Acta Parasitologica

, Volume 60, Issue 1, pp 40–49 | Cite as

The effect of trematode parthenites on the individual fecundity of Bithynia troscheli (Prosobranchia: Bithyniidae)

  • Elena A. SerbinaEmail author


We studied the long-term infection of the Bithynia troscheli (Paasch, 1842) snails with trematodes and estimated the influence of trematode parthenites on the individual fecundity of female snails from the Kargat River (Chany Lake, Russia). The prevalence of B. troscheli females infected by trematode parthenites varied from 7.12% to 17.35% in different years. Eleven redioid species from 5 families and 9 sporocystoid species from 5 families of trematodes were found during this investigation. Snails’ fecundity was analysed in relation to the type of infection (redioid or sporocystoid species). Fecund females of B. troscheli were uninfected or they had pre-patent infections from 5 families of trematodes (Psilostomidae, Notocotylidae, Prosthogonimidae, Lecithodendriidae, and Cyathocotylidae). 89.9% of infected B. troscheli females were infertile. Moreover, 13.57% and 1.29% egg capsules (of infected and uninfected females, respectively) were without embryos (χ2 = 323.24, p<0.001). The results of the two-way analysis of variability confirmed that trematode parthenites influenced significantly on the individual fecundity of B. troscheli. The age of B. troscheli females alone did not alter the individual fecundity, however age in combination with infection by tremathode parthenites influenced significantly the number of normal egg capsules. We also found that under unfavorable environmental conditions the proportion of fertile females increased by 23.7% among uninfected and by 219% among infected females.


Host-parasite system trematode parthenites redioid and sporocystoid species parasitic castration Gastropoda Bithyniidae Western Siberia 


