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Type: Article
Published: 2020-02-17
Page range: 121–140
Abstract views: 513
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North American Branchiobdellida (Annelida: Clitellata) or Crayfish Worms in France: the most diverse distribution of these exotic ectosymbionts in Europe

Royal Belgian Institute of Natural Sciences, Operational Directorate Taxonomy and Phylogeny, Vautier Street 29, B-1000 Brussels, Belgium
University of Maine at Presque Isle, 181 Main Street, Presque Isle, Maine 04769, USA
Annelida Ectosymbiosis French distribution Triannulata magna Cambarincola mesochoreus Cambarincola gracilis Cambarincola okadai Xironogiton victoriensis North American crayfish Pacifastacus leniusculus Procambarus clarkii Faxonius limosus Aust


Crayfishes and other invertebrates were collected during 2010 to 2016 from 519 sites located in the river basins of the Adour, Charente, Dordogne, Garonne, Loire, Seine, Rhône and Sélune in France. North American species included Pacifastacus leniusculus at 255 sites, Faxonius limosus at 206 sites, Procambarus clarkii at 56 sites, and the endemic Austropotamobius pallipes at two sites. However, branchiobdellidans were only recorded from 100 sites with 23 of these being sampled more than once, resulting in a total of 127 collections.

      The widely distributed western North American, P. leniusculus carried four of its endemic branchiobdellidan species: Cambarincola gracilis, C. okadai, Triannulata magna and Xironogiton victoriensis. X. victoriensis was found at the majority of sites, with C. okadai, C. gracilis, and T. magna at fewer locations. Although F. limosus was the second most numerous crayfish species collected, it did not carry any of its endemic North American branchiobdellidan species. However, it was found cohabiting with P. leniusculus at four sites but carried X. victoriensis at only one of these. European A. pallipes only occurred at two sites with individuals harboring X. victoriensis, although no cohabiting exotic crayfish were found. Crayfish were also absent from three sites where free-living X. victoriensis were recovered from substrate samples. Procambarus clarkii appeared at sites scattered across the country, while specimens with C. mesochoreus were restricted to the Adour drainage.

      This study has shown the widespread distribution of exotic branchiobdellidans in the wild and the virtual extinction of endemic species in France. In addition, we have provided the first European record of T. magna, and the first record of C. mesochoreus in France; the latter being only the second recording in Europe. With this comprehensive survey of their crayfish hosts in France, monitoring future exotic range expansions and endemic contraction or extinction can be traced. These data will be available to authorities for future planning in maintaining healthy freshwater bodies by reducing the damaging effects caused by exotic crayfishes.


  1. Ames, C.W., Helms, B.S. & Stoeckel, J.A. (2015) Habitat mediates the outcome of a cleaning symbiosis for a facultatively burrowing crayfish. Freshwater Biology, 60, 989–999.

    Bláha, M., Ložek, F., Buřič, M., Kouba, A. & Kozák, P. (2017) Native European branchiobdellids on non-native crayfishes: Report from the Czech Republic. Journal of Limnology, 77 (1), 164–168.

    Chiesa, S., Scalici, M., Lucentini, L. & Nonnis Marzano, F. (2015) Molecular identification of an alien temnocephalan crayfish parasite in Italian freshwaters. Aquatic Invasions, 10, 209–216.

    Dražina, T., Korša, A., Špoljar, M., Maguire, I. & Klobučar, G.I.V. (2018) Epifauna of native and alien freshwater crayfish species (Crustacea: Decapoda): a host-specific community? Freshwater Science, 37 (3), 593–604.

    Ďuriš Z., Horká I., Kristian J. & Kozák P. (2006) Some case of Macro-Epibiosis on the invasive crayfish Faxonius limosus in the Czech Republic. Bulletin Français de la Pêche et de la Pisciculture, 380/381, 1325–1337.

    Franzén, Å. (1962) Notes on the morphology and histology of Xironogiton instabilia (Moore, 1893) (Fam. Branchiobdellidae) with special reference to the muscle cells. Zoologiska Bidrag från Uppsala, 35, 369–383.

