Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2025-02-19
Page range: 190-200
Abstract views: 70
PDF downloaded: 27

A report of the unusual presence of Haplotaxis cf. gordioides in a terrestrial subsoil and first isotopic analysis of its trophic position

Department of Soil Science and Agrophysics; Faculty of Agriculture and Economics; University of Agriculture in Krakow; Krakow; Poland
Royal Belgian Institute of Natural Sciences; Taxonomy and Phylogeny (RBINS); 29 rue Vautier; 1000-Brussels; Belgium
School of Agriculture and Food Science; University College Dublin; Belfield; Dublin 4; Ireland
Annelida Clitellata Luvisol

Abstract

Haplotaxis is a genus of aquatic oligochaetes for which only limited information is available on its taxonomy, distribution, habitat and diet. During a soil survey in southern Poland, specimens of Haplotaxis cf. gordioides were unexpectedly found in terrestrial mineral subsoils, isolated from any apparent water source. This discovery provides an opportunity to investigate two aspects of Haplotaxis: habitat and diet. For the first time, the predatory nature of Haplotaxis has been assessed using stable isotope analysis of carbon and nitrogen and compared with detritivorous worms. In addition, the natural habitat of this genus was reconsidered through a literature review. This new terrestrial record raises questions about the habitat preference of Haplotaxis, suggesting that their rare soil presence may be due to challenges of extraction rather than actual absence. The finding highlights our limited understanding and exploration of subsoil fauna, including macrofauna. It also provides the first independent evidence for the predatory behaviour of Haplotaxis.

 

