Biological control of <i>Biomphalaria</i>, the intermediate host of <i>Schistosoma</i> spp.: a systematic review

Friani, Gabriela; Amaral, Ana Margarida Ribeiro do; Quinelato, Simone; Mello-Silva, Clélia Christina; Golo, Patrícia Silva

doi:10.1590/0103-8478cr20210714

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Parasitology • Cienc. Rural 53 (4) • 2023 • https://doi.org/10.1590/0103-8478cr20210714 copy

Biological control of Biomphalaria, the intermediate host of Schistosoma spp.: a systematic review

Controle biológico de Biomphalaria, hospedeiro intermediário do Schistosoma spp.: uma revisão sistemática

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT:

Schistosomiasis is an important vector-borne disease transmitted by an intermediate host: a freshwater mollusk. Control of these snail vectors is one of the strategies of the World Health Organization against the disease. The present study was based on a systematic review of published scientific papers concerning the biological control of snails (genus Biomphalaria), and identified the ongoing challenges and propose future perspectives. The review methodology was based on the PRISMA statement, the international databases Web of Science and Scopus for the period 1945-2021. In total, 47 papers were analyzed, published by authors from 14 different countries, the majority being from: France, Brazil, the United States, and Egypt. The most widely used strategy for biological control was predation by fish (12 studies). Fourteen papers were published in the most prolific decade 2010-2019; during which there was also a greater diversity of biological control agents in studies. In this context, we believed that one of the principal challenges of this approach is the successful simultaneous use of multiple types of biological control agent: predators, competitors, and/or microbial agents. This new approach may provide important insights for the development of new biological control agents or microbial-based products, with the potential to reduce the parasite load carried by schistosomiasis snail vector and control its transmission in a sustainable way.

Key words:
schistosomiasis; neglected diseases; predation; competition; microbial control

Universidade Federal de Santa Maria Universidade Federal de Santa Maria, Centro de Ciências Rurais , 97105-900 Santa Maria RS Brazil , Tel.: +55 55 3220-8698 , Fax: +55 55 3220-8695 - Santa Maria - RS - Brazil
E-mail: cienciarural@mail.ufsm.br

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[1] E-mail: clelia@ioc.fiocruz.br. ^*Corresponding author

