - original draft

Formal analysis

Data curation

https://orcid.org/0000-0002-4648-7112

da SilvaAlexandre Bonfim Pinheiro

Formal analysis

Writing - review editing

https://orcid.org/0000-0002-0211-5771

NogueiraRaiany Thuler

Data curation

Writing - original draft

https://orcid.org/0000-0003-3164-0871

RangelFlávia Cristina dos Santos

Data curation

Writing - original draft

GomesSuzete Rodrigues

Conceptualization

Data curation

Writing - original draft

Writing - review editing

Laboratório de Referência Nacional para Esquistossomose – Malacologia, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (LRNEM/IOC/Fiocruz), Brasil

Corresponding author. E-mail: maribiorural@gmail.com

07122023

2023

GIGABYTE_SERIES_0002

Vectors of human disease

15072023

29112023

2023

https://creativecommons.org/licenses/by/4.0/

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Planorbidae comprises approximately 40 genera of freshwater gastropods, including roughly 250 species. Among the Planorbidae subfamilies, the significance of Planorbinae is due to its genus Biomphalaria, whose species are intermediate hosts of the trematode Schistosoma mansoni Sambon, 1907, which causes schistosomiasis in humans and animals. Here, we present the analysis of the dataset of Planorbidae housed in the Collection of Mollusks of the Oswaldo Cruz Institute, with a special focus on Biomphalaria species. This dataset includes 7,267 lots originating from 55 countries, representing 20 genera and 75 species collected from 1948 to 2023. Collections were performed in all regions of Brazil, comprising specimens from 26 states and the Federal District, particularly from the Southeast and Northeast. Within the dataset, Biomphalaria includes 3,926 lots of 31 species from 42 countries. These records will help improve our comprehension of schistosomiasis transmission dynamics and the geographic distributions of these medically important species.

World Health Organization (WHO)

Pan American Health Organization (PAHO)

Brazilian Health Ministry (MS)

Oswaldo Cruz Foundation

FURNAS Centrais Elétricas Brasileiras S.A. - Eletrobras

Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ)

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

Collections of the lots of the studied period were funded by numerous institutions, including World Health Organization (WHO), Pan American Health Organization (PAHO), Brazilian Health Ministry (MS), Oswaldo Cruz Foundation, FURNAS Centrais Elétricas by Centrais Elétricas Brasileiras S.A. - Eletrobras, Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Data description

Background and context

The family Planorbidae includes around 40 genera of freshwater gastropods, with around 250 species widely distributed [1]. In this family, the subfamily Planorbinae includes six genera reported in Brazil: Acrorbis, Antillorbis, Biomphalaria, Drepanotrema, Helisoma, and Plesiophysa [2] (Figure 1). Biomphalaria includes species that act as intermediate hosts of the trematode Schistosoma mansoni, which causes schistosomiasis mansoni [3]. In Brazil, S. mansoni utilizes three species of the genus Biomphalaria as its natural intermediate hosts: Biomphalaria glabrata (Say, 1818), B. straminea (Dunker, 1848), and Biomphalaria tenagophila (d’Orbigny, 1835) [4, 5].

Figure 1.

Diversity of shell forms in Planorbidae from Brazil. (A) Biomphalaria straminea (CMIOC 5612), (B) Drepanotrema lucidum (CMIOC 5573), (C) Helisoma duryi (CMIOC 2318), (D) Antillorbis nordestensis (CMIOC 4550), (E) Acrorbis petricola (CMIOC 2744), (F) Plesiophysa dolichomastix (CMIOC 2041), and (G) Gundlachia ticaga (CMIOC 14689).

In this paper, we contributed a dataset derived from the Planorbidae species deposited in the Oswaldo Cruz Institute’s Mollusk Collection, mainly from Brazil, but also from numerous other countries. This material was mainly the result of decades of study in freshwater ecosystems by Dr. Wladimir Lobato Paraense, known for his studies on the biology and taxonomy of Brazilian planorbids, and by his team in the laboratory of Malacology of the Oswaldo Cruz Institute. Many other specialists also contributed and examined several specimens from this collection. In 1948, when Dr. Wladimir Lobato Paraense worked at the Public Health Special Service, a Brazilian institution responsible for the control of parasitic diseases in the Rio Doce Valley in Minas Gerais, including schistosomiasis [6, 7], he began his studies on the mollusks involved in the transmission of schistosomiasis in Brazil, creating the collection.

