Biomphalaria glabrata

Biomphalaria glabrata is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Planorbidae, the ram's horn snails.

Biomphalaria glabrata
An albino individual of Biomphalaria glabrata. (All snails in the family Planorbidae have the red oxygen transport pigment hemoglobin, but this is especially apparent in albino animals.)
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Mollusca
Class:	Gastropoda
Subclass:	Heterobranchia
Superorder:	Hygrophila
Family:	Planorbidae
Genus:	Biomphalaria
Species:	B. glabrata
Binomial name
Biomphalaria glabrata (Say, 1818)^[1]
Synonyms
Planorbis glabratus Say, 1818 Australorbis glabratus (Say, 1818) Taphius glabratus (Say, 1818) Planorbis guadaloupensis Sowerby Planorbis ferrugineus Spix, 1827 Planorbis olivaceus Spix, 1827 Planorbis nigricans Spix, 1827 Planorbis albescens Spix, 1827 Planorbis viridis Spix, 1827 Planorbis lugubris J. A. Wagner, 1827

Biomphalaria glabrata is an intermediate snail host for the trematode Schistosoma mansoni, which is one of the main schistosomes that infect humans.^[2] This snail is a medically important pest,^[3] because of transferring the disease intestinal schistosomiasis, the most widespread of all types of schistosomiasis.

The parasite Schistosoma mansoni (which these snails and other Biomphalaria snails carry) infects about 83.31 million people worldwide.^[4]

Biomphalaria glabrata/Schistosoma mansoni provides a useful model system for investigating the intimate interactions between host and parasite.^[2] There is a great deal of information available about this snail, because it has been, and continues to be, under intensive study by many malacologists, parasitologists and other researchers, on account of its medical significance.

The shell of this species, like all planorbids, is sinistral in coiling, but it is carried upside down, and thus it appears to be dextral.

Distribution

Biomphalaria glabrata is a Neotropical^[3] species. Its native distribution includes the Caribbean: Puerto Rico,^[5] Dominican Republic,^[6] Saint Lucia,^[7] Haiti (first report in 1891),^[8] Martinique, Guadeloupe,^[9] Antigua, Vieques, Saint Martin, Saint Kitts, Curaçao, Dominica (it was probably replaced by other Biomphalaria species in Dominica or it was eradicated),^[10] Montserrat and in South America: Venezuela, Suriname, French Guiana and Brazil.^[11]

This species has recently expanded its native range,^[3] but there is reduced its abundance in the Caribbean, because of competition with non-indigenous species and environmental change.^[12]

It inhabits new localities in the time of flooding.^[13]

Shell description

Like all planorbids, the shell of Biomphalaria glabrata is planispiral, in other words coiled flat like a rope, and the spire of the shell is sunken. Also, like all planorbids, this species has a sinistral shell, in other words, the coiling of the shell is left-handed. However, like all the snails in the subfamily Planobinae, this snail carries its coiled shell upside down, and thus the shell appears to be dextral in coiling. In other families of snails the spire is situated on top of the shell, here what shows on top of the shell is in fact the umbilicus.

Biomphalaria glabrata was discovered and described under the name Planorbis glabratus by American naturalist Thomas Say in 1818.^[1] Say's type description reads as follows:

Shell sinistral; whorls about five, glabrous or obsoletely rugose, polished, destitute of any appearance of carina; spire perfectly regular, a little concave; umbilicus large, regularly and deeply concave, exhibiting all the volutions to the summit; aperture declining, remarkably oblique with respect to the transverse diameter. Breadth nearly nine-tenths of an inch.

Unfortunately Say listed an incorrect type locality: North Carolina.^[1] The shell was probably actually from the West Indian island of Guadeloupe.^[11]

The shell of animals from natural habitats is usually olivaceous (olive drab) in color.^[11] The width of the shell of adults snails is 6–10 mm.^[14]

An adult shell consist of aragonite and sometimes there is also under 1.5% of vaterite especially near the margin of the shell.^[15]

Anatomy

The anatomy of the mantle cavity is described in Sullivan et al. (1974)^[16] and Jurberg et al. (1997).^[17]

Genetics

The genome length is estimated as about 929,10 Mb (millions of base pairs; 0.95 ± 0.01 pg),^[18][19] which is a small genome size among gastropods.^[20] Sequencing of the whole genome was approved as a priority by National Human Genome Research Institute in August 2004,^[21] Its participants also included the "Biomphalaria glabrata Genome Initiative" and the Genome Center at Washington University in St. Louis.^[13] The complete genome was sequenced in 2017.^[22]

The chromosomes in this snail are small, and the haploid number of chromosomes is 18.^[23]

A complete genome sequence from the mitochondria of this species has been available since 2004: the mitochondrial genome sequence has 13670 nucleotides.^[24][25]

The ancestor of Biomphalaria glabrata colonized Africa, and speciated into all of the African Biomphalaria species.^[26]

Phylogeny

A cladogram showing phylogenic relations of species in the genus Biomphalaria:^[26]

