Ecotoxicology

, Volume 26, Issue 4, pp 471–481 | Cite as

Ecotoxicity of boric acid in standard laboratory tests with plants and soil organisms

  • Juliska Princz
  • Leonie Becker
  • Adam Scheffczyk
  • Gladys Stephenson
  • Rick Scroggins
  • Thomas Moser
  • Jörg Römbke
Review

Abstract

To verify the continuous sensitivity of ecotoxicological tests (mainly the test organisms), reference substances with known toxicity are regularly tested. Ideally, this substance(s) would lack specificity in its mode action, be bioavailable and readily attainable with cost-effective means of chemical characterization. Boric acid has satisfied these criteria, but has most recently been characterized as a substance of very high concern, due to reproductive effects in humans, thus limiting its recommendation as an ideal reference toxicant. However, there is probably no other chemical for which ecotoxicity in soil has been so intensively studied; an extensive literature review yielded lethal (including avoidance) and sublethal data for 38 taxa. The ecotoxicity data were evaluated using species sensitivity distributions, collectively across all taxa, and separately according to species type, endpoints, soil type and duration. The lack of specificity in the mode of action yielded broad toxicity among soil taxa and soil types, and provided a collective approach to assessing species sensitivity, while taking into consideration differences in test methodologies and exposure durations. Toxicity was species-specific with Folsomia candida and enchytraied species demonstrating the most sensitivity; among plants, the following trend occurred: dicotyledonous (more sensitive) ≫ monocotyledonous ≫ gymnosperm species. Sensitivity was also time and endpoint specific, with endpoints such as lethality and avoidance being less sensitive than reproduction effects. Furthermore, given the breadth of data and toxicity demonstrated by boric acid, lessons learned from its evaluation are discussed to recommend the properties required by an ideal reference substance for the soil compartment.