Currently, this collection includes mainly freshwater and land gastropods involved in the transmission of other parasitic diseases, such as fascioliasis and angiostrongyliasis, both cerebral and abdominal, but also includes gastropod species that cause economic losses in agriculture (mainly exotic species) and among native species from the Brazilian Biomes. The collection contributes to science, research, and education. It also serves as a repository of knowledge about Brazilian and global mollusk biodiversity [6].

The datasets presented in this study consist of metadata associated with each batch of Planorbidae specimens, featuring varying numbers of specimens. We filled in the obligatory fields and have successfully passed screening using the integrated publishing toolkit (IPT) of the Fundação Oswaldo Cruz (FIOCRUZ). For each lot of Planorbidae, our dataset includes fields providing, in Darwin Core Standard format, the following information: (i) taxonomy (kingdom, phylum, class, order, family, genus, specificEpithet, verbatimIdentification, infraspecificEpithet, scientificName, scientificNameAuthorship, taxonRank); (ii) collection details, including the collectors, collection date, collection site description (verbatimEventDate, eventTime, habitat, samplingProtocol); (iii) geolocation data (stateProvince, county, locality, locationRemarks, verbatimLatitude, verbatimLongitude, decimalLatitude, decimalLongitude, geodeticDatum); and (iv) catalog reference data (otherCatalogNumbers). This dataset is also available in the Sistema de Informação sobre a Biodiversidade Brasileira (SiBBr; i.e., Information System on the Brazilian Biodiversity), which integrates data and information, constituting the Brazilian Node of the Global Biodiversity Information Facility (GBIF), in an online platform for public use [8].

Methods

This study included all reports of Planorbidae genera and species from the dataset obtained from the Oswaldo Cruz Institute’s Mollusk Collection (CMIOC). These lots are mainly from Brazil, but also include material from more than 50 countries and continents (Figure 2). The temporal coverage of the Planorbidae dataset is from 1948 to 2023.

Figure 2.

Spatial coverage of the occurrence dataset of Planorbidae, from 1948 to 2023, based on the CMIOC, including mainly lots are from Brazil (6,372 lots).

All mollusks were morphologically identified in the laboratory to their genus and species based on shell and anatomical characteristics through specimen dissections, literature, and comparison with the lots deposited in the CMIOC [2, 9–12].

Data validation and quality control

Over the years, Dr. Lobato Paraense and his group published several works on planorbids from Brazil [9, 13–33]. Their works described and redescribed species of Planorbinae, reinforcing the importance of planorbids in transmitting diseases. Data validation was also done via the GBIF data-validator tool upon data submission [8].

Results

The CMIOC has records of representatives of the family Planorbidae (Table 1) from 55 out of the 193 countries recognized by the United Nations in 2023, spanning across four out of the six continents. These countries include Germany, Angola, Antigua, Antigua and Barbuda, Argentina, Austria, Barbados, Belize, Bolivia, Brazil, Chile, China, Costa Rica, Colombia, Cuba, Egypt, El Salvador, Ecuador, United States of America, France, Ghana, Guadeloupe, Guatemala, Guyana, French Guiana, Haiti, Hong Kong, Hungary, England, Israel, Italy, Jamaica, Martinique, Mexico, Mozambique, Nicaragua, Panama, Paraguay, Peru, Puerto Rico, Portugal, Dominican Republic, Saint Croix, Saint Thomas, Saint Vincent, Saint Lucia, Sweden, Suriname, Tahiti, Tanzania, Trinidad, Uganda, Uruguay, and Venezuela. These reports cover the following coordinates: 90°0′0′′S and 90°0′0′′N Latitude; 180°0′0′′W and 180°0′0′′E Longitude.

