Skip to main content
SpringerLink
Log in

Exposure Impacts of Environmentally Relevant Concentrations of a Glufosinate Ammonium Herbicide Formulation on Larval Development and Thyroid Histology of Xenopus laevis

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Thyroid hormones play critical roles in body growth and development as well as reproduction. They also influence the activities of a wider variety of tissues and biological functions, such as osmoregulation, metabolism, and especially metamorphosis in organisms, such as frogs. These complex activities of thyroid hormones are prone to disruption by agricultural pesticides, often leading to modulation of growth and the reproductive system in particular. These substances include Glufosinate ammonium, Glyphosates, Imazapyr, Penoxsulam, and Diquat dibromide among other herbicides. In this study, the standardized Xenopus Metamorphosis Assay protocol was used to assess the potential thyroid-modulatory properties of the Glufosinate ammonium Basta formulation, at relevant environmental concentrations (0.05 mg/L, 0.15 mg/L, and 0.25 mg/L) for 21 days. The results showed that this formulation only reduced the hind-limb length among the morphological endpoints. Histological evaluation showed that the mean thyroid gland area and the mean thyroidal follicle epithelium height were significantly increased following 0.15 and 0.25 mg/L exposures. The present study confirmed that this Basta formulation interacts with the thyroid axis and therefore potentially pose health hazard to amphibian in particular and potentially metamorphic aquatic vertebrates. Furthermore, the result is a signal of inherent potential thyroid disrupting activities that must be further investigated and characterised in some of the aquatic herbicide formulations to safeguard the aquatic biodiversity.

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

  • Archer E, Petrie B, Kasprzyk-Horden B, Wolfaardt GM (2017) The fate of pharmaceuticals and personal care products (PPCPs), endocrine disrupting contaminants (EDCs), metabolites and illicit drugs in a WWTW and environmental waters. Chemosphere 174:437–446

    CAS  Google Scholar 

  • American Society for Testing and Materials (ASTM) (1998) Standard guide for conducting the frog embryo teratogenesis assay–Xenopus. E1439–98. In: Annual book of ASTM standards, vol 11.06. American Society for Testing and Materials, Philadelphia, pp 825–36

  • Babalola OO, van Wyk JH (2018) Comparative early life stage toxicity of African clawed frog, X. laevis following exposure to selected herbicide formulations applied to eradicate alien plants in South Africa. Arch Environ Contam Toxicol. https://doi.org/10.1007/S00244-017-0463-0

    Article  Google Scholar 

  • Bancroft JD, Stevens A (1977) Theory and practice of histological techniques. Churchill Livingstone, Edinburg

    Google Scholar 

  • Bergman A, Heindel J, Jobling S, Kidd K, Zoeller RT (2012) State of the science of endocrine-disrupting chemicals 2012. WHO & UNEP, Geveva

    Google Scholar 

  • Bergman A, Andersson A, Becher G, van den Berg M, Blumberg B, Bjerregaard P, Bornehag C, Bornman R, Brandt I, Brian JV, Casey SC, Fowler PA, Frouin H, Giudice LC, Iguchi T, Hass U, Jobling S, Juu A, Kidd KA, Kortenkamp A, Lind M, Martin OV, Muir D, Ochieng R, Olea N, Norrgren L, Ropstad RE, Ross PS, Rudén C, Scheringer M, Skakkebaek NE, Söder O, Sonnenschein C, Soto A, Swan S, Toppari J, Tyler CR, Vandenberg LR, Vinggaard AM, Wiberg K, Zoeller RT (2013) Science and policy on endocrine disrupters must not be mixed: a reply to a “common sense” intervention by toxicology journal editors. Environ Health 12:69

    Google Scholar 

  • Brande-Lavridsen N, Christensen-Dalsgaard J, Korsgaard B (2010) Effects of ethinylestradiol and the fungicide prochloraz on metamorphosis and thyroid gland morphology in L. temporaria. Open Zool J 3:7–16

    CAS  Google Scholar 

  • Brucker-Davis F (1998) Effects of environmental synthetic chemicals on thyroid function. Thyroid 8:827–849

    CAS  Google Scholar 

  • Coady KK, Murphy MB, Villeneuve DL, Hecker M, Carr JA, Solomon KR, Smith EE, Van Der Kraak G, Kendall RJ, Giesy JP (2005) Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, sex steroid hormones, and aromatase activity in juvenile X. laevis. Ecotoxicol Environ Saf 62(2):160–173