Keywords

Boric acid Toxicity Soil Reference substance Invertebrates SSD 

Supplementary material

10646_2017_1789_MOESM1_ESM.docx (143 kb)
Supplementary Information

References

  1. Aldenberg T, Jaworska JS (2000) Uncertainty of the hazardous concentration and fraction affected for normal species sensitivity distributions. Ecotox Environ Safe 46:1–18CrossRefGoogle Scholar
  2. Amorim MJB, Natal-da-Luz T, Sousa JP, Loureiro S, Becker L, Römbke J, Soares AMVM (2012) Boric acid as a reference substance: pros, cons and standardization. Ecotoxicology 21:919–924CrossRefGoogle Scholar
  3. Amorim MJB, Novais S, Römbke J, Soares AMVM (2008) Enchytraeus albidus (Enchytraeidae): A test organism in a standardised avoidance test? Effects of different chemical substances. Environ Int 34:363–371CrossRefGoogle Scholar
  4. Anaka A, Wickstrom M, Siciliano SD (2008) Increased sensitivity and variability of phytotoxicity responses in arctic soils to a reference toxicant, boric acid. Environ Toxicol Chem 27:720–726CrossRefGoogle Scholar
  5. ASTM International (2014) Standard guide for conducting terrestrial plant toxicity tests. E 1963-09(2014). West Conshohocken, PA, USAGoogle Scholar
  6. Becker L, Scheffczyk A, Oehlmann J, Römbke J, Moser T (2011) Effects of boric acid on varied plants and soil organisms. J Soils Sediments 11:238–248CrossRefGoogle Scholar
  7. Bicho RC, Gomes SIL, Soares AMVM, Amorim MJB (2015) Non-avoidance behaviour in enchytraeids to boric acid is related to the GABAergic mechanism. Environ Sci Pollut R 22:6898–6903CrossRefGoogle Scholar
  8. Butterwick L, de Oude N, Raymond K (1989) Safety assessment of boron in aquatic and terrestrial environment. Ecotox Environ Safe 17:339–371CrossRefGoogle Scholar
  9. CCME (Canadian Council of Ministers of the Environment) (2013) Determination of Hazardous concentrations with species sensitivity distributions, SSD master. Canadian Council of Ministers of the Environment, Ottawa, Ontario, Canada, Version 3.0Google Scholar
  10. EC (Environment Canada) (2004) Biological test method: tests for toxicity of contaminated soil to earthworms (Eisenia andrei, Eisenia fetida, or Lumbricus terrestris). Report EPS 1/RM/43. Ottawa, Ontario, CanadaGoogle Scholar
  11. EC (Environment Canada) (2005) Biological test method: test for measuring emergence and growth of terrestrial plants exposed to contaminants in soil. Report EPS 1/RM/45. Ottawa, ON, CanadaGoogle Scholar
  12. EC (Environment Canada) (2014) Biological test method: test for measuring survival and reproduction of springtails exposed to contaminants in soil. Report EPS 1/RM/47. Ottawa, Ontario, CanadaGoogle Scholar
  13. ECCC (Environment and Climate Change Canada), HC (Health Canada) (2016) Draft screening assessment - boric acid, its salts and its precursors. Ottawa, ONGoogle Scholar
  14. European Commission (2002) Draft working document - guidance document on terrestrial ecotoxicology under council directive 91/414/EEC. SANCO/10329/2002 rev 2 final. European CommissionGoogle Scholar
  15. ECHA (European Chemicals Agency) (2010) Member state committee support document for identification of boric acid as substance of very high concern because of its CMR properties. European Chemicals Agency, Helsinki, FinlandGoogle Scholar
  16. EFSA (European Food Safety Authority) (2007) Opinion of the scientific panel on plant protection products and their residues on a request from the commission related to the revision of annexes II and III to council Directive 91/414/EEC concerning the placing of plant protection products on the market – ecotoxicological studies. EFSA J 461:1–44Google Scholar
  17. EFSA (European Food Safety Authority) (2017) Scientific opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA J 15(2):4690 [225 pp]Google Scholar
  18. 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 25:2480–2489CrossRefGoogle Scholar
  19. Gourmelon A, Ahtiainen J (2007) Developing test guidelines on invertebrate development and reproduction for the assessment of chemicals, including potential endocrine active substances – The OECD perspective. Ecotoxicology 16:161–167CrossRefGoogle Scholar
  20. Goldberg S (1997) Reaction of boron with soils. Plant Soil 193:35–48CrossRefGoogle Scholar
  21. Gupta UC (1968) Relationship of total and hot-water soluble B, and fixation of added B to properties of Podzol soils. Soil Sci Soc Am Proc 32:45–48CrossRefGoogle Scholar
  22. Hofman J, Hovorkova I, Machat J (2009) Comparison and characterization of OECD artificial soils. In: Moser H, Römbke J (eds) Ecotoxicological characterisation of wastes: results and experiences of an international ring test. Springer, Berlin, Germany, pp 223–229CrossRefGoogle Scholar
  23. Huguier P, Manier N, Méline C, Bauda P, Pandard P (2013) Improvement of the Caenorhabditis elegans growth and reproduction test to assess the ecotoxicity of soils and complex matrices. Environ Tox Chem 32:2100–2108CrossRefGoogle Scholar
  24. ISO (International Organization for Standardization) (2014) Soil quality – Inhibition of reproduction of Collembola (Folsomia candida) by soil pollutants. ISO 11267:2014. Geneva, SwitzerlandGoogle Scholar
  25. ISO (International Organization for Standardization) (2012) Soil quality – Determination of the effects of pollutants on soil flora – Part 2: Effects of chemicals on the emergence and growth of higher plants. ISO 11269-2:2012. Geneva, SwitzerlandGoogle Scholar
  26. ISO (International Organization for Standardization) (2008) Soil quality – Avoidance test for testing the quality of soils and effects of chemicals on behaviour – Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei). 17512–1:2008. Geneva, SwitzerlandGoogle Scholar
  27. Jensen J, Smith SR, Krogh PH, Versteeg DJ, Temara A (2007) European risk assessment of LAS in agricultural soil revisited: species sensitivity distribution and risk estimates. Chemosphere 69:880–892CrossRefGoogle Scholar
