Effects of Nonschistosome Larval Trematodes on Biomphalaria Snails

  • Jose-Guillermo Esteban
  • Carla Muñoz-Antoli
  • Maria Trelis
  • Rafael Toledo


This chapter examines the most salient literature on the development of nonschistosome larval digeneans in Biomphalaria spp. (members of the ­superfamilies Clinostomoidea, Diplostomoidea, Echinostomatoidea, Paramphistomoidea, and Pronocephaloidea). For this purpose, the general biology of the nonschistosome trematode species that use Biomphalaria spp. as ­intermediate hosts are ­analyzed. Thereafter, the main features of these parasitic infections are studied with ­particular emphasis on topics such as the effect of the infections on the snail, the antagonism and/or competition between different digenean species in the snail, the ­immunology of the infection, and the genomic and proteomic aspects of these host–parasite interactions.


Intermediate Host Snail Host Infected Snail Trematode Species Shell Diameter 



This work was supported by Project CGL2005-02321/BOS of Ministerio de Educación y Ciencia (Spain) and FEDER (Europea Union) and by Project PROMETEO 2009/081 of Conselleria d’Educació of Generalitat Valenciana (Valencia, Spain).


  1. Adema CM, Arguello DF, Striker SA, Loker ES (1994a) A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa. J Parasitol 80:719–727PubMedGoogle Scholar
  2. Adema CM, Hertel LA, Loker ES (1997a) Infection with Echinostoma paraensei (Digenea) induces parasite-reactive polypeptides in the hemolymph of the gastropod host Biomphalaria glabrata. In: Beckage N (ed) Parasite effects on host physiology and behavior. Chapman, New York, pp 77–99Google Scholar
  3. Adema CM, Hertel LA, Miller RD, Loker ES (1997b) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 94:8691–8696PubMedGoogle Scholar
  4. Adema CM, Sapp KK, Hertel LA, Loker ES (2000) Immunobiology of the relationship of echinostomes with snail intermediate hosts. In: Fried B, Gracyzk TK (eds) Echinostomes as experimental models for biological research. Kluwer, Dordrecht, pp 149–173Google Scholar
  5. Adema CM, Van Deutekom-Mulder EC, Van der Knaap PW, Sminia T (1994b) Schistosomicidal activities of Lymnaea stagnalis hemocytes: the role of oxygen radicals. Parasitology 109:479–485PubMedGoogle Scholar
  6. Anderson JW, Fried B (1987) Experimental infection of Physa heterostropha, Helisoma trivolvis, and Biomphalaria glabrata (Gastropoda) with Echinostoma revolutum (Trematoda) cercariae. J Parasitol 73:49–54PubMedGoogle Scholar
  7. Ataev G, Coustau C (1999) Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility/resistance. Dev Comp Immunol 23:187–198PubMedGoogle Scholar
  8. Ataev GL, Dobrovol’skii AA, Avanessian AV, Loker ES (2001) Germinal elements and their development in Echinostoma caproni and Echinostoma paraensei (Trematoda) miracidia. J Parasitol 87:1160–1164PubMedGoogle Scholar
  9. Ataev G, Dobrovol’skii AA, Fournier A, Jourdane J (1997) Migration and development of mother sporocysts of Echinostoma caproni (Digenea, Echinostomatidae). J Parasitol 83:444–453PubMedGoogle Scholar
  10. Ataev GL, Dobrovol’skii AA, Isakova NP (2005) Development of the partenitae infrapopulation of Echinostoma caproni (Trematoda: Echinostomatidae). Parazitologiia 39:124–136, In RussianPubMedGoogle Scholar
  11. Ataev G, Fournier A, Coustau C (1998) Comparison of Echinostoma caproni mother sporocyst development in vivo and in vitro using Biomphalaria glabrata and B. glabrata embryonic cell line. J Parasitol 84:227–235PubMedGoogle Scholar
  12. Ataev GL, Isakova NP, Dobrovol’skii AA (2006) Development of mother sporocysts of Echinostoma caproni (Trematoda: Echinostomatidae). Parazitologiia 40:47–56, In RussianPubMedGoogle Scholar
  13. Bandstra SR, Fried B, Sherma J (2006) High-performance thin-layer chromatographic analysis of neutral lipids and phospholipids in Biomphalaria glabrata patently infected with Echinostoma caproni. Parasitol Res 99:414–418PubMedGoogle Scholar
  14. Basch PF, DiConza JJ (1975) Predation by Echinostome rediae upon Schistosome sporocysts in vitro. J Parasitol 61:1044–1047PubMedGoogle Scholar
