, Volume 605, Issue 1, pp 131–142 | Cite as

Population dynamics of free-swimming Annelida in four Dutch wastewater treatment plants in relation to process characteristics

  • Hellen J. H. Elissen
  • Edwin T. H. M. Peeters
  • Bastian R. Buys
  • Abraham Klapwijk
  • Wim Rulkens
Primary research paper


Free-swimming Annelida occasionally occur in very high densities in WWTPs (WasteWater Treatment Plants) and are nowadays applied for waste sludge reduction, but their growth is uncontrollable. In order to get more insight in the population dynamics of these free-swimming Annelida, and relate their presence to process characteristics, nine ATs (Aeration Tanks) of four Dutch WWTPs were regularly sampled over a 2.5-year period. For each species, peak periods in worm population growth were defined and population doubling times and half-lives calculated. Peak periods and doubling times were compared to those in natural systems. Process characteristics were obtained from the plant operators and related to the worm populations by multivariate analysis for the first time in large-scale WWTPs. The species composition in the WWTPs was limited and the most abundant free-swimming Annelida were in decreasing order Nais spp., Aeolosoma hemprichi, Pristina aequiseta, Aeolosoma variegatum, Chaetogaster diastrophus, and Aeolosoma tenebrarum.This latter species had never been found before in WWTPs. Worm absence sometimes coincided with the presence of anoxic zones, but this was possibly overcome by higher temperatures in the WWTPs. Worms were present all year round, even in winter, but no yearly recurrences of population peaks were observed, probably as a result of stable food supply and temperature, and the lack of predation in the WWTPs. Peak periods were similar between the ATs of each WWTP. The duration of the peak periods was on average 2–3 months for each species and the population doubling times in the peak periods were short (on average 2–6 days), which also corresponds to a stable favorable environment. The disappearance of worm populations from the WWTPs was presumably caused by declining asexual reproduction and subsequent removal with the waste sludge. Multivariate analysis indicated that 36% of the variability in worm populations was due to spatial and temporal patterns only. In addition, no more than 4% of the variability in worm populations was related to variations in process characteristics only and worm presence was usually associated with better sludge settleability. In conclusion, our data from large-scale WWTPs suggest that growth of free-swimming Annelida still seems uncontrollable and that their effects on treatment processes are unclear, which makes stable application in wastewater treatment for sludge reduction difficult.


Free-swimming aquatic worms Annelida Wastewater treatment Sludge Population dynamics Process characteristics 



This research was financially supported by the Dutch Economy, Ecology and Technology programme (EETK98021) and the Technology Foundation STW (WMK 4650). We would like to express our gratitude to Dennis Piron (WWTP Nijmegen), Annelies van der Ham, Janny van Vliet en Hans Huijsman (WWTP Zwolle), Jan Talsma (WWTP Drachten) and the other employees who were responsible for sending the samples and/or providing additional information. In addition, the authors would like to thank Christa Ratsak for her help. Also, we thank two anonymous reviewers for their useful comments.

