Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-07-10
Page range: 78–93
Abstract views: 261
PDF downloaded: 105

Haplotaxis gordioides (Hartmann in Oken, 1819) (Annelida, Clitellata) as a sub-cosmopolitan species: a commonly held view challenged by DNA barcoding

Royal Belgian Institute of Natural Sciences, Taxonomy and Phylogeny, 29 rue Vautier, B-1000 Brussels, Belgium
EAWAG: Swiss Federal Institute of Aquatic Science and Technology, Department of Aquatic Ecology, Überlandstrasse 133, CH8600 Dübendorf, Switzerland, Department of Evolutionary Biology and Environmental studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
EAWAG: Swiss Federal Institute of Aquatic Science and Technology, Department of Aquatic Ecology, Überlandstrasse 133, CH8600 Dübendorf, Switzerland, Department of Evolutionary Biology and Environmental studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
EAWAG: Swiss Federal Institute of Aquatic Science and Technology, Department of Aquatic Ecology, Überlandstrasse 133, CH8600 Dübendorf, Switzerland, Department of Evolutionary Biology and Environmental studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
Swiss Center for Applied Ecotoxicology (Ecotox Center), EPFL ENAC IIE-GE, 1015 Lausanne, Switzerland
Swiss Center for Applied Ecotoxicology (Ecotox Center), EPFL ENAC IIE-GE, 1015 Lausanne, Switzerland
aquatic oligochaetes Clitellata Haplotaxis gordioides DNA barcoding diversity


Haplotaxis Hoffmeister, 1843 is a poorly known genus: it is rarely collected because it usually inhabits groundwater, and many species are only known from immature specimens. Even the type species, Haplotaxis gordioides (Hartmann in Oken, 1819) remains poorly defined because of the absence of reference types. Most of the Haplotaxis species have been placed in synonymy with H. gordioides since the end of the 19th century, a situation that has remained essentially unchanged until now. As a result, the species is supposedly present on all continents, except Antarctica. This observation is all the more questionable as the aquatic subterranean environment is nowadays well known to harbour many species with restricted distribution, due to the strong hydrogeographic isolation and the low dispersal abilities of its inhabitants.

In this study we assessed the hypothesis of H. gordioides as a single species with wide distribution versus a complex of cryptic species with narrow distribution. We used a DNA-barcoding approach based on the COI mitochondrial marker of 46 Haplotaxis specimens collected in Switzerland, mostly as part of a countrywide sampling campaign to study groundwater macroinvertebrates.

Preliminary results suggested that H. gordioides is a complex of at least 6 cryptic species in Switzerland, which has important implications both for the knowledge of the exact identity of the type species and for the synonymy of most of the species described in the 19th century. However, as it is based on a single-locus approach, this study should be seen as the first step in an integrative taxonomic process that should include additional biological material, the study of complementary markers (especially nuclear), and the morphological study of specimens.


  1. Ahrens, D., Fujisawa, T., Krammer, H.J., Eberle, J., Fabrizi, S. & Vogler, A.P. (2016) Rarity and Incomplete Sampling in DNA-Based Species Delimitation. Systematic Biology, 65, 3, 478–494.

  2. Altermatt, F., Alther, R., Fišer, C., Jokela, J., Konec, M., Küry, D., Mächler, E., Stucki, P. & Westram, A.M. (2014) Diversity and distribution of freshwater amphipod species in Switzerland (Crustacea: Amphipoda). PLOS ONE, 9, 10, e110328.

  3. Altermatt, F., Alther, R., Fišer, C. & Švara, V. (2019) Die Amphipoden der Schweiz (Vol. 32). Neuchâtel: CSCF & SEG, 392 pp.

  4. Alther, R., Bongni, N., Borko, Š., Fišer, C. & Altermatt, F. (2020) Reiche Grundwasser-Fauna. Aqua & Gas, 7/8, 36–42.

  5. Alther, R., Bongni, N., Borko, Š., Fišer, C. & Altermatt, F. (2021) Citizen science approach reveals groundwater fauna in Switzerland and a new species of Niphargus (Amphipoda, Niphargidae). Subterranean Biology, 39, 1–31.

  6. Artheau, M. & Giani, N. (2006) A checklist of the groundfreshwater Oligochaeta and Polychaeta in France : an overview. Bulletin de l’Institut Royal des Sciences Naturelles de Belgique, Biologie, 76, 229–255.

  7. Borko, Š., Trontelj, P., Seehausen, O., Moškrič, A. & Fišer, C. (2021) A subterranean adaptive radiation of amphipods in Europe. Nature Communications, 12, 1, 3688.

  8. Bouckaert, R., Vaughan, T. G., Barido-Sottani, J., Duchene, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D., De Maio, N., Matschiner, M., Mendes, F.K., Müller, N.F., Ogilvie, H.A., du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D., Siveroni, I., Suchard, M.A., Wu, C.-H., Xie, D., Zhang, C., Stadler, T. & Drummond, A.J. (2019) BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 15, 4, e1006650.

