Skip to main content
SpringerLink
Log in

Differences in snail ecology lead to infection pattern variation of Echinostoma spp. larval stages

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

The infection patterns of parasites are often tied to host behavior. Although most studies have investigated definitive hosts and their parasites, intermediate host behavior may play a role in shaping the distribution and accumulation of parasites, particularly the larval stages. In an attempt to answer this question, more than 4,500 pulmonate snails were collected from 11 states in the mid-Atlantic and Midwestern United States in the summer of 2012. These snails were necropsied and echinostome metecercariae were commonly observed infecting the snails as 2nd intermediate hosts (20.0%). The snails included species of 3 genera with distinct differences in the infection patterns of Echinostoma spp. metacercariae among them. Physa spp. (comprising of P. acuta and P. gyrina) snails exhibited a significantly higher prevalence of infection (23.5%) than both Lymnaea columella (11.6%) and Helisoma spp. (comprising of H. anceps and H. trivolvis) (14.2%; P < 0.05), with no difference in prevalence observed between the latter 2 genera (P > 0.05). The intensity of metacercariae within the snail hosts was significantly different between the 3 genera (P < 0.05), with L. columella having the highest intensity (24.3 ± 5.6), followed by Physa spp. (15.2 ± 1.5) and Helisoma spp. (5.0 ± 0.9). Differences in prevalence and intensity were also observed when the different snail families co-habited the same body of water. The disparities in infection patterns are likely due to distinct differences in the behavioral and feeding ecology of the snail hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bickel D. 1965. The role of aquatic plants and submerged structures in the ecology of a freshwater pulmonate snail, Physa integra Hald. Sterkiana, 18, 17–20.

    Google Scholar 

  • Boss C.N., Laman T.G., Blankespoor H.D. 1984. Dispersal movements of four species of pulmonate and operculate snails in Douglas Lake, Michigan. The Nautilus, 98, 80–83.

    Google Scholar 

  • Bovbjerg R. 1965. Feeding and dispersal in the snail Stagnicola reflexa (Basommatophora: Lymnaeidae). Malacologia, 2, 199–207.

    Google Scholar 

  • Bovbjerg R. 1968. Responses to food in lymnaeid snails. Physiological Zoology, 41, 412–423.

    Google Scholar 

  • Bovbjer R. 1975. Dispersal and dispersion of pond snails in an experimental environment varying to three factors, singly and in combination. Physiological Zoology, 48, 203–215.

    Google Scholar 

  • Bush A.O., Lafferty K.D., Lotz J.M, Schostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 573–583.

    Article  Google Scholar 

  • Calow P. 1973. Field observations and laboratory experiments on the general food requirements of two species of freshwater snail, Planorbis contortus and Ancylus fluviatilis. Proceedings of the Malacological Society of London, 40, 483–490.

    Google Scholar 

  • Calow P. 1974. Evidence for bacterial feeding in Planorbis contortus L. (Gastropoda: Pulmonata). Proceedings of the Malacological Society of London, 20, 33–49.

    Google Scholar 

  • Calow P. 1975. The feeding strategies of two freshwater gastropods, Ancylus fluviatilis and Planorbis contortus L. in terms of ingestion rates and absorption efficiencies. Oecologia, 20, 33–49. DOI: 10.1007/BF00364320.

    Article  Google Scholar 

  • Charnov E., Orians G., Hyatt K. 1976. Ecological implications of resource depression. American Naturalist, 110, 247–259.

    Article  Google Scholar 

  • Clampitt P.T. 1970. Comparative ecology of the snails Physa gyrina and Physa integra. Malacologia, 10, 113–151.

    Google Scholar 

  • Clampitt P.T. 1975. How fast is a snail’s pace? Active and passive dispersal of Physa integra in Douglas Lake, Michigan. Malacological Review, 8, 121.

    Google Scholar 

  • Crowl T, Schnell G. 1990. Factors determining population-density and size distribution of a fresh-water snail in streams — Effects of spatial scale. Oikos, 59, 359–367.