  15. Beers K, Fried B, Fujino T, Sherma J (1995) Effects of diet on the lipid composition of the digestive gland-gonad complex of Biomphalaria glabrata (Gastropoda) infected with larval Echinostoma caproni (Trematoda). Comp Biochem Physiol 110B:729–737Google Scholar
  16. Behrens AC, Nollen PM (1992) Responses of Echinostoma caproni miracidia to gravity, light, and chemicals. Int J Parasitol 22:673–675PubMedGoogle Scholar
  17. Bouchut A, Coustau C, Gourbal B, Mitta G (2007) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach. Parasitology 134:575–588PubMedGoogle Scholar
  18. Bouchut A, Roger E, Coustau C, Gourbal B, Mitta G (2006a) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 36:175–184PubMedGoogle Scholar
  19. Bouchut A, Sautiere PE, Coustau C, Mitta G (2006b) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: Potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Trop 98:234–246PubMedGoogle Scholar
  20. Carney WP (1991) Echinostomiasis – a snail-borne intestinal trematode zoonosis. Southeast Asian J Trop Med Public Health 22:206–211PubMedGoogle Scholar
  21. Christensen NO, Frandsen F, Roushdy MZ (1980) The influence of environmental conditions and parasite-intermediate host-related factors on the transmission of Echinostoma liei. Z Parasitenkd 63:47–63Google Scholar
  22. Combes C (1992) Trematodes: Antagonism between species and sterilizing effects on snails in biological control. Parasitology 84:151–175Google Scholar
  23. Coustau C, Gourbal B, Mitta G, Adema C (2009) Echinostomes and snails: exploring complex interactions. In: Fried B, Toledo R (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 35–59Google Scholar
  24. Crompton DWT (1999) How much human helminthiasis is there in the world? J Parasitol 85:397–403PubMedGoogle Scholar
  25. Dar YD, Rondelaud D, Dreyfuss G (2005) Update of fasciolosis-transmitting snails in Egypt (review and comment). J Egypt Soc Parasitol 35:477–490PubMedGoogle Scholar
  26. De Jong-Brink M (1995) How schistosomes profit from the stress responses they elicit in their hosts. Adv Parasitol 35:177–256PubMedGoogle Scholar
  27. DeGaffe G, Loker ES (1998) Susceptibility of Biomphalaria glabrata to infection with Echinostoma paraensei: correlation with the effect of parasite secretory-excretory products on host hemocyte spreading. J Invertebr Pathol 71:64–72PubMedGoogle Scholar
  28. Dias MLGG, Eiras JC, Machado MH, Souza GTR, Pavanelli GC (2003) The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná river, Brazil. Parasitol Res 89:506–508PubMedGoogle Scholar
  29. Dias Neto E, de Souza CP, Rollinson D, Katz N, Pena SD, Simpson AJ (1993) The random amplification of polymorphic DNA allows the identification of strains and species of schistosome. Mol Biochem Parasitol 57:83–88PubMedGoogle Scholar
  30. Dubois G, Nassi H (1977) [Redescription of d’Apatemon (Apatemon) graciliformis Szidat, 1928 (Trematoda: Strigeidae) with a preliminary note on its life cycle]. Ann Parasitol Hum Comp 52:507–510PubMedGoogle Scholar
  31. El-Shazly AM, Helmy MM, Haridy FM, el-Sharkawy EM, Morsy TA (2002) Fasciola immature stages sought in Lymnaea species and Biomphalaria species in the water bodies of Dakahlia Governorate. J Egypt Soc Parasitol 32:109–118PubMedGoogle Scholar
  32. Escribano A, Williams T, Goulsson D, Cave RD, Chapman JW, Caballero P (2001) Consequences of interspecific competition on the virulence and genetic competition of nucleopolyhedrovirus in Spodoptera frugiperla larvae parasitized by Chelonus insularis. Biol Sci Technol 11:649–662Google Scholar
  33. Esteban JG, Muñoz-Antolí C (2009) Echinostomes: systematic and life cycles. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 1–34Google Scholar
  34. Farag HF, el-Sayad MH (1995) Biomphalaria alexandrina naturally infected with Fasciola gigantica in Egypt. Trans R Soc Trop Med Hyg 89:36PubMedGoogle Scholar
  35. Flores V, Brugni N (2005) Notocotylus biomphalariae n. sp. (Digenea: Notocotylidae) from Biomphalaria peregrina (Gastropoda: Pulmonata) in Patagonia, Argentina. Syst Parasitol 61:207–214PubMedGoogle Scholar
  36. Frazer BA, Fried B (1998) Single-species infections of Echinostoma caproni cercariae in pulmonate snails and concurrent infections of E. caproni and Echinostoma trivolvis cercariae in Biomphalaria glabrata. Int J Parasitol 28:595–597PubMedGoogle Scholar