  9. Brinkhurst, R.O. (1966) A taxonomic revision of the family Haplotaxidae (Oligochaeta). Journal of Zoology, Proceedings of the Zoological Society of London, 150, 29–51.

  10. Brinkhurst, R.O. (1984) The position of the Haplotaxidae in the evolution of oligochaete annelids. Hydrobiologia, 115, 25–36.

  11. Brinkhurst, R.O. (1988) A taxonomic analysis of the Haplotaxidae (Annelida, Oligochaeta). Canadian Journal of Zoology, 66, 2243–2252.

  12. Brinkhurst, R.O. (1994) Evolutionary relationships within the Clitellata : an update. Megadrilogica, 5 (10), 109–112.

  13. Brinkhurst, R.O. & Jamieson, B.G.M. (1971) Aquatic Oligochaeta of the World. Edinburgh: Oliver and Boyd, 860 pp.

  14. Dellicour, S. & Flot, J.F. (2018) The hitchhiker’s guide to single-locus species delimitation. Molecular Ecology Resources, 18, 6, 1234–1246.

  15. Dinerstein, E., Olson, D., Joshi, A., Vynne, C., Burgess, N.D., Wikramanayake, E., Hahn, N., Palminteri, S., Hedao, P., Noss, R., Hansen, M., Locke, H., Ellis, E.C., Jones, B., Barber, C.V., Hayes, R., Kormos, C., Martin, V., Crist, E., Sechrest, W., Price, L., Baillie, J.E.M., Weeden, D., Suckling, K., Davis, C., Sizer, N., Moore, R., Thau, D., Birch, T., Potapov, P., Turubanova, S., Tyukavina, A., de Souza, N., Pintea, L., Brito, J.C., Llewellyn, O.A., Miller, A.G., Patzelt, A., Ghazanfar, S.A., Timberlake, J., Klöser, H., Shennan-Farpón, Y., Kindt, R., Lillesø, J.P.B., van Breugel, P., Graudal, L., Voge, M., Al-Shammari, K.F. & Saleem, M. (2017) An Ecoregion-Based Approach to Protecting Half the Terrestrial Realm. BioScience, 67, 6, 534–545.

  16. Dole-Olivier, M.-J., Malard, F., Ferreira, D. & Gibert, J. (2005) Biodiversité dans les eaux souterraines. La Houille Blanche, 3, 39–44.

  17. Erséus, C., Williams, B.W., Horn, K.M., Halanych, K.M., Santos, S.R., James, S.W., des Châtelliers, M.C. & Anderson, F.E. (2020) Phylogenomic analyses reveal a Palaeozoic radiation and support a freshwater origin for clitellate annelids. Zoologica Scripta, 49, 5, 614–640.

  18. Ezard, T., Fujisawa, T. & Barraclough, T.G. (2021) Splits: species limits by threshold statistics (version 1.0-20). Available from: (accessed 6 December 2022)

  19. Fišer, C., Alther, R., Zaksek, V., Borko, S., Fuchs, A. & Altermatt, F. (2018) Translating Niphargus barcodes from Switzerland into taxonomy with a description of two new species (Amphipoda, Niphargidae). Zookeys, 760, 113–141.

  20. (4 November 2022) GBIF Occurrence Download: Haplotaxis gordioides (Hartmann, 1819).

  21. (4 November 2022) GBIF Occurrence Download: Haplotaxis spp.).

  22. Gibert, J., Culver, D.C., Dole-Olivier, M.-J., Malard, F., Christman, M.C. & Deharveng, L. (2009) Assessing and conserving groundwater biodiversity : synthesis and perspectives. Freshwater Biology, 54, 930–941.

  23. Gibert, J., Danielopol, D.L. & Stanford, J.A. (1994) Groundwater ecology. Academic Press, San Diego, California, 571 pp.

  24. Gibert, J., Stanford, J.A., Dole-Olivier, M.-J. & Ward, J.V. (1994) Basic attributes of groundwater ecosystems and prospects for research. In: Gibert, J., Danielopol, D.L. & Stanford, J.A. (Eds.), Groundwater Ecology. Academic Press, San Diego, pp. 7–40.

  25. Goulpeau, A., Penel, B., Maggia, M.-E., Marchán, D.F., Steinke, D., Hedde, M. & Decaëns, T. (2022) OTU Delimitation with Earthworm DNA Barcodes: A Comparison of Methods. Diversity, 14, 10.

  26. Hartmann, G.L. (1821) Beyträge zur Geschichte der Fadenwürmer, nebst Beschreibung einer bisher mit ihnen verwechselten Art von Regenwurm, Lumbricus Gordioides. Der Schweizerischen Gesellschaft für die gesammten Naturwissenschaften vorgelesen den 28 Junius 1819 von G. L. Hartmann. Neue Alpina, 1, 32–50.

  27. Hebert, P.D.N., Cywinska, A., Ball, S.L. & de Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B, 270, 313–321.

  28. Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35, 2, 518–522.