References

  1. Abarenkov, K., Tedersoo, L., Nilsson, R.H., Vellak, K., Saar, I., Veldre, V., Parmasto, E., Prous, M., Aan, A., Ots, M., Kurina, O., Ostonen, I., Jõgeva, J., Halapuu, S., Põldmaa, K., Toots, M., Truu, J., Larsson, K.-H. & Kõljalg, U. (2010) PlutoF—a Web Based Workbench for Ecological and Taxonomic Research, with an Online Implementation for Fungal ITS Sequences. Evolutionary Bioinformatics, 6, EBO.S6271. https://doi.org/10.4137/EBO.S6271
  2. Aquilina, L., Stumpp, C., Tonina, D. & Buffington, J.M. (2023) Hydrodynamics and geomorphology of groundwater environments. In: Groundwater Ecology and Evolution. Academic Press, San Diego, California, pp. 3–37. https://doi.org/10.1016/B978-0-12-819119-4.00014-7
  3. 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.
  4. Birkhofer, K., Bylund, H., Dalin, P., Ferlian, O., Gagic, V., Hambäck, P.A., Klapwijk, M., Mestre, L., Roubinet, E., Schroeder, M., Stenberg, J.A., Porcel, M., Björkman, C. & Jonsson, M. (2017) Methods to identify the prey of invertebrate predators in terrestrial field studies. Ecology and Evolution, 7 (6), 1942–1953. [PMID: 28331601, PMCID: PMC5355183] https://doi.org/10.1002/ece3.2791
  5. Brinkhurst, R.O. & Marchese, M.R. (1987) A contribution to the taxonomy of the aquatic Oligochaeta (Haplotaxidae, Phreodrilidae, Tubificidae) of South America. Canadian Journal of Zoology, 65, 3154–3165. https://doi.org/10.1139/z87-474
  6. Brinkhurst, R.O. & McKey-Fender, D. (1991) The anatomy of the pharynx of two predatory aquatic oligochaetes. Canadian Journal of Zoology, 69, 669–675. https://doi.org/10.1139/z91-098
  7. Brinkhurst, R.O. (1988) A taxonomic analysis of the Haplotaxidae (Annelida, Oligochaeta). Canadian Journal of Zoology, 66, 2243–2252. https://doi.org/10.1139/z88-332
  8. Cernosvitov, L. (1939) Etudes biospeologiques. X (1). Catalogue des oligochètes hypogés. Bulletin du Musée royal d'Histoire naturelle de Belgique, XV (22), 1–92.
  9. Creuzé des Châtelliers, M., Juget, J., Lafont, M. & Martin, P. (2009) Subterranean aquatic Oligochaeta. Freshwater Biology, 54, 678–690. https://doi.org/10.1111/j.1365-2427.2009.02173.x
  10. Dole, M. J. (1983) Le domaine aquatique souterrain de la plaine alluviale du Rhône à l'est de Lyon. I. Diversité hydrologique et biocénotique de trois stations représentatives de la dynamique fluviale. Vie et Milieu, 33 (3–4), 219–229.
  11. Dole-Olivier, M.J., Creuzé des Châtelliers, M., Galassi, D.M.P., Lafont, M., Mermillod-Blondin, F., Paran, F., Graillot, D., Gaur, S. & Marmonier, P. (2022) Drivers of functional diversity in the hyporheic zone of a large river. Science of the Total Environment, 843, 156985. https://doi.org/10.1016/j.scitotenv.2022.156985
  12. Dugès, A. (1837) Nouvelles observations sur la zoologie et l'anatomie des Annelides abranches sétigères. Annales des Sciences Naturelles, Zoologie, 2 (8), 15–35.
  13. Dumnicka, E. Galas, J. Krodkiewska, M. & Pociecha, A. (2020) The diversity of annelids in subterranean waters: A case study from Poland. Knowledge and Management of Aquatic Ecosystems, 421 (16), 1–11. https://doi.org/10.1051/kmae/2020007
  14. Eberhard, S.M., Halse, S.A. & Humphreys, W.F. (2005) Stygofauna in the Pilbara region, north-west Western Australia: a review. Journal of the Royal Society of Western Australia, 88, 167–176.
  15. Erséus, C. (2005) Haplotaxis gordioides – oväntat fynd i Sverige av en sällsynt ringmask [Haplotaxis gordioides - unexpected discovery in Sweden of a rare ringworm]. Fauna och Flora, 100 (4), 42–43.
  16. Forbes, S.A. (1890) On an American earthworm of the family Phreoryctidae. Bulletin of the Illinois State Laboratory of Natural History, 3, 107–116. https://doi.org/10.21900/j.inhs.v3.189
  17. Gates, G.E. (1971) On a new species of California earthworm, Haplotaxis ichthyophagous (Oligochaeta, Annelida). Proceedings of the Biological Society of Washington, 84 (25), 203–212.