  37. Fried B (2001) Biology of echinostomes except Echinostoma. Adv Parasitol 49:163–210PubMedGoogle Scholar
  38. Fried B, Graczyk TK (eds) (2000) Echinostomes as experimental models for biological research. Kluwer, Dordrecht, The Netherlands, p 273Google Scholar
  39. Fried B, Graczyk TK (2004) Recent advances in the biology of Echinostoma species in the “revolutum” group. Adv Parasitol 58:139–195PubMedGoogle Scholar
  40. Fried B, Huffman JE (1996) The biology of the intestinal trematode Echinostoma caproni. Adv Parasitol 38:311–368PubMedGoogle Scholar
  41. Fried B, King W (1989) Attraction of Echinostoma revolutum cercariae to Biomphalaria glabrata dialysate. J Parasitol 75:55–57Google Scholar
  42. Fried B, Reddy A (1999) Effects of snail-conditioned water from Biomphalaria glabrata on hatching of Echinostoma caproni miracidia. Parasitol Res 85:155–157PubMedGoogle Scholar
  43. Fried B, Frazer BA, Kanev I (1998) Comparative observations on cercariae and metacercariae of Echinostoma trivolvis and Echinoparyphium sp. J Parasitol 84:623–626PubMedGoogle Scholar
  44. Fried B, Frazer BA, Reddy A (1997a) Chemoattraction and penetration of Echinostoma trivolvis and E. caproni cercariae in the presence of Biomphalaria glabrata, Helisoma trivolvis, and Lymnaea elodes dialysate. Parasitol Res 83:193–197PubMedGoogle Scholar
  45. Fried B, Huffman JE, Keeler S, Peoples RC (2009) The biology of the caecal trematode Zygocotyle lunata. Adv Parasitol 69:1–40.Google Scholar
  46. Fried B, Idris N, Ohsawa T (1995) Experimental infection of juvenile Biomphalaria glabrata with cercariae of Echinostoma trivolvis. J Parasitol 81:308–310PubMedGoogle Scholar
  47. Fried B, LaTerra R, Kim Y (2002) Emergence of cercariae of Echinostoma caproni and Schistosoma mansoni from Biomphalaria glabrata under different laboratory conditions. J Helminthol 76:369–371PubMedGoogle Scholar
  48. Fried B, Schafer S, Kim S (1989) Effects of Echinostoma caproni infection on the lipid composition of Biomphalaria glabrata. Int J Parasitol 19:353–354PubMedGoogle Scholar
  49. Fried B, Scheuermarn S, Jr M (1987) Infectivity of Echinostoma revolutum miracidia for laboratory-raised pulmonate snails. J Parasitol 73:1047–1048PubMedGoogle Scholar
  50. Fried B, Schmidt KA, Sorensen RE (1997b) In vivo and ectopic encystment of Echinostoma revolutum and chemical excystation of the metacercariae. J Parasitol 83:251–254PubMedGoogle Scholar
  51. Fried B, Sherma J, Rao KS, Ackman RG (1993) Fatty acid composition of Biomphalaria glabrata (Gastropoda: Planorbidae) experimentally infected with the intramolluscan stages of Echinostoma caproni (Trematoda). Comp Biochem Physiol 104B:595–598Google Scholar
  52. Fryer SE, Oswald RC, Probert AJ, Runham NW (1990) The effect of Schistosoma haematobium infection on the growth and fecundity of three sympatric species of bulinid snails. J Parasitol 76:557–563PubMedGoogle Scholar
  53. Fujino T, Takahashi Y, Fried B (1995) A comparison of Echinostoma trivolvis and E. caproni using random amplified polymorphic DNA analysis. J Helminthol 69:263–264PubMedGoogle Scholar
  54. Fujino T, Wu Z, Nagano I, Takahashi Y, Fried B (1997) Specific primers for the detection of genomic DNA of Echinostoma trivolvis and E. caproni (Trematoda:Echinostomatidae). Mol Cell Probes 11:77–80PubMedGoogle Scholar
  55. Goodman JD, Panesar TS (1976) Parasymphylodora manteri n.sp., and adult trematode from fresh-water pulmonate snail, Biomphalaria choanomphala choanomphala, from Lake Victoria, Uganda. Trans Am Microsc Soc 95:204–209PubMedGoogle Scholar
  56. Haas W (2000) The behavioral biology of echinostomes. In: Fried B, Gracyzk TK (eds) Echinostomes as experimental models for biological research. Kluwer, Dordrecht, pp 175–197Google Scholar
  57. Haas W, Beran B, Loy C (2008) Selection of the host’s habitat by cercariae: from laboratory experiments to the field. J Parasitol 94:1233–1238PubMedGoogle Scholar
  58. Haas W, Haberl B, Kalbe M, Körner M (1995) Snail-host finding by miracidia and cercariae: chemical host cues. Parasitol Today 11:468–472Google Scholar
  59. Haberl B, Körner M, Spengler Y, Hertel J, Kalbe M, Haas W (2000) Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology 120:470–496Google Scholar