Table 1

Genera and species of the Planorbidae family deposited in the CMIOC.

Genus	Species
Acrobis	Acrorbis petricola
Antillorbis	Antillorbis nordestensis, Antillorbis salleanus
Biomphalaria	Biomphalaria adowensis, Biomphalaria alexandrina, Biomphalaria amazonica, Biomphalaria andecola, Biomphalaria choanomphala, Biomphalaria costata, Biomphalaria cousini, Biomphalaria glabrata, Biomphalaria havanensis, Biomphalaria helophila, Biomphalaria intermedia, Biomphalaria kuhniana, Biomphalaria nicaraguana, Biomphalaria obstructa, Biomphalaria occidentalis, Biomphalaria oligoza, Biomphalaria orbignyi, Biomphalaria pallida, Biomphalaria peregrina, Biomphalaria pfeifferi, Biomphalaria prona, Biomphalaria pucaraensis, Biomphalaria schrammi, Biomphalaria sericea, Biomphalaria stanleyi, Biomphalaria straminea, Biomphalaria subprona, Biomphalaria sudanica, Biomphalaria tenagophila, Biomphalaria thermala, Biomphalaria trigyra.
Drepanotrema	Drepanotema anatinum, Drepanotrema beltrani, Drepanotrema cimex, Drepanotrema depressissimum, Drepanotrema heloicum, Drepanotrema kermatoides, Drepanotrema limayanum, Drepanotrema lucidum, Drepanotrema pfeifferi, Drepanotrema pileatum, Drepanotrema simonsi, Drepanotrema surinamense
Ferrissia	Ferrissia fragilis
Gundlachia	Gundlachia radiata, Gundlachia ticaga
Gyraulus	Gyraulus acronicus, Gyraulus albus, Gyraulus boetzkesi, Gyraulus crista, Gyraulus percarinatus
Hebetancylus	Hebetancylus moricandi
Helisoma	Helisoma anceps, Helisoma campanulatum, Helisoma caribaeum, Helisoma corpulentum, Helisoma duryi, Helisoma foveale, Helisoma peruvianum, Helisoma trivolvis
Hippeutis	Hippeutis complanatus
Laevapex	Laevapex diaphanous
Planorbarius	Planorbarius corneus
Planorbis	Planorbis boissyi, Planorbis canonicus, Planorbis corneus, Planorbis metidjensis, Planorbis planorbis, Planorbis salleanus
Segmentina	Segmentina nitida
Tropicorbis	Tropicorbis riisei
Uncancylus	Uncancylus concentricus

In Brazil, the geographical distribution covers all five territorial regions, spanning the 26 states and the Federal District. The present database presents records of the occurrence of representatives of the family Planorbidae in a total of 592 municipalities (Midwest: recorded in 32 municipalities; Northeast: 120 municipalities; North: 27 municipalities; Southeast: 339 municipalities; and South: 74 municipalities). Biomphalaria is the most well-represented genus in CMIOC, including lots also from Africa, Asia, and Latin and North Americas, with a total of 3,926 lots. These specimens are registered in the following countries: Angola, Antigua, Argentina, Barbados, Belize, Bolivia, Chile, China, Costa Rica, Cuba, Egypt, El Salvador, Ecuador, United States, Ghana, Guadeloupe, Guatemala, Guyana, French Guiana, Haiti, Hong Kong, Jamaica, Martinique, Mexico, Mozambique, Nicaragua, Panama, Paraguay, Peru, Puerto Rico, Dominican Republic, Santa Lucia, Suriname, Tanzania, Trinidad, Uganda, Uruguay, and Venezuela (Table 2). Another well-represented genus of Planorbinae is Drepanotrema, which includes twelve species from different countries, with 2,312 lots (Table 3).

Table 2

Origin of the lots of Biomphalaria deposited in the CMIOC.