Biological control agent	Biomphalaria species	Target stage	Effect on Schistosoma assessed	Main results	Reference
Lebistes reticulatus (guppy)	B. glabrata	Egg mass/ young	No	Preference for eggs masses to hatch and snails shedding cercariae	OLIVER-GONZÁLEZ (1946)
Serranochromis macrocephala (fish)	Biomphalaria sp.	All stages	No	After three months, the tank was drained and no small snails were found in it	DE BONT & DE BONT (1952DE BONT, A. & DE BONT HERS, M. Mollusc control and fish-farming in Central Africa. Nature, v. 170, p. 323-324, 1952. Available from: <Available from: https://www.nature.com/articles/170323a0 >. Accessed: Jun. 17, 2020. doi: 10.1038/170323a0. https://www.nature.com/articles/170323a0... )
Marisa cornuarietis (snail)	B. glabrata, B. pfeifferi	Egg masses/ young	No	M. cornuarietis devoured egg masses and young Biomphalaria	CHERNIN et al. (1956aCHERNIN, E. et al. Studies on the biological control of schistosome-bearing snails. I. The control of Australorbis glabratus populations by the snail, Marisa cornuarietis, under laboratory conditions. American Journal of Tropical Medicine and Hygiene, v. 5, p. 297-307, 1956a. Available from: <Available from: https://www.ajtmh.org/view/journals/tpmd/5/2/article-p297.xml >. Accessed: Jul. 15, 2021. doi: 10.4269/ajtmh.1956.5.297. https://www.ajtmh.org/view/journals/tpmd... )
Helobdella fusca (leech)	Australorbis glabratus = B. glabrata	Young and newly hatched	No	Adult leeches anchor themselves in the shell until the snail is devoured	CHERNIN et al. (1956bCHERNIN, E. et al. Studies on the biological control of schistosome-bearing snails. II. The control of Australorbis glabratus populations by the leech, Helobdella fusca, under laboratory conditions. American Journal of Tropical Medicine and Hygiene, v. 5, p. 308-314, 1956b. Available from: <Available from: https://doi.org/10.4269/ajtmh.1956.5.308 >. Accessed: Jul. 15, 2021. doi: 10.4269/ajtmh.1956.5.308 https://doi.org/10.4269/ajtmh.1956.5.308... )
M. cornuarietis (snail)	B. glabrata	Adults	No	The disappearance of B. glabrata coincided with the introduction of Marisa	RUIZ-TIBEN et al. (1969RUIZ-TIBÉN, E. et al. Biological control of Biomphalaria-glabrata by Marisa cornuarietis in irrigation ponds in Puerto-Rico. Bulletin World Health Organization, v. 41, p. 329-333, 1969. Available from: <Available from: https://apps.who.int/iris/handle/10665/262234 >. Accessed: Jun. 18, 2021. https://apps.who.int/iris/handle/10665/2... )
Pomacea sp. (snail)	B. glabrata	Egg mass/ newly hatched	No	Pomacea sp. caused a reduction in the number eggs and impeded the establishment of B. glabrata colonies	PAULINYI & PAULINIPAULINYI, H. M. & PAULINI, E. Laboratory observations on biological-control of Biomphalaria-glabrata by a species of Pomacea (Ampullariidae). Bulletin World Health Organization, v. 46, p. 243-247, 1972. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/4537485/ >. Accessed: Jun. 3, 2021. https://pubmed.ncbi.nlm.nih.gov/4537485/... (1972)
