No effective method has yet been developed to prevent the threat posed by the emerging disease-cercarial dermatitis (swimmer's itch), caused by infective cercariae of bird schistosomes (Digenea: Schistosomatidae). In our previous studies, the New Zealand mud snail-Potamopyrgus antipodarum (Gray, 1853; Gastropoda, Tateidae)-was used as a barrier between the miracidia of Trichobilharzia regenti and the target snails Radix balthica. Since the presence of non-indigenous snails reduced the parasite prevalence under laboratory conditions, we posed three new research questions: (1) Do bird schistosomes show totally perfect efficacy for chemotactic swimming behavior? (2) Do the larvae respond to substances emitted by incompatible snail species? (3) Do the excretory-secretory products of incompatible snail species interfere with the search for a compatible snail host? The experiments were carried out in choice-chambers for the miracidia of T. regenti and T. szidati. The arms of the chambers, depending on the variant, were filled with water conditioned by P. antipodarum, water conditioned by lymnaeid hosts, and dechlorinated tap water. Miracidia of both bird schistosome species chose more frequently the water conditioned by snails-including the water conditioned by the incompatible lymnaeid host and the alien species, P. antipodarum. However, species-specific differences were noticed in the behavior of miracidia. T. regenti remained more often inside the base arm rather than in the arm filled with water conditioned by P. antipodarum or the control arm. T. szidati, however, usually left the base arm and moved to the arm filled with water conditioned by P. antipodarum. In conclusion, the non-host snail excretory-secretory products may interfere with the snail host-finding behavior of bird schistosome miracidia and therefore they may reduce the risk of swimmer's itch.

Department of Invertebrate Zoology and Parasitology Faculty of Biological and Veterinary Sciences Nicolaus Copernicus University in Torun Torun Poland

Department of Parasitology Faculty of Science Charles University Prague Czechia

Zobrazit více v PubMed

Anderson RM, Mercer JG, Wilson RA, Carter NP. Transmission 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. Parasitology. 1982;85(2):339–360. doi: 10.1017/S0031182000055323. PubMed DOI

Behrens AC, Nollen PM. Responses of Echinostoma caproni miracidia to gravity, light, and chemicals. International Journal for Parasitology. 1992;22(5):673–675. doi: 10.1016/0020-7519(92)90018-G. PubMed DOI

Christensen NO. Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. Journal of Helminthology. 1979;53(1):7–14. doi: 10.1017/S0022149X00005678. PubMed DOI

Cichy A, Marszewska A, Parzonko J, Żbikowski J, Żbikowska E. Infection of Potamopyrgus antipodarum (Gray, 1843) (Gastropoda: Tateidae) by trematodes in Poland, including the first record of aspidogastrid acquisition. Journal of Invertebrate Pathology. 2017;150:32–34. doi: 10.1016/j.jip.2017.09.003. PubMed DOI

Cichy A, Urbańska M, Marszewska A, Andrzejewski W, Żbikowska E. The invasive Chinese pond mussel Sinanodonta woodiana (Lea, 1834) as a host for native symbionts in European waters. Journal of Limnology. 2016;75(2):288–296.

Combes C, Moné H. Possible mechanisms of the decoy effect in Schistosoma mansoni transmission. International Journal for Parasitology. 1987;17(4):971–975. doi: 10.1016/0020-7519(87)90017-8. PubMed DOI

Gérard C, Le Lannic J. Establishment of a new host-parasite association between the introduced invasive species Potamopyrgus antipodarum (Smith) (Gastropoda) and Sanguinicola sp. Plehn (Trematoda) in Europe. Journal of Zoology. 2003;261(2):213–216.

Gérard C, Miura O, Lorda J, Cribb TH, Nolan MJ, Hechinger RF. A native-range source for a persistent trematode parasite of the exotic New Zealand mudsnail (Potamopyrgus antipodarum) in France. Hydrobiologia. 2017;785(1):115–126. doi: 10.1007/s10750-016-2910-8. DOI

Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368(9541):1106–1118. doi: 10.1016/S0140-6736(06)69440-3. PubMed DOI

Haas W. Parasitic worms: strategies of host finding, recognition and invasion. Zoology. 2003;106(4):349–364. doi: 10.1078/0944-2006-00125. PubMed DOI

Haas W, Van de Roemer A. Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata: penetration processes and stimulating host signals. Parasitology Research. 1998;84(10):787–795. doi: 10.1007/s004360050489. PubMed DOI