  28. Kliegel W (1980) Bor in Biologie, Medizin und Pharmazie: Physiologische Wirkungen und Anwendung von Borverbindungen. Springer-Verlag, Berlin, GermanyCrossRefGoogle Scholar
  29. Kot FS (2009) Boron sources, speciation and its potential impact on health. Rev Environ Sci Biotechnol 8:3–28CrossRefGoogle Scholar
  30. Krogh PH (2009) Toxicity testing with the Collembolans Folsomia fimetaria and Folsomia candida and the results of a ringtest. Danish Ministry of the environment, environmental project No. 1256, DenmarkGoogle Scholar
  31. OECD (Organization for Economic Cooperation and Development) (2000) Soil microorganisms: nitrogen transformation test. OECD guideline for the testing of chemicals No. 216. Paris, FranceGoogle Scholar
  32. OECD (Organization for Economic Cooperation and Development) (2005) Guidance document on the validation and international acceptance of new or updated test methods for hazard assessment. OECD environment, health and safety publications, series on testing and assessment No. 34. Paris, FranceGoogle Scholar
  33. OECD (Organization for Economic Cooperation and Development) (2008) Predatory mite (Hypoaspis (Geolaelaps) aculeifer) Reproduction test in soil. OECD guideline for the testing of chemicals No. 226. Paris, France.Google Scholar
  34. OECD (Organization for Economic Cooperation and Development) (2009) Collembolan reproduction test in soil. OECD guideline for the testing of chemicals No. 232. Paris, France.Google Scholar
  35. OECD (Organization for Economic Cooperation and Development) (2010) Guidance document on the determination of the toxicity of a test chemical to the dung beetle Aphodius constans. OECD guideline for the testing of chemicals No. 122. Paris, France.Google Scholar
  36. Owojori O, Healey J, Princz J, Siciliano SD (2011) Can avoidance behaviour of the mite Oppia nitens be used as a rapid toxicity test for soils contaminated with metals or organic chemicals? Environ Toxicol Chem 30:2594–2601CrossRefGoogle Scholar
  37. Owojori O, Waszak K, Römbke J (2014) Avoidance and reproduction tests with the predatory mite Hypoaspis aculeifer: effects of different chemical substances. Environ Toxicol Chem 33:230–237CrossRefGoogle Scholar
  38. Peijnenburg W, Capri E, Kula C, Liess M, Luttik R, Montforts M, Nienstedt K, Römbke J, Sousa JP, Jensen J (2012) Evaluation of exposure metrics for effect assessment of soil invertebrates. Crit Rev Env Sci Tec 42:1862–1893CrossRefGoogle Scholar
  39. Peylo A (2000) Bor im Holzschutz – Gibt es neue Erkenntnisse? Der praktische Schädlingsbekämpfer 52:28–31Google Scholar
  40. Posthuma L, Suter GW, Traas TP (2002) Species sensitivity distributions in ecotoxicology. Lewis Publishers, CRC Press, Boca Raton, FLGoogle Scholar
  41. Princz J (2004) Inter-laboratory validation of environment Canada’s new test methods for measuring soil toxicity using earthworms. Environment Canada, Ottawa, ONGoogle Scholar
  42. Princz J (2006) Inter-laboratory validation of environment Canada’s new test methods for measuring soil toxicity using plants. Environment Canada, Ottawa, ONGoogle Scholar
  43. Princz JI, Behan-Pelletier VM, Scroggins RP, Siciliano SD (2010) Oribatid mites in soil toxicity testing – the use of Oppia nitens as a new test species. Environ Toxicol Chem 29:971–979CrossRefGoogle Scholar
  44. Ratte HT (2007) Versuch einer politischen und wissenschaftlichen Standortbestimmung. UWSF – Zeitschrift für Umweltchemie und Ökotoxikologie 19(Special Issue 1):30–34CrossRefGoogle Scholar
  45. Römbke J, Ahtiainen J (2007) The search for the ‘ideal’ soil toxicity test reference substance. Integrated Environ Assess Manag 3:464–466CrossRefGoogle Scholar
  46. Silva PV, Silva ARR, Mendo S, Loureiro S (2014) Toxicity of tributyltin (TBT) to terrestrial organisms and its species sensitivity distribution. Sci Total Environ 466–467:1037–1046CrossRefGoogle Scholar
  47. Smit CE, Moser T, Römbke J (2012) A new OECD test guideline for the predatory soil mite Hypoaspis aculeifer: results of an international ring test. Ecotoxicol Environ Saf 82:56–62CrossRefGoogle Scholar
  48. Stantec Consulting Ltd, Aquaterra Environmental Consulting Ltd (2004) Developmental studies in support of environment Canada’s biological test methods for measuring soil toxicity using earthworms. Guelph, ONGoogle Scholar
  49. Stegger P, Ebke KP, Römbke J (2011) Boric acid as alternative reference substance for earthworm field tests. J Soils Sediments 11:330–335CrossRefGoogle Scholar
  50. Stephenson GL (2003) Terrestrial test methods for plants and soil invertebrates. Dissertation, University of GuelphGoogle Scholar
  51. US EPA (US Environmental Protection Agency) (1993) Re-registration eligibility decision facts – Boric acid: prevention, pesticides and toxic substances (7508W). EPA-738-F-93-006. Washington, USAGoogle Scholar
  52. VICH (International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products) (2005) Guideline on environmental impact assessment for veterinary medicinal products phase II guidance. European Medicines Agency, London, United Kingdom, VICH GL 38, CVMP/VICH/790/03/Google Scholar
  53. Wagner C, Løkke H (1991) Estimation of ecotoxicological protection levels from NOEC toxicity data. Water Res 25:1237–1242CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Juliska Princz
    • 1
  • Leonie Becker
    • 2
    • 3
  • Adam Scheffczyk
    • 2
  • Gladys Stephenson
    • 4
  • Rick Scroggins
    • 1
  • Thomas Moser
    • 2
  • Jörg Römbke
    • 2
  1. 1.Environment and Climate Change CanadaBiological Assessment and Standardization SectionOttawaCanada
  2. 2.ECT Oekotoxikologie GmbHFlörsheimGermany
  3. 3.Institute for Ecology, Evolution and Diversity, Goethe UniversityFrankfurt am MainGermany
  4. 4.Aquaterra Environmental Consulting Inc.OrtonCanada

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