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Molecular diversity of avian schistosomes in Danish freshwater snails

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Abstract

Avian schistosomes are widespread parasites of snails and waterfowl and may cause cercarial dermatitis (swimmer’s itch) in humans, a disease that is frequently reported in European countries. These parasites are known to occur in Denmark, but here, we applied a new approach using molecular tools to identify the parasites at species level. In order to do that, 499 pulmonate freshwater snails (Radix sp., Lymnaea stagnalis, Stagnicola sp. and Planorbarius corneus) were sampled from 12 lakes, ponds, and marshes in the greater Copenhagen area. Avian schistosome cercariae were identified by microscopy and subjected to molecular investigation by sequencing and phylogenetic analysis of the 5.8S and ITS2 ribosomal DNA for species identification. Additionally, snail hosts belonging to the genus Radix were identified by sequencing and phylogenetic analysis of partial ITS2 ribosomal DNA. Three out of 499 snails shed different species of Trichobilharzia cercariae: Trichobilharzia szidati was isolated from L. stagnalis, Trichobilharzia franki from Radix auricularia and Trichobilharzia regenti from Radix peregra. In the light of the public health risk represented by bird schistosomes, these findings are of concern and, particularly, the presence of the potentially neuro-pathogenic species, T. regenti, in Danish freshwaters calls for attention.

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References

  • Aldhoun JA, Faltýnková A, Karvonen A, Horák P (2009a) Schistosomes in the north: a unique finding from a prosobranch snail using molecular tools. Parasitol Int 58:314–317. doi:10.1016/j.parint.2009.03.007

    Article  CAS  PubMed  Google Scholar 

  • Aldhoun JA, Kolárová L, Horák P, Skírnisson K (2009b) Bird schistosome diversity in Iceland: molecular evidence. J Helminthol 83:173–180. doi:10.1017/S0022149X09289371

    Article  CAS  PubMed  Google Scholar 

  • Aldhoun JA, Podhorský M, Holická M, Horák P (2012) Bird schistosomes in planorbid snails in the Czech Republic. Parasitol Int 61:250–259. doi:10.1016/j.parint.2011.10.006

    Article  PubMed  Google Scholar 

  • Bargues MD, Vigo M, Horak P, Dvorak J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S (2001) European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol I 1:85–107. doi:10.1016/S1567-1348(01)00019-3

    Article  CAS  Google Scholar 

  • Bayssade-Dufour C, Vuong PN, René M, Martin-Loehr C, Martins C (2002) Visceral lesions in mammals and birds exposed to agents of human cercarial dermatitis. Bull Soc Pathol Exot 95:229–237

    PubMed  Google Scholar 

  • Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F, Amend AS, Jumpponen A, Unterseher M, Kristiansson E, Abarenkov K, Bertrand YJK, Sanli K, Eriksson KM, Vik U, Veldre V, Nilsson RH (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919. doi:10.1111/2041-210X.12073

    Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Berg K, Reiter HFH (1960) Observations on schistosome dermatitis in Denmark. Acta Derm Venereol 40:369–380

    Google Scholar 

  • Blair D (2006) Ribosomal DNA variation in parasitic flatworms. In: Maule AG, Marks NJ (eds) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. CABI, pp 96–123

  • Brant SV (2007) The occurrence of the avian schistosome Allobilharzia visceralis Kolárová, Rudolfová, Hampl et Skírnisson, 2006 (Schistosomatidae) in the tundra swan, Cygnus columbianus (Anatidae), from North America. Folia Parasitol (Praha) 54:99–104

    Article  CAS  Google Scholar 

  • Brant SV, Loker ES (2009) Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J Parasitol 95:941–963. doi:10.1645/GE-1870.1

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brant SV, Loker ES (2013) Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends Parasitol 29:449–459. doi:10.1016/j.pt.2013.06.004

    Article  PubMed Central  PubMed  Google Scholar 

  • Brown R, Soldánová M, Barrett J, Kostadinova A (2011) Small-scale to large-scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe. Parasitol Res 108:137–150. doi:10.1007/s00436-010-2047-z

    Article  PubMed  Google Scholar 

  • Buchmann K, Anne H, Bresciani J (2004) Snyltere angriber badegæster. Aktuel Naturvidenskab 1:8–10

    Google Scholar 

  • Chrisanfova GG, Lopatkin AA, Mishchenkov VA, Kheidorova EE, Dorozhenkova TE, Zhukova TV, Ryskov AP, Semyenova SK (2009) Genetic variability of bird schistosomes (class Trematoda, family Schistosomatidae) of Naroch Lake: identification of a new species in the Trichobilharzia ocellata group. Dokl Biochem Biophys 428:268–272. doi:10.1134/S1607672909050123

