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Earthworms as Bioindicators of Soil Quality

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Biology of Earthworms

Part of the book series: Soil Biology ((SOILBIOL,volume 24))

Abstract

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.

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References

  • Alberti G, Hauk B, Köhler HR, Storch V (1996) Dekomposition. Ecomed, Landsberg

    Google Scholar 

  • 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 24:347–356

    CAS  Google Scholar 

  • 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 23:382–387

    Article  CAS  Google Scholar 

  • 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, Berlin

    Google Scholar 

  • 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 41–48

    Google Scholar 

  • 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 2:5–15

    Article  CAS  Google Scholar 

  • Beyer WN, Gish CD (1980) Persistence in earthworms and potential hazards to birds of soil applied DDT, dieldrin and heptachlor. J Appl Ecol 17:295–307

    Article  CAS  Google Scholar 

  • 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 24:151–165

    Article  CAS  Google Scholar 

  • Beylich A, Graefe U (2009) Investigations of annelids at soil monitoring sites in Northern Germany: reference ranges and time-series data. Soil Org 81:175–196

    Google Scholar 

  • 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 5:717–719

    Article  CAS  PubMed  Google Scholar 

  • Bolton PJ, Phillipson J (1976) Burrowing, feeding, egestion and energy budgets of Allolobophora rosea (Savigny). Oecologia 23:225–245

    Article  Google Scholar 

  • Bouché MB (1972) Lombriciens de France. Ecologie et systematique. INRA Publ. 72-2, Paris, France

    Google Scholar 

  • Buckerfield JC, Lee KE, Davoren CW, Hannay JN (1997) Earthworms as indicators of sustainable production in dryland cropping in southern Australia. Soil Biol Biochem 29:547–554

    Article  CAS  Google Scholar 

  • 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 64:198–206

    Article  CAS  PubMed  Google Scholar 

  • Capowiez Y, Rault M, Mazzia C, Belzunces L (2003) Earthworm behaviour as a biomarker: a study case with imidacloprid. Pedobiologia 47:542–547

    Google Scholar 

  • Curry JP (2004) Factors affecting the abundance of earthworms in soils. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC, Boca Raton, pp 91–114

    Google Scholar 

  • Didden WAM (2003) Oligochaeta. In: Markert et al (eds) Bioindicators & biomonitors. Trace metals and other contaminants in the environment 6. Elsevier, Amsterdam, pp 555–576

    Google Scholar 

  • 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, Madison

    Google Scholar 

  • 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 41:1857–1865

    Article  CAS  Google Scholar 

  • 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 72–86

    Google Scholar 

  • Ellenberg H (1979) Zeigerwerte der Gefäßpflanzen Mitteleuropas. Goltze, Göttingen. Scripta Geobotanica 9

    Google Scholar 

  • 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 156:1304–1313

    Article  CAS  PubMed  Google Scholar 

  • European Commission (2002) Towards a thematic strategy for soil protection, Brussels. COM (2002) 179, 16/4/2002

    Google Scholar 

  • Evans AC (1947) A method of studying the burrowing activities of earthworms. Annu Mag Nat Hist 14:643–650

    Google Scholar 

  • 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 34:307–330

    Article  Google Scholar 

  • 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 167:494–502

    Article  Google Scholar 

  • Fründ HC, Frerichs C, Rück F (2005) Bewertung Schwermetall belasteter Böden mittels Regenwürmern – Siedlungsdichte und Vermeidungsverhalten im Fluchttest. Mitt Dtsch Bodenkundl Ges 107:191–192

    Google Scholar 

  • 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) http://eprints.dbges.de/90/2/Fruend_TrierDBG_2009.pdf. Cited 4 Feb 2010

  • 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 53:119–125

    Article  Google Scholar 

  • 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. http://www.umweltbundesamt.de/umweltproben/publikat/gies_et_al_oc2007.pdf

  • Graefe U (1993) Die Gliederung von Zersetzergesellschaften für die standortsökologische Ansprache. Mitt Dtsch Bodenkundl Ges 69:95–98

    Google Scholar 

  • Graefe U (1997) Bodenorganismen als Indikatoren des biologischen Bodenzustands. Mitt Dtsch Bodenkundl Ges 85:687–690