Biomphalaria

African species Biomphalaria stanleyi Biomphalaria pfeifferi Biomphalaria camerunensis Nilotic species complex Biomphalaria sudanica Biomphalaria choanomphala Biomphalaria alexandrina Biomphalaria smithi Biomphalaria glabrata Biomphalaria straminea complex Biomphalaria kuhniana Biomphalaria straminea Biomphalaria straminea Biomphalaria intermedia Biomphalaria amazonica Biomphalaria sp. Biomphalaria tenagophila Biomphalaria occidentalis Biomphalaria prona Biomphalaria andecola Biomphalaria sp. (? Biomphalaria havanensis) Biomphalaria sp. (? Biomphalaria havanensis) Biomphalaria temascalensis Biomphalaria obstructa Biomphalaria helophila Biomphalaria peregrina Biomphalaria schrammi

Ecology

Biomphalaria glabrata inhabits small streams, ponds^[27] and marshes. These snails can survive in aestivation for a few months when removed from their freshwater habitat or when the habitat dries out.^[28] For example, the snail lives in banana plantation drains in Saint Lucia.^[29]

Biomphalaria glabrata can also survive up to 16 hours in anaerobic water using lactic acid fermentation.^[30]

Like other species, this snail is "light sensitive" and can be disrupted by artificial light.^[31]

Feeding habits

Biomphalaria glabrata feeds on bacterial films, algae, diatoms and decaying macrophytes.^[32]

They can be fed using fish food and lettuce when they are kept in captivity.^[33]

Life cycle

Biomphalaria glabrata snails lay egg masses at rather a high rate (about 1 per day).^[5] One snail can lay 14,000 eggs during its whole life span.^[32]

The periostracum of the embryonic shell (inside the egg) begin to grow in 48-hour old embryos.^[34] Amorphous calcium carbonate appear in 54-60-hour old embryos.^[34] Calcification (formation of aragonite) of the embryonic shell starts in the time interval between 60-hour old embryos and 72-hour-old ones.^[33] The weight of the shell of 72-hour-old embryo is 0.64 μg.^[34]

The weight of the embryonic shell in 5-day-old (120-hours-old) embryos a very short time before hatching, is 30.3 μg, and the width is 500 μm.^[34] The juvenile snail hatches from 5 to 6 days old eggs.^[34] The weight of the juvenile shell is 2.04 mg in four weeks after hatching.^[34] There is no vaterite in juvenile shells.^[15]

The growth rate, maximum birth rate, and longevity of Biomphalaria glabrata was studied by Pimentel (1957).^[5] There can be up to seven generations in one year in laboratory.^[32] The generation time (the time it takes a snail from developing from an egg to laying an egg of its own) is 4–6 weeks.^[13] The lifespan is 15–18 months in natural conditions.^[32] The lifespan in laboratory conditions can be up to 18–24 months,^[32] but usually it is 9–12 months.^[13]

Biomphalaria glabrata is a simultaneous hermaphrodite,^[27] but self-fertilization is also possible.^[32] The mucus of this snail species contains species-specific signals that allow individual snails to identify others of the same species,^[35] but the causative mucus components decay within 10 to 30 min.^[27][35][36] The typically unilateral copulations^[37] are initiated when a male actor mounts the shell of a prospective mate. The male actor then moves towards the frontal left edge of the partner's shell, where he probes the female gonopore with his penis to subsequently achieve penis intromission. Following a typically 5–87 min penis intromission with usually successful sperm transfer,^[38] the male actor retracts to terminate copulation. Mating roles are subsequently exchanged in about 45% of all copulations, with the male actor now taking the female role, and vice versa.^[27] In 2009, Biomphalaria glabrata was a subject of the study focusing on the Coolidge effect in simultaneous hermaphrodites. The result of this research is that Biomphalaria glabrata shows the absence of any sex-specific effects of partner novelty, which means there is no Coolidge effect in this species.^[27]

Parasites

Biomphalaria glabrata is a major intermediate host for Schistosoma mansoni in the Americas and a vector of schistosomiasis.^[39]

In medical research, the most commonly used Biomphalaria glabrata snail stock (used for the maintenance of Schistosoma mansoni) is albino, i.e. it is without pigment. It is descended from a mutant albino stock which arose during research by Newton (1955).^[40] Not only did this albino variety prove to be highly susceptible to Schistosoma mansoni, but the lack of pigment allowed investigators using a dissecting microscope to view the development of the parasite within the snail. The black pigment normally found in snails that are taken from the field previously made this viewing too difficult.^[39]

There are both resistant and susceptible strains of B. glabrata. Li et al 2021 finds resistant snails to have innate immune receptors specifically to fight S. mansoni infection. These IIRs are expressed on particular immune cells.^[41]

Some other trematodes are also natural parasites of Biomphalaria glabrata:

• Ribeiroia marini^[42]
• Candidatus Paenibacillus glabratella – this bacterial pathogen is causing white nodules and high mortalities of snails.^[43]