Country	Species	Country	Species	Country	Species	Country	Species
Angola	B. adowensis	Ecuador	B. cousini	Hong Kong	B. straminea	Dominican Republic	B. glabrata
Antigua	B. glabrata		B. peregrina	Jamaica	B. helophila		B. helophila
Argentina	B. intermedia		B. sericea		B. pallida		B. straminea
	B. oligoza		B. trigyra	Martinique	B. glabrata	Saint Lucia	B. glabrata
	B. orbignyi	United States of America	B. glabrata		B. kuhniana	Suriname	B. glabrata
	B. peregrina		B. havanensis		B. straminea		B. kuhniana
	B. straminea		B. peregrina	Mexico	B. obstructa		B. straminea
	B. tenagophila		B. obstructa	Mozambique	B. pfeifferi	Tanzania	B. choanomphala
Barbados	B. helophila	Ghana	B. pfeifferi	Nicaragua	B. helophila		B. pfeifferi
Belize	B. helophila	Guadeloupe	B. glabrata		B. nicaraguana		B. sudanica
	B. obstructa		B. kuhniana		B. obstructa	Trinidad	B. straminea
Bolivia	B. andecola		B. schrammi	Panama	B. kuhniana	Uganda	B. stanleyi
	B. pucaraensis	Guatemala	B. helophila	Paraguay	B. peregrina	Uruguay	B. straminea
Chile	B. costata		B. obstructa		B. occidentalis		B. tenagophila
	B. peregrina		B. subprona		B. tenagophila		B. tenagophila guaibensis
	B. thermala	Guyana	B. glabrata		B. straminea	Venezuela	B. glabrata
China	B. straminea		B. schrammi	Peru	B. andecola		B. peregrina
Costa Rica	B. helophila		B. straminea		B. helophila		B. prona
	B. straminea	French Guiana	B. glabrata		B. peregrina		B. straminea
Cuba	B. havanensis	Haiti	B. glabrata		B. pucaraensis
	B. helophila		B. havanensis		B. tenagophila
Egypt	B. alexandrina		B. helophila		B. trigyra
El Salvador	B. helophila		B. pallida	Puerto Rico	B. glabrata
	B. obstructa		B. obstructa		B. helophila
			B. straminea		B. peregrina

Table 3

Origin of the lots of Drepanotrema deposited in the CMIOC.

Species	Country	Number of lots	Species	Country	Number of lots
Drepanotrema anatinum	Argentina	11	Drepanotrema kermatoides	Argentina	22
	Belize	1		Brazil	32
	Brazil	521		Ecuador	2
	Costa Rica	1		Paraguay	1
	Ecuador	1		Peru	10
	Guatemala	3		Uruguay	12
	Guyana	1	Drepanotrema limayanum	Peru	6
	Haiti	2	Drepanotrema pfeifferi	Argentina	1
	Jamaica	4		Chile	3
	Mexico	1	Drepanotrema pileatum	Brazil	8
	Nicaragua	1	Drepanotrema lucidum	Antigua	1
	Panama	1		Argentina	23
	Puerto Rico	5		Barbados	1
	Dominican Republic	2		Belize	2
	Saint Lucia	1		Brazil	808
	Suriname	2		Ecuador	2
	Trinidad	3		United States	1
	Uruguay	1		Guadeloupe	4
	Uruguay	2		Guatemala	1
	Venezuela	2		Haiti	1
Drepanotrema beltrani	Mexico	1		Jamaica	8
Drepanotrema cimex	Argentina	7		Mexico	3
	Brazil	369		Nicaragua	2
	Haiti	1		Paraguay	5
	Jamaica	3		Puerto Rico	6
	Puerto Rico	1		Dominican Republic	2
	Uruguay	3		Saint Vincent	1
	Venezuela	3		Saint Lucia	3
Drepanotrema depressissimum	Antigua	1		Uruguay	4
	Argentina	13		Trinidad	2
	Barbados	2		Venezuela	1
	Brazil	295	Drepanotrema simonsi	Puerto Rico	1
	Costa Rica	1	Drepanotrema surinamense	Costa Rica	2
	Guadeloupe	7		Ecuador	2
	Nicaragua	2		Guadeloupe	1
	Paraguay	1		Guyana	1
	Peru	1		Panama	4
	Saint Lucia	2		Suriname	4
	Uruguay	3
	Venezuela	1
Drepanotrema heloicum	Argentina	15
	Brazil	3
	Uruguay	8

Considering lots from Brazil, the collection at CMIOC includes representatives from all 11 species of Biomphalaria that occur nationwide. Among them, three species play a significant role in the biological cycle of Brazil [33] and have a wide distribution. Together, these species account almost 40% of the total Planorbidae lots in the collection. Specifically, B. straminea is the most represented species with 1,257 lots, while B. tenagophila, and B. glabrata account for 811 and 654 lots, respectively.