Supplementary material

10750_2008_9329_MOESM1_ESM.doc (60 kb)
Supplementary material


  1. Aston, R. J., 1973. Tubificids and water quality: a review. Environmental Pollution 5: 1–10.CrossRefGoogle Scholar
  2. Bell, G., 1984. Evolutionary and nonevolutionary theories of senescence. American Naturalist 124: 600–603.CrossRefGoogle Scholar
  3. Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045–1055.CrossRefGoogle Scholar
  4. Brinkhurst, R. O., 1971. A guide for the identification of British Aquatic Oligochaeta. 2nd revised edn. Freshwater Biological Association, Ambleside.Google Scholar
  5. Brinkhurst, R. O. & B. G. M. Jamieson, 1971. Aquatic Oligochaeta of the world. Oliver and Boyd, Edinburgh.Google Scholar
  6. Chapman, P. M., M. A. Farrell & R. O. Brinkhurst, 1982. Relative tolerances of selected aquatic oligochaetes to combinations of pollutants and environmental factors. Aquatic Toxicology 2: 69–78.CrossRefGoogle Scholar
  7. Christensen, B., 1984. Asexual propagation and reproductive strategies in aquatic Oligochaeta. Hydrobiologia 115: 91–95.CrossRefGoogle Scholar
  8. Curds, C. R., 1975. The organisms and their ecology. In C. R. Curds & H. A. Hawkes (Eds.), Ecological aspects of used-water treatment: 203–268.Google Scholar
  9. Hawkes, H. A. & M. R. N. Shephard, 1972. The effect of dosing frequency on the seasonal fluctuations and vertical distribution of solids and grazing fauna in sewage percolating filters. Water Research 6: 721–730.CrossRefGoogle Scholar
  10. Inamori, Y., Y. Kuniyasu & R. Sudo, 1987. Role of smaller metazoa in water purification and sludge reduction. Japanese Journal of Water Treatment Biology 23: 12–23 (in Japanese with English abstract).Google Scholar
  11. Inamori, Y., R. Suzuki & R. Sudo, 1983. Mass culture of small aquatic oligochaeta. Research report from the National Institute for Environmental Studies 47: 125–137 (translated from Japanese).Google Scholar
  12. Janssen, P. M. J., J. Verkuijlen & H. F. van der Roest, 2002. Slibpredatie door inzet van oligochaete wormen. Pilotonderzoek naar slibreductie op de rwzi Bennekom. STOWA, The Netherlands. Report 2002–17 (in Dutch with English abstract).Google Scholar
  13. Jongman, R. H., C. J. F. ter Braak & O. F. R. van Tongeren, 1987. Data analysis in community and landscape ecology. Pudoc, Wageningen, The Netherlands.Google Scholar
  14. Kuniyasu, K., N. Hayashi, Y. Inamori & R. Sudo, 1997. Effect of environmental factors on growth characteristics of Oligochaeta 33: 207–214 (translated from Japanese).Google Scholar
  15. Learner, M. A., 1979. The geographical distribution of Naididae (Oligochaeta) in Britain. Hydrobiologia 66: 135–140.CrossRefGoogle Scholar
  16. Learner, M. A. & H. A. Chawner, 1998. Macro-invertebrate associations in sewage filter-beds and their relationship to operational practice. Journal of Applied Ecology 35: 720–747.Google Scholar
  17. 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
  18. Lee, S., S. Basu, C. W. Tyler & I. W. Wei, 2004. Ciliate populations as bio-indicators at Deer Island Treatment Plant. Advances in Environmental Research 8: 371–378.CrossRefGoogle Scholar
  19. Liang, P., X. Huang & Y. Qian, 2006. Excess sludge reduction in activated sludge process through predation of Aeolosoma hemprichi. Biochemical Engineering Journal 28: 117–122.CrossRefGoogle Scholar
  20. Lochhead, G. & M. A. Learner, 1983. The effect of temperature on asexual population growth of three species of Naididae (Oligochaeta). Hydrobiologia 98: 107–112.CrossRefGoogle Scholar
  21. Loden, M. S., 1981. Reproductive ecology of Naididae (Oligochaeta). Hydrobiologia 83: 115–123.CrossRefGoogle Scholar
  22. Madoni, P., D. Davoli & E. Chierici, 1993. Comparative analysis of the activated sludge microfauna in several sewage treatment works. Water Research 27: 1485–1491.CrossRefGoogle Scholar
  23. Martín-Cereceda, M., S. Serrano & A. Guinea, 1996. A comparative study of ciliated protozoa communities in activated-sludge plants. FEMS Microbiology Ecology 21: 267–276.CrossRefGoogle Scholar
  24. Martinez, D. E. & J. S. Levinton, 1992. Asexual metazoans undergo senescence. Proceedings of the National Academy of Sciences of the United States of America 89: 9920–9923.PubMedCrossRefGoogle Scholar
  25. Michiels, I. C. & W. Traunspurger, 2004. A three year study of seasonal dynamics of a zoobenthos community in a eutrophic lake. Nematology 6: 655–669.CrossRefGoogle Scholar
  26. Milbrink, G. & T. Timm, 2001. Distribution and dispersal capacity of the Ponto-Caspian tubificid oligochaete Potamothrix moldaviensis Vejdovský et Mrázek, 1903 in the Baltic Sea Region. Hydrobiologia 463: 93–102.CrossRefGoogle Scholar
  27. Nandini, S. & S. S. S. Sarma, 2004. Effect of Aeolosoma sp. (Aphanoneura: Aeolosomatidae) on the population dynamics of selected cladoceran species. Hydrobiologia 526: 157–163.CrossRefGoogle Scholar