Experimental parasites include:

• Angiostrongylus vasorum – (experimental)^[44]
• Echinostoma caproni – (experimental)^[45]
• Echinostoma paraensei – (experimental)^[46]
• Echinostoma trivolvis – as second (experimental) intermediate host (referred as Echinostoma revolutum in Anderson & Fried (1987)).^[47][48]
• Plagiorchis elegans can experimentally infect Biomphalaria glabrata and it can cause its parasitic castration, but the snail is incompatible for its full development.^[49]

Interaction with schistosome

Schistosoma mansoni can infect juveniles of Biomphalaria glabrata much more easily than it can adults.^[13] Schistosoma mansoni causes parasitic castration in infected snails.^[13]

Interactions between snails and schistosomes are complex and there exists an urgent need to elucidate pathways involved in snail-parasite relationships as well as to identify those factors involved in the intricate balance between the snail internal defence system and trematode infectivity mechanisms that determine the success or failure of an infection.^[2]

Molluscs appear to lack an adaptive immune system like that found in vertebrates and, instead, are considered to use various innate mechanisms involving cell-mediated and humoral reactions (non-cellular factors in plasma/serum or hemolymph) that interact to recognize and eliminate invading pathogens or parasites in incompatible or resistant snails. However, a diverse family of fibrinogen-related proteins (FREPs)^[50] containing immunoglobulin-like domains has been discovered in Biomphalaria glabrata and may play a role in snail defence. Circulating haemocytes (macrophage-like defence cells) in the snail haemolymph are known to aggregate in response to trauma, phagocytose small particles (bacteria, and fungi) and encapsulate larger ones, such as parasites. Final killing is effected by hemocyte-mediated cytotoxicity mechanisms involving non-oxidative and oxidative pathways, including lysosomal enzymes and reactive oxygen/nitrogen intermediates. Certain alleles of cytosolic copper/zinc superoxide dismutase (SOD1) have been associated with resistance also suggesting these processes are important in the snail internal defence system.^[2]

On the schistosome's part the Roger group (in Roger et al 2008 a & b) find that S. mansoni produces mucins. Immunoprecipitation reveals FREPs and mucins bound to each other. This suggests FREPs are detecting these mucins and recognition or failure to recognize helps to determine the course of the infection interaction.^[50]

Predators

The freshwater snail Marisa cornuarietis is a predator of Biomphalaria glabrata: it feeds on its eggs, juvenile and adult snails.^[51] It also acts as a competitor.^[51][52]

Competitors

Melanoides tuberculata is considered to be a competitor of Biomphalaria glabrata, but all the intraspecific interactions are not fully understood yet.^[53] Although in various countries there were contradictory results,^[53] and despite this situation being unpredictable and thus possible ecological damage might result, Melanoides tuberculata is nonetheless used in an attempt to control or reduce populations of Biomphalaria glabrata in Brazil,^[53] in the West Indies,^[7] and in Venezuela.

Symbionts

A single-celled symbiont Capsaspora owczarzaki was discovered in the haemolymph of Biomphalaria glabrata in 2002.^[54]

Hybrid

There is one known hybrid: Biomphalaria glabrata × Biomphalaria alexandrina, from Egypt.^[55]

Toxicology

The absolute lethal concentration (LC₁₀₀) of glucose/mannose-binding lectins from plants Canavalia brasiliensis, Cratylia floribunda, Dioclea guianensis, Dioclea grandiflora and Dioclea virgata for adults of Biomphalaria glabrata is 50 μg mL⁻¹.^[56]

The latex of Euphorbia conspicua is toxic to adults of Biomphalaria glabrata.^[57]

Four species of the genus Solanum from Brazil are toxic to Biomphalaria glabrata.^[58]

Some species of Annona are toxic to adults of Biomphalaria glabrata and to its eggs.^[59]

References

This article incorporates public domain text from reference,^[1] CC-BY-2.5 text (but not under GFDL) from reference^[39] and CC-BY-2.0 text from references.^[2][27]