    Article  CAS  PubMed  Google Scholar 

  • Cipriani P, Mattiucci S, Paoletti M, Scialanca F, Nascetti G (2011) Molecular evidence of Trichobilharzia franki Müller and Kimmig, 1994 (Digenea: Schistosomatidae) in Radix auricularia from Central Italy. Parasitol Res 109:935–940. doi:10.1007/s00436-011-2295-6

    Article  PubMed  Google Scholar 

  • Cordellier M, Pfenninger A, Streit B, Pfenninger M (2012) Assessing the effects of climate change on the distribution of pulmonate freshwater snail biodiversity. Mar Biol 159:2519–2531. doi:10.1007/s00227-012-1894-9

    Article  Google Scholar 

  • Cort W (1928) Schistosome dermatitis in the United States (Michigan). J Am Med Assoc 90:1027–1029

    Article  Google Scholar 

  • Danish Ministry of Health (2000) Bekendtgørelse om lægers anmeldelse af smitsomme sygdomme m.v. Act no. 277 of 14 April 2000. https://www.retsinformation.dk/Forms/R0710.aspx?id=21406&exp=1. Accessed 7 May 2015

  • Dvorák J, Vanácová S, Hampl V, Flegr J, Horák P (2002) Comparison of european Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Faltýnková A, Našincová V, Kablasková L (2007) Larval trematodes (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

    Article  PubMed  Google Scholar 

  • Faltýnková A, Nasincová V, Kablásková L (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Syst Parasitol 69:155–178. doi:10.1007/s11230-007-9127-1

    Article  PubMed  Google Scholar 

  • Ferté H, Depaquit J, Carré S, Villena I, Léger N (2005) Presence of Trichobilharzia szidati in Lymnaea stagnalis and T. franki in Radix auricularia in northeastern France: molecular evidence. Parasitol Res 95:150–154. doi:10.1007/s00436-004-1273-7

    Article  PubMed  Google Scholar 

  • Frandsen F, Christensen N (1984) An introductory guide to the identification of cercariae from African freshwater snails with special reference to cercariae of trematode species of medical and veterinary importance. Acta Trop 41:181–202

    CAS  PubMed  Google Scholar 

  • Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can J Zool 80:2207–2217. doi:10.1139/Z02-198

    Article  CAS  Google Scholar 

  • Glöer P (2002) Tierwelt Deutschlands. Mollusca I - Die Süβwassergastropoden Nord- und Mitteleuropas. Conch-Books, Bad Kreuznach

    Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Horák P, Kolárová L (2000) Survival of bird schistosomes in mammalian lungs. Int J Parasitol 30:65–68

    Article  PubMed  Google Scholar 

  • Horák P, Kolářová L (2001) Bird schistosomes: do they die in mammalian skin? Trends Parasitol 17:66–69

    Article  PubMed  Google Scholar 

  • Horák P, Kolářová L (2011) Snails, waterfowl and cercarial dermatitis. Freshw Biol 56:779–790. doi:10.1111/j.1365-2427.2010.02545.x

    Article  Google Scholar 

  • Horák P, Kolářová L, Dvorák J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a new nasal schistosome from Europe. Parasite 5:349–357

    Article  PubMed  Google Scholar 

  • Horák P, Dvorák J, Kolárová L, Trefil L (1999) Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119:577–581

    Article  PubMed  Google Scholar 

  • Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 52:155–233

    Article  PubMed  Google Scholar 

  • Horák P, Mikeš L, Lichtenbergová L, Skála V, Soldánová M, Brant SV (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clin Microbiol Rev 28:165–190. doi:10.1128/CMR.00043-14

    Article  PubMed Central  PubMed  Google Scholar 

  • Hoyer M, Canfield D (1994) Bird abundance and species richness on Florida lakes: influence of trophic status, lake morphology, and aquatic macrophytes. Aquat Birds Trophic Web Lakes 297(280):107–119

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • Huňová K, Kašný M, Hampl V, Leontovyč R, Kuběna A, Mikeš L, Horák P (2012) Radix spp.: identification of trematode intermediate hosts in the Czech Republic. Acta Parasitol 57:273–284. doi:10.2478/s11686-012-0040-7

    PubMed  Google Scholar 

  • Jensen PN, Boutrup S, Svendsen LM, Blicher-Mathiesen G, Wiberg-Larsen P, Bjerring R, Hansen JW, Ellerman T, Thorling L, Holm AG (2013) Vandmiljø og natur 2012. NOVANA. Tilstand og udvikling - faglig sammenfatning. Aarhus Universitet, DCE - Nationalt Center for Miljø og Energi

