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Licensed Unlicensed Requires Authentication Published by De Gruyter October 22, 2016

Tranmission pattern differences of miracidia and cercariae larval stages of digenetic trematode parasites

Michael R. Zimmermann EMAIL logo , Kyle E. Luth and Gerald W. Esch
From the journal Acta Parasitologica


Digenetic trematodes have complex life cycles involving multiple hosts and free-living larval stages. Some species have 2 lar-val stages that infect snails, with miracidia and cercariae using these molluscs as first and second intermediate hosts, respec-tively. Although both larval stages may infect the same snail species, this is accomplished using different chemical cues and may be influenced by different biotic and abiotic factors. Significant differences in the infection patterns of these parasitic stages regarding host size and density were observed in 2 separate field studies. The prevalence of sporocysts/rediae and mean abundance of Echinostoma spp. metacercariae infection were positively correlated with host size, while the prevalence of Echinostoma spp. cercariae infection was positively correlated with host density across 5 different pulmonate snail species. Larger snails within a given species tend to be older and the increased exposure time may be responsible for the positive correlations with host size. Additionally, infection by miracidia in more vagile snail hosts was influenced by trematode species richness at a sample site, which may be attributed to increased encounter rate as a result of increased movement by the snail hosts. Echinostoma spp. metacercariae prevalence was influenced by host density, possibly due to high abundances of larval clones and their response to more generalized chemical cues attributed to low host specificity by cercariae. Although they can infect the same gastropod hosts, miracidia and cercariae infection are dependent on different factors at both the individual and population level of their snail hosts.


We want to acknowledge the Grady Britt Parasitology Fund and the Vecellio Grant at Wake Forest University for financial support of the research.


Anderson R.M., Mercer J.G., Wilson R.A., Carter N.P. 1982. Trans-mission of Schistosoma mansoni from man to snail: Experimental studies of miracidial survival and infectivity in relation to larval age, water temperature, host size and host age. Par-asitology, 85, 339–360. 10.1017/S0031182000055323Search in Google Scholar

Boss C.N., Laman T.G., Blankespoor H.D. 1984. Dispersal move-ments of four species of pulmonate and operculate snails in Douglas Lake, Michigan. The Nautilus, 98, 80–83Search in Google Scholar

Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitol-ogy meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. 10.2307/3284227Search in Google Scholar

Byers J.E., Blakeslee A.M.H., Linder E., Cooper A.B., Maguire T.J. 2008. Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology, 89, 439–451. 10.1890/06-1036.1Search in Google Scholar PubMed

Campbell R.A. 1997. Host-finding behavior of Cotylurus flabelliformis (Trematoda: Strigeidae) cercariae for snail hosts. Folia Parasitologica, 44, 199–204Search in Google Scholar

Carter N.P., Anderson R.M., Wilson R.A. 1982. Transmission of Schistosoma mansoni from man to snail: Laboratory studies on the influence of snail and miracidial densities on trans-mission success. Parasitology, 85, 361–372. 10.1017/ S0031182000055335Search in Google Scholar

Charnov E., Orians G., Hyatt K. 1976. Ecological implications of re-source depression. American Naturalist, 110, 247–25910.1086/283062Search in Google Scholar

Criscione C.D., Blouin M.S. 2007. Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution, 60, 553–562. 10.1111/j.0014-3820.2006.tb01136.xSearch in Google Scholar

Detwiler J.T., Minchella D.J. 2009. Intermediate host availability masks the strength of experimentally-derived colonisation patterns in echinostome trematodes. International Journal for Parasitology, 39, 585–590. 10.1016/j.ijpara.2008.10.008Search in Google Scholar PubMed

Detwiler J.T. 2010. The molecular ecology of echinostome trema-todes: Elucidating the phylogenetics and transmission dynamics of a freshwater helminth parasite. Ph.D. Thesis, Purdue University, West Lafayette, Indiana, USASearch in Google Scholar

