Effects of Larval Schistosomes on Biomphalaria Snails

  • Judith Humphries


The aim of this chapter is to provide a clearer understanding of the complex relationship between Biomphalaria snails and larval schistosome parasites. This chapter describes the numerous changes in host physiology, biochemistry, and behavior brought about by infection. Specifically, the effects of larval schistosomes on host mortality, growth, metabolism, reproduction, organic and inorganic elements, and behavior are focused on. The chapter concentrates on three Biomphalaria species; B. glabrata, B. alexandrina, and B. pfeifferi and one species of schistosome, Schistosoma mansoni.


Infected Snail Schistosome Infection Albumen Gland Juvenile Snail Accessory Sexual Organ 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Bai G, Johnston LA, Watson CO, Yoshino TP (1997) Phenoloxidase activity in the reproductive system of Biomphalaria glabrata: role in egg production and effect of schistosome infection. J Parasitol 83:852–858PubMedCrossRefGoogle Scholar
  2. Bebiano MJ, Langston WJ (1995) Induction of metallothionen synthesis in the gill and kidney of Littorina littoerea exposed to cadmium. J Mar Biol Assoc UK 75:173–186CrossRefGoogle Scholar
  3. Berriman M, Haas BJ, LoVerde PT, Wilson RA, Dillon GP, Cerqueira GC, Mashiyama ST, Al-Lazikani B, Andrade LF, Ashton PD, Aslett MA, Bartholomeu DC, Blandin G, Caffrey CR, Coghlan A, Coulson R, Day TA, Delcher A, DeMarco R, Djikeng A, Eyre T, Gamble JA, Ghedin E, Gu Y, Hertz-Fowler C, Hirai H, Hirai Y, Houston R, Ivens A, Johnston DA, Lacerda D, Macedo CD, McVeigh P, Ning Z, Oliveira G, Overington JP, Parkhill J, Pertea M, Pierce RJ, Protasio AV, Quail MA, Rajandream MA, Rogers J, Sajid M, Salzberg SL, Stanke M, Tivey AR, White O, Williams DL, Wortman J, Wu W, Zamanian M, Zerlotini A, Fraser-Liggett CM, Barrell BG, El-Sayed NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460:352–360PubMedCrossRefGoogle Scholar
  4. Blair L, Webster JP (2007) Dose-dependent schistosome-induced mortality and morbidity risk elevates host reproductive effort. J Evol Biol 20:54–61PubMedCrossRefGoogle Scholar
  5. Boissier J, Rivera ER, Mone H (2003) Altered behavior of the snail Biomphalaria glabrata as a result of infection with Schistosoma mansoni. J Parasitol 89:429–433PubMedCrossRefGoogle Scholar
  6. Boyle JP, Yoshino TP (2002) Monoamines in the albumen gland, plasma, and central nervous system of the snail Biomphalaria glabrata during egg-laying. Comp Biochem Physiol A 132:411–422CrossRefGoogle Scholar
  7. Boyle JP, Hillyer JF, Yoshino TP (2003) Pharmacological and autoradiographical characterization of serotonin transporter-like activity in sporocysts of the human blood fluke, Schistosoma mansoni. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 189:631–641PubMedCrossRefGoogle Scholar
  8. Brouwers JFHM, Smeenk IMB, Van Golde LMG, Tielens AGM (1997) The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni. Mol Biochem Parasitol 88:175–185PubMedCrossRefGoogle Scholar
  9. Cheng TC, Snyder RW (1963) Studies on host-parasite relationships between larval trematodes and their hosts. IV. A histochemical determination of glucose and its role in the metabolism of molluscan host and parasite. Trans Am Microsc Soc 82:343–346CrossRefGoogle Scholar
  10. Cheng TC, Lee FO (1971) Glucose levels in the mollusc Biomphalaria glabrata infected with Schistosoma mansoni. J Invertebr Pathol 18:395–399PubMedCrossRefGoogle Scholar
  11. Cline DJ, Fried B, Sherma J (1999) TLC and GC-MS identification of glucose and maltose in Biomphalaria glabrata (Gastropoda), and use of quantitative TLC to determine the effect of starvation on the amounts of these carbohydrates. Acta Chromatogr 9:79–86Google Scholar
  12. Coles GC (1972) Carbohydrate metabolism of larval Schistosoma mansoni. Int J Parasitol 2:341–352PubMedCrossRefGoogle Scholar
