Skip to main content
SpringerLink
Log in

Ring-Testing and Field-validation of a Terrestrial Model Ecosystem (TME) – An Instrument for Testing Potentially Harmful Substances: Effects of Carbendazim on Soil Microbial Parameters

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The effects of carbendazim on substrate induced respiration (SIR), dehydrogenase activity (DHA), phosphatase activity and thymidine incorporation by bacteria were evaluated in an experiment with an open intact Terrestrial Model Ecosystem (TME) and in a simultaneous field-validation study. Experiments were performed on four different European soils in Germany, The Netherlands, United Kingdom and Portugal. Data analysis focused on (i) detecting differences between experiments, especially in control values, (ii) checking similarity in data variability at each treatment level between experiments and (iii) analysing the resemblance of response to the model chemical in both experiments. Results obtained showed that control values from TME experiments were similar to those obtained on the respective field site, in most of the comparisons made for SIR, DHA and thymidine incorporation. Phosphatase activity revealed more differences, but values of both experiments had the same order of magnitude. At least part of the variation could be explained from the correlation of the microbial parameters with soil moisture content. Comparisons on data variability also revealed the absence of significant differences between experiments in all parameters in most cases, indicating that TMEs were able to represent the spatial variability found in the field. Effects of carbendazim, when occurring, were observed at treatment levels exceeding the highest recommended application rate of 0.36 kg a.i./ha. Effects on SIR and DHA were observed early in time, but effects on phosphatase activity and thymidine incorporation rate were found 8 or 16 weeks after chemical application. These effects were mild, and rarely a 50% inhibition on any of these parameters was seen at carbendazim dosages up to 87.5 kg a.i./ha. The response to the model chemical in TMEs and field plots was similar in most cases. These results give promising prospects for the use of TMEs as an integrative tool in higher tier levels of different assessment schemes.

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

Similar content being viewed by others

References

  • Acosta-Martinez, V. and Tabatabai, M.A. (2000). Enzyme activities in a limed agricultural soil. Biol. Fertil. Soils 31, 85-91.

    Google Scholar 

  • Adema, D.M.M., Barug, D. and Vonk, J.W. (1984). Comparison of the effects of several chemicals on microorganisms, higher plants and earthworms. Symposium International sur L'Écotoxicologie Terrestre, Las Arcs (Savoie), pp. 199-211.

  • Bååth, E. (1992). Thymidine incorporation into macromolecules of bacteria extracted from soil by homogenization-centrifugation. Soil Biol. Biochem. 24, 1157-65.

    Google Scholar 

  • Beck, T., Öhlinger, R. and Baumgarten, A. (1996). Substrate-induced respiration. In: F. Schinner, R. Öhlinger, E. Kandeler and R. Margesin (eds). Methods in Soil Biology, pp. 64-8. Berlin: Springer-Verlag.

    Google Scholar 

  • Bonmati, M., Ceccanti, B. and Nanniperi, P. (1991). Spatial variability of phosphatase, urease, protease, organic carbon and total nitrogen in soil. Soil Biol. Biochem. 23, 391-6.

    Google Scholar 

  • Chalam, A.V., Sasikala, C., Ramana, C.V. and Rao, P.R. (1996). Effect of pesticides on hydrogen metabolism of Rhodobacter sphaeroides and Rhodopseudomonas palustris. FEMS Microbiol. Ecol. 19, 1-4.

    Google Scholar 

  • Chiba, M., Bown, A.W. and Danic, D. (1987). Inhibition of yeast respiration and fermentation by benomyl, carbendazim, isocyanates, and other fungicidal chemicals. Can. J. Microbiol. 33, 157-61.

    PubMed  Google Scholar 

  • Christensen, H. (1993). Conversion factors for the thymidine incorporation technique estimated with bacteria in pure culture and on seedling roots. Soil Biol. Biochem. 25, 1085-96.

    Google Scholar 

  • Christensen, H. and Christensen, S. (1995). [3H]Thymidine incorporation technique to determine soil bacterial growth rate. In A. Kassim and P. Nannipieri (eds). Methods in Applied Soil Microbiology and Biochemistry, pp. 258-61. Academic Press.

  • Christensen, H., Griffiths, B. and Christensen, S. (1992). Bacterial incorporation of tritiated thymidine and populations of bacteriophagous fauna in the rhizosphere of wheat. Soil Biol. Biochem. 24, 703-9.