    Google Scholar 

  • Graefe U (2005) Makroökologische Muster der Bodenbiozönose. Mitt Dtsch Bodenkundl Ges 107:195–196

    Google Scholar 

  • Graefe U, Schmelz RM (1999) Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids. Newsletter on Enchytraeidae 6:59–67

    Google Scholar 

  • Graefe U, Gehrmann J, Stempelmann I (2001) Bodenzoologisches Monitoring auf EU-Level II-Dauerbeobachtungsflächen in Nordrhein-Westfalen. Mitt Dtsch Bodenkundl Ges 96:331–332

    Google Scholar 

  • Graff O (1964) Untersuchungen über die Bodenfauna im Ackerboden. Habilitation Thesis. University of Giessen, Germany

    Google Scholar 

  • 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 23–35

    Google Scholar 

  • Hauser S, Asawalam DO, Vanlauwe B (1998) Spatial and temporal gradients of earthworm casting activity in alley cropping systems. Agrofor Syst 41:127–137

    Article  Google Scholar 

  • 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 14:411–418

    Article  Google Scholar 

  • Hopkin SP (1989) Ecophysiology of metals in terrestrial invertebrates. Elsevier Applied Science, London

    Google Scholar 

  • Hund-Rinke K, Wiechering H (2001) Earthworm avoidance test for soil assessments, an alternative for acute and reproduction tests. J Soils Sediments 1:15–20

    Article  CAS  Google Scholar 

  • 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 3:7–12

    Article  CAS  Google Scholar 

  • Irmler U (1999) Die standörtlichen Bedingungen der Regenwürmer (Lumbricidae) in Schleswig-Holstein. Faun-Ök Mitt 7:509–518

    Google Scholar 

  • 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), Geneva

    Google Scholar 

  • Jager T (1998) Mechanistic approach for estimating bioconcentration of organic chemicals in earthworms. Environ Toxicol Chem 17:2080–2090

    Article  CAS  Google Scholar 

  • 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 112:367–380

    Article  Google Scholar 

  • Karlen DL, Andrews SS, Wienhold BJ, Zobeck TM (2008) Soil quality assessment: past, present and future. J Integr Biosci 6:3–14

    Google Scholar 

  • 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 169:651–660

    Article  Google Scholar 

  • Lanno R, Wells J, Conder J, Basta N (2004) The bioavailability of chemicals in soil for earthworms. Ecotoxicol Environ Saf 57:39–47

    Article  CAS  PubMed  Google Scholar 

  • Lee KE (1985) Earthworms their ecology and relationships with soil and land use. Academic Press, Sydney

    Google Scholar 

  • Lukkari T, Haimi J (2005) Avoidance of Cu- and Zn-contaminated soil by three ecologically different earthworm species. Ecotoxicol Environ Saf 62:35–41

    Article  CAS  PubMed  Google Scholar 

  • 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 17:730–1737

    Article  Google Scholar 

  • 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 3–40

    Google Scholar 

  • 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 24:111–135

    Google Scholar 

  • 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 13:9–20

    Article  Google Scholar 

  • 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 157:2622–2628

    Article  CAS  PubMed  Google Scholar 

  • Neuhauser EF, Cukic ZV, Malecki MR, Loehr RC, Durkin PR (1995) Bioconcentration and biokinetics of heavy metals in the earthworm. Environ Pollut 89:293–301

    Article  CAS  PubMed  Google Scholar 

  • Nordström S, Rundgren S (1974) Environmental factors and lumbricid associations in southern Sweden. Pedobiologia 14:1–27

    Google Scholar 

  • Palojärvi A, Nuutinen V (2002) The soil quality concept and its importance in the study of Finnish arable soils. Agric Food Sci Finland 11:329–342

    Google Scholar 

  • Paoletti MG (1999) The role of earthworms for assessment of sustainability and as bioindicators. Agric Ecosyst Environ 74:137–155

    Article  Google Scholar 

  • Peijnenburg WJGM, Vrijver MG (2009) Earthworms and their use in eco(toxico)logical modeling. In: Deviller J (ed) Ecotoxicology modeling. Springer, Heidelberg, pp 177–204