  13. Coppin JF, Lefebvre C, Caby S, Cocquerelle C, Vicogne J, Coustau C, Dissous C (2003) Gene expression changes in Schistosoma mansoni sporocysts induced by Biomphalaria glabrata embryonic cells. Parasitol Res 89:113–119PubMedCrossRefGoogle Scholar
  14. Cooper LA, Larson SE, Lewis FA (1996) Male reproductive success of Schistosoma mansoni-infected Biomphalaria glabrata. J Parasitol 82:428–431PubMedCrossRefGoogle Scholar
  15. Coustau C, Mitta G, Dissous C, Guillou F, Galiner R, Alliene JF, Modat S (2003) Schistosoma mansoni and Echinostoma caproni excretory-secretory products differentially affect gene expression in Biomphalaria glabrata embryonic cells. Parasitology 127:533–542PubMedCrossRefGoogle Scholar
  16. Crews AE, Yoshino TP (1989) Schistosoma mansoni: effect of infection in reproduction and gonadal growth in Biomphalaria glabrata. Exp Parasitol 68:326–334PubMedCrossRefGoogle Scholar
  17. Crews AE, Yoshino TP (1991) Schistosoma mansoni: influence of infection on levels of translatable mRNA and on polypeptide synthesis in the ovotestis and albumen gland of Biomphalaria glabrata. Exp Parasitol 72:368–380PubMedCrossRefGoogle Scholar
  18. Davies TW, Erasmus DA (1984) An ultrastructural study of the effect of parasitism by larval Schistosoma mansoni on the calcium reserves of the host, Biomphalaria glabrata. Cell Tissue Res 236:643–649PubMedCrossRefGoogle Scholar
  19. DeJong RJ, Morgan JAT, Paraense WL, Pointier JP, Amarista M, Ayeh-Kumi PFK, Babiker A, Barbosa CS, Bremond P, Canese AP, de Souza CP, Dominguez C, File S, Gutierrez A, Incani RN, Kawano T, Kazibwe F, Kpikpi J, Lwambo NJS, Mimpfoundi R, Poda JN, Sene M, Velasquez LE, Yong M, Adema CM, Hofkin BV, Mkoji GM, Loker ES (2001) Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human blood fluke Schistosoma mansoni. Mol Biol Evol 18:2225–2239PubMedCrossRefGoogle Scholar
  20. De Jong-Brink M (1995) How schistosomes profit from the stress responses they elicit in their hosts. Adv Parasitol 35:177–256PubMedCrossRefGoogle Scholar
  21. Dresden MH, Edlin EM (1975) Schistosoma mansoni: calcium content of cercariae and its effects on protease activity in vitro. J Parasitol 61:398–402CrossRefGoogle Scholar
  22. El-Ansary A, Sammour EM, Mohamed AM (2000) Susceptibility of Biomphalaria alexandrina to infection with Schistosoma mansoni: correlation with the activity of certain glycolytic enzymes. J Egypt Soc Parasitol 30:547–560PubMedGoogle Scholar
  23. El-Ansary A, Mohamed AM, Mamoud SS, El-Bardicy S (2003) On the pathogenicity of attenuated Schistosoma mansoni cercariae released from metabolically disturbed Biomphalaria alexandrina. J Egypt Soc Parasitol 33:777–794PubMedGoogle Scholar
  24. Etges FJ (1963) Effects of Schistosoma mansoni infection on chemosensitivity and orientation of Australorbis glabratus. Am J Trop Med Hyg 12:696–700Google Scholar
  25. Fernandez MA (1997) Schistosoma mansoni infections in the first three months of life of sympatric intermediate hosts from Brazil. Mem Inst Oswaldo Cruz 92:27–29PubMedCrossRefGoogle Scholar
  26. Fernandez MA, Pieri OS (2001) Infection by Schistosoma mansoni Sambon 1907 in the first four months of life of Biomphalaria straminea (Dunker, 1848) in Brazil. Mem Inst Oswaldo Cruz 96:185–192PubMedCrossRefGoogle Scholar
  27. Gabrashanska M, Damyanova A, Kanev I (1991) Mineral composition of Echinostoma revolutum (Froelich, 1802) and its host Lymnaea stagnalis (L.). Khelmintology 31:3–7Google Scholar
  28. Gerard C, Théron A (1996) Altered nutrition and assimilation of the snail host (Biomphalaria glabrata) as a consequence of the parasitic spatial constraint (Schistosoma mansoni). Acta Trop 61:51–55PubMedCrossRefGoogle Scholar
  29. Gerard C, Théron A (1997) Age/size- and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata. Oecologia 112:447–452CrossRefGoogle Scholar
  30. Gilbertson DE, Etges FJ, Ogle JD (1967) Free amino acids of Australorbis glabratus hemolymph: comparison of four geographic strains and effect of infection by Schistosoma mansoni. J Parasitol 53:545–568CrossRefGoogle Scholar