Astatoreochromis alluandi, Tilapia leucosticta, T. Zillii, Gambusia affinis (fishs)	B. pfeifferi	Adults	No	A. alluaudi reduced the number of B. pfeifferi. T. zilliie and T. leucosticta did not appear to be associated with reduction in the snail populations	MCMAHON et al. (1977MCMAHON, J. P. et al. Studies on biological-control of intermediate hosts of schistosomiasis in Western Kenya. Environmental Conservation, v. 4, p. 285-289, 1977. Available from: <Available from: https://www.cambridge.org/core/journals/environmental-conservation/article/abs/studies-on-biological-control-of-intermediate-hosts-of-schistosomiasis-in-western-kenya/0D878737CB643BAF8B114B51F2DD4050 >. Accessed: Jun. 5, 2021. doi: 10.1017/S0376892900026205. https://www.cambridge.org/core/journals/... )
T. rendalli and Sarotherodon mossambica (fishs)	B. glabrata	All stages	No	S. mossambica preyed on snails occasionally. T. rendalli reduced the snail population	GRABER et al. (1981GRABER, M. et al. Lutte biologique contre les mollusques vecteurs de Bilharziose. Action predatrice de Tilapia rendalli, Boulenger et de Sarotherodon mossambica, Peters a l’égard de Biomphalaria glabrata, Say. Hydrobiologia, v. 78, p. 253-257, 1981. Available from: <Available from: https://doi.org/10.1007/BF00008521 >. Accessed: Jun. 10, 2021. doi: 10.1007/BF00008521. https://doi.org/10.1007/BF00008521... )
T. nilotica (fish)	B. glabrata	Adult	No	The fish impeded hatching and thus limited the growth of the four study populations	ANDRADE (1982ANDRADE, R. M. Controle biológico de Biomphalaria glabrata (Say, 1818) através de Tilapia nilotica (Hasselquist, 1757), em laboratório (Pulmonata, Planorbidae. Pisces, Cichlidae). Revista da Sociedade Brasileira de Medicina Tropical, v. 15, p. 39-52, 1982. Available from: <Available from: https://doi.org/10.1590/S0037-86821982000100004 >. Accessed: Jun. 15, 2020. doi: 10.1590/S0037-86821982000100004. https://doi.org/10.1590/S0037-8682198200... )
H. triserialis lineata (leech)	B. glabrata	All stages	No	No predation of egg masses, but young specimens preyed on more than adults	GUIMARÃES et al. (1983GUIMARÃES, C. T. et al. Biological control: Helobdella-triserialis-lineata Blanchard, 1849 (Hirudinea, Glossiphonidae) over Biomphalaria glabrata Say, 1818 (Mollusca, Planorbidae), in laboratory. Revista de Saúde Pública, v. 17, p. 481-492, 1983. Available from: <Available from: https://www.scielo.br/j/rsp/a/78rdhnVYw8Mj3bgLDPrpsbh/abstract/?lang=pt >. Accessed: Jun. 3, 2021. doi: 10.1590/S0034-89101983000600005. https://www.scielo.br/j/rsp/a/78rdhnVYw8... )
H. triserialis lineata (leech)	B. straminea, tenagophila	All stages	No	Velocity of predation inversely proportional to the size of the snails, no predation of egg masses	GUIMARÃES et al. (1984GUIMARÃES, C. T. et al. Controle biológico: Helobdella triserialis Lineata (Hirudinea: Glossiphonidae) sobre Biomphalaria straminea e Biomphalaria tenagophila (Mollusca: Planorbidae), em laboratório. Revista de Saúde Pública, v. 18, p. 476-486, 1984. Available from: <Available from: https://www.scielo.br/j/rsp/a/LYNvN5KQ3X3gNwxRkmfjvfx/?lang=pt >. Accessed: Jun. 3, 2021. doi: 10.1590/S0034-89101984000600006. https://www.scielo.br/j/rsp/a/LYNvN5KQ3X... )