    Gelder, S.R. (1999) Zoogeography of branchiobdellidans (Annelida) and temnocephalidans (Platyhelminthes) ectosymbiotic on freshwater crustaceans, and their reactions to one another in vitro. Hydrobiologia, 406, 21–31.

    Gelder, S.R. (2004) Endemic ectosymbiotic branchiobdellidans (Annelida: Clitellata) reported on three “export” species of North American crayfish (Crustacea: Astacoidea). Freshwater Crayfish, 14, 221–227.

    Gelder, S.R. (2016) Clitellata: Branchiobdellida. In: Thorp, J. & Rogers, D.C. (Eds.), Keys to Nearctic Fauna: Thorp and Covich's Freshwater Invertebrates, Volume II. Academic Press, pp. 234–244.

    Gelder, S.R., Delmastro, G.B. & Ferraguti, M. (1994) A report on branchiobdellidans (Annelida: Clitellata) and a taxonomic key to the species in northern Italy, including the first record of Cambarincola mesochoreus on the introduced American red swamp crayfish. Bolletino di zoologia, 61, 179–183.

    Gelder, S.R., Delmastro, G.B. & Rayburn, J.N. (1999) Distribution of native and exotic branchiobdellidans (Annelida: Clitellata) on their respective crayfish hosts in northern Italy, with the first record of native Branchiobdella species on an exotic North American crayfish. Journal of Limnology, 58, 20–24.

    Gelder, S.R. & Hall, L.A. (1990) Description of Xironogiton victoriensis n.sp. from British Columbia, Canada, with remarks on other species and a Wagner analysis of Xironogiton (Clitellata: Branchiobdellida). Canadian Journal of Zoology, 68, 2352–2359.

    Gelder, S.R., Parpet, J.-F. & Quaglio, F. (2012) First report of two North American branchiobdellidans (Annelida: Clitellata) or crayfish worms on signal crayfish in Europe with a discussion of similar introductions into Japan. Annales de Limnologie. International Journal of Limnology, 48, 315–322.

    Gelder, S.R. & Williams B.W. (2015) Clitellata: Branchiobdellida. In: Thorp, J. & Rogers, D.C. (Eds.), Ecology and General Biology: Thorp and Covich's Freshwater Invertebrates, Volume I. Academic Press, 551–563.

    Gelder, S.R. & Williams, B.W. (2016) Global Overview of Branchiobdellida (Annelida: Clitellata). In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, New York, 628–654.

    Holdich, D.M., James, J., Jackson, C. & Peay, S. (2014) The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain, Ethology, Ecology & Evolution, 26 (2–3), 232–262.

    Holdich, D.M. & Lowery, R.S. (1988) Freshwater Crayfish. Biology, Management and Conservation. Croom Helm (Chapman & Hall), London, 497pp.

    Holdich, D.M. Reynolds, J.D. Souty-Grosset, C. & Silby, P.J. (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowledge and Management of Aquatic Ecosystems, 394–395, 11, 1–46.

    Holt, P.C. (1973) A free-living branchiobdellid (Annelida: Clitellata)? Transactions of the American Microscopical Society, 92, 152–153.

    Holt, P.C. (1974) An emendation of the genus Triannulata with the assignment of Triannulata montana to Cambarincola Ellis 1912 (Clitellata Branchiobdellida). Proceedings of the Biological Society of Washington, 87, 57–72.

    Holt, P.C. & Opell, B.D. (1993) A checklist of and illustrated key to the genera and species of the Central and North American Cambarincolidae (Clitellata: Branchiobdellida). Proceedings of the Biological Society of Washington, 106, 251–295.

    Hunt, R., Rhidian, J., James, J. & Cable, J. (2018) Transmission and terrestrial dispersal of non-native ectosymbionts on invasive crayfish. Hydrobiologia, 820, 135–144.

    James, J. Cable, J. Richardson, G. Davidson, K.E. & Mackie, A.S.Y. (2015) Two alien species of Branchiobdellida (Annelida: Clitellata) new to the British Isles: a morphological and molecular study. Aquatic Invasions, 10, 371–383.

