Skip to main content
SpringerLink
Log in

Outdoor Terrestrial Model Ecosystems are suitable to detect pesticide effects on soil fauna: design and method development

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Terrestrial Model Ecosystems (TME) were developed as one higher-tier option to detect and assess effects of pesticides on soil communities in a 1 year study using lindane (gamma-HCH) as a persistent and toxic reference pesticide. TME contained intact soil cores (diameter 300 mm, height 400 mm) including indigenous soil communities of undisturbed grassland. Forty units were placed outdoors between spring 2005 and 2006. The TME experiment was designed to provide data that fulfill the requirements of the revised European regulation on plant protection products (regulation 1107/2009/EEC replacing guideline 91/414/EC) with a focus on structural endpoints such as soil organisms and their community structure in case higher-tier evaluation is triggered. The key objective was to evaluate the dynamics and stability of species-diverse microarthropod communities of undisturbed grassland over at least 1 year after application. In grassland soils, less selection pressure towards insensitive species compared to arable land was presumed. Sufficient numbers of organisms and numerous TME replicates ensured that a statistical evaluation could be performed to estimate the sensitivity of the organisms upon application of lindane applied at high rates of 7.5 and 75 kg ai/ha. The application rates resulted in nominal concentrations of 10 and 100 mg ai/kg dry soil referred to the top 5 cm soil layer of 10 TME each; 20 untreated TME served as controls and were used to study the natural dynamics and the variability of populations under field conditions. Results showed that the grassland from which the soil cores were sampled contained communities of soil organisms marked by typical diversity of improved grassland. Lindane applied at excessive rates caused clear dose-related and long-lasting effects on the communities of microarthropods. On the contrary, lumbricids, the total feeding activity (bait lamina) and the growth of plant biomass were not affected up to 1 year after application. Based on the results of this study using a toxic reference insecticide, the methodology seems to be suitable for use in the regulatory context of the assessment of pesticides once protection goals, data requirements and the conceptual framework are defined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Becker H (1991) Bodenorganismen—Prüfungskategorien der Forschung. Umweltwissenschaften und Schadstoff-Forschung 3:19–24

    Article  Google Scholar 

  • Begon ME, Harper JL, Townsend CR (1998) Ökologie. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Boyle TP, Smillie GM, Anderson JC, Beeson DR (1990) A sensitivity analysis of nine diversity and seven similarity indices. Res J Water Pollut Control Fed 62:749–762

    Google Scholar 

  • Bretfeld G (1999) Synopses on palearctic collembola, volume 2: symphypleona. Abhandlungen und Berichte des Naturkundemuseum Görlitz 71:1–318

    Google Scholar 

  • Bundesministerium für Umwelt, Naturschutz und Reaktorsicherheit (BMU) (2001) SIDS Initial Assessment Report for SIAM 13-dimethylformamide. Bad Godesberg, Bonn, pp 1–287

  • Cairns J (1984) Are single species toxicity tests alone adequate for estimating environmental hazard? Environ Monit Assess 4:259–273

    Article  Google Scholar 

  • Christian E, Zicsi A (2005) Ein synoptischer Bestimmungsschlüssel der Regenwürmer Österreichs. Die Bodenkultur 50:121–131

    Google Scholar 

  • Cianciolo JM, Norton RA (2006) The ecological distribution of reproductive mode in oribatid mites, as related to biological complexity. Exp Appl Acarol 40:1–25

    Article  Google Scholar 

  • Coleman DC (2008) From peds to paradoxes: linkages between soil biota and their influences on ecological processes. Soil Biol Biochem 40:271–289

    Article  CAS  Google Scholar 

  • Daehler CC, Strong DR (1996) Can you bottle nature? The roles of microcosms in ecological research. Ecology 77:663–664

    Article  Google Scholar 

  • Engels M, Ratte HT (1992) Randomisierte Änlichkeitsanalyse von Lebensgemeinschaften am Beispiel von Mesokosmos-Versuchen in der Ökotoxikologie. Verhandlungen der Gesellschaft für Ökologie 21:303–308