  18. Giard, A. (1889) Sur l'habitat de Phreoryctes Menkeanus Hoffm. Bulletin scientifique de la France et de la Belgique, 1889, 171.
  19. Giard, A. (1894) Sur un nouveau ver de terre de la famille des Phreoryctidae (Phreoryctes endeca Gd.). Comptes Rendus Académie des Sciences de Paris, 118, 811–814.
  20. Gibert, J. & Deharveng, L. (2002) Subterranean Ecosystems : A Truncated Functional Biodiversity. BioScience, 52 (6), 473–481. https://doi.org/10.1641/0006-3568(2002)052[0473:SEATFB]2.0.CO;2
  21. Gibert, J., Danielopol, D.L. & Stanford, J.A. (1994) Groundwater ecology. Academic Press, San Diego, California, 571 pp.
  22. 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.
  23. Hesse, E. (1923) Sur l'habitat de Haplotaxis gordioides G. L. Hartmann. Bulletin de la Société Zoologique de France, 48 (1), 138–140.
  24. Hoffmeister, W. (1843) Beitrag zur Kenntnis deutscher Landanneliden. Archiv für Naturgeschichte, 9 (1–2), 183–198.
  25. Hoffmeister, W. (1845) Bie bis jetzt bekannten Arten aus der Familie der Regenwürmer. Als Grundlage zu einer Monographie dieser Familie. Friedriech Vieweg und Sohn, Braunschweig, 43 pp.
  26. Holmstrup, M., Slotsbo, S., Henriksen, P.G. & Bayley, M. (2016) Earthworms accumulate alanine in response to drought. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 199, 8–13. https://doi.org/10.1016/J.CBPA.2016.04.015
  27. Hrabě, S. (1931) Die Oligochaeten aus den Seen Ochrida und Prespa. Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere, 61 (1/2), 1-62.
  28. Hüppop, K. (2012) Adaptation to low food. In: Encyclopedia of caves. Academic Press, Elsevier, Whaltham, pp. 1–9. https://doi.org/10.1016/B978-0-12-383832-2.00001-3
  29. Hyodo, F. (2015) Use of isotope in insect trophic ecology. Entomological Science, 18, 295–312. https://doi.org/10.1111/ens.12128
  30. Kasprzak, K. (1979) Skąposzczety (Oligochaeta) Pienin. 2 Naididae, Tubificidae, Haplotaxidae, Lumbriculidae, Branchiobdellidae, XXIV. Fragmenta Faunistica, 24, 1–24. https://doi.org/10.3161/00159301FF1979.24.2.057
  31. Lafont, M., Durbec, A. & Ille, C. (1992) Oligochaete worms as biological describers of the interactions between surface and groundwaters: a first synthesis. Regulated Rivers: Research & Management, 7, 65–73. https://doi.org/10.1002/rrr.3450070109
  32. Leruth, R. (1939) La biologie du domaine souterrain et la faune cavernicole de la Belgique (Mémoires du Musée royal d'Histoire naturelle de Belgique ed. Vol. Mémoire No 87. Musée royal d’Histoire naturelle de Belgique, Bruxelles, 506 pp.
  33. Leuckart, R. (1861) Bericht über die wissenschaftlichen Leistungen in der Naturgeschichte der niederen Thiere während des Jahres 1859. Archiv für Naturgeschichte, 26 (2), 103–264.
  34. Leydig, F. (1865) Ueber Phreoryctes Menkeanus Hofm. nebst bemerkungen über den bau anderer Anneliden. Archiv für mikroskopische Anatomie, 1, 249–294. https://doi.org/10.1007/BF02961416
  35. Liu, Y. & Erséus, C. (2017) New specific primers for amplification of the Internal Transcribed Spacer region in Clitellata (Annelida). Ecology and Evolution, 7 (23), 10421–10439. https://doi.org/10.1002/ece3.3212
  36. Martin, P.J., Fend, S.V., Klinth, M.J., Martinsson, S., Torii, T. & Erséus, C. (2024) Towards an integrative revision of Haplotaxidae (Annelida: Clitellata). Zoological Journal of the Linnean Society, 202 (4), zlae141. https://doi.org/10.1093/zoolinnean/zlae141
  37. Martin, P., Knüsel, M., Alther, R., Altermatt, F., Ferrari, B. & Vivien, R. (2023) Haplotaxis gordioides (Hartmann in Oken, 1819) (Annelida, Clitellata) as a sub-cosmopolitan species: a commonly held view challenged by DNA barcoding. Zoosymposia, 23, 78–93. https://doi.org/10.11646/zoosymposia.23.1.10