    James, J. Davidson, K.E. Hunt, R. & Cable, J. (2017) Assessing the invasion potential of non-native branchiobdellidans: experimental studies of survival, reproduction and competition. Knowledge and Management of Aquatic Ecosystems, 418, 35–43.

    Keith, P. & Allardi, J. (1997) Bilan des introductions de poissons d’eau douce en France. Knowledge and Management of Aquatic Ecosystems, 344–345, 181–191.

    Kirjavainen, J. & Westman, K. (1999) Natural history and development of the introduced signal crayfish Pacifastacus leniusculus, in a small, isolated Finnish lake, from 1968 to 1993. Aquatic Living Resources, 12, 387–401.

    Kouba, A., Buřič, M. & Petrusek, A. (2015) Crayfish species in Europe. In: Kozák, P., Ďuriš, Z., Petrusek, A., Buřič, M., Horká, I., Kouba, A., Kozubíková–Balcarová, E. & Policar, T. (Eds.), Crayfish biology and culture. University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, Vodňany, Czech Republic, pp. 81–163.

    Kouba, A., Petrusek, A. & Kozák, P. (2014) Continental-wide distribution of crayfish species in Europe: Update and maps. Knowledge and Management of Aquatic Ecosystems, 413, 1–31.

    Kovács, T. & Juhász, P. (2007) Data to the distribution of crayfish worms (Branchiobdellidae) in Hungary. Folia Historico-Naturalia Musei Matraensis, 31, 77–79.

    Kozák, P., Policar, T., Buřič, M. & Kouba, A. (2015) Monitoring of crayfish appearance. In: Kozák, P., Ďuriš, Z., Petrusek, A., Buřič, M., Horká, I., Kouba, A., Kozubíková-Balcarová, E. & Policar, T. (Eds.), Crayfish biology and culture. University of South Bohemia in České Budějovice, Faculty of Fisheries and Protection of Waters, Vodňany, Czech Republic, pp. 367–391.

    Larson, E.R. & Williams, B.W. (2016) Historical biogeography of Pacifastacus crayfishes and their branchiobdellian and entocytherid ectosymbionts in western North America. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. Boca Raton, CRC Press, 404–447.

    Laurent, P.J. (2007) A French population of Pacifastacus leniusculus bears the North American parasite branchiobdellidan ectosymbiont Xironogiton victoriensis. Crayfish News: IAA News letter, 29, 5–6.

    Lecaplain, B. & Noël, F. (2015) Branchiobdellidées et Hirudinées du Nord-Ouest de la France, 24 pp. Available from:,NOEL-manuel_hirudin%c3%a9s_NOFrance_V2_Juillet2015.pdf (accessed 25 January 2017)

    Lévêque, C. (1997) Introductions de nouvelles espèces de poissons dans les eaux douces tropicales: objectifs et conséquences. Knowledge and Management of Aquatic Ecosystems, 344–345, 9–91.

    Longshaw, M. (2011) Diseases of crayfish: A review. Journal of Invertebrate Pathology, 106, 54–70.

    Martens, A., Grabow, K., Rapp, S. & Schoolmann, G. (2006) Der Krebsegel Xironogiton victoriensis wurde mit dem Signalkrebs Pacifastacus leniusculus auch nach Deutschland eingeschleppt (Annelida: Branchiobdellida; Crustacea: Astacidae). Lauterbornia, 58, 147–145.

    Martín-Torrijos, L., Gelder, S.R. & Diéguez-Uribeondo, J. (2018) A new kid in town: First case of an alien worm, Xironogiton victoriensis (Annelida: Clitellata) on a native European freshwater crayfish. Aquaculture, 496, 39–42.

    Nesemann, H. & Neubert, E. (1999) Süßwasserfauna von Mitteleuropa. Bd. 6 Annelida. 2. Clitellata: Branchiobdellida, Acanthobdellea, Hirudinea. Spectrum Akademischer Verlag GmbH, Heidelberg, Berlin, 192 pp.