    Google Scholar 

  • European Commission (2000) Commission Decision of 20 December 2000 concerning the non-inclusion of lindane in Annex I to Council Directive 91/414/EEC and the withdrawal of authorisations for plant-protection products containing this active substance (2000/801/EC). Off J Eur Communities L 324:42–43

    Google Scholar 

  • European Commission (2002) Draft working document. Guidance Document on Terrestrial Ecotoxicology under Council Directive 91/414/EEC. SANCO/10329/2002 rev. 2 final. European Commission, Brussels

    Google Scholar 

  • European Commission (2009) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC Off J Eur Union L 309:1–50

    Google Scholar 

  • European Food Safety Authority (2009) Critical comparison of available and potential higher tier testing approaches for the risk assessment of plant protection products, considering at least field and semi-field experimental designs, extrapolation from dose–response relationships, and increased dosages (aquatic and terrestrial). CFT/EFSA/PPR/2008/1. Lot 4:1–194

    Google Scholar 

  • FAO/WHO (1968) 1967 Evaluations of some pesticide residues in food. FAO/PL:1967/M/11/1; WHO/Food Add./68.30

  • Filzek PDB, Spurgeon DJ, Broll G, Svendsen C, Hankard PK, Parekh N, Stubberud HE, Weeks JM (2004) Metal effects on soil invertebrate feeding: measurements using the Bait Lamina method. Ecotoxicology 13:807–816

    Article  Google Scholar 

  • Fjellberg A (1980) Identification keys to Norwegian Collembola. Norsk Entomologist Forening, Norway

    Google Scholar 

  • Fjellberg A (1998) The Collembola of Fennoscandia and Denmark. Part I: Poduromorpha. Fauna Entomologica Scandinavica, vol 38. Brill, Leiden

    Google Scholar 

  • Förster B, Van Gestel CAM, Koolhaas JEE, Nentwig G, Rodrigues JML, Sousa JP, Jones SE, Knacker T (2004) Ring-testing and field-validation of a terrestrial model ecosystem (TME)—an instrument for testing potentially harmful substances: effects of carbendazim on organic matter breakdown and soil fauna feeding activity. Ecotoxicology 13:129–141

    Article  Google Scholar 

  • Frampton GK, Van den Brink PJ (2007) Collembola and macroarthropod community responses to carbamate, organophosphate and synthetic pyrethroid insecticides: direct and indirect effects. Environ Pollut 147:14–25

    Article  CAS  Google Scholar 

  • Frampton GK, Jänsch S, Scott-Fordsmand JJ, Römbke J, Van den Brink PJ (2006) Effects of pesticides on soil invertebrates in laboratory studies: a review and analysis using Species Sensitivity Distributions. Environ Toxicol Chem 25:2480–2489

    Article  CAS  Google Scholar 

  • Gescher A (1993) Metabolism of N,N-dimethylformamide: key to the understanding of its toxicity. Chem Res Toxicol 6:245–251

    Article  CAS  Google Scholar 

  • Gisi U, Schenker R, Schulin R, Stadelmann FX, Sticher H (1997) Bodenökologie. Thieme Verlag, Stuttgart

    Google Scholar 

  • Gosset WS (1908) The probable error of a mean. Biometrika 6:1–25

    Google Scholar 

  • Herbst M, Van Esch GJ (1991) International programme on chemical safety, environmental health criteria. 124—Lindane. World Health Organization, Geneva

    Google Scholar 

  • Hommen U, Veith D, Dülmer U (1994) A computer program to evaluate plankton data of freshwater field tests. In: Hill IR, Heimbach F, Leeuwangh P, Matthiessen P (eds) Freshwater field tests for hazard assessment of chemicals. Lewis Publishers, Boca Raton, pp 503–513

    Google Scholar 

  • ISO (2003a) Soil quality—sampling of soil invertebrates—Part 1: handsorting and formaline extraction of earthworms. ISO/DIS 23611-1

  • ISO (2003b) Soil quality—sampling of soil invertebrates—Part 2: sampling and extraction of microarthropods (Collembola and Acarina). ISO/DIS 23611-2

  • Jones TM, Lewis HT Jr, Getsinger JG (1966) Formamide as a component of liquid fertilizers. J Agric Food Chem 14:20–23