Biological control agent	Biomphalaria species	Target stage	Effect on Schistosoma assessed	Main results	Reference
Geophagus brasiliensis (fish)	B. tenagophila	Juvenile/ adult	No	The predator fed on the snails in both conditions, preying preferentially on snails of 5-11 cm	WEINZETTL & JURBERG (1990WEINZETTL, M. & JURBERG, P. Biological control of Biomphalaria tenagophila (Mollusca, Planorbidae), a schistosomiasis vector, using the fish Geophagus brasiliensis (Pisces, Cichlidae) in the laboratory or in a seminatural environment. Memórias Instituto Oswaldo Cruz, v. 85, p. 35-38, 1990. Available from: <Available from: https://www.scielo.br/j/mioc/a/7Zrf69d8N6GmDdLwnRn9ypf/?lang=en >. Accessed: Jun. 14, 2021. doi: 10.1590/S0074-02761990000100005. https://www.scielo.br/j/mioc/a/7Zrf69d8N... )
Procambarus clarkii (crayfish)	B. pfeifferi	Adult	No	P. clarkii reduced the abundance of snails by 5 days, after 30 days there were no live snails in the tanks containing 4 crayfish.	HOFKIN et al. (1991HOFKIN, B. V. et al. The North American crayfish Procambarus clarkii and the biological control of schistosome-transmitting snails in Kenya: Laboratory and field investigations. Biological Control, v. 1, p. 183-187, 1991. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/1049964491900658 >. Accessed: Jun. 23, 2021. doi: 10.1016/1049-9644(91)90065-8. https://www.sciencedirect.com/science/ar... )
M. cornuarietis and Ampullaria glauca (snails)	B. glabrata	All states	Yes	M. cornuarietis colonization was rapid, and all B. glabrata were eliminated, as was S. mansoni infection in local mice	POINTIER et al. (1991POINTIER, J. P. et al. Eradication of a sylvatic focus of Schistosoma mansoni using biological control by competitor snails. Biological Control, v. 1, p. 244-247, 1991. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/1049964491900739 >. Accessed: May. 03, 2021. doi: 10.1016/1049-9644(91)90073-9. https://www.sciencedirect.com/science/ar... )
P. clarkii (crayfish)	B. pfeifferi B. glabrata	Adult All stages	No	Crayfish consumed adult Biomphalaria, affecting the survival of juveniles snails	HOFKIN et al. (1992HOFKIN, B. V. et al. Predation of Biomphalaria and nontarget mollusks by the crayfish Procambarus clarkii: Implications for the biological control of schistosomiasis. Annals of Tropical Medicine & Parasitology, v. 86, p. 663-670, 1992. Available from: <Available from: https://www.tandfonline.com/doi/abs/10.1080/00034983.1992.11812723?journalCode=ypgh19/ >. Accessed: Jun. 4, 2021. doi:10.1080/00034983.1992.11812723. https://www.tandfonline.com/doi/abs/10.1... )
T. rendalli, Sargochromis codringtoni (fishes)	B. pfeifferi	Adult	No	T. rendalli was primarily herbivorous and S. codringtoni was malacophagous	CHIMBARI et al. (1996CHIMBARI, M. J. et al. Food selection behaviour of potential biological agents to control intermediate host snails of schistosomiasis: Sargochromis codringtoni and Tilapia rendalli. Acta Tropica, v. 61, p. 191-199, 1996. Available from: < Available from: https://www.sciencedirect.com/science/article/pii/0001706X95001444 >. Accessed: Jun. 5, 2021. doi: 10.1016/0001-706X(95)00144-4. https://www.sciencedirect.com/science/ar... )
Sargochromis codringtoni (fish)	B. pfeifferi	Adult	No	Each fish consumed approximately 800 snails within 1 week	CHIMBARI et al. (1997CHIMBARI, M. J. et al. Laboratory experiments on snail predation by Sargochromis codringtoni, a candidate for biological control of the snails that transmit schistosomiasis. Annals of Tropical Medicine & Parasitology, v. 91, p. 95-102, 1997. Available from: < Available from: https://www.sciencedirect.com/science/article/pii/0001706X95001444 >. Accessed: Jun. 5, 2021. doi: 0.1080/00034983.1997.11813116. https://www.sciencedirect.com/science/ar... )
M. cornuarietis (snail)	B. glabrata	All stages	No	B. glabrata disappeared from the ponds with M. cornuarietis	POINTIER & DAVID (2004POINTIER, J. P. & DAVID, P. Biological control of Biomphalaria glabrata, the intermediate host of schistosomes, by Marisa cornuarietis in ponds of Guadeloupe: long-term impact on the local snail fauna and aquatic flora. Biological Control, v. 29, p. 81-89, 2004. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S1049964403001373 >. Accessed: Jun. 4, 2021. doi: 10.1016/S1049-9644(03)00137-3. https://www.sciencedirect.com/science/ar... )
Clarias gariepinus (fish)	B. pfeifferi	Adult/ egg mass	No	It took 32 days to consume all the snails (with proper food) and 16 days (with limited food)	GASHAW et al. (2008GASHAW, F. et al. Assessment of the potential of competitor snails and African catfish (Clarias gariepinus) as biocontrol agents against snail hosts transmitting schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene, v. 102, p. 774-779, 2008. Available from: <Available from: https://academic.oup.com/trstmh/article-abstract/102/8/774/1896026?redirectedFrom=fulltext >. Accessed: Jun. 27, 2021. doi: 10.1016/j.trstmh.2008.04.045. https://academic.oup.com/trstmh/article-... )
P. clarkii (crayfish)	B. alexandrina	Adult	No	Laboratory: all snails were consumed; Field: reduction/ absence of snail	KHALIL & SLEEM (2011KHALIL, M. T. & SLEEM, S. H. Can the freshwater crayfish eradicate schistosomiasis in Egypt and Africa? Journal of American Science, v. 7, p. 457-462, 2011. Available from: <Available from: http://www.jofamericanscience.org/journals/am-sci/am0707/068_6295am0707_457_462.pdf >. Accessed: Jun. 27, 2021. http://www.jofamericanscience.org/journa... )