    Article  Google Scholar 

  • Cuker B. 1983. Competition and coexistence among the grazing snail Lymnaea, Chironomidae, and microcrustacea in an arctic epilithic lacustrine community. Ecology, 64, 10–15.

    Article  Google Scholar 

  • Detwiler J.T. 2010. The molecular ecology of echinostome trematodes: Elucidating the phylogenetics and transmission dynamics of a freshwater helminth parasite. Ph.D. Dissertation. Purdue University, West Lafayette, Indiana.

    Google Scholar 

  • Detwiler J.T, Minchella D.J. 2009. Intermediate host availability masks the strength of experimentally-driven colonization patterns in echinostome trematodes. International Journal for Parasitology, 39, 585–590. DOI: 10.1016/j.ijpara.2008.10.008.

    Article  PubMed  Google Scholar 

  • Detwiler J.T., Zajac A.M., Minchella D.J., Belden, L.K. 2012. Revealing cryptic parasite diversity in a definitive host: Echinostomes in muskrats. Journal of Parasitology 98: 1148–1155. DOI: 10.1645/GE-3117.1.

    Article  PubMed  Google Scholar 

  • Dillon R.T. 2000. The ecology of freshwater molluscs. Cambridge University Press, Cambridge, UK, 524 pp.

    Book  Google Scholar 

  • Esteban J. C., Munoz-Antoli C. 2009. Echinostomes: Systematics and life cycles. In: (Eds. B.R. Fried, R. Toledo), The biology of echinostomes: From the molecule to the community, Springer, LLC, New York, 1–34.

    Chapter  Google Scholar 

  • Ezenwa A. 2004. Host social behaviour and parasitic infection: A multifactorial approach. Behavioral Ecology, 15, 446–454. DOI: 10.1093/beheco/arh028.

    Article  Google Scholar 

  • Freeland W. 1976. Pathogens and evolution of primate sociality. Biotropica, 8, 12–24.

    Article  Google Scholar 

  • Foster G. 1973. Soil type and habitat of the aquatic snail Lymnaea (Galba) bulinoides Lea during the dry season. Basteria, 37, 41–46.

    Google Scholar 

  • Fried B., Peoples R.C., Saxton T.M., Huffman J.E. 2008. The association of Zygocotyle lunata and Echinostoma trivolvis with Chaetogaster limnaei limnaei, an ectosymbiont of Helisoma trivolvis. Journal of Parasitology, 94, 553–554. DOI: 10.1645/GE-1388.1

    Article  PubMed  Google Scholar 

  • Griggs J.L., Belden L.K. 2008. Effects of atrazine and metolachlor on the survivorship and infectivity of Echinostoma trivolvis trematode cercariae. Archives of Environmental Contamination and Toxicology, 54, 195–202. DOI: 10.1007/s00244-007-9029-x

    Article  CAS  PubMed  Google Scholar 

  • Hall S.R., Becker C.R., Simonis, J.L., Duffy M.A., Tessier A.J., Caceres C.E.. 2009. Friendly competition: Evidence for a dilution effect among competitors in a planktonic host-parasite system. Ecology, 90, 791–801. DOI: 10.1890/08-0838.1.

    Article  PubMed  Google Scholar 

  • Harris R.E., Charleston A.G. 1977. An examination of the marsh microhabitats of Lymnaea tomentosa and L. columella (Mollusca: Gastropoda) by path analysis. New Zealand Journal of Zoology, 4, 395–399. DOI: 10.1080/03014223.1977.9517964.

    Article  Google Scholar 

  • Hunter R. 1980. Effects of grazing on the quantity and density of freshwater aufwuchs. Hydrobiologia, 69, 251–259. DOI: 10.1007/BF00046800.

    Article  Google Scholar 

  • Johnson P.T.J., McKenzie V.J. 2009. Effects of environmental change on helminth infections in amphibians: Exploring the emergence of Ribeiroia and Echinostoma infections in North America. In: (Eds. B.R. Fried, R. Toledo R.) The biology of echinostomes: From the molecule to the community, Springer, LLC, New York, 249–280.