    Google Scholar 

  • Christensen, H., Rønn, R., Ekelund, F. and Christensen, S. (1995). Bacterial production determined by 3H-thymidine incorporation in field rhizospheres as evaluated by comparison to rhizodeposition. Soil Biol. Biochem. 27, 93-9.

    Google Scholar 

  • Dick, R.P. (1997). Soil enzyme activities as integrative indicators of soil health. In C.E. Pankhurst, B.M. Doube and V.V.S.R. Gupta (eds). Biological Indicators of Soil Health, pp. 121-56. Wallingford: CAB International.

    Google Scholar 

  • Dighton, J. (1997). Is it possible to develop microbial test systems to evaluate pollution effects on soil nutrient cycle? In N.M. Van Straalen and H. Løkke (eds). Ecological Risk Assessment of Contaminants in Soil, pp. 51-69. London: Chapman & Hall.

    Google Scholar 

  • Domsch, K.H., Jagnow, G. and Anderson, T.-H. (1983). An ecological concept for the assessment of side effects of agrochemicals on soil microorganisms. Res. Rev. 88, 66-105.

    Google Scholar 

  • Dzantor, E.K. and Felsot, A.S. (1991). Microbial responses to large concentrations of herbicides in soil. Environ. Toxicol. Chem. 10, 649-55.

    Google Scholar 

  • Eder, M., Knacker, T. and Römbke, J. (1992). Effects of pesticides on the decomposition process and the carboxymethylcellulase-activity in terrestrial ecosystems. In J.P.E. Anderson, D.J. Arnold, F. Lewis and L. Torstensson (eds). The International Symposium on Environmental Aspects of Pesticide Microbiology, pp. 74-8. Sweden; Sigtuna.

    Google Scholar 

  • Fairbrother, A., Glazebrook, P.W., Van Straalen, N. and Tarazona, J. (1999). Summary of the SETAC Workshop on Test Methods for Hazard Determination of Metals and Sparingly Soluble Metal Compounds in Soils. 19-23 June 1999, San Lorenzo del Escorial, Spain. Pensacola, USA: SETAC Press.

    Google Scholar 

  • Felsot, A.S. and Dzantor, E.K. (1995). Effect of alachlor concentration and an organic amendment on soil dehydrogenase activity and pesticide degradation rate. Environ. Toxicol. Chem. 14, 23-8.

    Google Scholar 

  • Förster, B., Eder, M., Morgan, E. and Knacker, T. (1996). A microcosm study of the effects of chemical stress, earthworms and microorganisms and their interactions upon litter decomposition. Eur. J. Soil Biol. 32, 25-33.

    Google Scholar 

  • Giller, K.E., Witter, E. and McGrath, S.P. (1998). Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol. Biochem. 30, 1389-414.

    Google Scholar 

  • Haanstra, L., Doelman, P. and Voshaar, J.H.O. (1985). The use of sigmoid dose response curves in soil ecotoxicological research. Plant Soil 84, 293-7.

    Google Scholar 

  • Harden, T., Joergensen, R.G., Meyer, B. and Wolters, V. (1993). Soil microbial biomass estimated by fumigation-extraction and substrate-induced respiration in two pesticide-treated soils. Soil Biol. Biochem. 25, 679-83.

    Google Scholar 

  • Hart, M.R. and Brookes, P.C. (1996a). Effects of two ergosterol-inhibition fungicides on soil ergosterol and microbial biomass. Soil Biol. Biochem. 28, 885-92.

    Google Scholar 

  • Hart, M.R. and Brookes, P.C. (1996b). Soil microbial biomass matter after 19 years of cumulative field applications of pesticides. Soil Biol. Biochem. 28, 1641-49.

    Google Scholar 

  • Heinemeyer, O., Insam, H., Kaiser, E.A. and Walenzik, G. (1989). Soil microbial biomass and respiration measurements: an automated technique based on infra-red gas analysis. Plant Soil 116, 191-5.

    Google Scholar 

  • Helweg, A. (1973). Influence of the fungicide benomyl on microorganisms in soil. Tidsskrift for Planteavl 77, 375-84.

