Skip to main content
SpringerLink
Log in

The impact of humic acid on toxicity of individual herbicides and their mixtures to aquatic macrophytes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study investigates the impact of humic acid (HA) on the toxicity of selected herbicides and their binary mixtures to aquatic plants. The focus was on two auxin simulators (2,4-D and dicamba) and two photosynthetic inhibitors (atrazine and isoproturon). The results suggested that the addition of HA to the standard synthetic medium does not affect Lemna minor growth nor the toxicity of atrazine, but increases the toxicity of 2,4-D and the binary mixture of atrazine and 2,4-D. The addition of HA to the standard synthetic medium reversibly decreased the growth (biomass) of Myriophyllum aquaticum and enhanced the toxicity of individually tested herbicides (isoproturon and dicamba) as well as their binary mixture. The results showed delayed toxic effects of auxin simulators, especially 2,4-D in the Lemna test. The recovery after the exposure to individual photosystem II inhibitors (atrazine and isoproturon) is fast in both plant species, regardless of the presence of HA. In the case of selected mixtures (atrazine + 2,4-D and isoproturon + dicamba), recovery of both plant species was noted, while the efficiency depended on the herbicide concentration in the mixture rather than the presence or absence of HA.

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

Similar content being viewed by others

References

  • Altenburger R, Arrhenius Å, Backhaus T, Coors A, Faust M, Zitzkat D (2013a) Ecotoxicological combined effects from chemical mixtures part 1: relevance and adequate consideration in environmental risk assessment of plant protection products and biocides. Federal Environment Agency (Umweltbundesamt) Wörlitzer Platz 1 06844 Dessau-Roßlau Germany, ISSN 1862-480

  • Altenburger R, Backhaus T, Boedeker W, Faust M, Scholze M (2013b) Simplifying complexity: mixture toxicity assessment in the last 20 years. Environ Toxicol Chem 32(8):1685–1687

    Article  CAS  Google Scholar 

  • Brain RA, Hosmer AJ, Desjardins D, Kendall TZ, Krueger H, Wall SB (2012) Recovery of duckweed from time-varying exposure to atrazine. Environ Toxicol Chem 31(5):1121–1128

    Article  CAS  Google Scholar 

  • Chefetz B, Yitzhak IB, Polubesova T (2004) Sorption-desorption behavior of triazine and phenylurea herbicides in Kishon river sediments. Water Res 38:4383–4394

    Article  CAS  Google Scholar 

  • Coors A, Frische T (2011) Predicting the aquatic toxicity of commercial pesticide mixtures. Environ Sci Eur 23:22

    Article  CAS  Google Scholar 

  • Ebke KP, Felten C, Doren L (2013) Impact of heterophylly on the sensitivity of Myriophyllum aquaticum biotests. Environ Sci Eur 25:1–9

    Article  Google Scholar 

  • EC (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 

  • EC (European Commission) (2013) Commission regulation (EU) no 283/2013 of 1 March 2013 setting out the data requirements for active substances, in accordance with the regulation (EC) no 1107/2009 of the European parliament and of the council concerning the placing of plant protection products on the market. Official Journal of European Union L93, 84 pp

  • EFSA (2011) Conclusion on pesticide peer review: conclusion on the peer review of the pesticide risk assessment of the active substance dicamba. European Food Safety Authority (EFSA), Parma, Italy. EFSA J 9(1):1965

    Article  CAS  Google Scholar 

  • EFSA (2014) Conclusion on pesticide peer review: conclusion on the peer review of the pesticide risk assessment of the active substance 2,4-D. European Food Safety Authority (EFSA), Parma, Italy. EFSA J 12(9):3812

    Google Scholar 

  • EFSA PPR Panel (European Food Safety Authority Panel on Plant Protection Products and their Residues) (2013) Guidance on tiered risk assessment for plant protection products for aquatic organisms in edge-of-field surface waters. EFSA J 11(7):3290, 268 pp. https://doi.org/10.2903/j.efsa.2013.3290

    Article  CAS  Google Scholar 

  • EFSA PPR Panel (European Food Safety Authority Panel on Plant Protection Products and their Residues) (2018) Scientific opinion on the state of the art of toxicokinetic/toxicodynamic (TKTD) effect models for regulatory risk assessment of pesticides for aquatic organisms. EFSA J 16(8):5377, 188 pp. https://doi.org/10.2903/j.efsa.2018.5377

    Article  Google Scholar 

  • EFSA Scientific Committee (European Food Safety Authority Scientific Committee) (2016) Recovery in environmental risk assessments at EFSA. EFSA J 14(2):4313, 85 pp. https://doi.org/10.2903/j.efsa.2016.4313

    Article  CAS  Google Scholar 

  • Haitzer M, Hoss S, Traunspurger W, Steinberg C (1998) Effects of dissolved organic matter (DOM) on the bioconcentration of organic chemicals in aquatic organisms—a review. Chemosphere 37(7):1335–1362