  60. Hertel LA, Adema CM, Loker ES (2005) Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 29:295–303PubMedGoogle Scholar
  61. Hertel J, Haberl B, Hamburger J, Haas W (2003) Description of a tandem repeated DNA sequence of Echinostoma caproni and methods for its detection in snail and plankton samples. Parasitology 126:443–449PubMedGoogle Scholar
  62. Hertel LA, Stricker SA, Loker ES (2000) Calcium dynamics of hemocytes of the gastropod Biomphalaria glabrata: effects of digenetic trematodes and selected bioactive compounds. Invertebr Biol 119:27–37Google Scholar
  63. Huffman JE, Fried B (1990) Echinostoma and echinostomiasis. Adv Parasitol 29:215–269PubMedGoogle Scholar
  64. Huizinga HW (1973) Ribeiroia marini: Pathogenesis and larval trematode antagonism in the snail, Biomphalaria glabrata. Exp Parasitol 33:350–364PubMedGoogle Scholar
  65. Humbert E, Coustau C (2001) Refractoriness of host hemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata - Echinostoma caproni system. Parasitology 122:651–660PubMedGoogle Scholar
  66. Hurd H (1990) Physiological and behavioural interactions between parasites and invertebrate hosts. Adv Parasitol 29:272–317Google Scholar
  67. Jeyarasasingam U, Heyneman D, Lim HK, Mansour N (1972) Life cycle of a new echinostome from Egypt, Echinostoma liei sp.nov. (Trematoda: Echinostomatidae). Parasitology 65:203–222Google Scholar
  68. Johnson PTJ, McKenzie VJ (2009) Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 249–280Google Scholar
  69. Johnson PTJ, Sutherland DR, Kinsella JM, Lunde KB (2004) Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem. Adv Parasitol 57:191–253PubMedGoogle Scholar
  70. Jourdane J (1983) Effects of hyperinfestations by Echinostoma togoensis Jourdane and Kulo, 1981 on growth and survival of Biomphalaria pfeifferi snails. Ann Parasitol Hum Comp 58:103–108PubMedGoogle Scholar
  71. Jourdane J, Mounkassa JB (1986) Topographic shifting of primary sporocysts of Schistosoma mansoni in Biomphalaria pfeifferi as a result of coinfection with Echinostoma caproni. J Invertebr Pathol 48:269–274PubMedGoogle Scholar
  72. Keeler SP, Huffman JE (2009) Echinostomes in the second intermediate host. In: Fried B, Toledo R (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 61–87Google Scholar
  73. Kechemir N, Jourdane J, Mas-Coma S (2002) Life cycle of a new African echinostome species reproducing by parthenogenesis. J Nat Hist 36:1777–1784Google Scholar
  74. King PH, Van As JG (1996) A description of the life stages of Echinoparyphium elegans (Trematoda: Echinostomatidae). S Afr J Zool 31:145–153Google Scholar
  75. Kostadinova A, Gibson DI (2000) The systematic of the Echinostomes. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer, Dordrecht, The Netherlands, pp 31–57Google Scholar
  76. Kostadinova A, Herniou EA, Barret J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176PubMedGoogle Scholar
  77. Kuris AM (1980) Effect of exposure to Echinostoma liei miracidia on growth and survival of young Biomphalaria glabrata snails. Int J Parasitol 10:303–308PubMedGoogle Scholar
  78. Kuris AM, Warren J (1980) Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second intermediate host, Biomphalaria glabrata. J Parasitol 66:630–635PubMedGoogle Scholar
  79. Langand J, Morand S (1998) Heritable non-susceptibility in an allopatric host-parasite system: Biomphalaria glabrata (Mollusca)-Echinostoma caproni (Plathelminth Digenea). J Parasitol 84:739–742Google Scholar
  80. Lardans V, Dissous C (1998) Snail control strategies for reduction of schistosomiasis transmission. Parasitol Today 14:413–417PubMedGoogle Scholar
  81. Laursen JR, Yoshino TP (1999) Biomphalaria glabrata embryonic (Bge) cell line supports in vitro miracidial transformation and early larval development of the deer liver fluke, Fascioloides magna. Parasitology 118:187–194PubMedGoogle Scholar
  82. Layman LR, Dory AC, Koehnlein KM, Fried B, Sherma J (1996) Nmeasurement of metallic ions in Biomphalaria glabrata (Gastropoda) infected with Echinostoma caproni (Trematoda) and in uninfected sanils. J Helminthol Soc Wash 63:256–258Google Scholar
  83. Léonard PM, Adema CM, Zhang S-M, Loker ES (2001) Structure of two FREP genes that encode IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene 269:155–165PubMedGoogle Scholar