    Google Scholar 

  • Ismail, B.S., Jokha, Y. and Omar, O. (1995). Effects of glucosinate-ammonium on microbial populations and enzyme activities in soils. Microbios 83, 185-90.

    Google Scholar 

  • Ismail, B.S., Omar, O. and Ingon, D. (1996). Effects of metolachlor on the activities of four soil enzymes. Microbios 87, 239-48.

    Google Scholar 

  • Kling, M. and Jakobsen, I. (1997). Direct application of carbendazim and propiconazole at field rates to the external mycelium of three arbuscular mycorrhizal fungi species: effect on 32P transport and succinate dehydrogenase activity. Mycorrhiza 7, 33-7.

    Google Scholar 

  • Knacker, T., Van Gestel, C.A.M., Jones, S.E., Soares, A.M.V.M., Schallnaß, H.-J., Förster, B. and Edwards, C.A. (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.

    PubMed  Google Scholar 

  • Kuhnt, G. and Muntau, H. (eds). (1994). EURO-Soils: Identification, Collection, Treatment, Characterization, pp. 1-144. Ispra, Italy: Joint Research Centre European Commission, Special Publication No. 1.94.60.

    Google Scholar 

  • Li, C.Y. and Nelson, E.E. (1985). Persistence of benomyl and captan and their effects on microbial activity in field soils. Bull. Environ. Contam. Toxicol. 34, 533-40.

    PubMed  Google Scholar 

  • Margesin, R. (1996). Acid and alkaline phosphomonoesterase activity with the substrate p-nitrophenyl phosphate. In F. Schinner, R. Öhlinger, E. Kandeler and R. Margesin (eds). Methods in Soil Biology, pp. 213-7. Berlin: Springer-Verlag.

    Google Scholar 

  • Megharaj, M., Singleton, I., Kookana, R. and Naidu, R. (1999). Persistence and effects of fenamiphos on native algal populations and enzymatic activities in soil. Soil Biol. Biochem. 31, 1549-53.

    Google Scholar 

  • Morgan, E. and Knacker, T. (1994). The role of laboratory terrestrial model ecosystems in the testing of potentially harmful substances. Ecotoxicology 3, 213-33.

    Google Scholar 

  • OECD (1984). OECD guidelines for testing of chemicals. Test guideline No. 208. Terrestrial plants, growth test. Organization for Economic Cooperation and Development, Paris.

    Google Scholar 

  • Öhlinger, R. (1996). Dehydrogenase activity with the substrate TTC. In F. Schinner, R. Öhlinger, E. Kandeler and R. Margesin (eds). Methods in Soil Biology, pp. 241-3. Berlin: Springer-Verlag.

    Google Scholar 

  • Peeples, J.L. (1974). Microbial activity in benomyl-treated soils. Phytopathology 64, 857-60.

    Google Scholar 

  • Pell, M., Stenberg, B. and Torstensson, L. (1998). Potential denitrification and nitrification tests for evaluation of pesticide effects in soil. Ambio 27, 29-34.

    Google Scholar 

  • Perucci, P. and Scarponi, L. (1994). Effects of the herbicide imazethapyr on soil microbial biomass and various soil enzyme activities. Biol. Fertil. Soils 17, 237-40.

    Google Scholar 

  • Perucci, P., Dumontet, S., Bufo, S.A., Mazzatura, A. and Casucci, C. (2000). Effects of organic amendment and herbicide treatment on soil microbial biomass. Biol. Fertil. Soils 32, 17-23.

    Google Scholar 

  • Rossel, D., Tarradellas, J., Bitton, G. and Morel, J.-L. (1997). Use of enzymes in soil ecotoxicology: a case for dehydrogenase and hydrolytic enzymes. In J. Tarradellas, G. Bitton and D. Rossel (eds). Soil Ecotoxicology, pp. 179-206. Boca Raton: Lewis Publishers.

    Google Scholar 

  • Schweiger, P.F. and Jakobsen, I. (1998). Dose-response relationships between four pesticides and phosphorus uptake by hyphae of arbuscular mycorrhizas. Soil Biol. Biochem. 30, 1415-22.

    Google Scholar 

  • Sinsabaugh, R.L. (1994). Enzymatic analysis of microbial patterns and process. Biol. Fertil. Soils 17, 69-74.