1. Say, T. (June 1818). "Account of two new genera, and several new species, of fresh water and land shells". Journal of the Academy of Natural Sciences of Philadelphia. 1 (2): 276–284.
2. Lockyer, Anne E; Spinks, Jenny; Kane, Richard A; Hoffmann, Karl F; Fitzpatrick, Jennifer M; Rollinson, David; Noble, Leslie R; Jones, Catherine S (2008). "Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni". BMC Genomics. 9 (1): 634. doi:10.1186/1471-2164-9-634. PMC 2631019. PMID 19114004.
3. Pointier, J. P.; David, P.; Jarne, P. (2005). "Biological invasions: The case of planorbid snails". Journal of Helminthology. 79 (3): 249–256. doi:10.1079/JOH2005292. PMID 16153319. S2CID 11158571..
4. Crompton, D. W. (1999). "How much human helminthiasis is there in the world?" (PDF). The Journal of Parasitology. 85 (3): 397–403. doi:10.2307/3285768. JSTOR 3285768. PMID 10386428. Archived from the original (PDF) on 23 February 2010.
5. Pimentel D. (October 1957) "Life history of Australorbis glabratus, the intermediate snail host of Schistosoma mansoni in Puerto Rico". Ecol 38(4): 576-580.
6. Steffey, E. P.; Howland Jr, D. (1977). "Isoflurane potency in the dog and cat". American Journal of Veterinary Research. 38 (11): 1833–1836. PMID 931167.
7. Pointier, J.P. (June 1993). "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. 54 (1): 13–18. doi:10.1016/0001-706x(93)90064-i. PMID 8103624.
8. Raccurt, Christian P.; Sodeman, William A.; Rodrick, Gary L.; Boyd, William P. (January 1985). "Biomphalaria glabrata in Haiti". Transactions of the Royal Society of Tropical Medicine and Hygiene. 79 (4): 455–457. doi:10.1016/0035-9203(85)90063-x. PMID 4082255.
9. Sturrock, R. F. (1974). "Ecological notes on habitats of the freshwater snail Biomphalaria glabrata, intermediate host of Schistosoma mansoni on St. Lucia, West Indies" (PDF). Caribbean Journal of Science. 14 (3–4): 149–162.
10. Reeves, Will K.; Dillon, Robert T.; Dasch, Gregory A. (March 2008). "Freshwater snails (Mollusca: Gastropoda) from the Commonwealth of Dominica with a discussion of their roles in the transmission of parasites". American Malacological Bulletin. 24 (1): 59–63. doi:10.4003/0740-2783-24.1.59. S2CID 6282227.
11. Paraense, W Lobato (September 2001). "The schistosome vectors in the Americas". Memórias do Instituto Oswaldo Cruz. 96 (suppl): 7–16. doi:10.1590/s0074-02762001000900002. PMID 11586421.
12. Morgan, J. A.; Dejong, R. J.; Snyder, S. D.; Mkoji, G. M.; Loker, E. S. (2001). "Schistosoma mansoni and Biomphalaria: Past history and future trends". Parasitology. 123 Suppl (7): S211–S228. doi:10.1017/s0031182001007703. PMID 11769285. S2CID 23030603.
13. The Genome Center at Washington University in St. Louis. Biomphalaria glabrata 30 October 2011 at the Wayback Machine Accessed 21 November.
14. Baeza Garcia, Alvaro; Pierce, Raymond J.; Gourbal, Benjamin; Werkmeister, Elisabeth; Colinet, Dominique; Reichhart, Jean-Marc; Dissous, Colette; Coustau, Christine; Wynn, Thomas A. (23 September 2010). "Involvement of the Cytokine MIF in the Snail Host Immune Response to the Parasite Schistosoma mansoni". PLOS Pathogens. 6 (9): e1001115. doi:10.1371/journal.ppat.1001115. PMC 2944803. PMID 20886098.
15. Hasse, B.; Ehrenberg, H.; Marxen, J. C.; Becker, W.; Epple, M. (2000). "Calcium Carbonate Modifications in the Mineralized Shell of the Freshwater SnailBiomphalaria glabrata". Chemistry. 6 (20): 3679–3685. doi:10.1002/1521-3765(20001016)6:20<3679::AID-CHEM3679>3.0.CO;2-#. PMID 11073237.
16. Sullivan, J. T.; Cheng, T. C. (1974). "Structure and function of the mantle cavity of Biomphalaria glabrata (Mollusca: Pulmonata)". Transactions of the American Microscopical Society. 93 (3): 416–420. doi:10.2307/3225446. JSTOR 3225446. PMID 4854431., JSTOR.