    Chapter  Google Scholar 

  • 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 http://eusoils.jrc.ec.europa.eu/projects/envasso/documents/ENV_Vol.IVb_Final2_web.pdf. Cited 9 Feb 2010

  • 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 158:317–322

    Article  Google Scholar 

  • Rahtkens K, von der Trenck T (2006) Schwermetalle in Regenwürmern Baden-Württembergs. Teil I: Metallgehalte in Regenwürmern von Wald-Dauerbeobachtungsflächen. UWSF-Z Umweltchem Ökotox 18:164–174

    Article  CAS  Google Scholar 

  • Römbke J, Jänsch S, Didden WAM (2005) The use of earthworms in ecological soil classification and assessment concepts. Ecotoxicol Environ Saf 62:249–265

    Article  PubMed  Google Scholar 

  • 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 60:820–832

    Article  Google Scholar 

  • Schrader S (1993) Semi-automatic image analysis of earthworm activity in 2D soil sections. Geoderma 56:257–264

    Article  Google Scholar 

  • Schrader S, Joschko M (1991) A method for studying the morphology of earthworm burrows and their function in respect to water movement. Pedobiologia 35:185–190

    Google Scholar 

  • SSSA (Soil Science Society of America) (1997) Glossary of soil science terms 1996. Soil Science Society of America Inc, Madison

    Google Scholar 

  • 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 50:427–432

    Article  Google Scholar 

  • Tischer S (2008) Lumbricidae communities in soil monitoring sites differently managed and polluted with heavy metals. Pol J Ecol 56:635–646

    CAS  Google Scholar 

  • Tischer S (2009) Earthworms (Lumbricidae) as bioindicators: the relationship between in-soil and in-tissue heavy metal content. Pol J Ecol 57:531–541

    Google Scholar 

  • Topoliantz S, Ponge JF (2003) Burrowing activity of the geophagous earthworm Pontoscolex corethrurus (Oligochaeta: Glossoscolecidae) in the presence of charcoal. Appl Soil Ecol 23:267–271

    Article  Google Scholar 

  • UBA (2007) Bodenbiologische Bewertung von Boden-Dauerbeobachtungsflächen (BDF) anhand von Lumbriciden. UBA-Texte 34/07. Umweltbundesamt, Berlin. Available at http://www.umweltbundesamt.de/uba-info-medien-e/search-public-e.php. Cited 4 Feb 2010

  • USDA-NRCS (2009) Earthworms. Soil quality indicator information sheet. http://soils.usda.gov/SQI/assessment/files/earthworms_sq_biological_indicator_sheet.pdf. Cited 17 Dec 2009

  • 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 329:29–41

    Article  PubMed  Google Scholar 

  • Yeardley RB, Lazorchak JM, Gast LC (1996) The potential of an earthworm avoidance test for evaluation of hazardeous waste sites. Environ Toxicol Chem 15:1532–1537

    Article  CAS  Google Scholar 

  • Yu YL, Wu XM, Li SN, Fang H, Tan YJ, Yu JQ (2005) Bioavailability of butachlor and myclobutanil residues in soil to earthworms. Chemosphere 59:961–967

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Agriculture and Landscape Architecture, Fachhochschule Osnabrück-University of Applied Sciences, Am Krümpel 31, 49090, Osnabrück, Germany

    Heinz-Christian Fründ

  2. IFAB Institute for Applied Soil Biology GmbH, Sodenkamp 62, 22337, Hamburg, Germany

    Ulfert Graefe

  3. Institute for Agricultural and Nutritional Sciences, Department of Soil Biology and Soil Ecology, Martin-Luther-Universität Halle, Von-Seckendorff-Platz 3, 06120, Halle (Saale), Germany

    Sabine Tischer

Authors
  1. Heinz-Christian Fründ
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  2. Ulfert Graefe
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  3. Sabine Tischer
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Correspondence to Heinz-Christian Fründ .

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Editors and Affiliations

  1. Fac. Agriculture, Dept. Soil Science, Ankara University, Ankara, 06110, Turkey

    Ayten Karaca

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Fründ, HC., Graefe, U., Tischer, S. (2011). Earthworms as Bioindicators of Soil Quality. In: Karaca, A. (eds) Biology of Earthworms. Soil Biology, vol 24. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14636-7_16

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