Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Acta Parasitologica

4 Issues per year

IMPACT FACTOR 2016: 1.160
5-year IMPACT FACTOR: 1.185

CiteScore 2016: 1.24

SCImago Journal Rank (SJR) 2016: 0.532
Source Normalized Impact per Paper (SNIP) 2016: 0.721

See all formats and pricing
More options …
Volume 60, Issue 1


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

Elena A. Serbina
  • Institute of Systematics and Ecology of Animals SB RAS. 11, Frunze St., Novosibirsk, 630091, Russia
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2014-12-30 | DOI: https://doi.org/10.1515/ap-2015-0006


We studied the long-term infection of 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 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.

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


  • 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.2010.01.012CrossrefWeb of ScienceGoogle Scholar

  • Baudoin M. 1975. Host castration as a parasitic strategy. Evolution 29, 335-352Google Scholar

  • Calvo-Ugarteburu G., McQuaid C.D. 1998. Parasitism and invasive species: effects of digenetic trematodes on mussels. Marine Ecology Progress Series, 169, 149-163Google Scholar

  • 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)90200-0 | CrossrefGoogle Scholar

  • 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, 109-117Google Scholar

  • 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

  • Ginecinskaya T.A. 1968. Trematodes, their life cycles, biology and evolution. Leningrad: Nauka 412 pp.Google Scholar

  • Gutierrez A., Perera G., Yong M., Sanchez J., Wong L. 2000. Lifehistory 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

  • 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

  • Hay K.B., Fredensborg B.L., Poulin R. 2005. Trematode-induced alterations in shell shape of the mud snail Zeacumantus sub carinatus (Prosobranchia: Batillariidae). Journal of the Marine Biological Association of the United Kingdom, 85, 989-992Google Scholar

  • 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, 268-271Google Scholar

  • 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/s00436-009-1572-0CrossrefWeb of ScienceGoogle Scholar

  • Кarpenko S.V., Chechulin А.I., Yurlova N.I., Serbina E.A., Vodyanitskaya S.N., Кrivopalov А.V., Fedorov К.P. 2008. Characteristic of Opisthorchosis foci in the Southern of West Siberia. Contemporary Problems of Ecology, 1, 517-521. DOI: 10. 1134/S1995425508050019CrossrefGoogle Scholar

  • 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. http://www.zin.ru/journals/parazitologiya/a2003-1/abstr2003-1-Kaliberdina.htm Google Scholar

  • 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

  • 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

  • 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

  • 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-2080.1CrossrefWeb of ScienceGoogle Scholar

  • 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, 229-237Google Scholar

  • 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.2007.04.022CrossrefWeb of ScienceGoogle Scholar

  • 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

  • Loker E.S. 1979. Effects of Schistosomatium douthitti infection on the growth, survival, and reproduction of Lymnaea catascopium Journal of Invertebrate Pathology, 34, 138-144Google Scholar

  • 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

  • Munoz-Antoli C., Marin А., 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/s00436-007-0710-9CrossrefWeb of ScienceGoogle Scholar

  • 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. http://www.zin.ru/journals/parazitologiya/a1999-1/abstr1999-1-Panova.htm Google Scholar

  • 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.x Web of ScienceCrossrefGoogle Scholar

  • 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

  • Reader T.A.J. 1971. The pathological effects of sporocysts, rediae and metacercariae on the digestive gland of Bithynia tentaculata (Mollusca: Gastropoda). Parasitology, 63, 483-489Google Scholar

  • 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-x CrossrefGoogle Scholar

  • 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

  • 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

  • Serbina E.A. 2006. Prevalence of Trematodas Family Psilostomatidae Odhner, 1913 in the South of West Siberia. Sibirskiy Ekologicheskiy Zhurnal, 13, 409-418Google Scholar

  • Serbina E.A. 2008a. The Methods of Determination for Gastropoda Age. Biologicheskie Nauki Kazakhstana, 1, 43-52Google Scholar

  • 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) http://www.zin.ru/journals/parazitologiya/content/2008/prz_2008_1_6_Serbina.pdf Google Scholar

  • 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/ S1995425510010054CrossrefWeb of ScienceGoogle Scholar

  • 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

  • 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/S19954255 13010150CrossrefWeb of ScienceGoogle Scholar

  • Serbina E.A. 2014. The influence of trematode metacercariae on the individual fecundity of Bithynia troscheli (Gastropoda: Bithyniidae). Parazitologiya, 48, 3-19Google Scholar

  • 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) http://www.vniigis.ru/assets/files/RPG/2011_4.pdf Google Scholar

  • 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

  • Shinagawa K., Urabe M., Nagoshi M. 2001. Effects of trematode infection on metabolism and activity in a freshwater snail, Semi sulcospira libertina. Diseases of Aquatic Organisms, 45, 141-144. PMID: 11463101 INIST-CNRS, Cote INIST: 21304, 35400009557860.0080Google Scholar

  • Sorensen R.E., Minchella D.J. 1998. Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails Oecologia, 115, 188-195. http://www.jstor.org/stable/4221995Google Scholar

  • 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

  • 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

  • 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/s11686-010-0024-4Web of ScienceGoogle Scholar

  • 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, 109-119Google Scholar

  • 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

  • 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, 707-708 Google Scholar

About the article

Received: 2014-04-22

Revised: 2014-07-19

Accepted: 2014-08-29

Published Online: 2014-12-30

Published in Print: 2014-03-01

Citation Information: Acta Parasitologica, Volume 60, Issue 1, Pages 40–49, ISSN (Online) 1896-1851, DOI: https://doi.org/10.1515/ap-2015-0006.

Export Citation

© 2015. Copyright Clearance Center

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Comments (0)

Please log in or register to comment.
Log in