The three species of Biomphalaria found in Brazil and recorded at CMIOC exhibit distinct geographic distributions within the country. However, there are certain states where these species overlap, indicating areas of coexistence (Figures 3–5).

Figure 3.

Spatial coverage of the occurrence dataset of B. straminea, from 1948 to 2023, based on the CMIOC, showing that most lots are from Rio Grande do Norte, with 256 lots.

Figure 4.

Spatial coverage of the occurrence dataset of B. tenagophila, from 1948 to 2023, based on the CMIOC, showing that most lots are from Rio de Janeiro State, with a total of 585 lots. The second more represented State is São Paulo, with 54 lots.

Figure 5.

Spatial coverage of the occurrence dataset of B. glabrata, from 1948 to 2023, based on the CMIOC, showing that most lots are from Bahia, with 302 lots.

B. straminea has the broadest geographic range among the three species in Brazil. It can be found in various states, from the North to the South of the country. Its distribution encompasses regions such as the Amazon, the Cerrado, the Caatinga, and the Atlantic Forest. The extensive presence of B. straminea highlights its significance as an intermediate host for the parasitic trematode. For a complete record of B. straminea in Brazil [34], CMIOC only lacks samples from the states of Santa Catarina and Roraima (Figure 3). On the other hand, B. tenagophila has a more restricted distribution compared to B. straminea. B. tenagophila is commonly found in areas of the South and Southeast of Brazil, primarily encompassing the states of São Paulo, Paraná, Santa Catarina, and Rio Grande do Sul (Figure 4). Finally, B. glabrata has a less limited geographic distribution than B. tenagophila in Brazil. Specifically, B. glabrata is predominantly found in coastal areas, particularly in the Northeast region of the country (Figure 5).

Data validation and quality control

Planorbidae specimens were identified by experienced taxonomists. The dataset is in Darwin Core format, and all mandatory fields are present and have undergone screening in the FIOCRUZ IPT.

Reuse potential

The presented dataset is important because it provides information on the distribution of Planorbidae, Planorbinae, and Biomphalaria in Brazil based on a renowned collection of medical malacology (i.e., CMIOC), traditionally known for its studies within the country. This dataset can provide the basis for future studies in evolution, ecology, and epidemiology, among others, especially for species of medical interest from the public health perspective. An important point of the current collection is the first recording of B. straminea in Amapá, serving as an important reference for research into the biodiversity of Planorbinae. These data expand the distribution of these species and provide occurrence information on the other species of this genus in Brazil. In addition to supporting the surveillance and control of schistosomiasis in Brazil, these data also contribute to the knowledge of Biomphalaria biodiversity. They are also an important resource for managing the CMIOC (Figure 6).

Figure 6.

Interactive map of the georeferenced occurrences hosted by GBIF [8]. https://www.gbif.org/dataset/2bd86564-44c0-4317-a04e-79b544a84a06

Data availability

The dataset used in this article is published through the FIOCRUZ – Oswaldo Cruz Foundation IPT – and is provided under a CC0 waiver from GBIF [8] and in the SiBBr repository [34].

Editor’s note

This paper is part of a series of Data Release articles working with GBIF and supported by TDR, the Special Programme for Research and Training in Tropical Diseases hosted at the World Health Organization, in order to publish datasets on vectors of human diseases [35].

Abbreviations

CMIOC, Collection of Mollusks of the Oswaldo Cruz Institute; FIOCRUZ, Fundação Oswaldo Cruz; GBIF, Global Biodiversity Information Facility; IPT: integrated publishing toolkit; SiBBr, Sistema de Informação sobre a Biodiversidade Brasileira.

