, Volume 823, Issue 1, pp 49–65 | Cite as

Variation of Clitellata (Annelida) assemblages related to water saturation in groundwater-dependent wetlands

  • J. SchenkováEmail author
  • M. Bílková
  • V. Polášková
  • M. Horsák
  • J. Schlaghamerský
Primary Research Paper


Aquatic invertebrates of groundwater-dependent wetlands can be sensitive to a drop in the groundwater table, which is considered one of the possible impacts of climate change. We investigated whether aquatic clitellate species are able to dwell in waterlogged substrates without surface water, in 27 spring fens studied across the Western Carpathians. A total of 78 clitellate species were recorded in pairs of samples from aquatic and semi-aquatic habitats. Semi-aquatic habitats had 27 species in common with aquatic habitats, but algal and fungal feeders were less frequent and abundant, and predatory leeches and Haplotaxis gordioides completely lacking. Terrestrial enchytraeid species enriched the semi-aquatic assemblages. The main change in clitellate composition was controlled by total organic carbon. The importance of further variables, however, differed between aquatic and semi-aquatic sites. Further analyses of semi-aquatic sites showed that the distribution of primarily aquatic species was mainly driven by physical and chemical variables, while that of soil dwellers was driven by depth. Except Tubifex tubifex and Nais communis, all aquatic species preferred the uppermost layer. Results indicate that, during extreme droughts, when aquatic habitats cease to exist, some aquatic clitellates can persist in the waterlogged substrate, while some aquatic specialists may face the risk of local extinction.


Oligochaeta Hirudinida Spring fens Semi-aquatic sites Environmental gradients Depth distribution 



We would like to thank Vít Syrovátka and Marek Polášek for their help with the visualization of the results, and Ondřej Hájek for the preparation of the map. The study was supported by research grants of the Czech Science Foundation (GA15-15548S and GA16-03881S) and by the institutional support of the Masaryk University for PhD students.