  • Jeppesen E, Kronvang B, Jørgensen TB, Larsen SE, Andersen HE, Søndergaard M, Liboriussen L, Bjerring R, Johansson LS, Trolle D, Lauridsen TL (2012) Recent climate induced changes in freshwaters in Denmark. In: Goldman CR, Kumagai M, Robarts RD (eds) Climate change and global warming of inland waters: impacts and mitigation for ecosystems and societies, 1st edn. Wiley, Chichester, pp 155–171

    Chapter  Google Scholar 

  • Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proc Natl Acad Sci U S A 104:15781–15786. doi:10.1073/pnas.0707763104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Jouet D, Ferté H, Hologne C, Kaltenbach ML, Depaquit J (2009) Avian schistosomes in French aquatic birds: a molecular approach. J Helminthol 83:181–189. doi:10.1017/S0022149X09311712

    Article  CAS  PubMed  Google Scholar 

  • Jouet D, Skírnisson K, Kolářová L, Ferté H (2010a) Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infect Genet Evol 10:1218–1227. doi:10.1016/j.meegid.2010.08.001

    Article  CAS  PubMed  Google Scholar 

  • Jouet D, Skírnisson K, Kolářová L, Ferté H (2010b) Final hosts and variability of Trichobilharzia regenti under natural conditions. Parasitol Res 107:923–930. doi:10.1007/s00436-010-1953-4

    Article  PubMed  Google Scholar 

  • Jouet D, Kolářová L, Patrelle C, Ferté H, Skírnisson K (2015) Trichobilharzia anseri n. sp. (Schistosomatidae: Digenea), a new visceral species of avian schistosomes isolated from greylag goose (Anser anser L.) in Iceland and France. Infect Genet Evol. doi:10.1016/j.meegid.2015.06.012

    PubMed  Google Scholar 

  • Kock S (2001) Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123:67–70

    Article  CAS  PubMed  Google Scholar 

  • Kolářová L, Horák P, Fajfrlík K (1992) Cercariae of Trichobilharzia szidati Neuhaus, 1952 (Trematoda: Schistosomatidae): the causative agent of cercarial dermatitis in Bohemia and Moravia. Folia Parasitol (Praha) 39:399–400

    Google Scholar 

  • Kolářová L, Rudolfová J, Hampl V, Skírnisson K (2006) Allobilharzia visceralis gen. nov., sp. nov. (Schistosomatidae-Trematoda) from Cygnus cygnus (L.) (Anatidae). Parasitol Int 55:179–186. doi:10.1016/j.parint.2005.10.009

    Article  PubMed  Google Scholar 

  • Kolářová L, Horák P, Skírnisson K (2010) Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis. J Helminthol 84:327–335. doi:10.1017/S0022149X09990721

    Article  PubMed  Google Scholar 

  • Kolářová L, Horák P, Skírnisson K, Marečková H, Doenhoff M (2013a) Cercarial dermatitis, a neglected allergic disease. Clin Rev Allergy Immunol 45:63–74. doi:10.1007/s12016-012-8334-y

    Article  PubMed  Google Scholar 

  • Kolářová L, Skírnisson K, Ferté H, Jouet D (2013b) Trichobilharzia mergi sp. nov. (Trematoda: Digenea: Schistosomatidae), a visceral schistosome of Mergus serrator (L.) (Aves: Anatidae). Parasitol Int 62:300–308. doi:10.1016/j.parint.2013.03.002

    Article  PubMed  Google Scholar 

  • Korbie DJ, Mattick JS (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat Protoc 3:1452–1456. doi:10.1038/nprot.2008.133

    Article  CAS  PubMed  Google Scholar 

  • Kouřilová P, Syrůcek M, Kolářová L (2004) The severity of mouse pathologies caused by the bird schistosome Trichobilharzia regenti in relation to host immune status. Parasitol Res 93:8–16. doi:10.1007/s00436-004-1079-7

    Article  PubMed  Google Scholar 

  • Larsen AH, Bresciani J, Buchmann K (2004) Increasing frequency of cercarial dermatitis at higher latitudes. Acta Parasitol 49:217–221

    Google Scholar 

  • Lawton SP, Lim RM, Dukes JP, Cook RT, Walker AJ, Kirk RS (2014) Identification of a major causative agent of human cercarial dermatitis, Trichobilharzia franki (Müller and Kimmig 1994), in southern England and its evolutionary relationships with other European populations. Parasit Vectors 7:277. doi:10.1186/1756-3305-7-277

    Article  PubMed Central  PubMed  Google Scholar 

  • Lehikoinen A, Jaatinen K (2012) Delayed autumn migration in northern European waterfowl. J Ornithol 153:563–570. doi:10.1007/s10336-011-0777-z