    CAS  Google Scholar 

  • Coady KK, Marino T, Thomas J, Currie R, Hancock G, Crofoot J, Mcnalley L, Mcfadden L, Geter D, Klecka G (2010) Evaluation of the amphibian metamorphosis assay: exposure to the goitrogen methimazole and the endogenous thyroid hormone-thyroxine. Environ Toxicol Chem 29(4):869–880

    CAS  Google Scholar 

  • Coady K, Marino T, Thomas J, Sosinski L, Neal B, Hammond L (2013) An evaluation of 2,4-dichlorophenoxyacetic acid in the amphibian metamorphosis assay and the fish short-term reproduction assay. Ecotoxicol Environ Saf 90:143–150

    CAS  Google Scholar 

  • Crump D, Werry K, Veldhoen N, Van Aggelen G, Helbing CC (2002) Exposure to the herbicide acetochlor alters thyroid hormone-dependent gene expression & metamorphosis in X. laevis. Environ Health Perspect 110:1199–1205

    CAS  Google Scholar 

  • Decherf S, Seugnet I, Fini JB, Clerget-Froidevaux MS, Demeneix BA (2010) Disruption of thyroid hormone-dependent hypothalamic set-points by environmental contaminants. Mol Cell Endocrinol 323:172–182

    CAS  Google Scholar 

  • Degitz SJ, Holcombe GW, Flynn KM, Kosian PA, Korte JJ, Tietge JE (2005) Progress towards development of an amphibian-based thyroid screening assay using Xenopus laevis. Organismal and thyroidal responses to the model compounds 6-propylthiouracil, methimazole, and thyroxine. Toxicol Sci 87(2):353–364

    CAS  Google Scholar 

  • Denver RJ (2013) Neuroendocrinology of amphibian metamorphosis. Curr Top Dev Biol 103:195–227

    CAS  Google Scholar 

  • Ebert E, Leist KH, Mayer D (1990) Summary of safety evaluation toxicity studies of glufosinate ammonium. Food Chem Toxicol 28:339–349

    CAS  Google Scholar 

  • EPA (2011) pesticides industry sales and usage 2006 and 2007 market estimates. U.S. Environmental Protection Agency. Biological and Economic Analysis Division Office of Pesticide Programs Office of Chemical Safety and Pollution Prevention U.S. Environmental Protection Agency Washington, DC 20460. www.epa.gov/documents/pesticides.

  • Faber MJ, Thompson DG, Stephenson GR, Boermans HJ (1998) Impact of glufosinate-ammonium and bialaphos on the phytoplankton community of a small eutrophic northern lake. Environ Toxicol 17(7):1282–1290

    CAS  Google Scholar 

  • Grim KC, Wolfe M, Braunbeck T, Iguchi T, Ohta Y, Tool O, Touart L, Wolf DC, Tietge J (2009) Thyroid histopathology assessments for the amphibian metamorphosis assay to detect thyroid-active substances. Toxicol Pathol 37:415–424

    CAS  Google Scholar 

  • Hack R, Ebert E, Ehling G, Leist KH (1994) Glufosinate ammonium—some aspects of its mode of action in mammals. Food Chem Toxicol 32(5):461–470

    CAS  Google Scholar 

  • Hayes TB, Khoury V, Narayan A, Nazir M, Park A, Brown T, Adame L, Chan E, Bucholz D, Stueve T, Gallipeau S (2010) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). PNAS 107:4612–4617

    CAS  Google Scholar 

  • Hill MP, Coetzee J (2017) The biological control of aquatic weeds in South Africa: current status and future challenges. Bothalia 47(2):190–198. https://doi.org/10.4102/abc.v47i2.2152

    Article  Google Scholar 

  • Jewell WT, Hess RA, Miller MG (1998) Testicular toxicity of molinate in the rat: metabolic activation via sulfoxidation. Toxicol Appl Pharmacol 149:159–166

    CAS  Google Scholar 

  • Jobling S, Tyler CR (2003) Endocrine disruption in wild freshwater fish. Pure Appl Chem 75:2219–2223