  31. Hahn UK, Bender RC, Bayne CJ (2001) Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87:292–299PubMedGoogle Scholar
  32. Ibrahim MM (2006) Energy allocation patterns in Biomphalaria alexandrina snails in response to cadmium exposure and Schistosoma mansoni infection. Exp Parasitol 112:31–36PubMedCrossRefGoogle Scholar
  33. Humiczewska M, Rajski K (2005) Lipids in the host-parasite system: digestive gland of Lymnaea truncatula infected with the developmental stages of Fasciola hepatica. Acta Parasitol 50:235–239Google Scholar
  34. Ishak MM, Mohamed AM, Sharaf AA (1975) Carbohydrate metabolism in uninfected and ­trematode-infected snails Biomphalaria alexandrina and Bulinus truncatus. Comp Biochem Physiol 51B:499–505Google Scholar
  35. Jamjoom MB, Banaja AEA (2007) Comparative studies on the susceptible and non-susceptible Biomphalaria alexandrina the intermediate snail host of Schistosoma mansoni in western Saudi Arabia. World J Med Sci 2:108–114Google Scholar
  36. Jarusiewicz JA, Sherma J, Fried B (2006) Thin layer chromatographic analysis of estivated Biomphalaria glabrata snails and those infected with Schistosoma mansoni. Comp Biochem Physiol B 145:346–349PubMedCrossRefGoogle Scholar
  37. Lee FO, Cheng TC (1971) Schistosoma mansoni: respirometric and partial pressure studies in infected Biomphalaria glabrata. Exp Parasitol 30:393–399PubMedCrossRefGoogle Scholar
  38. Lockyer AE, Spinks J, Kane RA, Hoffman KF, Fitzpatrick JM, Rollinson D, Noble LR, Jones CS (2008) Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in hemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 9:634PubMedCrossRefGoogle Scholar
  39. Looker DL, Etges FJ (1979) Effect of Schistosoma mansoni infection on fecundity and perivitelline fluid composition in Biomphalaria. J Parasitol 65:880–885PubMedCrossRefGoogle Scholar
  40. McClelland G, Bourns TKR (1969) Effects of Trichobilharzia ocellata on growth, reproduction, and survival of Lymnaea stagnalis. Exp Parasitol 24:137–146PubMedCrossRefGoogle Scholar
  41. Makanga B (1981) The effect of varying the number of Schistosoma mansoni miracidia on the reproduction and survival of Biomphalaria pfeifferi. J Invertebr Pathol 37:7–10PubMedCrossRefGoogle Scholar
  42. Mandlowitz A, Dusanic D, Lewert RM (1960) Peptidase and lipase activity of extracts of Schistosoma mansoni cercariae. J Parasitol 46:89–90CrossRefGoogle Scholar
  43. Manger P, Li J, Christensen BM, Yoshino TP (1996) Biogenic monoamines in the freshwater snail, Biomphalaria glabrata: influence of infection by the human blood fluke, Schistosoma mansoni. Comp Biochem Physiol 114:227–234CrossRefGoogle Scholar
  44. Massa DR, Chejlava MJ, Fried B (2007) High performance column liquid chromatographic analysis of selected carboxylic acids in Biomphalaria glabrata patently infected with Schistosoma mansoni. Parasitol Res 101:925–928PubMedCrossRefGoogle Scholar
  45. Mazuran N, Hrsak M, Tomic PD (1999) Effects of CaCl2 and CaBr2 on the fecundity of Planorbarius corneus L. Chemosphere 38:2345–2355CrossRefGoogle Scholar
  46. Meier M, Meier-Brook C (1981) Schistosoma mansoni: effect on growth, fertility, and development of distal male organs. Z Parasitenkd 66:121–131PubMedCrossRefGoogle Scholar
  47. Meuleman EA (1972) Host-parasite interrelationships between the freshwater pulmonate Biomphalaria pfeifferi and the trematode Schistosoma mansoni. Neth J Zool 22:355–427CrossRefGoogle Scholar
  48. Meyer F, Meyer H, Bueding E (1970) Lipid metabolism in the parasitic and free-living flatworms Schistosoma mansoni and Dugesia dorotocephala. Biochim Biophys Acta 210:257–266PubMedCrossRefGoogle Scholar
  49. Minchella DJ, Loverde PT (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. Am Nat 118:876–881CrossRefGoogle Scholar