    Article  CAS  Google Scholar 

  • Holmstrup M, Bindesbol AM, Jannekke Oostingh G, Duschl A, Scheil V, Kohler HR, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762

    Article  CAS  Google Scholar 

  • Huber SA, Balz A, Abert M, Pronk W (2011) Characterisation of aquatic humic and non-humic matter with size exclusion chromatography-organic carbon detection-organic nitrogen detection (LC-OCD-OND). Water Res 45:879–885

    Article  CAS  Google Scholar 

  • Kattwinkel M, Liess M, Arena M, Bopp S, Streissl F, Rombke J (2015) Recovery of aquatic and terrestrial populations in the context of European pesticide risk assessment. Environmental Reviews 23:382–394

    Article  CAS  Google Scholar 

  • Kienzler A, Berggren E, Bessems J, Bopp S, van der Linden S, Worth A (2014) Assessment of mixtures—review of regulatory requirements and guidance. JRC Science and Policy Reports. Luxembourg: Publications Office of the European Union, ISBN 97892-79-38479-0

  • Knauer K, Hommen U (2012) Sensitivity, variability, and recovery of functional and structural endpoints of an aquatic community exposed to herbicides. Ecotoxicol Environ Saf 78:178–183

    Article  CAS  Google Scholar 

  • Knauer K, Homazava N, Junghaus J, Werner I (2017) The influence of particles on bioavailability and toxicity of pesticides in surface water. Integr Environ Assess Manag 13(4):585–600

    Article  CAS  Google Scholar 

  • Knežević V, Tunić T, Gajić P, Savić D, Marjan P, Tenji D, Teodorović I (2016) Getting more ecologically relevant information from laboratory tests: recovery of Lemna minor after exposure to herbicides and their mixtures. Arch Environ Contam Toxicol 71:572–588

    Article  CAS  Google Scholar 

  • Laskowski R, Bednarska AJ, Kramarz PE, Loureiro S, Scheil V, Kudlek J, Holmstrup M (2010) Interactions between toxic chemicals and natural environmental factors—a meta-analysis and case studies. Sci Total Environ 408:3763–3774

    Article  CAS  Google Scholar 

  • Lipczynska-Kochany E (2018) Effect of climate change on humic substances and associated impacts on the quality of surface water and groundwater: a review. Sci Total Environ 640–641:1548–1565

    Article  CAS  Google Scholar 

  • Lokke H (2010) Novel methods for integrated risk assessment of cumulative stressors—results from the No Miracle project. Sci Total Environ 408:3719–3724

    Article  CAS  Google Scholar 

  • Maltby L, Arnold D, Arts G, Davis J, Heimbach F, Pickl C, Poulsen V (2010) Aquatic macrophyte risk assessment for pesticides. SETAC, Pensacola, FL, USA

    Google Scholar 

  • Matilainen A (2007) Removal of the natural organic matter in different stages of the drinking water treatment processes. PhD Dissertation, Tempere University of Technology

  • Monteith DT, Stoddard JL, Evans CD, de Wit HA, Forsius M, Hogasen T, Wilander A, Skjelkvale BL, Jeffries DS, Vuorenmaa J, Keller B, Kopacek J, Vesely J (2007) Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450(22):537–541

    Article  CAS  Google Scholar 

  • Nikkila A, Paulsson M, Almgren K, Blanck H, Kukkonen JVK (2001) Atrazine uptake, elimination, and bioconcentration by periphyton communities and Daphnia magna: effects of dissolved organic carbon. Environ Toxicol Chem 20(5):1003–1011

    Article  CAS  Google Scholar 

  • Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35:971–986

    Article  CAS  Google Scholar 

  • OECD (Organization for Economic Cooperation and Development) (2006) Guidelines for the testing of chemicals. Test no. 221: Lemna sp. growth inhibition test. Paris, France

  • OECD (Organization for Economic Cooperation and Development) (2011) Ring-test protocol: standardized method for investigating test substance impact on rooted aquatic macrophytes. Paris, France

  • Pflugmacher S, Spangenberg M, Steinberg CEW (1999) Dissolved organic matter (DOM) and effects on the aquatic macrophyte Ceratophyllum demersum in relation to photosynthesis, pigment pattern and activity of detoxication enzymes. J Appl Bot Food Qual 73(5-6):184–190

    CAS  Google Scholar 

  • Pflugmacher S, Pietsch C, Rieger W, Steinberg CEW (2006) Dissolved natural organic matter (NOM) impacts photosynthetic oxygen production and electron transport in coontail Ceratophyllum demersum. Sci Total Environ 357:169–175

    Article  CAS  Google Scholar 

  • Phyu YL, Palmer CG, Warne MSJ, Dowse R, Mueller S, Chapman J, Hose GC, Lim RP (2013) Assessing the chronic toxicity of atrazine, permethrin, and chlorothalonil to the cladoceran Ceriodaphnia cf. dubia in laboratory and natural river water. Arch Environ Contam Toxicol 64:419–426