Dillon R.T. 2000. Gastropod autoecology. In: Dillon R. T. (Ed.). The ecology of freshwater molluscs, Cambridge University Press, Cambridge, UK, pp. 57–11610.1017/CBO9780511542008.004Search in Google Scholar

Esch G.W., Fernandez J.C. 1994. Snail-trematode interactions and parasite community dynamics in aquatic systems: A review. The American Midland Naturalist, 131, 209–237. 10.2307/2426248Search in Google Scholar

Esch G.W., Barger M.A., Fellis K.J. 2002. The transmission of digenetic trematodes: Style, elegance, complexity. Integrative Comparative Biology, 42, 304–312. 10.1093/icb/42.2.304Search in Google Scholar PubMed

Esteban J.C., Munoz-Antoli C. 2009. Echinostomes: Systematics and life cycles. In: Fried B.R., and Toledo R. (Eds.) The biology of echinostomes: From the molecule to the community, Springer, LLC, New York, New York, pp. 1–3410.1007/978-0-387-09577-6_1Search in Google Scholar

Evans N.A., Whitfield P.J., Dobson A.P. 1981. Parasite utilization of a host community: The distribution and occurrence of metacercarial cysts of Echinoparyphium recurvatum (Digenea: Echinostomatidae) in seven species of molluscs at Harting Pond, Sussex. Parasitology, 83, 1–12. 10.1017/S0031182000049982Search in Google Scholar

Faltynkova A., Nasincova V., Kablaskova L. 2007a. Larval trema-todes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in central Europe: A survey of species and key to their identification. Systematic Parasitology, 69, 155–178. 10.1007/s11230-007-9127-1Search in Google Scholar PubMed

Faltynkova A., Nasincova V., Kablaskova L. 2007b. Larval trema-todes (Digenea) of the great pond snail Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in central Europe: A survey of species and key to their identification. Parasite, 14, 39–51. 10.1051/parasite/2007141039Search in Google Scholar PubMed

Fenton A., Fairbairn J.P., Norman R., Hudson P.J. Parasite transmission: Reconciling theory and reality. Journal of Animal Ecology, 71, 893–905. 10.1046/j.1365-2656.2002.00656.xSearch in Google Scholar

Fernandez J., Esch G.W. 1991a. Guild structure of larval trematods in the snail Helisoma anceps: Patterns and processes at the individual host level. Journal of Parasitology, 77, 528–539. 10.2307/3283156Search in Google Scholar

Fernandez J., Esch G.W. 1991b. The component community structure of larval trematodes in the pulmonate snail Helisoma anceps. Journal of Parasitology, 77, 540–550. 10.2307/3283157Search in Google Scholar

Haas W. 2003. Parasitic worms: Strategies of host finding, recognition and invasion. Zoology, 106, 349–364. 10.1078/0944-200600125Search in Google Scholar

Haas W., Korner M., Hutterer E., Wegner M., Haberl B.. 1995. Find-ing and recognition of the snail intermediate hosts by 3 species of echinostome cercariae. Parasitology, 110, 133–142. 10.1017/S0031182000063897Search in Google Scholar

Haberl B., Korner 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, 479–48610.1017/S0031182099005697Search in Google Scholar

Hechinger R.F., Wood A.C., Kuris A.M. 2011. Social organization in a flatworm: Trematode parasites form soldier and reproductive castes. Proceedings of the Royal Society of London, 278, 656–665. 10.1098/rspb.2010.1753Search in Google Scholar PubMed PubMed Central

Johnson P.T.J., Preston D.L., Hoverman J.T., Henderson J.S., Paull S.H., Richgels K.L.D., Redmond M.D. 2012. Species diversity re-duces parasite infection through cross-generation effects on host abundance. Ecology, 93, 56–64. 10.1890/11-0636.1Search in Google Scholar PubMed