  29. Hoffmeister, W. (1843) Beitrag zur Kenntnis deutscher Landanneliden. Archiv für Naturgeschichte, 9, 1, 183–198.

  30. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 6, 587–589.

  31. Liu, Y., Fend, S.V., Martinsson, S. & Erséus, C. (2017) Extensive cryptic diversity in the cosmopolitan sludge worm Limnodrilus hoffmeisteri (Clitellata, Naididae). Organisms Diversity & Evolution, 1–19.

  32. Luo, A., Ling, C., Ho, S.Y.W. & Zhu, C.D. (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology, 67 (5), 830–846.

  33. Martin, P., Lagnika, M., Sonet, G. & Ibikounle, M. (2017) DNA barcoding and diversity of groundwater oligochaetes in Benin (West Africa). Scientific abstracts of the 7th International Barcode of Life Conference. Genome, 60, 11, 971.

  34. Martin, P. & Ohtaka, A. (2008) A new phreodrilid species (Annelida: Clitellata: Phreodrilidae) from Lake Biwa, Japan. Species Diversity, 13, 221–230.

  35. Michaelsen, W. (1899) Beiträge zur Kenntnis der Oligochäten. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Thiere., 12, 105–144.

  36. Michaelsen, W. (1905) Die Oligochaeten des Baikal-Sees. Wissenschaftliche Ergebnisse einer Zoologischen Expedition nach dem Baikal-See unter Leitnung des Professors Alexis Korotneff in den Jahren 1900 - 1902. Kiew und Berlin: Commissions-Verlag von R. Friedländer & Sohn, 69 pp.

  37. Nguyen, L.T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 1, 268–274.

  38. Oken, L. (1819) Versammlung der Schweizer Naturforscher zu St. Gallen, vom 26, 27. und 28. Julius 1819. In: Oken, L. (Ed.), Isis oder Encyclopädische Zeitung von Oken. Litterarischer Anzeiger, Nr. XLV. Erster Band, Heft I-VI, Jena, pp. 178–179.

  39. Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-Based Species Delimitation for the DNA Taxonomy of Undescribed insects. Systematic Biology, 55, 4, 1–15.

  40. Puillandre, N., Brouillet, S. & Achaz, G. (2021) ASAP: assemble species by automatic partitioning. Molecular Ecology Resources, 21, 2, 609–620.

  41. Rambaut, A., Suchard, M.A., Xie, W. & Drummond, A.J. (2021) Tracer v1.7.2. Available from: (accessed 6 December 2022)

  42. Schmelz, R.M., Beylich, A., Boros, G., Dózsa-Farkas, K., Graefe, U., Hong, Y., Römbke, J., Schlaghamerský, J. & Martinsson, S. (2017) How to deal with cryptic species in Enchytraeidae, with recommendations on taxonomical descriptions. Opuscula Zoologica Budapest, 48, Suppl. 2, 45–51.

  43. Schminke, H.K. & Gad, G. (2007) Grundwasser Deutschlands. Ein Bestimmungswerk: Deutsche Vereinigung für Wasserwirtschaft, Abwasser und Abfall (Verlag), 628 pp.

  44. Studer, A., Knüsel, M., Alther, R., Hürlemann, S. & Altermatt, F. (2022) Erfassung der Grundwasserflohkrebse. Studie zur Artenvielfalt und Verbreitung im Einzugsgebiet der Töss. Aqua & Gas, 102, 4, 14–19.

  45. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38, 7, 3022–3027.

  46. Timm, T. & Martin, P.J. (2015) Chapter 21 - Clitellata: Oligochaeta. In: Thorp, J.H. & Rogers, D.C. (Eds.), Thorp and Covich’s Freshwater Invertebrates (Fourth Edition). Academic Press, Boston, pp. 529–549.

  47. Tkach, V.V. & Pawłowski, J. (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica, 44, 147–148.

  48. Trontelj, P., Douady, C.J., Fišer, C., Gibert, J., Gorički, Š., Lefébure, T., Sket, B. & Zakšek, V. (2009) A molecular test for cryptic diversity in ground water : how large are the ranges of macro-stygobionts? Freshwater Biology, 54, 727–744.

  49. Vivien, R., Apothéloz-Perret-Gentil, L., Pawlowski, J., Werner, I., Lafont, M. & Ferrari, B.J.D. (2020) High-throughput DNA barcoding of oligochaetes for abundance-based indices to assess the biological quality of sediments in streams and lakes. Scientific Reports, 10, 1, 2041.

  50. Vivien, R., Holzmann, M., Werner, I., Pawlowski, J., Lafont, M. & Ferrari, B.J.D. (2017) Cytochrome c oxidase barcodes for aquatic oligochaete identification: development of a Swiss reference database. PeerJ, 5, e4122.

  51. Vivien, R., Lafont, M., Werner, I., Laluc, M. & Ferrari, B.J.D. (2019) Assessment of the effects of wastewater treatment plant effluents on receiving streams using oligochaete communities of the porous matrix. Knowledge & Management of Aquatic Ecosystems, 420, 18.