  84. Lie KJ (1973) Larval trematode antagonism: principles and possible application as a control method. Exp Parasitol 33:343–349PubMedGoogle Scholar
  85. Lie KJ (1982) Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata. A discussion of the interference hypothesis. Trop Geogr Med 34:111–122PubMedGoogle Scholar
  86. Lie KJ, Basch PF (1966) Life history of Echinostoma barbosai sp. n. (Trematoda: Echinostomatidae). J Parasitol 52:1052–1057PubMedGoogle Scholar
  87. Lie KJ, Basch PF (1967) The life history of Echinostoma paraensei sp. n. (Trematoda: Echinostomatidae). J Parasitol 53:1192–1199PubMedGoogle Scholar
  88. Lie KJ, Heyneman D (1976) Studies on resistance in snails. 3. Tissue reactions to Echinostoma lindoense sporocysts in sensitized and resensitized Biomphalaria glabrata. J Parasitol 62:51–58PubMedGoogle Scholar
  89. Lie KJ, Basch PF, Hoffman MA (1967) Antagonism between Paryphostomum segregatum and Echinostoma barbosai in the snail Biomphalaria straminea. J Parasitol 53:1205–1209PubMedGoogle Scholar
  90. Lie KJ, Heyneman D, Jeyarasasingam V, Mansour N, Lee HF, Lee HA, Kostanian N (1975) The life cycle of Echinoparyphium ralphaudyi sp. n. (Trematoda: Echinostomatidae). J Parasitol 61:59–65PubMedGoogle Scholar
  91. Lie KJ, Heyneman D, Richards CS (1977) Studies on resistance in snails: interference by nonirradiated echinostome larvae with natural resistance to Schistosoma mansoni in Biomphalaria glabrata. J Invertebr Pathol 29:118–125PubMedGoogle Scholar
  92. Lim HK, Heyneman D (1972) Intramolluscan inter-trematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological control. Adv Parasitol 10:191–268PubMedGoogle Scholar
  93. Lo CT (1973) Experimental second intermediate hosts of Echinostoma malayanum Leiper, 1911. J Parasitol 59:746–747PubMedGoogle Scholar
  94. Loker ES, Adema CM (1995) Schistosomes, echinostomes and snails: comparative immunobiology. Parasitol Today 11:120–124Google Scholar
  95. Loker ES, Bayne CJ (1986) Immunity to trematode larvae in the snail Biomphalaria. Zoolog Symp 56:199–220Google Scholar
  96. Loker ES, Hertel LA (1987) Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. J Parasitol 73:503–513PubMedGoogle Scholar
  97. Loker ES, Boston ME, Bayne CJ (1989) Differential adherence of M-line Biomphalaria glabrata hemocytes to Schistosoma mansoni and Echinostoma paraensei larvae, and experimental manipulation of hemocyte binding. J Invertebr Pathol 54:260–268PubMedGoogle Scholar
  98. Loker ES, Cimino DF, Hertel LA (1992) Excretory-secretory products of Echinostoma paraensei sporocyst mediate interference with Biomphalaria glabrata hemocyte functions. J Parasitol 78:104–115PubMedGoogle Scholar
  99. Loker ES, Coustau C, Ataev GL, Jourdane J (1999) In vitro culture of rediae of Echinostoma caproni. Parasite 6:169–174PubMedGoogle Scholar
  100. Maldonado A, Lanfredi R (2009) Echinostomes in the wild. In: Fried B, Toledo R (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 129–145Google Scholar
  101. Maldonado A Jr, Vieira GO, Garcia JS, Rey L, Lanfredi RM (2001) Biological aspects of a new isolate of Echinostoma paraensei (Trematoda: Echinostomatidae): susceptibility of sympatric snails and the natural vertebrate host. Parasitol Res 87:853–859PubMedGoogle Scholar
  102. Maldonado A Jr, Vieira GO, Lanfredi RM (2003) Echinostoma luisreyi n. sp. (Platyhelminthes: Digenea) by light and scanning electron microscopy. J Parasitol 89:800–808PubMedGoogle Scholar
  103. Marcilla A (2009) Echinostomes: genomics and proteomics. In: Fried B, Toledo R (eds) The biology of echinostomes: from the molecule to the community. Springer, New York, pp 207–228Google Scholar
  104. Marsit CJ, Fried B, Sherma J (2000) Neutral lipids in cercariae, encysted metacercariae, and rediae of Echinostoma caproni. J Helminthol 74:365–367PubMedGoogle Scholar
  105. McCarthy AM (1999) The influence of second intermediate host species on the infectivity of metacercarial cysts of Echinoparyphium recurvatum. J Helminthol 73:143–145Google Scholar
  106. Meece JK, Nollen PM (1996) A comparison of the adult and miracidial stages of Echinostoma paraensei and E. caproni. Int J Parasitol 26:37–43PubMedGoogle Scholar