  1. Barquín, J. & M. Scarsbrook, 2008. Management and conservation strategies for coldwater springs. Aquatic Conservation Marine and Freshwater Ecosystems 18: 580–591.CrossRefGoogle Scholar
  2. Bertrand, G., N. Goldscheider, J.-M. Gobat & D. Hunkeler, 2012. Review: from multi-scale conceptualization to a classification system for inland groundwater-dependent ecosystems. Hydrogeology Journal 20: 5–25.CrossRefGoogle Scholar
  3. Bojková, J., J. Schenková, M. Horsák & M. Hájek, 2011. Species richness and composition patterns of clitellate (Annelida) assemblages in the treeless spring fens: the effect of water chemistry and substrate. Hydrobiologia 677: 159–171.CrossRefGoogle Scholar
  4. Briones, M. J. I., P. Ineson & T. G. Piearce, 1997. Effects of climate change on soil fauna; responses of enchytraeids, Diptera larvae and tardigrades in a transplant experiment. Applied Soil Ecology 6: 117–134.CrossRefGoogle Scholar
  5. Cantonati, M., L. Füreder, R. Gerecke, I. Jüttner & E. J. Cox, 2012. Crenic habitats, hotspots for freshwater biodiversity conservation: toward an understanding of their ecology. Freshwater Science 31: 463–480.CrossRefGoogle Scholar
  6. Cragg, J. B., 1961. Some aspects of the ecology of moorland animals. Journal of Ecology 49: 477–506.CrossRefGoogle Scholar
  7. Dawson, T. P., P. M. Berry & E. Kampa, 2003. Climate change impacts on freshwater wetland habitats. Journal for Nature Conservation 11: 25–30.CrossRefGoogle Scholar
  8. Dumnicka, E., 2000. Studies on Oligochaeta taxocens in streams, interstitial and cave waters of southern Poland with remarks on Aphanoneura and Polychaeta distribution. Acta Zoologica Cracoviensia 43: 339–392.Google Scholar
  9. Dumnicka, E., 2001. Some remarks on the origin of stygobiontic oligochaetes. Mémoires de Biospéleologie 28: 39–45.Google Scholar
  10. Erman, D. C. & N. A. Erman, 1975. Macroinvertebrate composition and production in some Sierra Nevada minerotrophic peatlands. Ecology 56: 591–603.CrossRefGoogle Scholar
  11. Erséus, C., M. J. Wetzel & L. Gustavsson, 2008. ICZN rules—a farewell to Tubificidae (Annelida, Clitellata). Zootaxa 1744: 66–68.CrossRefGoogle Scholar
  12. ESRI, 2003. ArcGIS 8.3. Environmental Systems Research Institute, Redlands, CA, USA,
  13. Giere, O., 1993. Meiobenthology, the Microscopic Fauna in Aquatic Sediments. Springer, Berlin Heidelberg.Google Scholar
  14. Glazier, D. S., 1991. The fauna of North American temperate cold springs: patterns and hypotheses. Freshwater Biology 26: 527–542.CrossRefGoogle Scholar
  15. Gower, J. C., 1975. Generalized procrustes analysis. Psychometrika 40: 33–51.CrossRefGoogle Scholar
  16. Graefe, U. & R. M. Schmelz, 1999. Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids. In Schmelz R. M. & Sühlo K. (eds), Proceedings of the 3rd International Symposium on Enchytraeidae, Osnabrück, Germany: 3–4 July 1998, Universitätsverlag Rasch, Osnabrück (Newsletter on Enchytraeidae 6): 59–67.Google Scholar
  17. Green, T. R., M. Taniguchi, H. Kooi, J. J. Gurdak, D. M. Allen, K. M. Hiscock, H. Treidel & A. Aureli, 2011. Beneath the surface of global change: impacts of climate change on groundwater. Journal of Hydrology 405: 532–560.CrossRefGoogle Scholar
  18. Hájek, M. & P. Hekera, 2004. Can seasonal variation in fen water chemistry influence the reliability of vegetation-environment analyses? Preslia 76: 1–14.Google Scholar
  19. Hájek, M., P. Hekera & P. Hájková, 2002. Spring fen vegetation and water chemistry in the Western Carpathian flysch zone. Folia Geobotanica 37: 205–224.CrossRefGoogle Scholar
  20. Hájek, M., P. Hájková, K. Rybníček & P. Hekera, 2005. Present vegetation of spring fens and its relation to water chemistry. In Poulíčková, A., M. Hájek & K. Rybníček (eds), Ecology and Palaeoecology of Spring Fens of the West Carpathians. Palacký University, Olomouc: 69–96.Google Scholar
  21. Hájek, M., M. Horsák, P. Hájková & D. Dítě, 2006. Habitat diversity of central European fens in relation to environmental gradients and an effort to standardise fen terminology in ecological studies. Perspectives in Plant Ecology, Evolution and Systematics 8: 97–114.CrossRefGoogle Scholar
  22. Hannigan, E. & M. Kelly-Quinn, 2012. Composition and structure of macroinvertebrate communities in contrasting open-water habitats in Irish peatlands: implications for biodiversity conservation. Hydrobiologia 692: 19–28.CrossRefGoogle Scholar
  23. Healy, B., 1987. The depth distribution of Oligochaeta in an Irish quaking marsh. Hydrobiologia 155: 235–247.CrossRefGoogle Scholar
  24. Healy, B. & T. Bolger, 1984. The occurrence of species of semi-aquatic Enchytraeidae (Oligochaeta) in Ireland. Hydrobiologia 115: 159–170.CrossRefGoogle Scholar
