Skip to main content

Advertisement

SpringerLink
Log in

Fate and effects of ivermectin on soil invertebrates in terrestrial model ecosystems

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The effect of ivermectin on soil organisms was assessed in Terrestrial Model Ecosystems (TMEs). Intact soil cores were extracted from a pasture in England and kept for up to 14 weeks in the laboratory. Ivermectin was applied to the soil surface via spiked cow dung slurry at seven concentration rates ranging from 0.25 to 180 mg/TME, referring to concentrations of 0.19–227 mg ivermectin/kg soil dry weight in the uppermost (0–1 cm) soil layer. After 7, 28 and 96 days following the application soil cores were destructively sampled to determine ivermectin residues in soil and to assess possible effects on microbial biomass, nematodes, enchytraeids, earthworms, micro-arthropods, and bait-lamina feeding activity. No significant effect of ivermectin was found for microbial respiration and numbers of nematodes and mites. Due to a lack of dose–response patterns no effect concentrations could be determined for the endpoints enchytraeid and collembolan numbers as well as total earthworm biomass. In contrast, EC50 values for the endpoint feeding rate could be calculated as 0.46, 4.31 and 15.1 mg ivermectin/kg soil dry weight in three soil layers (0–1, 0–5 and 0–8 cm, respectively). The multivariate Principal Response Curve (PRC) was used to calculate the NOECcommunity, based on earthworm, enchytraeid and collembolan abundance data, as 0.33 and 0.78 mg ivermectin/kg soil dw for day 7 and day 96, respectively. The results shown here are in line with laboratory data, indicating in general low to moderate effects of ivermectin on soil organisms. As shown by the results of the bait-lamina tests, semi-field methods such as TMEs are useful extensions of the battery of potential test methods since complex and ecologically relevant endpoints can be included.

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

  • Bembridge JD, Kedwards TJ, Edwards PJ (1998) Variation in earthworm populations and methods for assessing responses to perturbations. In: Sheppard SC, Bembridge JD, Holmstrup M, Posthuma L (eds) Advances in earthworm ecotoxicology. SETAC Press, Pensacola, pp 341–352

    Google Scholar 

  • Bouché M (1972) Lombriciens de France. Ecologie et Systematique. INRA Publ. 72–2. Institut National de Recherches Agriculturelles, Paris, p 671

    Google Scholar 

  • EC (2001) Directive 2001/82/EC of the European Parliament and of the Council of 6 November 2001 on the Community code relating to veterinary medicinal products. Off J Eur Communities L311:1–66

    Google Scholar 

  • EMEA (2008) Revised guideline on environmental impact assessment for veterinary medicinal products in support of the VICH guidelines GL6 and GL38. Committee for Medicinal Products for Veterinary Use (CVMP), European Medicines Agency, London. EMEA/CVMP/ERA/418282/2005-Rev.1

  • Floate KD, Wardhaugh KG, Boxall ABA, Sherratt TN (2005) Fecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annu Rev Entomol 50:153–179

    Article  CAS  Google Scholar 

  • Förster B, Garcia MVB, Francimari O, Römbke J (2006) Effects of carbendazim and lambda-cyhalothrin on soil invertebrates and leaf litter decomposition in semi-field and field tests under tropical conditions (Amazonia, Brazil). Eur J Soil Biol 42:S171–S179

    Article  Google Scholar 

  • Graff O (1953) Die Regenwürmer Deutschlands. Schrift Forschungsinst Landwirt 7:1–70

    Google Scholar 

  • Grønvold J, Stendal Svendsen T, Kraglund H-O, Bresciani J, Monrad J (2004) Effect of the antiparasitic drugs fenbendazole and ivermectin on the soil nematode Pristionchus maupasi. Vet Parasitol 124:91–99

    Article  Google Scholar 

  • Helling B, Pfeiff G, Larink O (1998) A comparison of feeding activity of collembolan and enchytraeid in laboratory studies using the bait-lamina test. Appl Soil Ecol 7:202–212

    Article  Google Scholar 

  • ISO (1997) Soil quality—determination of soil microbial biomass. Part 1. Substrate-induced respiration method. ISO 14240-1. International Organization for Standardization, Geneva