Haberl B, Kalbe M, Fuchs H, Ströbel M, Schmalfuss G, Haas W. Schistosoma mansoni and S. haematobium: miracidial host-finding behaviour is stimulated by macromolecules. International Journal for Parasitology. 1995;25(5):551–560. doi: 10.1016/0020-7519(94)00158-K. PubMed DOI

Haberl B, Körner M, Spengler Y, Hertel J, Kalbe M, Haas W. Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology. 2000;120(Pt. 5):479–486. doi: 10.1017/S0031182099005697. PubMed DOI

Hassan AHM, Haberl B, Hertel J, Haas W. Miracidia of an Egyptian strain of Schistosoma mansoni differentiate between sympatric snail species. Journal of Parasitology. 2003;89(6):1248–1250. doi: 10.1645/GE-85R. PubMed DOI

Hechinger RF. Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa. 2012;3418(1):1–27. doi: 10.11646/zootaxa.3418.1.1. DOI

Hertel J, Holweg A, Haberl B, Kalbe M, Haas W. Snail odour-clouds: spreading and contribution to the transmission success of Trichobilharzia ocellata (Trematoda, Digenea) miracidia. Oecologia. 2006;147(1):173–180. doi: 10.1007/s00442-005-0239-5. PubMed DOI

Hopper JV, Poulin R, Thieltges DW. Buffering role of the intertidal anemone Anthopleura aureoradiata in cercarial transmission from snails to crabs. Journal of Experimental Marine Biology and Ecology. 2008;367(2):153–156. doi: 10.1016/j.jembe.2008.09.013. DOI

Horák P, Kolářová L. Bird schistosomes: do they die in mammalian skin? Trends in Parasitology. 2001;17(2):66–69. doi: 10.1016/S1471-4922(00)01770-0. PubMed DOI

Horák P, Mikeš L, Lichtenbergová L, Skála V, Soldánová M, Brant SV. Avian schistosomes and outbreaks of cercarial dermatitis. Clinical Microbiology Reviews. 2015;28(1):165–190. doi: 10.1128/CMR.00043-14. PubMed DOI PMC

Horák P, Mikeš L, Rudolfová J, Kolářová L. Penetration of Trichobilharzia cercariae into mammals: dangerous or negligible event? Parasite. 2008;15(3):299–303. doi: 10.1051/parasite/2008153299. PubMed DOI

Johnson PTJ, Thieltges DW. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology. 2010;213(6):961–970. doi: 10.1242/jeb.037721. PubMed DOI

Jouet D, Ferté H, Depaquit J, Rudolfová J, Latour P, Zanella D, Kaltenbach ML, Léger N. Trichobilharzia spp. in natural conditions in Annecy Lake. France Parasitology Research. 2008;103(1):51–58. doi: 10.1007/s00436-008-0926-3. PubMed DOI

Kalbe M, Haberl B, Haas W. Schistosoma mansoni miracidial host-finding: species specificity of an Egyptian strain. Parasitology Research. 1996;82(1):8–13. doi: 10.1007/s004360050059. PubMed DOI

Kalbe M, Haberl B, Haas W. Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates released from the host snails. Parasitology Research. 1997;83(8):806–812. doi: 10.1007/s004360050344. PubMed DOI

Kalbe M, Haberl B, Haas W. Snail host finding by Fasciola hepatica and Trichobilharzia ocellata: compound analysis of miracidia-attracting glycoproteins. Experimental Parasitology. 2000;96(4):231–242. doi: 10.1006/expr.2000.4579. PubMed DOI

Kalbe M, Haberl B, Hertel J, Haas W. Heredity of specific host-finding behaviour in Schistosoma mansoni miracidia. Parasitology. 2004;128(Pt. 6):635–643. doi: 10.1017/S0031182004005037. PubMed DOI

Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecology Letters. 2006;9(4):485–498. doi: 10.1111/j.1461-0248.2006.00885.x. PubMed DOI

Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM. Parasite spillback: a neglected concept in invasion ecology? Ecology. 2009;90(8):2047–2056. doi: 10.1890/08-1085.1. PubMed DOI

Kock S. Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae) Parasitology. 2001;123(1):67–70. doi: 10.1017/S0031182001008101. PubMed DOI

Kopp K, Jokela J. Resistant invaders can convey benefits to native species. Okois. 2007;116(2):295–301. doi: 10.1111/j.0030-1299.2007.15290.x. DOI