    Article  CAS  Google Scholar 

  • Kampichler C (2001) Use of enclosed model ecosystems in soil ecology: a bias towards laboratory research. Soil Biol Biochem 3:269–275

    Article  Google Scholar 

  • Knacker T, Van Gestel CAM, Jones SE, Soares AMVM, Schallnaß HJ, Förster B, Edwards CA (2004) Ring-testing and field-validation of a terrestrial model ecosystem (TME)—an instrument for testing potentially harmful substances: conceptual approach and study design. Ecotoxicology 13:9–27

    Article  CAS  Google Scholar 

  • Koolhaas JEE, Van Gestel CAM, Römbke J, Soares AMVM, Jones SE (2004) Ring-testing and field-validation of a terrestrial model ecosystem (TME)—an instrument for testing potentially harmful substances: effects of carbendazim on soil microarthropod communities. Ecotoxicology 13:75–88

    Article  CAS  Google Scholar 

  • Kratz W (1998) The Bait-Lamina Test—general aspects, applications and perspectives. Environ Sci Pollut Res 5:94–96

    Article  CAS  Google Scholar 

  • Krieg W, Becker R, Schick H (2007) In-door terrestrial model ecosystem—experiences with TME filled with mixed field soil. SETAC Europe 17th annual meeting, Abstract Book. pp 258–259

  • Kryazhimskii FV, Bolshakov VN (2008) Functional-ecological role of biological diversity in populations and communities. Russ J Ecol 39:383–389

    Article  Google Scholar 

  • Landesanstalt für Umweltschutz Baden-Württemberg (LUBW) (1993) Stoffbericht Hexachlorcyclohexan (HCH). Texte und Berichte zur Altlastenbearbeitung 18/95

  • Larink O, Kratz W (1994) Köderstreifen-Workshop in Braunschweig—ein Resümee. Braunschweiger Naturkundliche Schriften 4:647–651

    Google Scholar 

  • Lebrun P, Van Straalen NM (1995) Oribatid mites: prospects for their use in ecotoxicology. Exp Appl Acarol 19:361–379

    Article  Google Scholar 

  • Lichtenstein EP, Millington WF, Cowley GT (1962) Effect of various insecticides on growth and respiration of plants. Agric Food Chem 10:251–256

    Article  CAS  Google Scholar 

  • Lock K, De Schamphelaere KAC, Janssen CR (2002) The effect of lindane on terrestrial invertebrates. Arch Environ Contam Toxicol 42:217–221

    Article  CAS  Google Scholar 

  • MacFadyen A (1961) Improved funnel type extractors for soil arthropods. J Anim Ecol 30:171–184

    Article  Google Scholar 

  • Mann HB, Whitney DR (1947) On a test of whether one of two random variables is larger than the other. Ann Math Stat 18:50–60

    Article  Google Scholar 

  • Montforts MHMM (2006) Assessment of persistency and bioaccumulation in pesticide registration frameworks within the Organization for Economic Cooperation and Development. Integr Environ Assess Manag 2:13–21

    Article  CAS  Google Scholar 

  • Morgan E, Knacker T (1994) The role of laboratory terrestrial model ecosystems in the testing of potentially harmful substances. Ecotoxicology 3:213–233

    Article  CAS  Google Scholar 

  • Neher DA (1999) Soil community composition and ecosystem processes—comparing agricultural ecosystems with natural ecosystems. Agrofor Syst 45:159–185

    Article  Google Scholar 

  • OECD (2006) Guidance document on simulated freshwater lentic field tests (outdoor microcosms and mesocosms). OECD series on testing and assessment 53. OECD, Paris

  • Potapov M (2001) Synopses on Palearctic Collembola, volume 3: Isotomidae. Abhandlungen und Berichte des Naturkundemuseum Görlitz 73:1–603

    Google Scholar 

  • Römbke J, Höfer H, Garcia MVB, Martius C (2006) Feeding activities of soil organisms at four different forest sites in Central Amazonia using the bait lamina method. J Trop Ecol 22:313–320

