Earthworms as Bioindicators of Soil Quality

  • Heinz-Christian FründEmail author
  • Ulfert Graefe
  • Sabine Tischer
Part of the Soil Biology book series (SOILBIOL, volume 24)


Earthworms can indicate soil quality by (1) the abundance and species composition of the earthworm fauna at a particular site, (2) the behavior of individual earthworms in contact with a soil substrate (preference/avoidance/activity), (3) the accumulation of chemicals from the soil into the body, and (4) the biochemical/cytological stress-biomarkers in the earthworm. Earthworms are assessed in several long-term soil monitoring programs in Europe. Abundance data of earthworms may not only represent soil quality because weather and food are also important factors of influence. The ISO-avoidance test and tests with 2D (two-dimensional) terraria are laboratory assays with behavioral endpoints that can supplement the field monitoring of earthworm abundance. The analysis of chemical concentrations in earthworms has been used to indicate the risk of secondary poisoning for worm-feeding predators and to get an estimate of the bioavailability of contaminants in the soil. Bioaccumulation factors (BAF) for chemicals in earthworms can differ considerably from site to site and from species to species indicating that the bioavailability of a contaminant is influenced by chemical, physical, behavioral, and physiological parameters.


Soil Quality Avoidance Test Soil Substrate Earthworm Species Heptachlor Epoxide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alberti G, Hauk B, Köhler HR, Storch V (1996) Dekomposition. Ecomed, LandsbergGoogle Scholar
  2. Andersen C, Laurensen J (1982) Distribution of heavy metals in Lumbricus terrestris. Aporrectodea longa and A. rosea measured by atomic absorption and X-ray fluorescence spectrometry. Pedobiologia 24:347–356Google Scholar
  3. Auerswald K, Weigand S, Kainz M, Philipp C (1996) Influence of soil properties on the population and activity of geophagous earthworms after five years of bare fallow. Biol Fertil Soils 23:382–387CrossRefGoogle Scholar
  4. Barth N, Brandtner W, Cordsen E, Dann T, Emmerich KH, Feldhaus D, Kleefisch B, Schilling B, Utermann J (2000) Boden-Dauerbeobachtung – Einrichtung und Betrieb von Boden-Dauerbeobachtungsflächen. In: Rosenkranz D, Bachmann G, König W, Einsele G (eds) Bodenschutz, vol 3, 32. Lfg. XI/00, BerlinGoogle Scholar
  5. Bauchhenß J (2005) Zeitliche Veränderungen der Regenwurm-Taxozönosen auf Grünland- und auf Ackerflächen. In: 20 Jahre Bodendauerbeobachtung in Bayern. Zwischenbilanz der wichtigsten Ergebnisse 1985-2005. LfL-Schriftenreihe 8/2005. Landesanstalt für Landwirtschaft, Freising-Weihenstephan, pp 41–48Google Scholar
  6. Belfroid A, Seinen W, Van Gestel K, Hermens J, Van Leeuwen K (1995) Modelling the accumulation of hydrophobic organic chemicals in earthworms: application of the equilibrium partitioning theory. Environ Sci Pollut Res 2:5–15CrossRefGoogle Scholar
  7. Beyer WN, Gish CD (1980) Persistence in earthworms and potential hazards to birds of soil applied DDT, dieldrin and heptachlor. J Appl Ecol 17:295–307CrossRefGoogle Scholar
  8. Beyer WN, Stafford C (1993) Survey and evaluation of contaminants in earthworms and in soils derived from dredged material at confined disposal facilities in the Great Lakes Region. Environ Monit Assess 24:151–165CrossRefGoogle Scholar
  9. Beylich A, Graefe U (2009) Investigations of annelids at soil monitoring sites in Northern Germany: reference ranges and time-series data. Soil Org 81:175–196Google Scholar
  10. Bispo A, Cluzeau D, Creamer R, Dombos M, Graefe U, Krogh PH, Sousa LP, Peres G, Rutgers M, Winding A, Römbke J (2009) Indicators for monitoring soil biodiversity. Integr Environ Assess Manag 5:717–719CrossRefPubMedGoogle Scholar