17. Jurberg, Pedro; Cunha, Rodolfo A; Rodrigues, Marcelo Luis (March 1997). "Behavior of Biomphalaria glabrata Say, 1818 (Gastropoda: Planorbidae): I. Morphophysiology of the Mantle Cavity". Memórias do Instituto Oswaldo Cruz. 92 (2): 287–295. CiteSeerX 10.1.1.732.9688. doi:10.1590/s0074-02761997000200026. PMID 24159674. S2CID 25179919.
18. Gregory, T. R. (2003). "Genome size estimates for two important freshwater molluscs, the zebra mussel (Dreissena polymorpha) and the schistosomiasis vector snail (Biomphalaria glabrata)" (PDF). Genome. 46 (5): 841–844. doi:10.1139/g03-069. PMID 14608401. Archived from the original (PDF) on 23 February 2010.
19. Adema, Coen M.; Hillier, LaDeana W.; Jones, Catherine S.; Loker, Eric S.; Knight, Matty; Minx, Patrick; Oliveira, Guilherme; Raghavan, Nithya; Shedlock, Andrew (16 May 2017). "Whole genome analysis of a schistosomiasis-transmitting freshwater snail". Nature Communications. 8: 15451. Bibcode:2017NatCo...815451A. doi:10.1038/ncomms15451. ISSN 2041-1723. PMC 5440852. PMID 28508897.
20.   Knight M., Adema C. M., Raghavan N., Loker E. S., Lewis F. A. & Tettelin H. (2003) "Obtaining the genome sequence of the mollusc Biomphalaria glabrata: a major intermediate host for the parasite causing human schistosomiasis". Online at http://www.genome.gov/Pages/Research/Sequencing/SeqProposals/BiomphalariaSEQv.2.pdf National Human Genome Research Institute. Accessed 20 November 2009
21. Approved Sequencing Targets 27 July 2012 at the Wayback Machine. Last updated 14 September 2009. Accessed 21 November 2009
22. Briggs, Helen (16 May 2017). "Snail's DNA secrets unlocked in fight against river disease". BBC News. Retrieved 16 May 2017.
23. Goldman M. A., Loverde P. T., Chrisman C. L., & Franklin D. A. (1984) "Chromosomal evolution in planorbid snails of the genera Bulinus and Biomphalaria". Malacologia 25(2): 427-446.
24. DeJong, R. J.; Emery, A. M.; Adema, C. M. (2004). "The mitochondrial genome of Biomphalaria glabrata (Gastropoda: Basommatophora), intermediate host of Schistosoma mansoni". Journal of Parasitology. 90 (5): 991–997. doi:10.1645/GE-284R. PMID 15562597. S2CID 25744207.
25. [Organism%3Anoexp] , accessed 20 November 2009.
26. Dejong, R. J.; Morgan, J. A.; Paraense, W. L.; Pointier, J. P.; Amarista, M.; Ayeh-Kumi, P. F.; Babiker, A.; Barbosa, C. S.; Brémond, P.; Pedro Canese, A.; De Souza, C. P.; Dominguez, C.; File, S.; Gutierrez, A.; Incani, R. N.; Kawano, T.; Kazibwe, F.; Kpikpi, J.; Lwambo, N. J.; Mimpfoundi, R.; Njiokou, F.; Noël Poda, J.; Sene, M.; Velásquez, L. E.; Yong, M.; Adema, C. M.; Hofkin, B. V.; Mkoji, G. M.; Loker, E. S. (2001). "Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni". Molecular Biology and Evolution. 18 (12): 2225–2239. doi:10.1093/oxfordjournals.molbev.a003769. PMID 11719572., .
27. Häderer, Ines K; Werminghausen, Johanna; Michiels, Nico K; Timmermeyer, Nadine; Anthes, Nils (2009). "No effect of mate novelty on sexual motivation in the freshwater snail Biomphalaria glabrata". Frontiers in Zoology. 6 (1): 23. doi:10.1186/1742-9994-6-23. PMC 2766376. PMID 19818155.
28. Majoros, Gábor; Fehér, Zoltán; Deli, Tamás; Földvári, Gábor (November 2008). "Establishment of Biomphalaria tenagophila snails in Europe". Emerging Infectious Diseases. 14 (11): 1812–1814. doi:10.3201/eid1411.080479. PMC 2630743. PMID 18976582.
29. Sturrock, R. F. (1975). "Distribution of the snail Biomphalaria glabrata, intermediate host of Schistosoma mansoni, within a St Lucian field habitat". Bulletin of the World Health Organization. 52 (3): 267–272. PMC 2366373. PMID 1084797.
30. Brand, T. V.; Baernstein, H. D.; Mehlman, B. (1950). "Studies on the anaerobic metabolism and the aerobic carbohydrate consumption of some fresh water snails". The Biological Bulletin. 98 (3): 266–276. doi:10.2307/1538675. JSTOR 1538675. PMID 15420230., article and PDF