  107. Meyrowitsch D, Christensen NO, Hindsbo O (1991) Effects of temperature and host density on the snail-finding capacity of cercariae of Echinostoma caproni (Digenea: Echinostomatidae). Parasitology 102:391–396PubMedGoogle Scholar
  108. Minchella DJ (1985) Host life history variation in response to parasitism. Parasitology 90:205–216Google Scholar
  109. Minchella DJ, LoVerde PT (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. Am Nat 118:876–881Google Scholar
  110. Mohamed SH (1992) Ultrastructure aspects of intramolluscan developing cercariae of Echinostoma liei. J Egypt Soc Parasitol 22:479–485PubMedGoogle Scholar
  111. Monroy FP, Loker ES (1993) Production of heterogeneous carbohydrate-binding proteins by the host snail Biomphalaria glabrata following exposure to Echinostoma paraensei and Schistosoma mansoni. J Parasitol 79:416–423PubMedGoogle Scholar
  112. Monroy F, Hertel LA, Loker ES (1992) Carbohydrate-binding plasma proteins from the gastropod Biomphalaria glabrata: strain specificity and the effects of trematode infection. Dev Comp Immunol 16:355–366PubMedGoogle Scholar
  113. Morgan JAT, Blair D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111:609–615PubMedGoogle Scholar
  114. Morgan JAT, Blair D (1998a) Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116:289–297PubMedGoogle Scholar
  115. Morgan JAT, Blair D (1998b) Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. Int J Parasitol 28:493–502PubMedGoogle Scholar
  116. Mouahid A, Moné H (1988) Echinoparyphium elegans (Looss, 1899) (Digenea: Echinostomatidae): the life cycle and redescription of the adult with a revision of the 43-spined members of the genus Echinoparyphium. Syst Parasitol 12:149–157Google Scholar
  117. Muñoz-Antolí C, Marin A, Toledo R, Esteban JG (2007) Effect of Echinostoma friedi (Trematoda: Echinostomatidae) experimental infection on longevity, growth and fecundity of juvenile Radix peregra (Gastropoda: Lymnaeidae) and Biomphalaria glabrata (Gastropoda: Planorbidae) snails. Parasitol Res 101:1663–1670PubMedGoogle Scholar
  118. Muñoz-Antoli C, Trelis M, Toledo R, Esteban JG (2006) Infectivity of Echinostoma friedi miracidia to different snail species under experimental conditions. J Helminthol 80:323–325PubMedGoogle Scholar
  119. Nassi H (1978) Données sur le cycle biologique de Ribeiroia marini guadeloupensis n. ssp., trematoda stérilisant Biomphalaria glabrata en Guadaloupe. Acta Trop 35:41–56PubMedGoogle Scholar
  120. Nassi H (1979) Coïncidence entre le blocage précoce de la ponte de Biomphalaria glabrata (Gasteropoda: Pulmonata) et la localisation cérébrale des jeunes rédies mères de Ribeiroia marini guadeloupensis (Trematoda: Cathaemasiidae). C R Acad Sci III 289:165–168Google Scholar
  121. Nassi H (1980) Données experimentales sur le cycle biologique de Petasiger caribbensis n. sp. (Trematoda: Echinostomatidae) parasite larvaire de Biomphalaria glabrata en Guadeloupe. Ann Parasitol Hum Comp 55:41–55Google Scholar
  122. Nassi H, Bayssade-Dufour C (1980) Life cycle of Clinostomum golvani n. sp. (Trematoda: Clinostomidae) a larval parasite of Biomphalaria glabrata, the snail vector of Schistosoma mansoni in Guadeloupe. Ann Parasitol Hum Comp 55:527–540, In FrenchPubMedGoogle Scholar
  123. Nassi H, Dupouy J (1988) Étude experimentale du cicle biologique d´Echinostoma parvocirrus n. sp. (Trematoda: Echinostomatidae), parasite larvaire de Biomphalaria glabrata en Guadeloupe. Ann Parasitol Hum Comp 63:103–118Google Scholar
  124. Nassi H, Pointier JP, Golvan YJ (1979) Bilan d’un essai de contrôle de Biomphalaria glabrata en Guadaloupe â l’aide d’un trématode stérilisant. Ann Parasitol Hum Comp 54:185–192PubMedGoogle Scholar
  125. Noda S, Loker ES (1989a) Effect of infection with Echinostoma paraensei on the circulating hemocyte population of the host snail Biomphalaria glabrata. Parasitology 98:35–41PubMedGoogle Scholar
  126. Noda S, Loker ES (1989b) Phagocytic activity of hemocytes of M-line Biomphalaria glabrata snails: effect of exposure to the trematode Echinostoma paraensei. J Parasitol 75:261–269PubMedGoogle Scholar
  127. Nowak TS, Loker ES (2005) Echinostoma paraensei: differential gene transcription in the sporocyst stage. 109:94–105PubMedGoogle Scholar