    Chapter  Google Scholar 

  • Johnson P.T.J., Thieltges D.W. 2010. Diversity, decoys and the dilution effect: How ecological communities affect disease risk. The Journal of Experimental Biology, 213, 961–970. DOI: 10.1242/jeb.037721.

    Article  CAS  PubMed  Google Scholar 

  • Liang Y. 1974. Cultivation of Bulinus (Physopsis) globosus and Biomphalaria pfeifferi pfeifferi, snail hosts of schistosomiasis. Sterkiana, 53–54, 1–75.

    Google Scholar 

  • Loehle C. 1995. Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–335.

    Article  Google Scholar 

  • Lowe R.L., Hunter R.D. 1988. Effect of grazing by Physa integra on periphyton community structure. Journal of the North American Benthological Society, 7, 29–36.

    Article  Google Scholar 

  • Loys R.E., van Oosterhout C., Cable J. 2010. Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS One, 10, e13285. DOI: 10.1371/journal.pone.0013285.

    Google Scholar 

  • Malek E. 1958. Factors conditioning the habitat of bilharziasis intermediate hosts of the family Planoribidae. Bulletin of the World Heath Organization 18: 785–818.

    Google Scholar 

  • Moller A., Dufva R., Allander K. 1993. Parasites and the evolution of host social behavior. Advances in the Study of Behavior, 22, 65–102.

    Article  Google Scholar 

  • Morely N.J., Lewis J.W., Adam, M.E. 2004. Metacercarial utilization of a naturally infected single species (Lymnaea peregra) snail community by Echinoparyphium recurvatum. Journal of Helminthology, 78, 51–56. DOI: 10.1079/JOH2003201.

    Article  Google Scholar 

  • Morgan J.A.T., Blair D. 1995. Nuclear rDNA ITS sequenc variation in the trematode genus Echinostoma: An aid to establishing relationships within the 37-collar-spine group. Parasitology, 111, 609–615. DOI: 10.1017/S003118200007709X.

    Article  CAS  PubMed  Google Scholar 

  • Reavell P. 1980. A study of the diets of some British freshwater gastropods. Journal of Conchology, 30, 253–271.

    Google Scholar 

  • Sapp K.K., Esch G.W. 1994. The effects of spatial and temporal heterogeneity as structuring forces for parasite communities in Helisoma anceps and Physa gyrina. American Midland Naturalist, 132, 91–103. DOI: 10.2307/2426204.

    Article  Google Scholar 

  • Schmidt K.A., Fried B.F. 1997. Prevalence of larval trematodes in Helisoma trivolvis (Gastropoda) from a farm pond in Northampton County, Pennsylvania with special emphasis on Echinostoma trivolvis (Trematoda) cercariae. Journal of the Helminological Society of Washington, 64, 157–159.

    Google Scholar 

  • Sheldon S.P. 1987. The effects of herbivorous snails on submerged communities in Minnesota lakes. Ecology, 68, 1920–1931.

    Article  Google Scholar 

  • Storey R. 1970. The importance of mineral particles in the diet of Limnaea pereger (Muller). Journal of Conchology, 27, 191–195.

    Google Scholar 

  • Swamikannu X., Hoagland K. 1989. Effects of snail grazing on the diversity and structure of a periphyton community in a eutrophic pond. Canadian Journal of Aquatic Science, 46, 1698–1704. DOI: 10.1139/f89-215.

    Article  Google Scholar 

  • Walter J. 1980. The density of the pond snails Lymnaea auricularia and L. peregra in Lake Zurich (Gastropoda: Basommatophora). Schweizerische Zeitschrift fur Hydrologie, 42, 65–71.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Wake Forest University, 1834 Gulley Dr., Winston-Salem, North Carolina, 27106, USA

    Michael R. Zimmermann, Kyle E. Luth & Gerald W. Esch

Authors
  1. Michael R. Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kyle E. Luth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gerald W. Esch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael R. Zimmermann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zimmermann, M.R., Luth, K.E. & Esch, G.W. Differences in snail ecology lead to infection pattern variation of Echinostoma spp. larval stages. Acta Parasit. 59, 502–509 (2014). https://doi.org/10.2478/s11686-014-0275-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-014-0275-6

Keywords

Search

Navigation