Declarations

Ethical approval

The authors declare that ethical approval was not required for this type of research.

Competing interests

The authors declare that they have no competing interests.

Funding

Acknowledgements

We thank Clara Baringo Fonseca (SiBBr - Rede Nacional de Ensino e Pesquisa - Rnp) for their support during the dataset preparation and Paloma Helena Fernandes Shimabukuro from GBIF for their encouragement while we developed this study. We also thank all CMIOC staff for their contribution over the years.

References

1StrongEE, GargominyO, PonderWF Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Freshwater Animal Diversity Assessment, 2008; 595: 149–166. doi:10.1007/s10750-007-9012-6.

2FernandezMA, FeitosaES, ThiengoSC. Planorboidea, Planorbidae, Planorbinae. In: DamboreneaC, RogersDC, ThorphHJ (eds), Key to Neotropical and Antarctic Fauna. vol. 5, (4): Academic Press, 2020; pp. 313–327.

3World Health Organization. Schistosomiasis. 2020. Retrieved from https://www.who.int/news-room/fact-sheets/detail/schistosomiasis.

4CarvalhoOS. Moluscos Hospedeiros Intermediários de Schistosoma Mansoni do Brasil/Omar dos Santos Carvalho. Belo Horizonte: Instituto Rene Rachou /Fundação Oswaldo Cruz, 2020; p. 124.

5ParaenseWL. Biomphalaria straminea, B. tenagophila and B. occidentalis: comparative anatomy, histology and susceptibility to Schistosoma mansoni. Mem. Inst. Oswaldo Cruz, 1986; 81: 87–97.

6GomesSR, FernandezMA, SilvaEF The Oswaldo Cruz Institute Mollusk Collection: improvements on diversity and infrastructure over the last years. Arq. Ciên. Mar, 2016; 49: 60–68.

7VargaI, VanD. Fronteiras da urbanidade sanitária: sobre o controle da malária. Rev. Saúde Pública, 2007; 16: 28–44.

8SoutoADSS, ThiengoSC. GBIF Coleção de Moluscos do Instituto Oswaldo Cruz. Fundação Oswaldo Cruz. Occurrence dataset. 2023; https://doi.org/10.15468/rptb83.

9ParaenseWL. Estado atual da sistemática dos planorbídeos brasileiros. Arq. Mus. Nac., 1975; 55: 105–128.

10SimoneLR. Land and Freshwater Molluscs of Brazil. São Paulo: Editora EGB, Fapesp, 2006; p. 390.

11FernandezMA, ThiengoSC, AmaralR. Técnicas Malacológicas. Vigilância e Controle de Moluscos de Moluscos de Importância Médica: Diretrizes Técnicas. Editora do Ministério da Saúde, 2008; pp. 43–70.

12SantosSB, OvandoXMC, LacerdaEM. Planorbioidea, Planorbidae, Ancylinae. In: DamboreneaC, RogersDC, ThorpHJ (eds), Keys to Neotropical and Antarctic Fauna. Academic Press, 2020; pp. 302–307.

13ParaenseWL. Australorbis intermedius sp. n. from Brazil. Rev. Bras. Biol., 1962; 22: 343–350.

14ParaenseWL. Biomphalaria amazonica and B. cousini, two new species of Neotropical planorbid molluscs. Rev. Bras. Biol., 1966; 26: 115–126.

15ParaenseWL. The Brazilian species of Drepanotrema. IX: D. pileatum sp. n. Rev. Bras. Biol., 1971; 31: 271–276.

16ParaenseWL. Biomphalaria oligoza n. n. for Tropicorbis philippianus (Dunker) sensu Lucena. Rev. Bras. Biol., 1974; 34: 379–386.

17ParaenseWL. Lymnaea viatrix: a study of topotypic specimens (Mollusca: Lymnaeidae). Rev. Bras. Biol., 1976; 36: 419–428.