Lévesque B, Giovenazzo P, Guerrier P, Laverdière D, Prud’Homme H. Investigation of an outbreak of cercarial dermatitis. Epidemiology and Infection. 2002;129(2):379–386. doi: 10.1017/S0950268802007379. PubMed DOI PMC

Marszewska A, Cichy A. Unionid clams and the zebra mussels on their shells (Bivalvia: Unionidae, Dreissenidae) as hosts for trematodes in lakes of the Polish lowland. Folia Malacologica. 2015;23(2):149–154. doi: 10.12657/folmal.023.011. DOI

Marszewska A, Cichy A, Bulantová J, Horák P, Żbikowska E. Potamopyrgus antipodarum as a potential defender against swimmer’s itch in European recreational water bodies-experimental study. PeerJ. 2018;6:e5045. doi: 10.7717/peerj.5045. PubMed DOI PMC

Marszewska A, Cichy A, Heese T, Żbikowska E. The real threat of swimmers’ itch in anthropogenic recreational water body of the Polish Lowland. Parasitology Research. 2016;115(8):3049–3056. doi: 10.1007/s00436-016-5060-z. PubMed DOI PMC

McCullough FS. The role of mollusciciding in schistosomiasis control. Geneva: World Health Organization; 1992.

Meuleman EA, Huyer AR, Mooij JH. Maintenance of the life cycle of Trichobilharzia ocellata via the duck Anas platyrhynchos and the pond snail Lymnaea stagnalis. Netherlands Journal of Zoology. 1983;34(3):414–417. doi: 10.1163/002829684X00236. DOI

Mouritsen KN, Poulin R. The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia. 2003;135(1):131–137. doi: 10.1007/s00442-003-1183-x. PubMed DOI

Piechocki A, Wawrzyniak-Wydrowska B. Guide to freshwater and marine mollusca of Poland. Poznań: Bogucki Wydawnictwo Naukowe; 2016.

Rind S. Dendritobilharzia pulverulenta (Trematoda: Schistosomatidae) in New Zealand. New Zealand Journal of Zoology. 1989;16(2):215–220. doi: 10.1080/03014223.1989.10422571. DOI

Sapp KK, Loker ES. Mechanisms underlying digenean-snail specificity: role of miracidial attachment and host plasma factors. Journal of Parasitology. 2000;86(5):1012–1020. PubMed

Selbach C, Rosenkranz M, Poulin R. Cercarial behavior determines risk of predation. Journal of Parasitology. 2019;105(2):330–333. doi: 10.1645/18-165. PubMed DOI

Seppälä O, Leicht K. Quality attracts parasites: host condition-dependent chemo-orientation of trematode larvae. Functional Ecology. 2015;29(6):791–795. doi: 10.1111/1365-2435.12392. DOI

Soldánová M, Selbach C, Sures B. The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLOS ONE. 2016;11(2):e0149678. doi: 10.1371/journal.pone.0149678. PubMed DOI PMC

Thieltges DW, Bordalo MD, Hernández AC, Prinz K, Jensen KT. Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology. 2008;135(9):1111–1116. doi: 10.1017/S0031182008004526. PubMed DOI

Thieltges DW, Jensen KT, Poulin R. The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology. 2008;135(4):407–426. doi: 10.1017/S0031182007000248. PubMed DOI

Tracz ES, Al-Jubury A, Buchmann K, Bygum A. Outbreak of swimmer’s itch in Denmark. Acta Dermato-Venereologica. 2019;99(12):1116–1120. PubMed

Vielma S, Lagrue C, Poulin R, Selbach C. Non-host organisms impact transmission at two different life stages in a marine parasite. Parasitology Research. 2019;118(1):111–117. doi: 10.1007/s00436-018-6121-2. PubMed DOI

Zar JH. Biostatistical analysis. Englewood Cliffs: Prentice Hall; 1984.

Żbikowska E, Kobak J, Żbikowski J, Kaklewski J. Infestation of Lymnaea stagnalis by digenean flukes in the Jeziorak Lake. Parasitology Research. 2006;99(4):434–439. doi: 10.1007/s00436-006-0178-z. PubMed DOI

Żbikowski J, Żbikowska E. Invaders of an invader-trematodes in Potamopyrgus antipodarum in Poland. Journal of Invertebrate Pathology. 2009;101(1):67–70. doi: 10.1016/j.jip.2009.02.005. PubMed DOI