    Google Scholar 

  • Sparling, G.P. (1997). Soil microbial biomass activity and nutrient cycling as indicators of soil health. In C.E. Pankhurst, B.M. Doube and V.V.S.R. Gupta (eds). Biological Indicators of Soil Health, pp. 97-119. Wallingford: CAB International.

    Google Scholar 

  • Stenberg, B., Johansson, M., Pell, M., Sjödahl-Svensson, K., Stenström, J. and Torstensson, L. (1998). Microbial biomass and activities in soil as affected by frozen and cold storage. Soil Biol. Biochem. 30, 393-402.

    Google Scholar 

  • Torstensson, L. (1993). Ammonium oxidation, a rapid method to test chemical influence on nitrification in soil. Guideline 05. In L. Torstensson (ed.). Guidelines. Soil Biological Variables in Environmental Hazard Assessment, pp. 48-58. Solna, Sweden: Swedish Environmental Protection Agency, Report No. 4262.

    Google Scholar 

  • Torstensson, L., Pell, M. and Stenberg, B. (1998). Need of a strategy for evaluation of arable soil quality. Ambio 27, 4-8.

    Google Scholar 

  • Tu, C.M. (1995). Effect of 5 insecticides on microbial and enzymatic-activities in sandy soil. J. Environ. Sci. Health Part B-Pestic. Food Contam. Agric. Wast. 30, 289-306.

    Google Scholar 

  • Van Faassen, H.G. (1974). Effect of the fungicide benomyl on some metabolic processess, and on numbers of bacteria and actinomycetes in the soil. Soil Biol. Biochem. 6, 131-3.

    Google Scholar 

  • Velthorst, E.J. (1993). Manual for chemical water analysis. Department of Soil Science and Geology, Agricultural University, Wageningen, The Netherlands.

    Google Scholar 

  • Vink, K. and Van Straalen, N.M. (1999). Effects of benomyl and diazinon on isopod-mediated leaf litter decomposition in microcosms. Pedobiologia 43, 345-59.

    Google Scholar 

  • Wainwright, M. and Pugh, G.J. (1974). The effects of fungicides on certain chemical and microbial properties of soils. Soil Biol. Biochem. 6, 263-7.

    Google Scholar 

  • Welp, G. and Brummer, G.W. (1997). Toxicity of increased amounts of chemicals and the dose-response curves for heterogeneous microbial populations in soil. Ecotoxicol. Environ. Safety 37, 37-44.

    PubMed  Google Scholar 

  • Weyers, A. and Schuphan, I. (1998). Variation of effect endpoint parameters in a terrestrial model ecosystem. Ecotoxicology 7, 335-41.

    Google Scholar 

  • Weyers, A., Sokull-Klüttgen, B., Knacker, T., Martin, S. and Van Gestel, C.A.M. (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.

    PubMed  Google Scholar 

  • Zar, J.H. (1996). Biostatistical Analysis, 3rd edn. London: Prentice-Hall International.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto do Ambiente e Vida, Dep. Zoologia da Universidade de Coimbra, P3004-517, Coimbra, Portugal

    J. Paulo Sousa

  2. Departamento de Biologia, Universidade de Aveiro, 3810-193, Aveiro, Portugal

    José M.L. Rodrigues, Susana Loureiro & Amadeu M.V.M. Soares

  3. School of Agricultural and Forestry Sciences, University of Wales, Bangor, Gwynedd, LL57 2UW, Wales, UK

    Susan E. Jones

  4. ECT Oekotoxikologie GmbH, Boettgerstrasse 2-14, D-65439, Floersheim am Main, Germany

    Bernhard Förster

  5. Institute of Ecological Science, Vrije Universiteit, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

    Cornelis A.M. Van Gestel

Authors
  1. J. Paulo Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José M.L. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susana Loureiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amadeu M.V.M. Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Susan E. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bernhard Förster
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cornelis A.M. Van Gestel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amadeu M.V.M. Soares.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paulo Sousa, J., Rodrigues, J.M., Loureiro, S. et al. Ring-Testing and Field-validation of a Terrestrial Model Ecosystem (TME) – An Instrument for Testing Potentially Harmful Substances: Effects of Carbendazim on Soil Microbial Parameters. Ecotoxicology 13, 43–60 (2004). https://doi.org/10.1023/B:ECTX.0000012404.08568.e2

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:ECTX.0000012404.08568.e2

Search

Navigation