  28. Peeters, E. T. H. M., A. Dewitte, A. A. Koelmans, J. A. van der Velden & P. J. den Besten, 2001. Evaluation of bioassays versus contaminant concentrations in explaining the macroinvertebrate community structure in the rhine-meuse delta, The Netherlands. Environmental Toxicology and Chemistry 20: 2883–2891.PubMedCrossRefGoogle Scholar
  29. Poole, J. E. P. & J. C. Fry, 1980. A study of the protozoan and metazoan populations of three oxidation ditches. Water Pollution Control 79: 19–27.Google Scholar
  30. Ratsak, C. H., 1994. Grazer induced sludge reduction in wastewater treatment. PhD thesis, Vrije Universiteit, the Netherlands.Google Scholar
  31. Ratsak, C. H., 2001. Effects of Nais elinguis on the performance of an activated sludge plant. Hydrobiologia 463: 217–222.CrossRefGoogle Scholar
  32. Ratsak, C. H. & J. Verkuijlen, 2006. Sludge reduction by predatory activity of aquatic oligochaetes in wastewater treatment plants: science or fiction? A review. Hydrobiologia 564: 197–211.CrossRefGoogle Scholar
  33. Reynoldson, T. B., 1939. On the life-history and ecology of Lumbricillus lineatus Müll. (Oligochaeta). Annals of Applied Biology 26: 782–799.CrossRefGoogle Scholar
  34. Reynoldson, T. B., 1948. An ecological study of the enchytraeid worm population of sewage bacterial beds. Synthesis of field and laboratory data. Journal of Animal Ecology 17: 27–38.Google Scholar
  35. Schönborn, W., 1984. The annual energy transfer from the communities of Ciliata to the population of Chaetogaster diastrophus(Gruithuizen) in the river Saale. Limnologica 16: 15–23.Google Scholar
  36. Schönborn, W., 1985. Die ökologische Rolle der Gattung Nais(Oligochaeta) in der Saale. Zoologischer Anzeiger Jena 215: 311–328.Google Scholar
  37. Solbé, J. F. de L. G., 1975. The organisms and their ecology. In Curds, C. R. & H. A. Hawkes (eds), Ecological aspects of used-water treatment: 305–335.Google Scholar
  38. Statistics Netherlands (CBS), 2007. ’CBS Statline’ webpage,
  39. Ter Braak, C. J. F., 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.CrossRefGoogle Scholar
  40. Ter Braak, C. J. F., 1990. Update notes: CANOCO, (version 3.1). Wageningen University, Agricultural Mathematics Group, Wageningen.Google Scholar
  41. Ter Braak, C. J. F. & P. Smilauer, 1998. CANOCO reference manual and user’s guide to Canoco for Windows: Software for canonical community ordination (version 4.0). Microcomputer Power, Ithaca, NY.Google Scholar
  42. Timm, T., 1999. A guide to the Estonian Annelida. Vol. 1. Estonian Academy Publishers, Tallinn.Google Scholar
  43. Van Loosdrecht, M. C. M. & M. Henze, 1999. Maintenance, endogeneous respiration, lysis, decay and predation. Water Science and Technology 39: 107–117.CrossRefGoogle Scholar
  44. Wallace, J. B. & J. R. Webster, 1996. The role of macroinvertebrates in stream ecosystem function. Annual Review of Entomology 41: 115–139.PubMedCrossRefGoogle Scholar
  45. Wei, Y. & J. Liu, 2005. The discharged excess sludge treated by Oligochaeta. Water Science and Technology 52: 265–272.PubMedGoogle Scholar
  46. Wei, Y. & J. Liu, 2006. Sludge reduction with a novel combined worm-reactor. Hydrobiologia 564: 213–222.CrossRefGoogle Scholar
  47. Wei, Y., R. T. van Houten, A. R. Borger, D. H. Eikelboom & Y. Fan, 2003a. Minimization of excess sludge production for biological wastewater treatment. Water Research 37: 4453–4467.PubMedCrossRefGoogle Scholar
  48. Wei, Y., R. T. van Houten, A. R. Borger, D. H. Eikelboom & Y. Fan, 2003b. Comparison performances of membrane bioreactor and conventional activated sludge processes on sludge reduction induced by Oligochaete. Environmental Science and Technology 37: 3171–3180.PubMedCrossRefGoogle Scholar
  49. Williams, N. V., J. F. de L. G. Solbé & R. W. Edwards, 1968. Aspects of the distribution, life history and metabolism of the enchytraeid worms Lumbricullus rivalis (Levinsen) and Enchytraeus coronatus(N. & C.) in a percolating filter. Journal of Applied Ecology 6: 171–183.Google Scholar
  50. Zhang, B., 1997. A study on microbial activities and the role of predators in membrane separation activated sludge process. PhD thesis, University of Tokyo, Japan.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Hellen J. H. Elissen
    • 1
    • 2
  • Edwin T. H. M. Peeters
    • 3
  • Bastian R. Buys
    • 1
  • Abraham Klapwijk
    • 1
  • Wim Rulkens
    • 1
  1. 1.Department of Environmental TechnologyWageningen UniversityWageningenThe Netherlands
  2. 2.Wetsus—Centre for Sustainable Water Technology LeeuwardenThe Netherlands
  3. 3.Aquatic Ecology and Water Quality Management GroupWageningen University WageningenThe Netherlands

Personalised recommendations