31. Pimentel-Souza, F.; Schall, V. T.; Lautner, R. Jr.; Barbosa, N. D. C.; Schettino, M; Fernandes, N. (1984). "Behavior of Biomphalaria glabrata (Gastropoda: Pulmonata) under different lighting conditions". Canadian Journal of Zoology. 62 (11): 2328–2334. doi:10.1139/z84-340.
32. What is Biomphalaria glabrata? 4 June 2010 at the Wayback Machine UNM Biology Department Home Page. Accessed 20 November 2009.
33. Marxen, J. C.; Prymak, O.; Beckmann, F.; Neues, F.; Epple, M. (2008). "Embryonic shell formation in the snail Biomphalaria glabrata: a comparison between scanning electron microscopy (SEM) and synchrotron radiation micro computer tomography (SRµCT)". Journal of Molluscan Studies. 74 (1): 19–26. doi:10.1093/mollus/eym044.
34. Neues, Frank; Epple, Matthias (12 November 2008). "X-ray Microcomputer Tomography for the Study of Biomineralized Endo- and Exoskeletons of Animals". Chemical Reviews. 108 (11): 4734–4741. doi:10.1021/cr078250m. PMID 18754688.
35. Townsend, C. R. (1974). "Mucus trail following by the snail Biomphalaria glabrata (Say)". Animal Behaviour. 22 (1): 170–177. doi:10.1016/S0003-3472(74)80066-7.
36. Wells, M. J.; Buckley, S.K.L. (1972). "Snails and trails". Animal Behaviour. 20 (2): 345–355. doi:10.1016/S0003-3472(72)80057-5.
37. Trigwell, J. A.; Dussart, G. B. J.; Vianey-Liaud, M. (1997). "Pre-copulatory behaviour of the freshwater hermaphrodite snail Biomphalaria glabrata (Say, 1818) (Gastropoda: Pulmonata)"". Journal of Molluscan Studies. 63: 116–120. doi:10.1093/mollus/63.1.116.
38. Vianey-Liaud, M (1995). "Bias in the production of heterozygous pigmented embryos from successively mated Biomphalaria glabrata (Gastropoda: Planorbidae) albino snails". Malacological Review. 28: 97–106.
39. Lewis, Fred A.; Liang, Yung-san; Raghavan, Nithya; Knight, Matty; Loukas, Alex (30 July 2008). "The NIH-NIAID Schistosomiasis Resource Center". PLOS Neglected Tropical Diseases. 2 (7): e267. doi:10.1371/journal.pntd.0000267. PMC 2480520. PMID 18665228.
40. Newton, W. L. (1955). "The establishment of a strain of Australorbis glabratus which combines albinism and high susceptibility to infection with Schistosoma mansoni". J. Parasitol. 41 (5): 526–528. doi:10.2307/3273814. JSTOR 3273814. PMID 13264025.
41. Buckley, Katherine M.; Yoder, Jeffrey A. (15 December 2021). "The evolution of innate immune receptors: investigating the diversity, distribution, and phylogeny of immune recognition across eukaryotes". Immunogenetics. Springer. 74 (1): 1–4. doi:10.1007/s00251-021-01243-4. ISSN 0093-7711. PMC 8671053. PMID 34910229. (KMB ORCID: 0000-0002-6585-8943). (JAY ORCID: 0000-0002-6083-1311).
42. Basch, P. F.; Sturrock, R. F. (1969). "Life History of Ribeiroia marini (Faust and Hoffman, 1934) comb. n. (Trematoda: Cathaemasiidae)". Journal of Parasitology. 55 (6): 1180–1184. doi:10.2307/3277252. JSTOR 3277252.
43. Duval, D.; Galinier, R.; Mouahid, G.; Toulza, E.; Allienne, J. F.; et al. (2015). "A Novel Bacterial Pathogen of Biomphalaria glabrata: A Potential Weapon for Schistosomiasis Control?". PLOS Neglected Tropical Diseases. 9 (2): e0003489. doi:10.1371/journal.pntd.0003489. PMC 4342248. PMID 25719489.
44. Barçante; Barçante, T. A.; Dias, S. R. C.; Lima, W. D. S. (2003). "Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905: emergence of third-stage larvae from infected Biomphalaria glabrata snails". Parasitology Research. 91 (6): 471–475. doi:10.1007/s00436-003-1000-9. PMID 14557873. S2CID 22501974.
45. Schneck, J. L.; Fried, B. (2004). "Effects of snail size on encystment of Echinostoma caproni in juvenile Biomphalaria glabrata (NMRI strain) and observations on the survival of infected snails". Journal of Helminthology. 78 (3): 277–279. doi:10.1079/JOH2004235. PMID 15469634.
46. Degaffé, G.; Loker, E. S. (1998). "Susceptibility of Biomphalaria glabratato Infection with Echinostoma paraensei: Correlation with the Effect of Parasite Secretory–Excretory Products on Host Hemocyte Spreading". Journal of Invertebrate Pathology. 71 (1): 64–72. doi:10.1006/jipa.1997.4710. PMID 9446739..