Jokela J., Lively C.M. 1995. Spatial variation in infection by digenetic trematodes in a population of freshwater snails (Pota-mopyrgus antipodarum). Oecologia, 103, 509–517. 10.1007/BF00328690Search in Google Scholar PubMed

Kalbe M., Haberl B., Haas W. 2000. Snail host finding by Fasciola hepatica and Trichobilharzia ocellata: Compound analysis of “miracidia-attracting glycoproteins.” Experimental Parasitology, 96, 231–242. 10.1006/expr.2000.4579Search in Google Scholar PubMed

Kuris A.M., Warren J. 1980. Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second in-termediate host, Biomphalaria glabrata. Journal of Parasitology, 66, 630–635. 10.2307/3280520Search in Google Scholar

Kuris A.M., Lafferty K.D. 1994. Community structure: Larval trematodes in snail hosts. Annual Review of Ecology and Systematics, 25, 189–21710.1146/ in Google Scholar

Loy C., Haas W. 2001. Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitology Research, 87, 878–882. 10.1007/s004360100462Search in Google Scholar PubMed

McCarthy A.M. 1990. The influence of second intermediate host dis-persion pattern upon the transmission of cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology, 101, 43–47. 10.1017/S0031182000079737Search in Google Scholar

McCarthy A.M. 1999a. Photoperiodic cercarial emergence patterns of the digeneans Echinoparyphium recurvatum and Plagiorchis sp. from a mixed infection in Lymnaea peregra. Journal of Helminthology, 73, 59–62. 10.1017/S0022149X99 000074Search in Google Scholar

McCarthy A.M. 1999. The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurva-tum (Digenea: Echinosomatidae). Parasitology, 118, 383–38810.1017/S003118209900400XSearch in Google Scholar PubMed

Morley N.J. 2012. Thermodynamics of miracidial survival and me-tabolism. Parasitology, 139, 1640–1651. 10.1017/S00 31182012000960Search in Google Scholar

Morley N.J., Crane M., Lewis J.W. 2004a. Influence of cadmium ex-posure on the incidence of first intermediate host encystment by Echinoparyphium recurvatum cercariae in Lymnaea peregra. Journal of Helminthology, 78, 329–332. 10.1079/ JOH2004267Search in Google Scholar

Morley N.J., Lewis J.W., Adam M.E. 2004b. Metacercarial utilization of a naturally infected single species (Lymnaea peregra) snail community by Echinoparyphium recurvatum. Journal of Helminthology, 78, 51–56. 10.1079/JOH2003201Search in Google Scholar

Morley N.J., Lewis J.W. 2015. Thermodynamics of trematode infec-tivity. Parasitology, 142, 585–597. 10.1017/S00311 8201400163Search in Google Scholar

Muñoz-Antoli C., Toledo R., Esteban J. 2000. The life cycle and transmission dynamics of the larval stages of Hypoderaeum conoideum. Journal of Helminthology, 74, 165–172. 10.1017/S0022149X00000238Search in Google Scholar

Muñoz-Antoli C., Trelis C.M., Espert A., Toledo R., Esteban J.G. 2003. Interactions related to non-host snails in the host-finding process of Euparyphium albuferensis and Echinostoma friedi (Trematoda: Echinostomatidae) miracidia. Parasitology Research, 91, 353–356. 10.1007/s00436-003-0968-5Search in Google Scholar

Negron-Aponte H., Jobin W.R. 1977. Guidelines for spacing and timing of samples to detect populations of Schistosoma mansoni cercariae in the field. International Journal for Parasitology, 7, 123–126. 0.1016/0020-7519(77)90078-9Search in Google Scholar

Rauch G., Kalbe M., Reusch T.B. H. How a complex life cycle can improve a parasite’s sex life. Journal of Evolutionary Biology, 18, 1069–1075. 10.1111/j.1420-9101.2005.00895.xSearch in Google Scholar PubMed