    Article  Google Scholar 

  • Roß-Nickoll M, Lennartz G, Fürste A, Mause R, Ottermanns R, Schäfer S, Smolis M, Theissen B, Toschki A, Ratte HT (2004) Die Arthropodenfauna von Nichtzielflächen und die Konsequenzen für die Bewertung der Auswirkungen von Pflanzenschutzmitteln auf den terrestrischen Bereich des Naturhaushaltes Umweltbundesamt, Berlin, pp 1–148

  • Rothmaler W (2002a) Exkursionsflora von Deutschland. Gefäßpflanzen—Atlasband. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Rothmaler W (2002b) Exkursionsflora von Deutschland. Gefäßpflanzen—rundband. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219

    Article  Google Scholar 

  • Schäffer A, Van den Brink PJ, Heimbach F, Hoy S, De Jong F, Römbke J, Sousa JP, Ross-Nickoll M (2008) Semi-field methods are a useful tool for the environmental risk assessment of pesticides in soil. Environ Sci Pollut Res 50:176–177

    Article  Google Scholar 

  • Schäffer A, van den Brink PJ, Heimbach F, Hoy SP, de Jong FMW, Römbke J, Roß-Nickoll M, Sousa JP (2010) Guidance from the SETAC Europe workshop: “semi-field methods for the environmental risk assessment of pesticides in soil (PERAS)”, Coimbra, Portugal, 8–10 Oct 2007. Society of Environmental Toxicology and Chemistry, Brussels, pp 1–107

  • Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596

    Article  CAS  Google Scholar 

  • Scheu S (2002) The soil food web: structure and perspectives. Eur J Soil Biol 38:11–20

    Article  Google Scholar 

  • Schneider K, Scheu S, Maraun M (2007) Microarthropod density and diversity respond little to spatial isolation. Basic Appl Ecol 8:26–35

    Article  Google Scholar 

  • Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27(379–423):623–656

    Google Scholar 

  • Siepel H (1996) Biodiversity of soil microarthropods: the filtering of species. Biodivers Conserv 5:251–260

    Article  Google Scholar 

  • Smith EP (1986) Randomized similarity analysis of multispecies laboratory and field studies. In: El Shaarawi AH, Kwiatkowski RE (eds) Statistical aspects of water quality monitoring, developments in water science, vol 27. Elsevier Science Publishers B.V., Amsterdam, pp 261–269

    Google Scholar 

  • SPSS Inc. (2005) SPSS 14.0 for Windows SPSS. Science Marketing Dept., Chicago

  • Stach J (1960) The Apterygotan fauna of Poland in relation to the world fauna of this group of insects. Tribe: Orchesellini. Polska Akademia Nauk, Krakau

  • Stach J (1963) The Apterygotan fauna of Poland in relation to the world fauna of this group of insects. Tribe: Entomobryini. Polska Akademia Nauk, Krakau

  • Strenzke K (1952) Untersuchungen über die Tiergemeinschaften des Bodens: Die Oribatiden und ihre Synusien in den Böden Norddeutschlands. Zool Stuttg 104:1–173

    Google Scholar 

  • Tanaka M (1970) The bio-economics on the populations of Isotoma (Desoria) trispinata MAC GILLIVRAY (Collembola; Isotomidae) and Onychiurus (Protaphorura) sp. (Collembola; Onychiuridae) in a grassfield. Publ Amakusa Mar Biol Lab 2:51–120

    Google Scholar 

  • Ter Braak CJF, Smilauer P (1998) Canoco Reference Manual and User’s Guide to Canoco for Windows. Software for canonical community ordination (version 4). Micro Computer Power, Ithaca

    Google Scholar 

  • Thibaud JM, Schulz HJ, Da Gama Assalino MM (2004) Synopses on Palearctic Collembola, volume 4: Hypogastruridae. Abhandlungen und Berichte des Naturkundemuseum Görlitz 75(2):1–287

    Google Scholar 

  • Toschki A (2008) Eignung unterschiedlicher Monitoring-Methoden als Grundlage zum risk-assessment für Agrarsysteme—Am Beispiel einer biozönologischen Reihenuntersuchung und einer Einzelfallstudie. Dissertation am Institut für Umweltforschung der RWTH-Aachen

  • Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120

    Article  Google Scholar 

  • Ulman E (1972) Lindane, monograph of an insecticide. Verlag K. Schillinger, Freiberg im Breisgau

  • Van den Brink PJ, Ter Braak CJF (1997) Ordination of responses to toxic stress in experimental ecosystems. Toxicol Ecotoxicol News Rev 4:173–177

    Google Scholar 

  • Van den Brink PJ, Ter Braak CJF (1998) Multivariate analysis of stress in experimental ecosystems by Principal Response Curves and similarity analysis. Aquat Ecol 32:163–178

    Article  Google Scholar 

  • Van den Brink PJ, Ter Braak CJF (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148

    Article  Google Scholar 

  • Veeranagouda Y, Emmanuel Paul PV, Gorla P, Siddavattam D, Karegoudar TB (2006) Complete mineralisation of dimethylformamide by Ochrobactrum sp. DGVK1 isolated from the soil samples collected from the coalmine leftovers. Appl Microbiol Biotechnol 71:369–375

    Article  CAS  Google Scholar 

  • Von Törne E (1990) Assessing feeding activities of soil-living animals. I. Bait-Lamina tests. Pedobiologia 34:89–101

    Google Scholar 

  • Weigmann G (2006) Hornmilben (Oribatida) In: Dahl, Tierwelt Deutschlands 76. Goecke and Evers, Keltern

  • Weigmann G, Kratz W (1981) Die deutschen Hornmilbenarten und ihre ökologische Charakteristik. Zool Beiträge 27:459–489

    Google Scholar 

  • Weyers A, Sokull-Klüttgen B, Knacker T, Martin S, Van Gestel CAM (2004) Use of terrestrial model ecosystem data in environmental risk assessment for industrial chemicals, biocides and plant protection products in the EU. Ecotoxicology 13:163–176

    Article  CAS  Google Scholar 

  • Wiles JA, Frampton GK (1996) A field bioassay approach to assess the toxicity of insecticide residues on soil to Collembola. Pest Sci 47:273–285

    Article  CAS  Google Scholar 

  • Williams DA (1971) A test for differences between treatment means when several dose levels are compared with a zero dose control. Biometrics 27:103–117

    Article  CAS  Google Scholar 

  • Williams DA (1972) The comparison of several dose levels with a zero dose control. Biometrics 28:519–531

    Article  CAS  Google Scholar 

  • Willmann C (1931) Moosmilben oder Oribatiden (Cryptostigmata). In: Dahl F (ed) Die Tierwelt Deutschlands, Bd. 22, vol 5. Gustav Fischer, Jena, pp 79–200

  • Zimdars B, Dunger W (1994) Synopses on Palearctic Collembola, volume 1: Tullbergiinae. Abhandlungen und Berichte des Naturkundemuseum Görlitz 68:1–71

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Environmental Research (BioV), RWTH Aachen University, Worringerweg 1, 52074, Aachen, Germany

    B. Scholz-Starke, B. Theißen, H. T. Ratte, A. Schäffer & M. Roß-Nickoll

  2. Bayer CropScience AG, Alfred-Nobel-Str. 50, 40789, Monheim am Rhein, Germany

    A. Nikolakis, T. Leicher & C. Lechelt-Kunze

  3. RIFCON GmbH, Am Wallgraben 1, 42799, Leichlingen, Germany

    F. Heimbach

  4. Forschungsinstitut für Ökosystemanalyse und -bewertung e.V. (gaiac), Worringerweg 1, 52056, Aachen, Germany

    A. Toschki

Authors
  1. B. Scholz-Starke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Nikolakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Leicher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Lechelt-Kunze
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. Heimbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. B. Theißen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. Toschki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. H. T. Ratte
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. Schäffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. M. Roß-Nickoll
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Scholz-Starke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scholz-Starke, B., Nikolakis, A., Leicher, T. et al. Outdoor Terrestrial Model Ecosystems are suitable to detect pesticide effects on soil fauna: design and method development. Ecotoxicology 20, 1932–1948 (2011). https://doi.org/10.1007/s10646-011-0732-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0732-z

Keywords

Search

Navigation