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  1. Alda P., Bonel N., Cazzaniga N.J., Martorelli S.R. 2010. Effects of parasitism and environment on shell size of the South American intertidal mud snail Heleobia australis (Gastropoda). Estuarine, Coastal and Shelf Science 87, 305–310. doi:10.1016/j.ecss.2010.01.012CrossRefGoogle Scholar
  2. Baudoin M. 1975. Host castration as a parasitic strategy. Evolution 29, 335–352CrossRefGoogle Scholar
  3. Calvo-Ugarteburu G., McQuaid C.D. 1998. Parasitism and invasive species: effects of digenetic trematodes on mussels. Marine Ecology Progress Series, 169, 149–163CrossRefGoogle Scholar
  4. Cheng T.C., Sullivan J.T., Harris K.R. 1973. Parasitic castration of the marine prosobranch gastropod Nassarius obsoletus by the sporocyst of Zoogonus rubellus (Trematoda): histopathology. Journal of Invertebrate Pathology, 21, 183–190. DOI: 10.1016/0022-2011(73)90200-0CrossRefGoogle Scholar
  5. Fredensborg B.L., Mouritsen K.N., Poulin R. 2005. Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series, 290, 109–117CrossRefGoogle Scholar
  6. Galaktionov K.V., Dobrovolskij A.A. 2003. The Biology and Evolution of Trematodes. An Essay on the Biology, Morphology, Life Cycles, Transmission, and Evolution of Digenetic Trematodes. Boston, Dordrecht, London: Kluwer Academic Publ. 592 pp.Google Scholar
  7. Ginecinskaya T.A. 1968. Trematodes, their life cycles, biology and evolution. Leningrad: Nauka 412 pp.Google Scholar
  8. Ginecinskaya T.A. 1968. Trematodes, their life cycles, biology and evolution. Leningrad: Nauka 412 pp. (In Russian).Google Scholar
  9. Gutierrez A., Perera G., Yong M., Sanchez J., Wong L. 2000. Life-history Traits of Fossaria cubensis (Gastropoda: Lymnaeidae) under Experimental Exposure to Fasciola hepatica (Trematoda: Digenea). Memórias do Instituto Oswaldo Cruz, 95, 747–752. DOI: 10.1590/S0074-02762000000500025 ISSN: 1678-8060 PMID: 10998229CrossRefGoogle Scholar
  10. Hassanine R.M.E.-S. 2006. The life cycle of Diploproctodaeum arothroni Bray and Nahhas, 1998 (Digenea: Lepocreadiidae), with a comment on the parasitic castration of its molluscan intermediate host. Journal of Natural History, 40, 1211–1222. DOI: 10.1080/02678290600883767CrossRefGoogle Scholar
  11. Hay K.B., Fredensborg B.L., Poulin R. 2005. Trematode-induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association of the United Kingdom, 85, 989–992CrossRefGoogle Scholar
  12. Hordijk P.L., van Loenhout H., Ebberink R.H.M., de Jong-Brink M., Joosse J. 1991. Neuropeptide schistosomin inhibits hormonally-induced ovulation in the freshwater snail Lymnaea stagnalis. Journal of Experimental Zoology, 259, 268–271CrossRefGoogle Scholar
  13. Huffman J.E., Klockars J., Keeler S.P., Fried B. 2009. Histopathological effects of the intramolluscan stages of Zygocotyle lunata, Echinostoma trivolvis and Ribeiroia ondatrae on Helisoma trivolvis and observations on keratin in the trematode larvae. Parasitology, 105, 1385–1389. DOI 10.1007/s00436-009-1572-0CrossRefGoogle Scholar
  14. Karpenko S.V., Chechulin A.I., Yurlova N.I., Serbina E.A., Vodyanitskaya S.N., Krivopalov K.V., Fedorov K.P. 2008. Characteristic of Opisthorchosis foci in the Southern of West Siberia. Contemporary Problems of Ecology, 1, 517–521. DOI: 10.1134/S1995425508050019CrossRefGoogle Scholar
  15. Kaliberdina M.V., Granovitch A.I. 2003. Infection of the mollusc Littorina saxatilis with parthenites of trematodes and their impact onto a shell form: analysis of populations inhabiting the littoral shore of the White sea. Parazitologiya, 1, 69–86. Scholar
  16. Kozminsky E.V. 2003. Growth, demographic structure of population and determination of Bithynia tentaculata (Gastropoda, Prosobranchia) age. Zoologicheskiy Zhurnal. 82, 567–576. ISSN: 0044-5134Google Scholar
  17. Kozminsky E.V. 2012. Effect of infection by trematodes on the fertility of Bithynia tentaculata (Gastropoda: Bithyniidae). Biologicheskie Nauki Kazakhstana, 4, 96–104. (In Russian)Google Scholar
  18. Kube S., Kube J., Bick A. 2006. A loss of fecundity in a population of mudsnails Hydrobia ventrosa caused by larval trematodes does not measurably affect host population equilibrium level. Parasitology, 132, 725–732. DOI: 10.1017/S0031182005009704CrossRefGoogle Scholar
  19. Kumkate S., Onmek N., Boonburapong B., Singhakaew S., Leardkamolkarn V. 2009. Estrogen-Related Fecundity Reduction of Lymnaea ollula Following Fasciola gigantica Infection. Journal of Parasitology, 95, 1391–1396. DOI: 10.1645/GE-2080.1CrossRefGoogle Scholar
  20. Lafferty K.D. 1993. Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Marine Ecology Progress Series, 96, 229–237CrossRefGoogle Scholar
  21. Lagrue C., McEwan J., Poulin R., Keeney D.B. 2007. Cooccurrences of parasite clones and altered host phenotype in a snail trematode system. International Journal for Parasitology, 37, 1459–1467. DOI:10.1016/j.ijpara.2007.04.022CrossRefGoogle Scholar
  22. Levri E.P., Dillard J., Martin T. 2005. Trematode infection correlates with shell shape and defence morphology in a freshwater snail Parasitology, 130, 699–708. DOI:10.1017/S0031182005007286CrossRefGoogle Scholar
  23. Loker E.S. 1979. Effects of Schistosomatium douthitti infection on the growth, survival, and reproduction of Lymnaea catascopium Journal of Invertebrate Pathology, 34, 138–144CrossRefGoogle Scholar
  24. McCarthy H.O., Fitzpatrick S.M., Irwin S.W.B. 2004. Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages. Parasitology, 128, 7–14. DOI: 10.1017/S0031182003004190CrossRefGoogle Scholar
  25. Muñoz-Antoli C., Marín A., Toledo R., Esteban J-G. 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. Parasitology Research, 101, 1663–1670. DOI: 10.1007/s00436-007-0710-9CrossRefGoogle Scholar