  50. Mohamed AM, Ishak MM (1979) Growth raste and changes in tissue carbohydrates during schistosome infection of the snail Biomphalaria alexandrina. Hydrobiologia 76:17–21CrossRefGoogle Scholar
  51. Mostafa OMS (2007) Effects of Schistosoma mansoni and Schistosoma haematobium infections on calcium content in their intermediate hosts. Parasitol Res 101:963–966PubMedCrossRefGoogle Scholar
  52. Nabih I, El Dardiri Z, El-Ansary A, Rizk M (1990) Measurement of some selected enzymatic activities in infected Biomphalaria alexandrina snails. Cell Mol Biol 36:637–642PubMedGoogle Scholar
  53. Ong JHL, Chejlava M, Fried B, Koehnlein KM, Bosavage GL, Sherma J (2004) Effects of Schistosoma mansoni infection on inorganic elements in the snail Biomphalaria glabrata. J Helminthol 78:343–346PubMedCrossRefGoogle Scholar
  54. Patocka N, Ribiero P (2007) Characterization of a serotonin transporter in the parasitic flatworm, Schistosoma mansoni: cloning, expression and functional analysis. Mol Biochem Parasitol 154:125–133PubMedCrossRefGoogle Scholar
  55. Pinheiro J, Amato S (1995) Calcium determination in the shell of Lymnaea columella (Mollusca, Gastropoda) infected with Fasciola hepatica (Platyhelminthes, Digenea). Braz Arch Biol Technol 38:761–767Google Scholar
  56. Rupprecht H, Becker W, Schwanbek A (1989) Alterations in Biomphalaria glabrata components during long term infection with Schistosoma mansoni infection. Parasitol Res 75:233–237PubMedCrossRefGoogle Scholar
  57. Santhanagopalan V, Yoshino TP (2000) Monoamines and their metabolites in the freshwater snail Biomphalaria glabrata. Comp Biochem Physiol A Mol Integr Physiol 125:469–478PubMedCrossRefGoogle Scholar
  58. Schmale H, Becker W (1977) Studies on the urea cycle of Biomphalaria glabrata during normal feeding activity, in starvation and with infection of Schistosoma mansoni. Comp Biochem Physiol 58A:321–330Google Scholar
  59. Schnell S, Becker W, Winkler A (1985) Amino acid metabolism in the freshwater pulmonate Biomphalaria glabrata infected with the trematode Schistosoma mansoni. Comp Biochem Physiol 81B:1001–1008Google Scholar
  60. Schwanbeck A, Becker W, Rupprecht H (1986) Quantification of parasite development in the host-parasite system Biomphalaria glabrata and Schistosoma mansoni. Z Parasitenkd 72:365–373CrossRefGoogle Scholar
  61. Schwartz CFW, Carter CE (1982) Effect of Schistosoma mansoni on glycogen synthase and phosphorylase from Biomphalaria glabrata (Mollusca). J Parasitol 68:236–242PubMedCrossRefGoogle Scholar
  62. Shaw MK, Erasmus DA (1987) Biomphalaria glabrata: changes in calcium reserves following parasitism by larval Schistosoma mansoni. Parasitology 95:267–276PubMedCrossRefGoogle Scholar
  63. Sire C, Durand P, Pointier JP, Théron A (1999) Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. J Parasitol 85:436–441PubMedCrossRefGoogle Scholar
  64. Smith ME, Steiner SA, Isseroff H (1994) Urea: inhibitor of growth and reproduction in Bulinus truncatus. Comp Biochem Physiol 108A:569–577CrossRefGoogle Scholar
  65. Sorensen RE, Minchella DJ (2001) Snail-trematode life history interactions: past trends and future directions. Parasitology 123:S3–S18PubMedCrossRefGoogle Scholar
  66. Stanislawski E, Becker W (1979) Influences of semi-synthetic diets, starvation and infection with Schistosoma mansoni (Trematoda) on the metabolism of Biomphalaria glabrata (Gastropoda). Comp Biochem Physiol 63A:527–533CrossRefGoogle Scholar
  67. Stanislawski E, Becker W, Muller G (1979) Alterations of the free amino acid content in the hemolymph of Biomphalaria glabrata (Pulmonata) in starvation and after infection with Schistosoma mansoni (Trematoda). Comp Biochem Physiol 63B:477–482Google Scholar
  68. Sturrock BM (1966) The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Ann Trop Med Hyg 60:187–197Google Scholar
  69. Sturrock BM, Sturrock RF (1970) Laboratory studies of the host-parasite relationship of Schistosoma mansoni and Biomphalaria glabrata from St. Lucia, West Indies. Ann Trop Med Parasitol 64:357–363PubMedGoogle Scholar