    Odier, A. (1823) Mémoire sur le Branchiobdelle, nouveau genre d’Annélides de la famille des Hirudinées. Mémoires de la Société d’histoire naturelle de Paris, 1, 69–78.

    Ohtaka, A., Gelder, S.R. & Smith, R.J. (2017) Long-anticipated new records of an ectosymbiotic branchiobdellidan and an ostracod on the North American red swamp crayfish, Procambarus clarkii (Girard, 1852) from an urban stream in Tokyo, Japan. Plankton & Benthos Research, 12, 123–128.

    Oscoz, J., Tomás, P. & Durán, C. (2010) Review and new records of non-indigenous freshwater invertebrates in the Ebro River basin (Northeast Spain). Aquatic Invasions, 5, 263–284.

    Petrusek, A., Filipová, L., Kozubíková-Balcarová, E. & Grandjean, F. (2017) High genetic variation of invasive signal crayfish in Europe reflects multiple introductions and secondary translocations. Freshwater Science, 36, 838–850.

    Quaglio, F., Fioravanti, M.L., Gelder, S.R., Giannetto, S., Trentini, M., Nobile, L, Maxia, M. & Morolli, C. (2002) Infestation of the branchiobdellidan, Xironogiton victoriensis (Annelida, Clitellata), on the signal crayfish (Pacifastacus leniusculus) from Auenbachl Creek, Alto Adige/Süd Tyrol, Italy. Freshwater Crayfish, 13, 274–279.

    Quaglio, F., Trentini, M., Mazzoni, D. & Nobile, L. (1999) Observations on Temnocephalid (Platyhelminthes) ectosymbionts in Australian freshwater crayfish (Cherax destructor Clark) introduced in Italy. Freshwater Crayfish, 12, 335–342

    Scalici, M., Chiesa, S., Gherardi, F., Ruffini, M., Gibertini, G. & Nonnis Marzano, F. (2009) The new threat to Italian inland waters from the alien crayfish “gang”: the Australian Cherax destructor Clark, 1936. Hydrobiologia, 632, 341–345.

    Skelton, J., Farrell, K.J., Creed, R.P., Williams, B.W., Ames, C., Helms, B.S., Stoekel, J. & Brown, B.L. (2013) Servants, scoundrels, and hitchhikers: current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida). Freshwater Science, 32 (4), 1345–1357.

    Subchev, M.A. (2008) Branchiobdellidans (Annelida: Clitellata) found in the crayfish and annelid collections of the French National Museum of Natural History (Paris), and on recently collected crayfishes from France. Acta zoologica Bulgarica, 60, 233–237.

    Subchev, M.A. (2014) The genus Branchiobdella Odier, 1823 (Annelida, Clitellata, Branchiobdellida): A review of its European Species. Acta Zoologica Bulgarica, 66 (1), 5–20.

    Subchev, M.A. (2016) First report of Branchiobdella Odier, 1923 from Belgium. Acta Zoologica Bulgarica, 68 (1), 141–143.

    Timm, T. (1991) Branchiobdellida (Oligochaeta) from the farthest South-East of the U.S.S.R. Zoologica Scripta, 20, 321–331.

    Vayssière, A. (1898) Description du Temnocephala mexicana, nov. sp. Annales de la Faculté des Sciences de Marseille, 8, 227–235.

    Vedia, I., Oscoz, J., Rueda, J., Miranda, R., García-Roger, E.M., Baquero, E. & Gelder, S.R. (2014) An alien ectosymbiotic branchiobdellidan (Annelida: Clitellata) adopting exotic crayfish: a biological co-invasion with unpredictable consequences. Inland Waters, 5, 89–92.

    Vogt, G. (1999) Disease of European freshwater crayfish, with particular emphasis on interspecific transmission of pathogens. In: Gherardi, F. & Holdich, D.M. (Eds.), Crayfish in Europea as alien species. How to make the best of a bad situation? A.A. Balkema, Brookfield, pp. 87–103.