18ParaenseWL. Biomphalaria occidentalis sp. n. from South America (Mollusca Basommatophora Pulmonata). Mem. Inst. Oswaldo Cruz, 1981; 76: 199–211.

19ParaenseWL. Lymnaea rupestris sp. n. from southern Brazil (Pulmonata: Lymnaeidae). Mem. Inst. Oswaldo Cruz, 1982; 77: 437–443.

20ParaenseWL. Lymnaea diaphana: a study of topotypic specimens (Pulmonata: Lymnaeidae). Mem. Inst. Oswaldo Cruz, 1984; 79: 75–81.

21ParaenseWL. Biomphalaria kuhniana (Clessin, 1883), planorbid mollusc from South America. Mem. Inst. Oswaldo Cruz, 1988; 83: 1–12.

22ParaenseWL. Biomphalaria obstructa (Morelet, 1849): a study of topotypic specimens (Mollusca: Pulmonata: Planorbidae). Mem. Inst. Oswaldo Cruz, 1990; 85: 391–399.

23ParaenseWL. Biomphalaria subprona (Martens, 1899 (Gastropoda: Planorbidae). Mem. Inst. Oswaldo Cruz, 1996; 91: 187–190.

24ParaenseWL. Plesiophysa dolichomastix sp. n. (Gastropoda: Planorbidae). Mem. Inst. Oswaldo Cruz, 2002; 97: 505–508.

25ParaenseWL, PointierJP. Physa acuta Draparnaud 1805 (Gastropoda: Physidae): a study of topotypic specimens. Mem. Inst. Oswaldo Cruz, 2003; 98: 513–517.

26ThiengoSC, FernandezMA, BoaventuraMF Freshwater snails and schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: I- Metropolitan Mesoregion. Mem. Inst. Oswaldo Cruz, 2001; 96: 177–184.

27ThiengoSC, FernandezMA, BoaventuraMFF Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: III – Baixada Mesoregion. Mem. Inst. Oswaldo Cruz, 2002; 97: 43–46.

28ThiengoSC, FernandezAM, BoaventuraMF Freshwater snails and schistosomiasis mansoni in the state of Rio de Janeiro, Brazil. II- Centro Fluminense Mesoregion. Mem. Inst. Oswaldo Cruz, 2002; 97: 621–626.

29ThiengoSC, MattosAC, BoaventuraMFF Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: V - Norte Fluminense Mesoregion. Mem. Inst. Oswaldo Cruz, 2004; 99: 99–103.

30ThiengoSC, MattosAC, BoaventuraMFF Freshwater snails and schistosomiasis mansoni in the State of Rio de Janeiro, Brazil: IV - Sul Fluminense Mesoregion. Mem. Inst. Oswaldo Cruz, 2004; 99: 275–280.

31ThiengoSARC, SantosSB, FernandezMA. Malacofauna límnica da área de influência do lago da usina hidrelétrica de Serra da Mesa, Goiás, Brasil: I. Estudo qualitativo. Rev. Bras. Zool., 2005; 22: 867–874.

32ThiengoSC, MattosAC, SantosSB Freshwater snails and schistosomiasis mansoni in the state of Rio de Janeiro, Brazil: VI - Noroeste Fluminense Mesoregion. Mem. Inst. Oswaldo Cruz, 2006; 101: 239–245.

33ThiengoST, FernandezMA. Moluscos. In: Vigilância e controle de moluscos de importância epidemiológica: diretrizes técnicas: Programa de Vigilância e Controle da Esquistossomose. Brasília: Ministério da Saúde, Departamento de Vigilância Epidemiológica, 2008; pp. 13–36, ISBN 978-85-334-1438-9.

34Fiocruz/CMIOC - Coleção de Moluscos do Instituto Oswaldo Cruz. v1.48. FIOCRUZ - Oswaldo Cruz Foundation. Dataset/Occurrence. http://ipt.fiocruz.br/ipt/resource?r=fiocruz_cmioc&v=1.48.

35Vectors of Human Disease Series. GigaByte. 2022; https://doi.org/10.46471/GIGABYTE_SERIES_0002.