Biological control agent	Biomphalaria species	Target stage	Effect on Schistosoma assessed	Main results	Reference
Macrobrachium vollenhovenii (prawn)	Biomphalaria sp.	All stages	Yes (theoretically)	Reintroduction of male shrimp controlled snail, decreasing the prevalence of schistosomiasis	SAVAYA et al. (2014SAVAYA, A. A. M. I. T. et al. The prawn Macrobrachium vollenhovenii in the Senegal river basin: Towards sustainable restocking of all-male populations for biological control of schistosomiasis. Plos Neglected Tropical Diseases, v. 8, e3060, 2014. Available from: <Available from: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0003060 >. Accessed: Jun. 5, 2021. doi: 10.1371/journal.pntd.0003060. https://journals.plos.org/plosntds/artic... )
M. vollenhovenii (prawn)	B. pfeifferi	Not specified	Yes	80% reduction of infected snails, prevalence of human schistosomiasis 50% lower and egg load 50% lower	SOKOLOW et al. (2015SOKOLOW, S. H. et al. 2015. Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host. Proceedings of the National Academy of Sciences, v. 112, p. 9650-9655, 2015. Available from: <Available from: https://www.pnas.org/content/114/33/E7028 >. Accessed: Jun. 17, 2021. doi: 10.1073/pnas.1712011114. https://www.pnas.org/content/114/33/E702... )
Gambusia affinis (fish)	B. pfeifferi	All stages	No	All egg masses and neonate snails were preyed, and number of adult snails reduced	SULIEMAN et al. (2015SULIEMAN, Y. et al. Laboratory evaluation of the biological control of the snail, Biomphalaria pfeifferi, the intermediate host of Schistosoma mansoni, using the fish, Gambusia affinis. Egyptian Journal of Biological Pest Control, v. 25, p. 351-354, 2015. Available from: <Available from: https://ejbpc.springeropen.com/ >. Accessed: Jun. 7, 2021. https://ejbpc.springeropen.com/... )
Sepedon ruficeps (larva of Diptera)	B. pfeifferi	Not specified	Yes	Parasitized B. pfeifferi were attacked more frequently	AGBOHO et al. (2017AGBOHO, A. P. et al. Potential of Sepedon ruficeps Becker (Diptera: Sciomyzidae) larvae for biological control of intermediate snail hosts of schistosomiasis in Benin (West Africa). International Journal of Multidisciplinary and Current Research, v. 5, p. 1035-1040, 2017. Available from: <Available from: http://ijmcr.com/potential-of-sepedon-ruficeps-becker-diptera-sciomyzidae-larvae-for-biological-control-of-intermediate-snail-hosts-of-schistosomiasis-in-benin-west-africa >. Accessed: Jun. 14, 2021. http://ijmcr.com/potential-of-sepedon-ru... )
Sphaerodema urinator (water bug)	B. alexandrina	Not specified	No	The predator attacked and ingested the snails, preferring small snails	YOUNES et al. (2017YOUNES, A. et al. Biological control of snail hosts transmitting schistosomiasis by the water bug, Sphaerodema urinator. Parasitology Research, v. 116, p. 1257-1264, 2017. Available from: <Available from: https://link.springer.com/article/10.1007%2Fs00436-017-5402-5 >. Accessed: Jun. 5, 2021. doi: 10.1007/s00436-017-5402-5. https://link.springer.com/article/10.100... )
Labeo niloticus and Cyrinus carbio (fishes)	B. pfeifferi	All stages	No	Both fish are efficient predators of the egg mass and neonates, and reduce the number of adult snails	AFIFI & AHMED (2018AFIFI, A. A & AHMED, A. A. The efficiency of two Nile fishes as biocontrol agents against different stages of schistosomiasis intermediate host. Journal of The Faculty of Science and Technology, v. 5, 2018. Available from: <Available from: https://journal.oiu.edu.sd/index.php/JFST/article/view/359 >. Accessed: Jul. 14, 2021. doi: <https://doi.org/10.52981/jfst.vi5.359>. https://journal.oiu.edu.sd/index.php/JFS... )