  11. Bolton PJ, Phillipson J (1976) Burrowing, feeding, egestion and energy budgets of Allolobophora rosea (Savigny). Oecologia 23:225–245CrossRefGoogle Scholar
  12. Bouché MB (1972) Lombriciens de France. Ecologie et systematique. INRA Publ. 72-2, Paris, FranceGoogle Scholar
  13. Buckerfield JC, Lee KE, Davoren CW, Hannay JN (1997) Earthworms as indicators of sustainable production in dryland cropping in southern Australia. Soil Biol Biochem 29:547–554CrossRefGoogle Scholar
  14. Capowiez Y, Bérard A (2006) Assessment of the effects of imidacloprid on the behavior of two earthworm species (Aporrectodea nocturna and Allolobophora icterica) using 2D terraria. Ecotoxicol Environ Saf 64:198–206CrossRefPubMedGoogle Scholar
  15. Capowiez Y, Rault M, Mazzia C, Belzunces L (2003) Earthworm behaviour as a biomarker: a study case with imidacloprid. Pedobiologia 47:542–547Google Scholar
  16. Curry JP (2004) Factors affecting the abundance of earthworms in soils. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC, Boca Raton, pp 91–114Google Scholar
  17. Didden WAM (2003) Oligochaeta. In: Markert et al (eds) Bioindicators & biomonitors. Trace metals and other contaminants in the environment 6. Elsevier, Amsterdam, pp 555–576Google Scholar
  18. Doran JW, Colemann DC, Bezdicek DF, Stewart BA (1994) Defining soil quality for a sustainable environment. Soil Science Society of America Special Publ. No.35, MadisonGoogle Scholar
  19. Eggleton P, Inward K, Smith J, Jones DT, Sherlock E (2009) A six year study of earthworm (Lumbricidae) populations in pasture woodland in southern England shows their responses to soil temperature and soil moisture. Soil Biol Biochem 41:1857–1865CrossRefGoogle Scholar
  20. Ehrmann O, Brauckmann HJ, Emmerling C, Fründ HC (2007) Erfassung und Bewertung von Regenwurmpopulationen – Vorschlag für ein mehrstufiges Bewertungsverfahren. In: Bodenbiologische Bewertung von Boden-Dauerbeobachtungsflächen (BDF) anhand von Lumbriciden. UBA-Texte 34/07, pp 72–86Google Scholar
  21. Ellenberg H (1979) Zeigerwerte der Gefäßpflanzen Mitteleuropas. Goltze, Göttingen. Scripta Geobotanica 9Google Scholar
  22. Ernst G, Zimmermann S, Christie P, Frey B (2008) Mercury, cadmium and lead concentrations in different ecophysiological groups of earthworms in forest soils. Environ Pollut 156:1304–1313CrossRefPubMedGoogle Scholar
  23. European Commission (2002) Towards a thematic strategy for soil protection, Brussels. COM (2002) 179, 16/4/2002Google Scholar
  24. Evans AC (1947) A method of studying the burrowing activities of earthworms. Annu Mag Nat Hist 14:643–650Google Scholar
  25. Evans AC, Guild WJ, Mc L (1947) Studies on the relationships between earthworms and soil fertility I. Biological studies in the field. Ann Appl Biol 34:307–330CrossRefGoogle Scholar
  26. Fründ HC, Egbert E, Dumbeck G (2004) Spatial distribution of earthworms [Lumbricidae] in recultivated soils of the Rhenish lignite-mining area, Germany. J Plant Nutr Soil Sci 167:494–502CrossRefGoogle Scholar
  27. Fründ HC, Frerichs C, Rück F (2005) Bewertung Schwermetall belasteter Böden mittels Regenwürmern – Siedlungsdichte und Vermeidungsverhalten im Fluchttest. Mitt Dtsch Bodenkundl Ges 107:191–192Google Scholar
  28. Fründ HC, Wallrabenstein H, Leißner S, Blohm R (2009b) Developing a soil quality test with 2D terraria and Aporrectodea caliginosa. Berichte der DBG (Workshop Experimentieren mit Regenwürmern, Trier 20–21.03.2009) Cited 4 Feb 2010
  29. Fründ HC, Butt K, Capowiez Y, Eisenhauer N, Emmerling C, Ernst G, Potthoff M, Schädler M, Schrader S (2010) Using earthworms as model organisms in the laboratory: recommendations for experimental implementations. Pedobiologia 53:119–125CrossRefGoogle Scholar
  30. Gies A, Schroeter-Kermani C, Ruedel H, Paulus M, Wiesmueller GA (2007) Frozen environmental history: the German environmental specimen bank. Organohalogen Compd 69: 504-507. Available via Umweltbundesamt.