    Google Scholar 

  • ISO (2006) Soil quality—sampling of soil invertebrates. Part 1. Hand-sorting and formalin extraction of earthworms. ISO 23611-1. International Organization for Standardization, Geneva

    Google Scholar 

  • Jensen J, Krogh PH, Sverdrup LE (2003) Effects of the antibacterial agents tiamulin, olanquindox and metronidazole and the anthelmintic ivermectin on the soil invertebrate species Folsomia fimetaria (Collembola) and Enchytraeus crypticus (Enchytraeidae). Chemosphere 50:437–443

    Article  Google Scholar 

  • Jensen J, Diao X, Hansen AD (2009) Single- and two-species tests to study effects of the anthelmintics ivermectin and morantel, and the coccidiostatic monensin on soil invertebrates. Environ Toxicol Chem 28:316–323

    Article  CAS  Google Scholar 

  • Knacker T, Van Gestel CAM, Jones SE, Soares AMVM, Schallnaß H-J, 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 

  • Knacker T, Duis K, Ternes T, Fenner K, Escher B, Schmitt H, Römbke J, Garric J, Hutchinson T, Boxall ABA (2005) The EU-project ERAPharm. Incentives for the further development of guidance documents? Environ Sci Pollut Res 12:62–65

    Article  Google Scholar 

  • Krogh KA, Søeborg T, Brodin B, Halling-Sørensen B (2008) Sorption and mobility of ivermectin in different soils. J Environ Qual 37:2202–2211

    Article  CAS  Google Scholar 

  • Krogh KA, Jensen GG, Schneider MK, Fenner K, Halling-Sørensen B (2009) Analysis of the dissipation kinetics of ivermectin at different temperatures and in four different soils. Chemosphere 75:1097–1104

    Article  CAS  Google Scholar 

  • Liebig M, Fernandez AA, Blübaum-Gronau E, Boxall A, Brinke M, Carbonell G, Egeler P, Fenner K, Fernandez C, Fink G, Garric J, Halling-Sørensen B, Jensen J, Knacker T, Krogh KA, Küster A, Löffler D, Porcel Cots MA, Pope L, Prasse C, Römbke J, Rönnefahrt I, Schneider MK, Schweitzer N, Tarazona JV, Ternes TA, Traunspurger W, Wehrhan A, Duis K (2010) Environmental risk assessment of ivermectin—a case study. Integr Environ Assess Manag 6(Suppl. 1):567–587

    Article  CAS  Google Scholar 

  • Moser T, Schallnaß H-J, Jones SE, Van Gestel CAM, Koolhaas JE, Rodrigues JML, Römbke J (2004) Ring-testing and field-validation of a Terrestrial Model Ecosystem (TME)—an instrument for testing potentially harmful substances: effects of carbendazim on nematodes. Ecotoxicology 13:61–74

    Article  CAS  Google Scholar 

  • Nielsen CO, Christensen B (1959) The Enchytraeidae, critical revision and taxonomy of European species. Nat Jutl 8–9:1–60

    Google Scholar 

  • Nielsen CO, Christensen B (1961) The Enchytraeidae, critical revision and taxonomy of European species. Supplement 1. Nat Jutl 10:1–23

    Google Scholar 

  • Nielsen CO, Christensen B (1963) The Enchytraeidae, critical revision and taxonomy of European species. Supplement 2. Nat Jutl 10:1–19

    Google Scholar 

  • Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22

    Google Scholar 

  • Römbke J, Floate KD, Jochmann R, Schäfer MA, Puniamoorthy N, Knäbe S, Lehmhus J, Rosenkranz B, Scheffczyk A, Schmidt T, Sharples A, Blanckenhorn WU (2009) Lethal and sublethal toxic effects of a test chemical (ivermectin) on the yellow dung fly (Scathophaga stercoraria) based on a standardized international ring test. Environ Toxicol Chem 28:2117–2124

    Article  Google Scholar 

  • Römbke J, Krogh KA, Moser T, Scheffczyk A, Liebig M (2010) Effects of the veterinary pharmaceutical ivermectin on soil invertebrates in laboratory tests. Arch Environ Contam Toxicol 58:332–340

    Article  Google Scholar 

  • s'Jacob JJ, van Bezooijen J (1984) Manual for practical work in nematology, revised edition. Department of Nematology, Agricultural University, Wageningen, The Netherlands, 76 pp