  25. Horsák, M., V. Rádková, J. Bojková, V. Křoupalová, J. Schenková, V. Syrovátka & J. Zajacová, 2015. Drivers of aquatic macroinvertebrate richness in spring fens in relation to habitat specialization and dispersal mode. Journal of Biogeography 42: 2112–2121.CrossRefGoogle Scholar
  26. Horsák, M., V. Polášková, M. Zhai, J. Bojková, V. Syrovátka, V. Šorfová, J. Schenková, M. Polášek, T. Peterka & M. Hájek, 2018. Spring-fen habitat islands in a warming climate: partitioning the effects of mesoclimate air and water temperature on aquatic and terrestrial biota. Science of the Total Environment 634: 355–365.CrossRefPubMedGoogle Scholar
  27. Hrabě, S., 1942. Poznámky o zvířeně ze studní a pramenů na Slovensku. Sborník Přírodovědeckého klubu v Brně 24: 23–30.Google Scholar
  28. IPCC, 2014. Climate change 2014—impacts, adaptation and vulnerability: regional aspects. Cambridge University Press, New York.Google Scholar
  29. Jackson, D. A., 1995. PROTEST: a PROcrustean randomization TEST of community environment concordance. Écoscience 2: 297–303.CrossRefGoogle Scholar
  30. Juget, J. & M. Lafont, 1994. Theoretical habitat templets, species traits, and species richness: aquatic oligochaetes in the Upper Rhône River and its floodplain. Freshwater Biology 31: 327–340.CrossRefGoogle Scholar
  31. Kløve, B., P. Ala-Aho, G. Bertrand, J. J. Gurdak, H. Kupfersberger, J. Kværner, T. Muotka, H. Mykrä, E. Preda, P. Rossi, C. B. Uvo, E. Velasco & M. Pulido-Velazquez, 2014. Climate change impacts on groundwater and dependent ecosystems. Journal of Hydrology 518: 250–266.CrossRefGoogle Scholar
  32. Košel, V., 2001. Hirudinológia pre hydrobiológov v praxi. In Makovinská, J. & L. Tóthová (eds), Zborník z hydrobiologického kurzu 2001. Rajecké Teplice: 37–54.Google Scholar
  33. Křoupalová, V., J. Bojková, J. Schenková, P. Pařil & M. Horsák, 2011. Small-scale distribution of aquatic macroinvertebrates in two spring fens with different groundwater chemistry. International Review of Hydrobiology 96: 235–256.CrossRefGoogle Scholar
  34. Laiho, R., N. Silvan, H. Cárcamo & H. Vasander, 2001. Effects of water level and nutrients on spatial distribution of soil mesofauna in peatlands drained for forestry in Finland. Applied Soil Ecology 16: 1–9.CrossRefGoogle Scholar
  35. Learner, M. A., G. Lochhead & B. D. Hughes, 1978. A review of the biology of British Naididae (Oligochaeta) with emphasis on the lotic environment. Freshwater Biology 8: 357–375.CrossRefGoogle Scholar
  36. Martínez-Ansemil, E. & R. Collado, 1996. Distribution patterns of aquatic oligochaetes inhabiting watercourses in the Northwestern Iberian Peninsula. Hydrobiologia 334: 73–83.CrossRefGoogle Scholar
  37. Martinsson, S., E. Rota & C. Erséus, 2015a. Revision of Cognettia (Clitellata, Enchytraeidae): re-estabilishment of Chamaedrilus and description of cryptic species in the sphagnetorum complex. Systematics and Biodiversity 13: 257–277.CrossRefGoogle Scholar
  38. Martinsson, S., E. Rota & C. Erséus, 2015b. On the identity of Chamaedrilus glandulosus (Michaelsen, 1881) (Clitellata, Enchytraeidae), with the description of a new species. Zookeys 501: 1–14.CrossRefGoogle Scholar
  39. Neubert, E. & H. Nesemann, 1999. Annelida, Clitellata; Branchiobdellida, Acanthobdellea, Hirudinea. Spektrum Akademischer Verlag, Berlin.Google Scholar
  40. Nijboer, R. C., M. J. Wetzel & P. F. M. Verdonschot, 2004. Diversity and distribution of Tubificidae, Naididae, and Lumbriculidae (Annelida: Oligochaeta) in the Netherlands: an evaluation of 20 years of monitoring data. Hydrobiologia 520: 127–141.CrossRefGoogle Scholar
  41. Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. Henry, H. Stevens, E. Szoecs & H. Wagner, 2017. vegan: Community ecology package. 2013. R-package version 2.4–3. Available at:
  42. Omesová, M. & J. Helešic, 2004. On the processing of freeze-core samples with notes on the impact of sample size. Scripta Facultatis Scientiarum Naturalium Universitatis Masarykianae Brunensis. Biology. Studies in Hydrobiology 29: 59–66.Google Scholar
  43. Pižl, V., 2002. Žížaly České republiky. Earthworms of the Czech Republic, Sborník přírodovědeckého klubu v Uherském Hradišti, Supp: 9.Google Scholar
  44. Plum, N. M. & J. Filser, 2005. Floods and drought: Response of earthworms and potworms (Oligochaeta: Lumbricidae, Enchytraeidae) to hydrological extremes in wet grassland. Pedobiologia 49: 443–453.CrossRefGoogle Scholar
  45. Prendergast-Miller, M., V. Standen, I. D. Leith & L. J. Sheppard, 2009. Response of enchytraeid worm populations to different forms of nitrogen (ammonia, ammonium, and nitrate) deposition. Soil Organisms 81: 225–236.Google Scholar