Sandland G.J., Goater C.P., Danylchuk A.J. Population dynamics of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas) from four northern Alberta lakes. Journal of Parasitology, 87, 744–748. 10.1645/ 0022-3395Search in Google Scholar

Sapp K.K., Esch G.W. 1994. The effects of spatial and temporal het-erogeneity as structuring forces for parasite communities in Helisoma anceps and Physa gyrina. American Midland Naturalist, 132, 91–103. 10.2307/2426204Search in Google Scholar

Schmidt K.A., B. Fried. 1996. Emergence of cercariae of Echinostoma trivolvis from Helisoma trivolvis under different conditions. Journal of Parasitology, 82, 674–676. 10.2307/ 3283806Search in Google 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. 10.1007/s004420050507Search in Google Scholar

Toledo R., Muñoz-Antoli C., Perez M., Esteban J.G. 1999. Survival and infectivity of Hypoderaeum conoideum and Euparyphium albuferensis cercariae under laboratory conditions. Journal of Helmintology, 73, 177–182. 10.1017/S0022149X990 0027XSearch in Google Scholar

Toledo R., Espert A., Carpena I., Muñoz-Antoli C., Esteban J.G. 2003. An experimental study of the reproductive success of Echinostoma friedi (Trematoda: Echinostomatidae) in the golden hamster. Parasitology, 126, 433–441. 10.1017/ S0031182003213068Search in Google Scholar

Toledo R., Carpena I., Espert A., Sotillo J., Muñoz-Antoli C., Este-ban J.G. 2006. Transmission success of Echinostoma friedi (Trematoda: Echinostomatidae) in rats. Journal of Parasitology, 92, 16–20. 10.1645/GE-574R1.1Search in Google Scholar

Upatham E.S. 1972. Exposure or caged Biomphalaria glabrata (Say) to investigate dispersion of miracidia of Schistosoma mansoni Sambon in outdoor habitats in St. Lucia. Journal of Helminothology, 46, 297–30610.1017/S0022149X00023294Search in Google Scholar

Upatham E.S. 1973. Location of Biomphalaria glabrata (Say) by miracidia of Schistosoma mansoni Sambon in natural standing and running waters on the West Indian Island of St. Lucia. International Journal for Parasitology, 3, 289–297. 10.1016/0020-7519(73)90106-9Search in Google Scholar

Upatham E.S. 1974. Infectivity of Schistosoma mansoni cercariae in natural St. Lucian habitats. Annals of Tropical Medicine & Parasitology, 68, 235–236. 10.1080/00034983.1974. 11686941Search in Google Scholar

Williams J.A., Esch G.W. 1991. Infraand component community dynamics in the pulmonate snail Helisoma anceps, with special emphasis on the hemiurid trematode Halipegus occidualis. Journal of Parasitology, 77, 246–253. 10.2307/ 3283091Search in Google Scholar

Wilson R.A., Taylor S.L. 1978. The effect of variations in host and parasite density on the level of parasitization of Lymnaea trun-catula by Fasciola hepatica. Parasitology, 76, 91–98. 10.1017/S0031182000047429Search in Google Scholar

Zimmermann M.R., Luth K.E., Esch G.W. 2014a. Differences in snail ecology lead to infection pattern variation of Echinos-toma spp. larval stages. Acta Parasitologica, 59, 502–509. 10.2478/s11686-014-0275-6Search in Google Scholar PubMed

Zimmermann M.R., Luth K.E., Esch G.W. 2014b. Microhabitat dif-ferences surrounding a pond affects the distribution of trematode parasites among a pulmonate snail community. Helminthologia, 51, 301–308. 10.2478/s11687-0140245-4Search in Google Scholar

Received: 2016-1-11
Revised: 2016-5-16
Accepted: 2016-6-13
Published Online: 2016-10-22
Published in Print: 2016-12-1

© 2016 W. Stefański Institute of Parasitology, PAS

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