    Article  CAS  Google Scholar 

  • PubChem Compound Database (2018) CID=2256.https://pubchem.ncbi.nlm.nih.gov/compound/2256. Accessed 1 November 2018

  • Ratte M, Ratte H (2014) Myriophyllum toxicity test: result of a ring test using M. aquaticum and M. spicatum grown in a water-sediment system—ring test report. OECD environment, health and safety publications, series on testing and assessment, no. 206. ENV/JM/MONO(2014)22. Paris, France

  • Reitsema RE, Meire P, Schoelynck J (2018) The future of freshwater macrophytes in a changing world: dissolved organic carbon quantity and quality and its interactions with macrophytes. Front Plant Sci 9(629):1–15

    Google Scholar 

  • Sabater S, Segner H, Posthuma L, Barcelo D (2015) The evidence—what actions are needed to effectively transfer from science to policy? An academic perspective. Environ Toxicol Chem 34(6):1208–1210

    Article  CAS  Google Scholar 

  • Spark KM, Swift RS (2002) Effect of soil composition and dissolved organic matter on pesticide sorption. Sci Total Environ 298:147–161

    Article  CAS  Google Scholar 

  • SRPS ISO (2007) Kvalitet vode—Smernice za određivanje ukupnog organskog ugljenika (TOC) i rastvorenog organskog ugljenika (DOC). Test br. 8245. Institut za standardizaciju Srbije, Beograd, Srbija (in Serbian)

  • Steinberg CEW, Paul A, Pflugmacher S, Meinelt T, Renate K, Wiegand C (2003) Pure humic substances have the potential to act as xenobiotic chemicals: a review. Fresenius Environ Bull 12(5):391–401

    CAS  Google Scholar 

  • Steinberg CEW, Meinelt T, Timofeyev MA, Bittner M, Menzel R (2008) Humic substances part 2: interactions with organisms. Environ Sci Pollut Res 15(2):128–135

    Article  Google Scholar 

  • Tarazona JV (2015) Assessing the effects of chemicals in freshwaters under multiple stress: a regulatory science perspective. Environ Toxicol Chem 34(6):1210–1211

    Article  CAS  Google Scholar 

  • Teodorović I, Knežević V, Tunić T, Čučak M, Nikolić Lečić J, Leovac A, Ivančev Tumbas I (2012) Myriophyllum aquaticum versus Lemna minor: sensitivity and recovery potential after exposure to atrazine. Environ Toxicol Chem 31(2):417–426

    Article  CAS  Google Scholar 

  • Tunić T, Knežević V, Kerkez Đ, Tubić A, Šunjka D, Lazić S, Brkić D, Teodorović I (2015) Some arguments in favour of a Myriophyllum aquaticum growth inhibition test in a water-sediment system as an additional test in risk assessment of herbicides. Environ Toxicol Chem 34(9):2104–2115

    Article  CAS  Google Scholar 

  • Van den Brink PJ (2008) Ecological risk assessment: from book-keeping to chemical stress ecology. Environ Sci Technol 142:8999–9004

    Article  CAS  Google Scholar 

  • Vighi M, Finizio A, Villa S (2006) The evolution of the environmental quality concept: from the US EPA Red Book to the European Water Framework Directive. Environ Sci Pollut Res 13:9–14

    Article  CAS  Google Scholar 

  • Yu S, Liu J, Yin Y, Shen M (2018) Interactions between engineered nanoparticles and dissolved organic matter: a review on mechanisms and environmental effects. J Environ Sci 63:198–217

    Article  Google Scholar 

Download references

Funding

This study was financially supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia via Grant No. 172028.

Author information

Authors and Affiliations

  1. Faculty of Sciences, Department of Biology and Ecology, University of Novi Sad, Trg Dositeja Obradovića 3, Novi Sad, 21 000, Serbia

    Varja Mihajlović, Tanja Tomić & Ivana Teodorović

  2. Faculty of Sciences, Department of Chemistry, Biochemistry and Environmental Protection, University of Novi Sad, Trg Dositeja Obradovića 3, Novi Sad, 21 000, Serbia

    Aleksandra Tubić, Jelena Molnar Jazić & Ivana Ivančev Tumbas

  3. Faculty of Agriculture, University of Novi Sad, Trg Dositeja Obradovića 8, Novi Sad, 21 000, Serbia

    Dragana Šunjka & Sanja Lazić

Authors
  1. Varja Mihajlović
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tanja Tomić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aleksandra Tubić
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jelena Molnar Jazić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ivana Ivančev Tumbas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dragana Šunjka
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sanja Lazić
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ivana Teodorović
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Varja Mihajlović.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 361 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mihajlović, V., Tomić, T., Tubić, A. et al. The impact of humic acid on toxicity of individual herbicides and their mixtures to aquatic macrophytes. Environ Sci Pollut Res 26, 23571–23582 (2019). https://doi.org/10.1007/s11356-019-05629-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05629-6

Keywords

Search

Navigation