  46. R Development Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
  47. Rádková, V., V. Syrovátka, J. Bojková, J. Schenková, V. Křoupalová & M. Horsák, 2014. The importance of species replacement and richness differences in small-scale diversity patterns of aquatic macroinvertebrates in spring fens. Limnologica 47: 52–61.CrossRefGoogle Scholar
  48. Richards, K. S., 1977. Structure and function in the oligochaete epidermis (Annelida). Symposia of the Zoological Society of London 39: 171–193.Google Scholar
  49. Römbke, J., J.-P. Sousa, T. Schouten & F. Riepert, 2006. Monitoring of soil organisms: a set of standardized field methods proposed by ISO. European Journal of Soil Biology 42: 61–64.CrossRefGoogle Scholar
  50. Sawyer, R. T., 1986. Leech Biology and Behaviour, Vol. II. Clarendon Press, Oxford.Google Scholar
  51. Schenková, J., M. Bílková & M. Horsák, 2016. The response of Clitellata (Annelida) to environmental gradients in spring fens. Limnologica 57: 73–82.CrossRefGoogle Scholar
  52. Schmelz, R. M. & R. Collado, 2010. A guide to European terrestrial and freshwater species of Enchytraeidae (Oligochaeta). Soil Organisms 82: 1–176.Google Scholar
  53. Schmelz, R. M., R. Collado & J. Römbke, 2015. Cognettia Nielsen & Christensen, 1959 (Annelida, Oligochaeta, enchytraeidae): proposed precedence over Euenchytraeus Bretscher, 1906 and Chamaedrilus Friend, 1913. The Bulletin of Zoological Nomenclature 72: 186–192.CrossRefGoogle Scholar
  54. Schwank, P., 1981. Turbellarien, Oligochaeten und Archianneliden des Breitenbachs und anderer oberhessischer Mittelgebirgsbäche. II. Die Systematik und Autökologie der einzelnen Arten. Schlitzer Produktionsbiologische Studien (43-2). Archiv für Hydrobiologie, Supplement 62: 86–147.Google Scholar
  55. Seys, J., M. Vincx & P. Meire, 1999. Spatial distribution of oligochaetes (Clitellata) in the tidal freshwater and brackish parts of the Schelde estuary (Belgium). Hydrobiologia 406: 119–132.CrossRefGoogle Scholar
  56. Silvan, N., R. Laiho & H. Vasander, 2000. Changes in mesofauna abundance in peat soils drained for forestry. Forest Ecology and Management 133: 127–133.CrossRefGoogle Scholar
  57. Smith, M. E. & J. R. Kaster, 1986. Feeding habits and dietary overlap of Naididae (Oligochaeta) from a bog stream. Hydrobiologia 137: 193–201.CrossRefGoogle Scholar
  58. Springett, J. A., J. E. Brittain & B. P. Springett, 1970. Vertical movement of Enchytraeidae (Oligochaeta) in moorland soils. Oikos 21: 16–21.CrossRefGoogle Scholar
  59. Standen, V., 1982. Associations of Enchytraeidae (Oligochaeta) in experimentally fertilized grasslands. Journal of Animal Ecology 51: 501–522.CrossRefGoogle Scholar
  60. Svendsen, J. A., 1957a. The distribution of Lumbricidae in an area of Pennine moorland. Journal of Animal Ecology 26: 411–421.CrossRefGoogle Scholar
  61. Svendsen, J. A., 1957b. The behaviour of lumbricids under moorland conditions. Journal of Animal Ecology 26: 423–439.CrossRefGoogle Scholar
  62. Terhivuo, J. & A. Saura, 2006. Dispersal and clonal diversity of North-European parthenogenetic earthworms. Biological Invasions 8: 1205–1218.CrossRefGoogle Scholar
  63. Timm, T., 2009. A guide to the freshwater Oligochaeta and Polychaeta of Northern and Central Europe. Lauterbornia 66: 1–235.Google Scholar
  64. Tolasz, R., 2007. Climate Atlas of Czechia. Český hydrometeorologický ústav Olomouc. Univerzita Palackého v Olomouci, Olomouc.Google Scholar
  65. van Asselen, S., P. H. Verburg, J. E. Vermaat & J. H. Janse, 2013. Drivers of wetland conversion: a global meta-analysis. PLoS ONE 8(11): e81292.CrossRefPubMedPubMedCentralGoogle Scholar
  66. van Duinen, G. A., T. Timm, A. J. P. Smolders, A. M. T. Brock & W. C. E. P. Verberk, 2006. Differential response of aquatic oligochaete species to increased nutrient availability—a comparative study between Estonian and Dutch raised bogs. Hydrobiologia 564: 143–155.CrossRefGoogle Scholar
  67. von Fumetti, S., F. W. Wigger & P. Nagel, 2017. Temperature variability and its influence on macroinvertebrate assemblages of alpine springs. Ecohydrology 10: 1–9.Google Scholar
  68. Verdonschot, P. F. M., 2007. Spatial and temporal re-distribution of Naididae (tubificoid naidids and naidids s.str., Annelida, Clitellata) in Europe due to climate change: a review based on observational data. Acta Hydrobiologica Sinica 31: 116–138.Google Scholar
  69. Vu, V. Q., 2011. Ggbiplot: a ggplot2 based biplot. R Package. Version: 0.55. Available at:

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Masaryk University BrnoBrnoCzech Republic

Personalised recommendations