  26. Panova M.V., Sergievsky S.O., Granovitch A.I. 1999. Abnormal shell shape of the intertidal molluscs Littorina saxatilis and Littorina obtusata infected with trematodes. Parazitologiya, 33, 13–25. Scholar
  27. Paull S.H., Johnson P.T.J. 2011. High temperature enhances host pathology in a snail-trematode system: possible consequences of climate change for the emergence of disease. Freshwater Biology, 56, 767–778. DOI:10.1111/j.1365-2427.2010.02547.xCrossRefGoogle Scholar
  28. Probst S., Kube J. 1999. Histopathological effects of larval trematode infections in mudsnails and their impact on host growth: what causes gigantism in Hydrobia ventrosa (Gastropoda: Prosobranchia)? Journal of Experimental Marine Biology and Ecology, 238, 49–68. DOI:10.1016/S0022-0981(99)00002-7CrossRefGoogle Scholar
  29. Reader T.A.J. 1971. The pathological effects of sporocysts, rediae and metacercariae on the digestive gland of Bithynia tentaculata (Mollusca: Gastropoda). Parasitology, 63, 483–489CrossRefGoogle Scholar
  30. Sandland G.J., Minchella D.J. 2003. Effects of diet and Echinostoma revolutum infection on energy Allocation patterns in juvenile Lymnaea elodes snails. Oecologia, 134, 479–486. DOI: 10.1007/s00442-002-1127-xCrossRefGoogle Scholar
  31. Serbina E.A. 2002. Bithyniidae Snails in Water Bodies in the South of West Siberia and Their Role in the Life Cycle of Trematodes. PhD (Novosibirsk) 162 pp.Google Scholar
  32. Serbina E.A. 2005. Reproduction of Bithyniidae Snails (Mollusca: Gastropoda: Prosobranchia) from Chany Lake Basin (South of Western Siberia), Sibirskii Ekologicheskii Zhurnal, 2, 267–278Google Scholar
  33. Serbina E.A. 2006. Prevalence of Trematodas Family Psilostomatidae Odhner, 1913 in the South of West Siberia. Sibirskiy Ekologicheskiy Zhurnal, 13, 409–418Google Scholar
  34. Serbina E.A. 2008a. The Methods of Determination for Gastropoda Age. Biologicheskie Nauki Kazakhstana, 1, 43–52Google Scholar
  35. Serbina E.A. 2008b. Characteristics of the seasonal development of Schistogonimus rarus (Trematoda: Prosthogonimidae). An essay on quantitative estimation of the trematode in the ecosystem of the Malye Chany Lakes (south of Western Siberia). Parazitologiya, 42, 53–65. (In Russian) Scholar
  36. Serbina E.A. 2010a. Shell as an Indicator of the Growth Rate of Freshwater Gastropods of the Family Bithyniidae. Contemporary Problems of Ecology, 3, 19–27. DOI: 10.1134/S1995425510010054CrossRefGoogle Scholar
  37. Serbina E.A. 2010b. Coevolution of the Host — Parasite systems (Bithyniidae-Trematode). Biodiversity and Ecology of Parasites. [Editor-in-Chief: S.A. Be’er,]. Transactions of Center for Parasitology Nauka, Moscow, 46, 239–259Google Scholar
  38. Serbina E.A. 2013. A Quantitative Estimation of the Role of Bithyniidae Snails (Gastropoda: Prosobranchia) in the Ecosystems of the Southern Part of Western Siberia (Russia) Contemporary Problems of Ecology, 6, 28–33. DOI: 10.1134/S1995425513010150CrossRefGoogle Scholar
  39. Serbina E.A. 2014. The influence of trematode metacercariae on the individual fecundity of Bithynia troscheli (Gastropoda: Bithyniidae). Parazitologiya, 48, 3–19Google Scholar
  40. Serbina E.A., Bonina O.M. 2011. Revealing local nidi of opisthorchidoses in flood-lands of river Ob and in Novosibirsk manmade lake. Message 2. Prosobranchia mollusca’s number and infection of their by parteniters of trematoda. Russian parazitologiya zhurnal, 4, 55–59. (In Russian) Scholar
  41. Serbina E.A., Yurlova N.I. 2002. Involvement of Codiella troscheli (Mollusca Prosobranchia) in the life cycle of Metorchis albidus (Trematoda: Opisthorchidae). Meditsinskaya Parazitologiya i Parazitarnye Bolezni, 3, 21–23Google Scholar
  42. Shinagawa K., Urabe M., Nagoshi M. 2001. Effects of trematode infection on metabolism and activity in a freshwater snail, Semisulcospira libertina. Diseases of Aquatic Organisms, 45, 141–144. PMID: 11463101 INIST-CNRS, Cote INIST: 21304, 35400009557860.0080CrossRefGoogle Scholar
  43. Sorensen R.E., Minchella D.J. 1998. Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails Oecologia, 115, 188–195. Scholar
  44. Sorensen R.E., Minchella D.J. 2001. Snail-trematode life history interactions: past trends and future directions. Parasitology, 123, 3–18. DOI 10.1017/S0031182001007843CrossRefGoogle Scholar
  45. Sudarikov V.E., Shigin A.A., Kurochkin Yu.V., Lomakin V.V., Stenko R.P. Yurlova N.I. 2002. Metacercariae of trematodes parasites of freshwater hydrobionts in Central Russia. Nauka, Moscow 298 pp.Google Scholar
  46. Tolstenkov O.O., Terenina N.B., Serbina E.A., Gustafsson M.K.S. 2010. The spatial relationship between the musculature and the 5-HT and FMRFamide immunoreactivities in cercaria, metacercaria and adult Opisthorchis felineus (Digenea). Acta Parasitologica, 55, 123–132. DOI: 10.2478/s11686-010-0024-4CrossRefGoogle Scholar
  47. Wilson R.A., Denison J. 1980. The parasitic castration and gigantism of Lymnaea truncatula infected with the larval of Fasciola hepatica. Zeitschrift Fur Parasitenkunde, Berlin, Germany. 61, 109–119CrossRefGoogle Scholar
  48. Zhokhov A.E., Pugacheva M.N. 1995. Effects of the trematode infestation on the reproductive function of the clam Pisidium amnicum (Bivalvia, Pisidae): organism and population levels. Russian Journal of Ecology, 26, 112–116Google Scholar
  49. Zischke J.A., Zischke D.P. 1965 The effects of Echinostoma revolutum larval infection on the growth and reproduction of the snail host Stagnicola palustris. American Zoologist, 5, 707–708Google Scholar

Copyright information

© W. Stefański Institute of Parasitology, PAS 2015

Authors and Affiliations

  1. 1.Institute of Systematics and Ecology of Animals SB RAS. 11NovosibirskRussia

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