  31. Graefe U (1993) Die Gliederung von Zersetzergesellschaften für die standortsökologische Ansprache. Mitt Dtsch Bodenkundl Ges 69:95–98Google Scholar
  32. Graefe U (1997) Bodenorganismen als Indikatoren des biologischen Bodenzustands. Mitt Dtsch Bodenkundl Ges 85:687–690Google Scholar
  33. Graefe U (2005) Makroökologische Muster der Bodenbiozönose. Mitt Dtsch Bodenkundl Ges 107:195–196Google Scholar
  34. Graefe U, Schmelz RM (1999) Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids. Newsletter on Enchytraeidae 6:59–67Google Scholar
  35. Graefe U, Gehrmann J, Stempelmann I (2001) Bodenzoologisches Monitoring auf EU-Level II-Dauerbeobachtungsflächen in Nordrhein-Westfalen. Mitt Dtsch Bodenkundl Ges 96:331–332Google Scholar
  36. Graff O (1964) Untersuchungen über die Bodenfauna im Ackerboden. Habilitation Thesis. University of Giessen, GermanyGoogle Scholar
  37. Harris RF, Bezdicek DF (1994) Descriptive aspects of soil quality/health. In: Doran JW et al. (eds) Defining soil quality for a sustainable environment, SSSA Special Publication No. 35, Madison, pp 23–35Google Scholar
  38. Hauser S, Asawalam DO, Vanlauwe B (1998) Spatial and temporal gradients of earthworm casting activity in alley cropping systems. Agrofor Syst 41:127–137CrossRefGoogle Scholar
  39. Henson-Ramsey H, Levine J, Kennedy-Stoskopf S, Taylor SK, Shea D, Stoskopf MK (2009) Development of a dynamic pharmacokinetic model to estimate bioconcentration of xenobiotics in earthworms. Environ Model Assess 14:411–418CrossRefGoogle Scholar
  40. Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier Applied Science, LondonGoogle Scholar
  41. Hund-Rinke K, Wiechering H (2001) Earthworm avoidance test for soil assessments, an alternative for acute and reproduction tests. J Soils Sediments 1:15–20CrossRefGoogle Scholar
  42. Hund-Rinke K, Achazi R, Römbke J, Warnecke D (2003) Avoidance test with Eisenia fetida as indicator for the habitat function of soils: a laboratory comparison test. J Soils Sediments 3:7–12CrossRefGoogle Scholar
  43. Irmler U (1999) Die standörtlichen Bedingungen der Regenwürmer (Lumbricidae) in Schleswig-Holstein. Faun-Ök Mitt 7:509–518Google Scholar
  44. ISO 17512-1 (2008) Soil quality – avoidance test for determining the quality of soils and effects of chemicals on behaviour – Part 1: test with earthworms (Eisenia fetida and Eisenia andrei). ISO (International Organization for Standardization), GenevaGoogle Scholar
  45. Jager T (1998) Mechanistic approach for estimating bioconcentration of organic chemicals in earthworms. Environ Toxicol Chem 17:2080–2090CrossRefGoogle Scholar
  46. Joschko M, Fox CA, Lentzsch P, Kiesel J, Hierold W, Krück S, Timmer J (2006) Spatial analysis of earthworm biodiversity at the regional scale. Agric Ecosyst Environ 112:367–380CrossRefGoogle Scholar
  47. Karlen DL, Andrews SS, Wienhold BJ, Zobeck TM (2008) Soil quality assessment: past, present and future. J Integr Biosci 6:3–14Google Scholar
  48. Krück S, Joschko M, Schultz-Sternberg R, Kroschewski B, Tessmann J (2006) A classification scheme for earthworm populations (Lumbricidae) in cultivated agricultural soils in Brandenburg, Germany. J Plant Nutr Soil Sci 169:651–660CrossRefGoogle Scholar