Biological control agent	Biomphalaria species	Target stage	Effect on Schistosoma assessed	Main results	Reference
M. cornuarietis (snail)	B. glabrata	Young/adults	No	After 2 years, the ponds with M. cornuarietis had no A. glabratus	FERGUSON et al. (1958FERGUSON, F. F. et al. Potential for biological control of Australorbis glabratus, the intermediate host of Puerto Rican schistosomiasis. American Journal of Tropical Medicine and Hygiene, v. 7, p. 491-493, 1958. Available from: <Available from: https://www.ajtmh.org/view/journals/tpmd/7/5/article-p491.xml >. Accessed: Jul. 15, 2021. doi: 10.4269/ajtmh.1958.7.491. https://www.ajtmh.org/view/journals/tpmd... )
M. cornuarietis (snail)	B. glabrata	Young/adults	No	A. glabratus disappeared after 1.5 years, there are no schistosomiasis infections in preschool children	OLIVER-GONZALEZ & FERGUSON (1959OLIVER-GONZÁLEZ, J. & FERGUSON, F. F. Probable biological control of schistosomiasis mansoni in a Puerto-Rican watershed. American Journal of Tropical Medicine and Hygiene, v. 8, p. 56-59, 1959. Available from: <Available from: https://www.ajtmh.org/view/journals/tpmd/8/1/article-p56.xml >. Accessed: Jul. 18, 2021. doi: 10.4269/ajtmh.1959.8.56. https://www.ajtmh.org/view/journals/tpmd... )
M. cornuarietis (snail)	B. glabrata	Adults	No	The disappearance of B. glabrata coincided with the introduction of Marisa	RUIZ-TIBEN et al. (1969RUIZ-TIBÉN, E. et al. Biological control of Biomphalaria-glabrata by Marisa cornuarietis in irrigation ponds in Puerto-Rico. Bulletin World Health Organization, v. 41, p. 329-333, 1969. Available from: <Available from: https://apps.who.int/iris/handle/10665/262234 >. Accessed: Jun. 18, 2021. https://apps.who.int/iris/handle/10665/2... )
M. cornuarietis (snail)	B. glabrata	Adults	No	The study emphasized the low cost and simplicity of the method	JOBIN & BERRÍOS-DURÁN (1970JOBIN, W. R. & BERRÍOS-DURÁN, L. A. Cost of harvesting and spreading Marisa cornuarietis for biological control of Biomphalaria glabrata in Aibonito, Puerto Rico. Bulletin World Health Organization, v. 42, p. 177-979, 1970. Available from: <Available from: https://apps.who.int/iris/handle/10665/262315 >. Accessed: Jun. 3, 2021. https://apps.who.int/iris/handle/10665/2... )
Pomacea sp. (snail)	B. glabrata	Egg mass/ newly hatched	No	Pomacea sp. caused a reduction in the number eggs and impeded the establishment of B. glabrata colonies	PAULINYI & PAULINI (1972PAULINYI, H. M. & PAULINI, E. Laboratory observations on biological-control of Biomphalaria-glabrata by a species of Pomacea (Ampullariidae). Bulletin World Health Organization, v. 46, p. 243-247, 1972. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/4537485/ >. Accessed: Jun. 3, 2021. https://pubmed.ncbi.nlm.nih.gov/4537485/... )
T. granifera (snail)	B. glabrata	All stages	No	B. glabrata was eliminated from 22 months after T. granifera was introduced	PRENTICE (1983PRENTICE, M. A. Displacement of Biomphalaria glabrata by the snail Thiara granifera in field habitats in St. Lucia, West Indies. Annals of Tropical Medicine & Parasitology, v. 77, p. 51-59, 1983. Available from: <Available from: https://www.tandfonline.com/doi/abs/10.1080/00034983.1983.11811672 >. Accessed: Jun. 10, 2021. doi: 10.1080/00034983.1983.11811672. https://www.tandfonline.com/doi/abs/10.1... )
Ampullaria glauca (snail)	B. glabrata	All stages	Yes	A. glauca decimated the plant Pistia stratiotes (habitat of B. glabrata), reducing the population snails and S. mansoni	POINTIER (1988POINTIER, J. P. Decline of a sylvatic focus of Schistosoma mansoni in Guadeloupe (French West Indies) following the competitive displacement of the snail host Biomphalaria glabrata by Ampullaria glauca. Oecologia, v. 75, p. 38-43, 1988. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/28311831/ >. Accessed: Jul. 16, 2021. doi: 10.1007/BF00378811. https://pubmed.ncbi.nlm.nih.gov/28311831... )
Thiara tuberculata (snail)	B. glabrata and B. straminea	All stages	No	Decline of Biomphalaria populations and the complete after two years	POINTIER et al. (1989POINTIER, J. P. et al. Biological control of Biomphalaria glabrata and Biomphalaria straminea by the competitor snail Thiara tuberculata in a transmission site of schistosomiasis in Martinique, French-West-Indies. Annals of Tropical Medicine and Parasitology, v. 83, p. 363-369, 1989. Available from: <Available from: http://dx.doi.org/10.1080/00034983.1989.11812342 >. Accessed: Jul. 25, 2021. doi: 10.1080/00034983.1989.11812342. http://dx.doi.org/10.1080/00034983.1989.... )