  38. Martin, P., Martínez-Ansemil, E., Pinder, A., Timm, T. & Wetzel, M.J. (2008) Global diversity of oligochaetous clitellates ("Oligochaeta"; Clitellata) in freshwater. Hydrobiologia, 595, 117–127. https://doi.org/10.1007/s10750-007-9009-1
  39. Michaelsen, W. (1899) Beiträge zur Kenntnis der Oligochäten. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Thiere, 12, 105–144. https://doi.org/10.5962/bhl.part.2028
  40. 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. Commissions-Verlag von R. Friedländer & Sohn, Kiew und Berlin, 69 pp.
  41. Michaelsen, W. (1932) Ein neuer Phreoryctes von der Tropeninsel Poeloe Berhala. Miscellanea Zoologica Sumatrana, 71, 1–7.
  42. Noll, F.C. (1874) Ueber einen neuen Ringelwurm des Rheins. Archiv für Naturgeschichte, 40, 1, 260–270.
  43. O’Connor, F.B. (1962) The extraction of Enchytraeidae from soil. Progress in Soil Zoology, 1962, 279–285.
  44. Pleşa, C., Botea, F. & Racoviţă, G. (1964) Cercetări asupra faunei biotopurilor acvatice subterane din bazinul Crişului Repede [Research on the fauna of subterranean aquatic biotopes in the Criș Repede basin]. Lucrările Institutului de Speologie "Emil Racoviţă", 3, 367–396.
  45. Robertson, A., Brancelj, A., Stein, H. & Hahn, H.J. (2023) Classifying groundwater ecosystems. In: Malard, F., Griebler, C. & Rétaux, S. (Eds.), Groundwater Ecology and Evolution. Academic Press, San Diego, California, pp. 39–60. https://doi.org/10.1016/B978-0-12-819119-4.00007-X
  46. Schlotthauber, C. (1860) Beiträge zur Helminthologie. Amtlicher Bericht über die Versammlung Deutscher Naturforscher und Aerzte, Göttingen, 34, 121–133.
  47. Schmidt, O., Curry, J.P., Dyckmans, J., Rota, E. & Scrimgeour, C.M. (2004) Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. Pedobiologia, Jena, 48, 171–180. https://doi.org/10.1016/j.pedobi.2003.12.003
  48. Semernoy, V.P. (2004) Oligochaeta of Lake Baikal. Nauka, Novosibirsk, 528 pp.
  49. Stegman, L.C. (1960) A preliminary survey of earthworms of the Tully forest in central New York. Ecology, 41 (4), 779–782. https://doi.org/10.2307/1931812
  50. Stephenson, J. (1930) The Oligochaeta. Oxford University Press, Oxford, 978 pp.
  51. Tétry, A. (1938) Contribution à l’étude de la faune de l’Est de la France. Imprimerie Georges Thomas, Nancy, 453 pp.
  52. Tétry, A. (1940) Les oligochètes de Belgique. Bulletin du Musée royal d’Histoire naturelle de Belgique, 16 (31), 1–24.
  53. Thienemann, A. (1912) Der Bergbach des Sauerlandes. Faunistischbiologische Untersuchungen. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 1912, 1–12.
  54. Thienemann, A. (1913) Die Salzwassertierwelt Westfalens. Verhandlungen der Deutschen Zoologischen Gesellschaft, 23, 56–68.
  55. Thienemann, A. (1928) Haplotaxis gordioides, G. L. Hartmann als terrestrischer Wurm. Archiv für Hydrobiologie, 19, 377.
  56. Timm, T. & Martin, P. (2019) Phylum Annelida. Class Clitellata: Subclass Oligochaeta. In: Rogers, D.C. & Thorp, J.H. (Eds.), Thorp and Covich's Freshwater Invertebrates. 4th Edition. Keys to Palaearctic Fauna. Academic Press, Boston, Massachusetts, pp. 364–482.
  57. Timm, T. & Martin, P.J. (2015) Chapter 21. Clitellata: Oligochaeta. In: Thorp, J.H. & Rogers, D.C. (Eds.), Thorp and Covich's Freshwater Invertebrates. 4th Edition. Academic Press, Boston, Massachusetts, pp. 529–549. https://doi.org/10.1016/B978-0-12-385026-3.00021-8
  58. Timm, T. (2023) A database of aquatic Oligochaeta (Annelida, Clitellata) with updated order names. Zoosymposia, 23, 35–40. https://doi.org/10.11646/zoosymposia.23.1.7
  59. Vandel, A. (1922) Sur la faune d'eau douce des Pyrénées orientales. Bulletin de la Société Zoologique de France, 47 (5), 163–170.
  60. Yamaguchi, H. (1937) Studies on the aquatic Oligochaeta of Japan. II. Occurrence of the subterranean oligochaete Haplotaxis gordioides (Hartmann) in Japan. Annotationes Zoologicae Japonenses, 16, 68–73.