  49. Lanno R, Wells J, Conder J, Basta N (2004) The bioavailability of chemicals in soil for earthworms. Ecotoxicol Environ Saf 57:39–47CrossRefPubMedGoogle Scholar
  50. Lee KE (1985) Earthworms their ecology and relationships with soil and land use. Academic Press, SydneyGoogle Scholar
  51. Lukkari T, Haimi J (2005) Avoidance of Cu- and Zn-contaminated soil by three ecologically different earthworm species. Ecotoxicol Environ Saf 62:35–41CrossRefPubMedGoogle Scholar
  52. Ma WC, van Kleunen A, Immerzeel J, de Maagd PGJ (1998) Bioaccumulation of polycyclic aromatic hydrocarbons by earthworms: assessment of equilibrium partitioning theory in in situ studies and water experiments. Environ Toxicol Chem 17:730–1737CrossRefGoogle Scholar
  53. Markert BA, Breure AM, Zechmeister HG (2003) Definition, strategies and principles for bioindication/biomonitoring of the environment. In: Markert et al (eds) Bioindicators & biomonitors. Trace metals and other contaminants in the environment 6. Elsevier, Amsterdam, pp 3–40Google Scholar
  54. Mascato R, Mato S, Trigo D, Marino F, Diaz Cosin DJ (1987) Factores del suelo y destribucion de las lombrices de tierra en dos zonas de Galicia: Comparacion de diferentes metodos estadisticos. Rev Ecol Biol Sol 24:111–135Google Scholar
  55. Morgan JE, Morgan AJ (1999) The accumulation of metals (Cd, Cu, Pb, Zn and Ca) by two ecologically contrasting earthworm species (Lumbricus rubellus and Aporrectodea caliginosa): implications for ecotoxicological testing. Appl Soil Ecol 13:9–20CrossRefGoogle Scholar
  56. Nahmani J, Hodson ME, Devin S, Vijver MG (2009) Uptake kinetics of metals by the earthworm Eisenia fetida exposed to field-contaminated soils. Environ Pollut 157:2622–2628CrossRefPubMedGoogle Scholar
  57. Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR (1995) Bioconcentration and biokinetics of heavy metals in the earthworm. Environ Pollut 89:293–301CrossRefPubMedGoogle Scholar
  58. Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27Google Scholar
  59. Palojärvi A, Nuutinen V (2002) The soil quality concept and its importance in the study of Finnish arable soils. Agric Food Sci Finland 11:329–342Google Scholar
  60. Paoletti MG (1999) The role of earthworms for assessment of sustainability and as bioindicators. Agric Ecosyst Environ 74:137–155CrossRefGoogle Scholar
  61. Peijnenburg WJGM, Vrijver MG (2009) Earthworms and their use in eco(toxico)logical modeling. In: Deviller J (ed) Ecotoxicology modeling. Springer, Heidelberg, pp 177–204CrossRefGoogle Scholar
  62. Peres G, Cluzeau D, Cortet J, Chaussod R (2008) Decline in soil biodiversity, Pilot area Brittany, France. In: Stephens M, Micheli E, Jones AR, Jones RJA (eds) Environmental assessment of soil for monitoring, volume IVb: prototype evaluation – pilot studies. Office for Official Publications of the European Communities, Luxembourg. pp 263–286 Cited 9 Feb 2010
  63. Prinsloo MW, Reinecke SA, Przybylowicz WJ, Mesjas-Przybylowicz J, Reinecke AJ (1990) Micro-PIXE studies of Cd distribution in the nephridia of the earthworm Eisenia fetida (Oligochaeta). Nucl Instrum Methods Phys Res B 158:317–322CrossRefGoogle Scholar