47. Anderson, J. W.; Fried, B. (1987). "Experimental infection of Physa heterostropha, Helisoma trivolvis, and Biomphalaria glabrata (Gastropoda) with Echinostoma revolutum (Trematoda) Cercariae". The Journal of Parasitology. 73 (1): 49–54. doi:10.2307/3282342. JSTOR 3282342. PMID 3572665..
48. Fried, B.; Idris, N.; Ohsawa, T. (1995). "Experimental infection of juvenile Biomphalaria glabrata with cercariae of Echinostoma trivolvis". The Journal of Parasitology. 81 (2): 308–310. doi:10.2307/3283941. JSTOR 3283941. PMID 7707214., JSTOR
49. Zakikhani, M.; Smith, J. M.; Rau, M. E. (2003). "Effects of Plagiorchis elegans (Digenea: Plagiorchiidae) Infection of Biomphalaria glabrata (Pulmonata: Planorbidae) on a Challenge Infection with Schistosoma mansoni (Digenea: Schistosomatidae)". The Journal of Parasitology. 89 (1): 70–75. doi:10.1645/0022-3395(2003)089[0070:EOPEDP]2.0.CO;2. JSTOR 3286083. PMID 12659305. S2CID 26097458.
50. Hanington, Patrick C.; Zhang, Si-Ming (9 November 2010). "The Primary Role of Fibrinogen-Related Proteins in Invertebrates Is Defense, Not Coagulation". Journal of Innate Immunity. Karger. 3 (1): 17–27. doi:10.1159/000321882. ISSN 1662-811X. PMC 3031514. PMID 21063081.
51. Kobayashi, H. (1986). "An experimental study of epidermal keratin phosphorylation --epidermal keratin as a substrate protein of cAMP-dependent protein kinase". Hokkaido Igaku Zasshi. 61 (3): 453–462. PMID 2427426.
52. Ruiz-Tibén, E; Palmer, J. R.; Ferguson, F (1969). "Biological control of Biomphalaria glabrata by Marisa cornuarietis in irrigation ponds in Puerto Rico". Bulletin of the World Health Organization. 41 (2): 329–333. PMC 2427426. PMID 5308710.
53. Giovanelli, A.; Vieira, M. V.; da Silva, C. L. P. A. C. (2005). "Interaction Between The Intermediate Host Of Schistosomiasis In Brazil, Biomphalaria Glabrata (Say, 1818) And A Possible Competitor, Melanoides Tuberculata (Müller, 1774) A Field Study". Journal of Molluscan Studies. 71 (1): 7–13. doi:10.1093/mollus/eyi004.
54. Hertel L. A., Bayne C. J. & Loke E. S. (2002), "The symbiont Capsaspora owczarzaki, nov. Gen. Nov. Sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea", International Journal for Parasitology, 32 (9): 1183–91, doi:10.1016/S0020-7519(02)00066-8, PMID 12117501
55. Yousif, F.; Ibrahim, A.; Abdel Kader, A.; El-Bardicy, S. (1998). "Invasion of the Nile Valley in Egypt by a hybrid of Biomphalaria glabrata and Biomphalaria alexandrina, snail vectors of Schistosoma mansoni". Journal of the Egyptian Society of Parasitology. 28 (2): 569–582. PMID 9707685.
56. Santos, A. F. d.; Cavada, B. S.; Rocha, B. A. M. da; Nascimento, K. S. d.; Sant'Ana, A. E. G. (2010). "Toxicity of some glucose/mannose-binding lectins to Biomphalaria glabrata and Artemia salina". Bioresource Technology. 101 (2): 794–798. doi:10.1016/j.biortech.2009.07.062. PMID 19765980.
57. Santos, A. F. d.; Azevedo, D. P. L. d.; Mata, R. d. C. d. S.; Mendonça, D. I. M. D. d.; Sant'Ana, A. E. G. (2007). "The lethality of Euphorbia conspicua to adults of Biomphalaria glabrata, cercaria of Schistosoma mansoni and larvae of Artemia salina". Bioresource Technology. 98 (1): 135–139. doi:10.1016/j.biortech.2005.11.020. PMID 16458000.
58. Silva, T. M. S.; Câmara, C. A.; Agra, M. d. F.; Carvalho, M. G. d.; Frana, M. T.; Brandoline, S. V. P. B.; Paschoal, L. d. S.; Braz-Filho, R. (2006). "Molluscicidal activity of Solanum species of the Northeast of Brazil on Biomphalaria glabrata". Fitoterapia. 77 (6): 449–452. doi:10.1016/j.fitote.2006.05.007. PMID 16842935.
59. Santos, A. F. d.; Sant'Ana, A. E. G. (2001). "Molluscicidal properties of some species of Annona". Phytomedicine. 8 (2): 115–120. doi:10.1078/0944-7113-00008. PMID 11315753.