    Article  Google Scholar 

  • Lehikoinen A, Jaatinen K, Vähätalo AV, Clausen P, Crowe O, Deceuninck B, Hearn R, Holt CA, Hornman M, Keller V, Nilsson L, Langendoen T, Tománková I, Wahl J, Fox AD (2013) Rapid climate driven shifts in wintering distributions of three common waterbird species. Glob Chang Biol 19:2071–2081. doi:10.1111/gcb.12200

    Article  PubMed  Google Scholar 

  • Lichtenbergová L, Horák P (2012) Pathogenicity of Trichobilharzia spp. for vertebrates. J Parasitol Res 761968. doi: 10.1155/2012/761968

  • Littlewood DT, Curini-Galletti M, Herniou EA (2000) The interrelationships of proseriata (Platyhelminthes: seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. doi:10.1006/mpev.2000.0802

    Article  CAS  PubMed  Google Scholar 

  • Loy C, Haas W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitol Res 87:878–882. doi:10.1007/s004360100462

    Article  CAS  PubMed  Google Scholar 

  • Morley NJ, Lewis JW (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140:1211–1224. doi:10.1017/S0031182012001783

    Article  CAS  PubMed  Google Scholar 

  • Müller V, Kimmig P (1994) Trichobilharzia franki n. sp. - die Ursache für Badedermatitiden in südwestdeutchen Baggerseen. Appl Parasitol 35:12–31

    PubMed  Google Scholar 

  • Neuhaus W (1952) Biologie und entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae), einem erreger von dermatitis beim menschen. Zeitschrift für Parasitenkd 15:203–266

    CAS  Google Scholar 

  • Nilsson L (2008) Changes of numbers and distribution of wintering waterfowl in Sweden during forty years, 1967–2006. Ornis Svecica 18:135–226

    Google Scholar 

  • Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163. doi:10.1016/S0065-308X(05)60002-4

    Article  PubMed  Google Scholar 

  • Pfenninger M, Cordellier M, Streit B (2006) Comparing the efficacy of morphologic and DNA-based taxonomy in the freshwater gastropod genus Radix (Basommatophora, Pulmonata). BMC Evol Biol 6:100. doi:10.1186/1471-2148-6-100

    Article  PubMed Central  PubMed  Google Scholar 

  • Picard D, Jousson O (2001) Genetic variability among cercariae of the Schistosomatidae (Trematoda: Digenea) causing swimmer’s itch in Europe. Parasite 8:237–242

    Article  CAS  PubMed  Google Scholar 

  • Podhorský M, Huůzová Z, Mikeš L, Horák P (2009) Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitol 54:28–36. doi:10.2478/s11686-009-0011-9

    Article  Google Scholar 

  • Poulin R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132:143–151. doi:10.1017/S0031182005008693

    Article  CAS  PubMed  Google Scholar 

  • Puslednik L, Ponder WF, Dowton M, Davis AR (2009) Examining the phylogeny of the Australasian Lymnaeidae (Heterobranchia: Pulmonata: Gastropoda) using mitochondrial, nuclear and morphological markers. Mol Phylogenet Evol 52:643–659. doi:10.1016/j.ympev.2009.03.033

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  • Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DTJ, Horák P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95:79–89. doi:10.1007/s00436-004-1262-x

    Article  PubMed  Google Scholar 

  • Rudolfová J, Littlewood DTJ, Sitko J, Horák P (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitol (Praha) 54:88–93

    Article  Google Scholar 

  • Simon-Martin F, Simon-Vicente F (1999) The life cycle of Trichobilharzia salmanticensis n. sp. (Digenea: Schistosomatidae), related to cases of human dermatitis. Res Rev Parasitol 59:13–18

    Google Scholar 

  • Skírnisson K, Aldhoun JA, Kolárová L (2009) A review on swimmer’s itch and the occurrence of bird schistosomes in Iceland. J Helminthol 83:165–171. doi:10.1017/S0022149X09336408

    Article  PubMed  Google Scholar 

  • Soldánová M, Selbach C, Kalbe M, Kostadinova A, Sures B (2013) Swimmer’s itch: etiology, impact, and risk factors in Europe. Trends Parasitol 29:65–74. doi:10.1016/j.pt.2012.12.002

    Article  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wesenberg-Lund C (1934) Contributions to the development of the trematoda digenea. Part II. The biology of the freshwater cercariae in Danish freshwaters. Levin & Munksgaard, København

    Google Scholar 

  • Zbikowska E, Nowak A (2009) One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe. Parasitol Res 105:301–311. doi:10.1007/s00436-009-1462-5

    Article  PubMed  Google Scholar 

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The authors would like to thank Thomas K. Kristensen for valuable assistance with the field work.

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Christiansen, A.Ø., Olsen, A., Buchmann, K. et al. Molecular diversity of avian schistosomes in Danish freshwater snails. Parasitol Res 115, 1027–1037 (2016). https://doi.org/10.1007/s00436-015-4830-3

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