  64. Rahtkens K, von der Trenck T (2006) Schwermetalle in Regenwürmern Baden-Württembergs. Teil I: Metallgehalte in Regenwürmern von Wald-Dauerbeobachtungsflächen. UWSF-Z Umweltchem Ökotox 18:164–174CrossRefGoogle Scholar
  65. Römbke J, Jänsch S, Didden WAM (2005) The use of earthworms in ecological soil classification and assessment concepts. Ecotoxicol Environ Saf 62:249–265CrossRefPubMedGoogle Scholar
  66. Rutgers M, Schouten AJ, Bloem J, van Eekeren N, de Goede RGM, Jagersop Akkerhuis GAJM, van der Wal A, Mulder C, Brussaard L, Breure AM (2009) Biological measurements in a nationwide soil monitoring network. Eur J Soil Sci 60:820–832CrossRefGoogle Scholar
  67. Schrader S (1993) Semi-automatic image analysis of earthworm activity in 2D soil sections. Geoderma 56:257–264CrossRefGoogle Scholar
  68. Schrader S, Joschko M (1991) A method for studying the morphology of earthworm burrows and their function in respect to water movement. Pedobiologia 35:185–190Google Scholar
  69. SSSA (Soil Science Society of America) (1997) Glossary of soil science terms 1996. Soil Science Society of America Inc, MadisonGoogle Scholar
  70. Timmermann A, Bos D, Ouwehand J, de Goede RGM (2006) Long-term effects of fertilisation regime on earthworm abundance in a semi-natural grassland area. Pedobiologia 50:427–432CrossRefGoogle Scholar
  71. Tischer S (2008) Lumbricidae communities in soil monitoring sites differently managed and polluted with heavy metals. Pol J Ecol 56:635–646Google Scholar
  72. Tischer S (2009) Earthworms (Lumbricidae) as bioindicators: the relationship between in-soil and in-tissue heavy metal content. Pol J Ecol 57:531–541Google Scholar
  73. Topoliantz S, Ponge JF (2003) Burrowing activity of the geophagous earthworm Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) in the presence of charcoal. Appl Soil Ecol 23:267–271CrossRefGoogle Scholar
  74. UBA (2007) Bodenbiologische Bewertung von Boden-Dauerbeobachtungsflächen (BDF) anhand von Lumbriciden. UBA-Texte 34/07. Umweltbundesamt, Berlin. Available at Cited 4 Feb 2010
  75. USDA-NRCS (2009) Earthworms. Soil quality indicator information sheet. Cited 17 Dec 2009
  76. Van Zwieten L, Rust J, Kingston T, Merrington G, Morris S (2004) Influence of copper fungicide residues on occurrence of earthworms in avocado orchard soils. Sci Total Environ 329:29–41CrossRefPubMedGoogle Scholar
  77. Yeardley RB, Lazorchak JM, Gast LC (1996) The potential of an earthworm avoidance test for evaluation of hazardeous waste sites. Environ Toxicol Chem 15:1532–1537CrossRefGoogle Scholar
  78. Yu YL, Wu XM, Li SN, Fang H, Tan YJ, Yu JQ (2005) Bioavailability of butachlor and myclobutanil residues in soil to earthworms. Chemosphere 59:961–967CrossRefPubMedGoogle Scholar

Copyright information

© Springer Berlin Heidelberg 2011

Authors and Affiliations

  • Heinz-Christian Fründ
    • 1
    Email author
  • Ulfert Graefe
    • 2
  • Sabine Tischer
    • 3
  1. 1.Department of Agriculture and Landscape ArchitectureFachhochschule Osnabrück-University of Applied SciencesOsnabrückGermany
  2. 2.IFAB Institute for Applied Soil Biology GmbHHamburgGermany
  3. 3.Institute for Agricultural and Nutritional Sciences, Department of Soil Biology and Soil EcologyMartin-Luther-Universität HalleHalle (Saale)Germany

Personalised recommendations