  70. Théron A, Mone H, Gerard C (1992) Spatial and energy compromise between host and parasite: the Biomphalaria glabrata-Schistosoma mansoni system. Int J Parasitol 22:91–94PubMedCrossRefGoogle Scholar
  71. Théron A, Gerard C (1994) Development of accessory sexual organs in Biomphalaria glabrata (Planorbidae) in relation to timing of infection by Schistosoma mansoni: consequences for energy utilization patterns by the parasite. J Molluscan Stud 60:25–31CrossRefGoogle Scholar
  72. Thompson SN (1987) Effect of Schistosoma mansoni on the gross lipid composition of its vector Biomphalaria glabrata. Comp Biochem Physiol 87B:357–360Google Scholar
  73. Thompson SN, Lee RWK (1987) Characterization of the 31P NMR spectrum of the schistosome vector Biomphalaria glabrata and of the changes following infection by Schistosoma mansoni. J Parasitol 73:64–76PubMedCrossRefGoogle Scholar
  74. Thompson SN, Mejia-Scales V (1989) Effects of Schistosoma mansoni on the nutrition of its intermediate host, Biomphalaria glabrata. J Parasitol 75:329–332PubMedCrossRefGoogle Scholar
  75. Thornhill JA, Jones JT, Kusel JR (1986) Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni. Parasitology 93:443–450PubMedCrossRefGoogle Scholar
  76. Van Aardt WJ, de Kock KN, Naudé K (2003) The respiratory properties of Biomphalaria glabrata exposed to Schistosoma mansoni infection, starvation, CO and choices of different oxygen concentrations. Exp Parasitol 103:93–101PubMedCrossRefGoogle Scholar
  77. Veldhuijzen JP (1975) Glucose-tolerance in the pond snail Lymnaea stagnalis as affected by temperature and starvation. Neth J Zool 25:206–218CrossRefGoogle Scholar
  78. Von Brand T, Files VS (1947) Chemical and histological observations on the influence of Schistosoma mansoni on Australorbis glabratus. J Parasitol 33:476–482CrossRefGoogle Scholar
  79. Wagner SD, Pachuski J, Fried B, Sherma J (2002) Thin layer chromatographic analysis of carbohydrates and amino acids in Schistosoma mansoni (Trematoda) cercariae. Acta Chromatogr 12:159–169Google Scholar
  80. Warr E, Meredith JM, Nimmo DD, Basu S, Hurd H, Eggleston P (2006) A tapeworm molecule manipulates vitellogenin expression in the beetle Tenebrio molitor. Insect Mol Biol 15:497–505PubMedCrossRefGoogle Scholar
  81. Webster JP, Hoffmann JI, Berdoy M (2003) Parasite infection, host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite. Proc R Soc Lond B 270:1481–1485CrossRefGoogle Scholar
  82. Webster JP, Woolhouse MEJ (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proc R Soc Lond B 266:391–396CrossRefGoogle Scholar
  83. White MW, Chejlava M, Freid B, Sherma J (2005) Effects of various larval digeneans on the calcium carbonate content of the shells of Helisoma trivolvis, Biomphalaria glabrata and Physa sp. Parasitol Res 95:252–255PubMedCrossRefGoogle Scholar
  84. Williams CL, Gilbertson DE (1983) Altered feeding response as a cause for the altered heartbeat rate and locomotor activity of Schistosoma mansoni-infected Biomphalaria glabrata. J Parasitol 69:671–676PubMedCrossRefGoogle Scholar
  85. Woolhouse MEJ (1989) The effect of schistosome infection on the mortality rates of Bulinus globosus and Biomphalaria pfeifferi. Ann Trop Med Parasitol 83:137–141PubMedGoogle Scholar
  86. Yousif F, Haroun N, Ibrahim A, El-Bardicy S (1996) Biomphalaria glabrata: a new threat for schistosomiasis transmission in Egypt. J Egypt Soc Parasitol 26:191–205PubMedGoogle Scholar
  87. Zhang SM, Nian H, Wang B, Loker ES, Adema CN (2009) Schistosomin from the snail Biomphalaria glabrata: Expression studies suggest no involvement in trematode-mediated castration. Mol Biochem Parasitol 165:79–86PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2011

Authors and Affiliations

  1. 1.Biology DepartmentLawrence UniversityAppletonUSA

Personalised recommendations