  128. Ostrowski de Núñez M (1976) Sobre el ciclo biológico de Hippocrepis fuelleborni Travassos y Vogelsang 1930 (Trematoda, Notocotylidae). Physis, Sección B 35:125–130Google Scholar
  129. Ostrowski de Núñez M, Spatz L, González Cappa SM (2003) New intermediate hosts in the life cycle of Zygocotyle lunata in South America. J Parasitol 89:193–194PubMedGoogle Scholar
  130. Paul RE, Un VA, Krettli AU, Brey PT (2002) Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proc Biol Sci 269:2551–2557PubMedGoogle Scholar
  131. Pechenik JA, Fried B (1995) Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111:373–378Google Scholar
  132. Perez MK, Fried B, Sherma J (1994) High-performance thin-layer chromatographic analysis of sugars in Biomphalaria glabrata (Gastropoda) infected with Echinostoma caproni (Trematoda). J Parasitol 80:336–338PubMedGoogle Scholar
  133. Perez MK, Fried B, Sherma J (1995) Comparison of mobile phases HPTLC qualitative and quantitative analysis, on preadsorbent silica gel plates, of phospholipids in Biomphalaria glabrata (Gastropoda) infected with Echinostoma caproni (Trematoda). J Planar Chromatogr Mod TLC 7:340–343Google Scholar
  134. Petrie JL, Burg EF 3rd, Cain GD (1996) Molecular characterization of Echinostoma caproni and E. paraensei by random amplification of polymorphic DNA (RAPD) analysis. J Parasitol 82:360–362PubMedGoogle Scholar
  135. Platt TR, Burnside L, Bush E (2009) The role of light and gravity in the experimental transmission of Echinostoma caproni (Digenea: Echinostomatidae) cercariae to the second intermediate host, Biomphalaria glabrata (Gastropoda: Pulmonata). J Parasitol 95:512–516PubMedGoogle Scholar
  136. Pointier JP, Jourdane J (2000) Biological control of the snail hosts of schistosomiasis in areas of low transmission: the example of the Caribbean area. Acta Trop 77:53–60PubMedGoogle Scholar
  137. Ponder EL, Fried B, Sherma J (2004) Free-pool amino acids in Biomphalaria glabrata infecetd with Echinostoma caproni as determined by thin-layer chromatography. J Parasitol 90:665–666PubMedGoogle Scholar
  138. Reddy A, Fried B (1996) In vitro studies on intraspecific and interspecific chemical attraction in daughter rediae on Echinostoma trivolvis and E. caproni. Int J Parasitol 26:1081–1085PubMedGoogle Scholar
  139. Reddy A, Frazer BA, Fried B, Sherma J (1997) Chemoattraction of Echinostoma trivolvis (Trematoda) rediae to lipophilic excretory-secretory products and thin layer-chromatographic analysis of redial lipids. Parasite 4:37–40Google Scholar
  140. Reddy A, Ponder EL, Fried B (2004) Effects of copper sulfate toxicity on cercariae and metacercariae of Echinostoma caproni and Echinostoma trivolvis and on the survival of Biomphalaria glabrata snails. J Parasitol 90:1332–1337PubMedGoogle Scholar
  141. Richard J, Brygoo ER (1978) Life cycle of the trematode Echinostoma caproni Richard, 1964 (Echinostomatoidea). Ann Parasitol Hum Comp 53:265–275PubMedGoogle Scholar
  142. Riley EM, Chappell LH (1992) Effect of infection with Diplostomum spathaceum on the intestinal defense system of Lymnaea stagnalis. J Invertebr Pathol 59:190–196Google Scholar
  143. Sandland GJ, Rodgers JK, Minchella DJ (2007) Interspecific antagonism and virulence in hosts exposed to two parasite species. J Invertebr Pathol 96:43–47PubMedGoogle Scholar
  144. Schell SC (1985) Trematodes of North America, North of Mexico. University Press of Idaho, Moscow, Idaho, p 263Google Scholar
  145. Schmidt KA, Fried B, Haseeb MA (1998) Effect of Echinostoma caproni infection on survival, growth, and fecundity of Biomphalaria glabrata. J Helminthol Soc Wash 65:95–98Google Scholar
  146. Schneck JL, Fried B (2004) Effects of snail size on encystment of Echinostoma caproni in juvenile Biomphalaria glabrata (NMRI strain) and observations on survival of infected snails. J Helminthol 78:277–279PubMedGoogle Scholar
  147. Shetty PH, Fried B, Sherma J (1992) Effects of patent Echinostoma caproni infection on the sterol composition of the digestive gland-gonad complex of Biomphalaria glabrata as determined by gas-liquid chromatography. J Helminthol 66:68–71Google Scholar