Biological control agent	Biomphalaria species	Target stage	Effect on Schistosoma assessed	Main results	Reference
M. cornuarietis and Ampullaria glauca (snails)	B. glabrata	All states	Yes	M. cornuarietis colonization was rapid, and all B. glabrata were eliminated, as was S. mansoni infection in local mice	POINTIER et al. (1991POINTIER, J. P. et al. Eradication of a sylvatic focus of Schistosoma mansoni using biological control by competitor snails. Biological Control, v. 1, p. 244-247, 1991. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/1049964491900739 >. Accessed: May. 03, 2021. doi: 10.1016/1049-9644(91)90073-9. https://www.sciencedirect.com/science/ar... )
Melanoides (=Thiara) tuberculata (snail)	B. pfeifferi	All stages	No	Both species persisted over the study period, with M. tuberculata more abundant	MKOJI et al. (1992MKOJI, G. M. et al. Does the snail Melanoides tuberculata have a role in biological control of Biomphalaria pfeifferi and other medically important african pulmonates. Annals of Tropical Medicine & Parasitology, v. 86, p. 201-204, 1992. Available from: <Available from: https://www.tandfonline.com/doi/abs/10.1080/00034983.1992.11812654 >. Accessed: Jun. 04, 2021. doi: 10.1080/00034983.1992.11812654. https://www.tandfonline.com/doi/abs/10.1... )
M. tuberculata (snail)	B. glabrata	All stages	No	Reduction of B. glabrata populations to very low levels, reducing/eliminating S. mansoni	POINTIER (1993POINTIER, J. P. The introduction of Melanoides tuberculata (Mollusca: Thiaridae) to the island of Saint Lucia (West Indies) and its role in the decline of Biomphalaria glabrata, the snail intermediate host of Schistosoma mansoni. Acta Tropica, v. 54, p. 13-18, 1993. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/0001706X9390064I?via%3Dihub >. Accessed: Jun. 12, 2021. doi: 10.1016/0001-706x(93)90064-i. https://www.sciencedirect.com/science/ar... )
M. tuberculata (snail)	B. glabrata	All stages	No	B. glabrata population was reduced until it disappeared	POINTER et al. (1993)
M. tuberculata (snail)	B. glabrata	All stages	No	The population of B. glabrata reached lower density in the 4th year	GIOVANELLI et al. (2003GIOVANELLI, A. et al. Apparent competition through facilitation between Melanoides tuberculata and Biomphalaria glabrata and the control of schistosomiasis. Memórias do Instituto Oswaldo Cruz, v. 98, p. 429-431, 2003. Available from: <Available from: https://www.scielo.br/j/mioc/a/szFBkJkHzVff6zgYZxv9SRx/abstract/?lang=en >. Accessed: Jul. 15, 2021. doi: 10.1590/S0074-02762003000300025. https://www.scielo.br/j/mioc/a/szFBkJkHz... )
B. tenagophila Taim strain (resistant to S. mansoni)	B. tenagophila susceptible to S. mansoni	Adult	Yes (theoretically)	The introduction of the Taim strain would produce resistant descendants	COELHO et al. (2004COELHO, P. M. Z. et al. Biomphalaria tenagophila/Schistosoma mansoni interaction: Premises for a new approach to biological control of schistosomiasis. Memórias do Instituto Oswaldo Cruz, v. 99, p. 109-111, 2004. Available from: <Available from: https://pubmed.ncbi.nlm.nih.gov/9093434/ >. Accessed: Jun. 4, 2021. doi: 10.1080/00034983.1997.11813116. https://pubmed.ncbi.nlm.nih.gov/9093434/... )
M. cornuarietis (snail)	B. glabrata	All stages	No	B. glabrata disappeared from the ponds with M. cornuarietis	POINTIER & DAVID (2004POINTIER, J. P. & DAVID, P. Biological control of Biomphalaria glabrata, the intermediate host of schistosomes, by Marisa cornuarietis in ponds of Guadeloupe: long-term impact on the local snail fauna and aquatic flora. Biological Control, v. 29, p. 81-89, 2004. Available from: <Available from: https://www.sciencedirect.com/science/article/abs/pii/S1049964403001373 >. Accessed: Jun. 4, 2021. doi: 10.1016/S1049-9644(03)00137-3. https://www.sciencedirect.com/science/ar... )