Further reading

• Genetics as known up to 2006:
  • Adema, Coen M; Luo, Mei-Zhong; Hanelt, Ben; Hertel, Lynn A; Marshall, Jennifer J; Zhang, Si-Ming; DeJong, Randall J; Kim, Hye-Ran; Kudrna, David; Wing, Rod A; Soderlund, Cari; Knight, Matty; Lewis, Fred A; Caldeira, Roberta Lima; Jannotti-Passos, Liana K; Carvalho, Omar dos Santos; Loker, Eric S (October 2006). "A bacterial artificial chromosome library for Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni". Memórias do Instituto Oswaldo Cruz. 101 (suppl 1): 167–177. doi:10.1590/s0074-02762006000900027. hdl:1807/56944. PMID 17308766.
• Feeding behaviour:
  • Townsend, C. R. (1973). "The food-finding orientation mechanism of Biomphalaria glabrata (Say)". Animal Behaviour. 21 (3): 544–548. doi:10.1016/s0003-3472(73)80014-4. PMID 4748749.
  • Boissier, Jérôme; Rivera, Ezequiel R.; Moné, Hélène (June 2003). "Altered Behavior of the Snail Biomphalaria glabrata as a Result of Infection with Schistosoma mansoni". Journal of Parasitology. 89 (3): 429–433. doi:10.1645/0022-3395(2003)089[0429:ABOTSB]2.0.CO;2. PMID 12880237. S2CID 43703731.
• Egg-laying process:
  • Boyle, J. P.; Yoshino, T. P. (1 February 2000). "The Effect of Water Quality on Oviposition in Biomphalaria glabrata (Say, 1818)(planorbidae), and a Description of the Stages of the Egg-laying Process". Journal of Molluscan Studies. 66 (1): 83–94. doi:10.1093/mollus/66.1.83.
• Competition in laboratory:
  • Giovanelli, A.; Vieira, M. V.; da Silva, C. L. P. A. C. (2002). "Interaction between the Intermediate Host of Schistosomiasis in Brazil Biomphalaria glabrata (Planorbidae) and a Possible Competitor Melanoides tuberculata (Thiaridae): I. Laboratory Experiments" (PDF). Memórias do Instituto Oswaldo Cruz. 97 (3): 363–369. doi:10.1590/s0074-02762002000300016. PMID 12048567.
• Circulatory system:
  • Santos, Marco Antonio Vasconcelos; Diniz, José Antonio Picanço (September 2009). "Aspectos ultraestruturais de hemócitos de Biomphalaria glabrata Say (1818) (Gastropoda: Planorbidae) analisados sob microscopia eletrônica de transmissão" [Ultrastructural aspects of hemocytes from Biomphalaria glabrata Say (1818) (Gastropoda: Planorbidae) analysed with transmission electronic microscopy]. Acta Amazonica (in Portuguese). 39 (3): 707–712. doi:10.1590/S0044-59672009000300027.
• Biochemistry:
  • Marxen, Julia C.; Nimtz, Manfred; Becker, Wilhelm; Mann, Karlheinz (August 2003). "The major soluble 19.6 kDa protein of the organic shell matrix of the freshwater snail Biomphalaria glabrata is an N-glycosylated dermatopontin". Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics. 1650 (1–2): 92–98. doi:10.1016/S1570-9639(03)00203-6. PMID 12922172.
• Interactions with Schistosome:
  • Moné, Y.; Gourbal, B.; Duval, D.; Du Pasquier, L.; Kieffer-Jaquinod, S.; et al. (2010). "A Large Repertoire of Parasite Epitopes Matched by a Large Repertoire of Host Immune Receptors in an Invertebrate Host/Parasite Model". PLOS Neglected Tropical Diseases. 4 (9): e813. doi:10.1371/journal.pntd.0000813. PMC 2935394. PMID 20838648.
• Mineralogy:
  • Marxen, J. C.; Becker, W.; Finke, D.; Hasse, B.; Epple, M. J. (2003). "Early mineralization in Biomphalaria glabrata: microscopic and structural results". Journal of Molluscan Studies. 69 (2): 113–121. doi:10.1093/mollus/69.2.113.
  • Prymak, O.; Tiemann, H.; Sötje, I.; Marxen, J. C.; Klocke, A.; Kahl-Nieke, B. R.; Beckmann, F.; Donath, T.; Epple, M. (2005). "Application of synchrotron-radiation-based computer microtomography (SRμCT) to selected biominerals: Embryonic snails, statoliths of medusae, and human teeth". Journal of Biological Inorganic Chemistry. 10 (6): 688–695. doi:10.1007/s00775-005-0023-3. PMID 16187072. S2CID 25109955.

• Phylogeography:
  • Dejong, R. J.; Morgan, J. A.; Wilson, W. D.; Al-Jaser, M. H.; Appleton, C. C.; Coulibaly, G.; d'Andrea, P. S.; Doenhoff, M. J.; Haas, W.; Idris, M. A.; Magalhães, L. A.; Moné, H.; Mouahid, G.; Mubila, L.; Pointier, J. P.; Webster, J. P.; Zanotti-Magalhães, E. M.; Paraense, W. L.; Mkoji, G. M.; Loker, E. S. (2003). "Phylogeography of Biomphalaria glabrata and B. Pfeifferi, important intermediate hosts of Schistosoma mansoni in the New and Old World tropics". Molecular Ecology. 12 (11): 3041–3056. Bibcode:2003MolEc..12.3041D. doi:10.1046/j.1365-294X.2003.01977.x. PMID 14629384. S2CID 25911829.

• Toxicology:
  • De s. Luna, J.; Dos Santos, A. F.; De Lima, M. R. F.; De Omena, M. C.; De Mendonça, F. A. C.; Bieber, L. W.; Sant'Ana, A. E. G. (2005). "A study of the larvicidal and molluscicidal activities of some medicinal plants from northeast Brazil". Journal of Ethnopharmacology. 97 (2): 199–206. doi:10.1016/j.jep.2004.10.004. PMID 15707752.

External links

 

Wikimedia Commons has media related to Biomphalaria glabrata.

• Biomphalaria glabrata Genome Initiative
• Biomphalaria glabrata genome page at NCBI