  • Schaeffer A, De Jong F, Hoy S, Römbke J, Heimbach F, Sousa JP, Ross-Nickoll M, Van den Brink P (2007) Guidance from the SETAC Europe Workshop Coimbra, Portugal: semi-field methods for the environmental risk assessment of pesticides in soil (PERAS). CRC Press, Boca Raton, p 105

    Google Scholar 

  • Sims RW, Gerard BM (1999) Earthworms. In: Kermack DM, Bames RSK (eds) Synopses of the British fauna (new series) No. 31. E.J. Brill/Dr. W. Backhuys, London, 171 pp

  • Southey JF (1986) Laboratory methods for work with plant and soil nematodes. Reference book 402, 6th edn. Ministry of Agriculture, Fisheries and Food, Her Majesty’s Stationery Office, London

    Google Scholar 

  • Standen V (1982) Associations of Enchytraeidae (Oligochaeta) in experimentally fertilized grassplots. J Anim Ecol 51:501–522

    Article  Google Scholar 

  • Stop-Bøwitz C (1969) A contribution to our knowledge of the systematics and zoogeography of Norwegian earthworms. Nytt Mag Zool 17:169–280

    Google Scholar 

  • Ter Braak CJF, Šmilauer P (2002) CANOCO Reference Manual and CanoDraw for Windows User’s Guide: software for canonical community ordination (version 4.5). MicroComputer Power, Ithaca, 500 pp

  • 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 

  • Van den Brink P, Van Donk E, Gylstra R, Crum S, Brock T (1995) Effects of chronic low concentrations of the pesticides chloropyrifos and atrazine in indoor freshwater microcosms. Chemosphere 31:3181–3200

    Article  Google Scholar 

  • Van den Brink P, Van Wijngaarden RPA, Gylstra R, Lucassen WGH, Brock TCM, Leeuwangh P (1996) Effects of the insecticide Dursban 4E (active ingredient chloropyrifos) in outdoor experimental ditches: II. Invertebrate community responses and recovery. Environ Toxicol Chem 15:1143–1153

    Article  Google Scholar 

  • Van den Brink PJ, Tarazona JV, Solomon KR, Knacker T, Van den Brink NW, Brock TCM, Hoogland JP (2005) The use of terrestrial and aquatic microcosm and mesocosms for the ecological risk assessment of veterinary pharmaceuticals. Environ Toxicol Chem 24:820–829

    Article  Google Scholar 

  • VICH (2000) Environmental impact assessment (EIAs) for veterinary medicinal products (VMPs). International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products, VICH GL 6 (Ecotoxicity Phase I). EMEA, London, United Kingdom. 9 pp

  • VICH (2004) Environmental impact assessment for veterinary medicinal products. International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products, VICH GL 38 (Ecotoxicity Phase II). EMEA, London, United Kingdom. 33 pp

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

    Google Scholar 

  • Von Törne E (1990b) Schätzungen von Fressaktivitäten bodenlebender Tiere. II. Mini-Köder-Tests. Pedobiologia 34:269–279

    Google Scholar 

Download references

Acknowledgments

This work was funded by the European Union under the 6th framework program in the STREP ERAPharm (SSPI-CT-2003-511135).

Author information

Authors and Affiliations

  1. ECT Oekotoxikologie GmbH, Boettgerstrasse 2-14, 65439, Floersheim/Main, Germany

    Bernhard Förster, Anja Coors, Markus Liebig, Thomas Moser & Jörg Römbke

  2. Central Science Laboratory (CSL), Sand Hutton, York, YO41 1LZ, UK

    Alistair Boxall & Louise Pope

  3. Department of Terrestrial Ecology, National Environmental Research Institute, Vejlsoevej 25, 8600, Silkeborg, Denmark

    John Jensen

Authors
  1. Bernhard Förster
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alistair Boxall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anja Coors
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John Jensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Markus Liebig
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Louise Pope
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thomas Moser
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jörg Römbke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jörg Römbke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Förster, B., Boxall, A., Coors, A. et al. Fate and effects of ivermectin on soil invertebrates in terrestrial model ecosystems. Ecotoxicology 20, 234–245 (2011). https://doi.org/10.1007/s10646-010-0575-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0575-z

Keywords

Search

Navigation