  148. Sorensen RE, Curtis J, Minchella DJ (1998) Intraspecific variation in the rDNA ITS loci of 37-collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. J Parasitol 84:992–997PubMedGoogle Scholar
  149. Stein PC, Basch PF (1977) Metacercarial cyst formation in vitro of Echinostoma paraensei. J Parasitol 63:1031–1040PubMedGoogle Scholar
  150. 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
  151. Sullivan JJ (1985) Juvenile snails as hosts for echinostome metacercariae. Southeast Asian J Trop Med Public Health 16:343–344Google Scholar
  152. Sullivan JT (1988) Hematopoiesis in three species of gastropods following infection with Echinostoma paraensei (Trematoda: Echinostomatidae). Trans Am Microsc Soc 107:355–361Google Scholar
  153. Thornhill JA, Jones JT, Kusel JR (1986) Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni. Parasitology 93:443–450PubMedGoogle Scholar
  154. Ueta MT, Deberaldini ER, Da Silva N, De Toledo P (1981) Ciclo biológico de Paraibatrema inesperata n. g., n. sp. (Trematoda, Paramphistomidae) a partir de metacercárias desenvolvidas en Biomphalaria tenagophila (D’Orbigny, 1835) (Mollusca, Planorbidae). Mem Inst Oswaldo Cruz 76:15–21PubMedGoogle Scholar
  155. Van der Knaap WP, Loker ES (1990) Immune mechanisms in trematode-snail interactions. Parasitol Today 6:175–182PubMedGoogle Scholar
  156. Vergote D, Bouchut A, Sautière PE, Roger E, Galinier R, Rognon A, Coustau C, Salzet M, Mitta G (2005) Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 35:215–224PubMedGoogle Scholar
  157. Violante-González J, García-Varela M, Rojas-Herrera A, Gil Guerrero S (2009) Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitol Res 105:803–807PubMedGoogle Scholar
  158. Wagner SD, Kim Y, Fried B, Sherma J (2001) Thin-layer chromatographic analysis glucose, maltose, and raffinose in Biomphalaria glabrata (Gastropoda) infecetd with Echinostoma caproni (Trematoda). J Planar Chromatogr Mod TLC 14:459–461Google Scholar
  159. Walker AJ (2006) Do trematode parasites disrupt defence-cell signalling in their snail hosts? Trends Parasitol 22:154–159PubMedGoogle Scholar
  160. White MM, Chejlava M, Fried 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 95:252–255PubMedGoogle Scholar
  161. Yoshino TP, Vasta GR (1996) Parasite-invertebrate host immune interaction. In: Cooper EL (ed) Advances in comparative and environmental physiology, vol 24. Springer, Berlin, pp 125–167Google Scholar
  162. Yousif F, Haroun N (1986) Intramolluscan development of Echinostoma liei (Trematoda: Echinostomatidae) in its snail host Biomphalaria alexandrina. J Egypt Soc Parasitol 16:127–140PubMedGoogle Scholar
  163. Zakikhani M, Rau ME (1998) Effects of Plagiorchis elegans (Digenea: Plagiorchiidae) infection on the reproduction of Biomphalaria glabrata (Pulmonata: Planorbidae). J Parasitol 84:927–930PubMedGoogle Scholar
  164. Zakikhani M, Smith JM, Rau ME (2003) Effects of Plagiorchis elegans (Digenea: Plagiorchiidae) infection of Biomphalaria glabrata (Pulmonata: Planorbidae) on a challenge infection with Schistosoma mansoni (Digenea: Schistosomatidae). J Parasitol 89:70–75PubMedGoogle Scholar
  165. Zhang S-M, Loker ES (2003) The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Fibrinogen-related proteins. Dev Comp Immunol 27:175–187PubMedGoogle Scholar
  166. Zhang S-M, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305:251–254PubMedGoogle Scholar
  167. Zhang S-M, Léonard PM, Adema CM, Loker ES (2001) Parasite responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 53:684–694PubMedGoogle Scholar
  168. Zhang S-M, Nian H, Zeng Y, Dejon RJ (2008a) Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev Comp Immunol 32:1119–1130PubMedGoogle Scholar
  169. Zhang S-M, Zeng Y, Loker ES (2008b) Expression profiling and binding porperties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immunol 14:175–189Google Scholar

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© Springer Science+Business Media LLC 2011

Authors and Affiliations

  • Jose-Guillermo Esteban
  • Carla Muñoz-Antoli
  • Maria Trelis
  • Rafael Toledo
    • 1
  1. 1.Departamento de Biología Celular y Parasitología, Facultad de FarmaciaUniversidad de ValenciaValenciaSpain

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