    CAS  Google Scholar 

  • Jones DK, Hammond J, Relyea RA (2011) Competitive stress can make the herbicide Roundup more deadly to larval amphibians. Environ Toxicol Chem 30:446–454

    CAS  Google Scholar 

  • Kataoka H, Ryu S, Sakiyama N, Makita M (1996) Simple and rapid determination of the herbicides glyphosate and glufosinate in river water, soil and carrot samples by gas chromatography with flame photometric detection. J Chromatogr A 726(1–2):253–258

    CAS  Google Scholar 

  • Kloas W, Lutz I, Einspanier R (1999) Amphibians as a model to study endocrine disruptors: II. Estrogenic acitivity of environmental chemicals in vitro and in vivo. Sci Total Environ 225:59–68

    CAS  Google Scholar 

  • Kloas W, Urbatzka R, Opitz R, Würtz S, Behrends T, Hermelink B, Hofmann F, Jagnytsch O, Kroupova H, Lorenz C, Neumann N, Pietsch C, Trubiroha A, Van Ballegooy C, Wiedemann C, Lutz I (2009) Endocrine disruption in aquatic vertebrates. Trends Comp Endocrinol Neurobiol 1163:187–200

    CAS  Google Scholar 

  • Koyama K, Koyama K, Goto K (1997) Cardiovascular effects of herbicide containing glufosinate and a surfactant: in vitro & in vivo analyses in rat. Toxicol Appl Pharmacol 145:409–414

    CAS  Google Scholar 

  • Marlatt VL, Veldhoen N, Lo BP, Bakker D, Rehaume V, Vallée K, Haberl M, Shang D, van Aggelen GC, Skirrow RC, Elphick JR, Helbing CC (2013) Triclosan exposure alters postembryonic development in a Pacific tree frog (Pseudacris regilla) Amphibian Metamorphosis Assay (TREEMA). Aquatic Toxicol 126:85–94

    CAS  Google Scholar 

  • Miyata K, Ose K (2012) Thyroid hormone-disrupting effects and the amphibian metamorphosis assay. J Toxicol Pathol 25:1–9

    CAS  Google Scholar 

  • Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). North-Holland Publishing Co., Amsterdam

    Google Scholar 

  • Nugegoda D, Kibria G (2017) Effects of environmental chemicals on fish thyroid function: Implications for fisheries and aquaculture in Australia. Gen Comp Endocrinol 244:40–53

    CAS  Google Scholar 

  • Opitz R, Braunbeck T, Bo¨gi C, Pickford DB, Nentwig G, (2005) Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid disrupting activities of environmental compounds. Environ Toxicol Chem 24(3):653–664

    CAS  Google Scholar 

  • Opitz R, Hartmann S, Blank T, Braunbeck T, Lutz I, Kloas W (2006a) Evaluation of histological and molecular endpoints for enhanced detection of thyroid system disruption in Xenopus laevis tadpoles. Toxicol Sci 90:337–348

    CAS  Google Scholar 

  • Opitz R, Lutz I, Nguyen NH, Scanlan TS, Kloas W (2006b) Analysis of thyroid hormone receptor beta A mRNA expression in Xenopus laevis tadpoles as a means to detect agonism and antagonism of thyroid hormone action. Toxicol Appl Pharmacol 212:1–13

    CAS  Google Scholar 

  • Organization for Economic Cooperation and Development (2009) Guideline for the testing of Chemicals: the amphibian metamorphosis assay. OECD Series on Testing and Assessment, Paris, p 2009

    Google Scholar 

  • Organisation for Economic Cooperation and Development (2007)Validation of the amphibian metamorphosis assay as a screen for thyroid-active chemicals: integrated summary report. AMA integrated report.https://www.oecd.org/officialdocuments. Accessed Mar 2019.

  • Organisation for Economic Co-operation and Development (OECD) (2008) Series on testing and assessment. No. 91. Report of the validation of the amphibian metamorphosis assay (PHASE 3) ENV/JM/MON 18. www.oecd.org/officialdocuments. Accessed Jan 2018.

  • Qian K, He S, Tang T, Shi T, Li J, Cao Y (2011) A rapid liquid chromatography method for determination of glufosinate residue in maize after derivatisation. Food Chem 127(2):722–726

    CAS  Google Scholar 

  • Rosenfeld CS, Denslow ND, Orlando EF, Gutierrez-Villagomez JM, Trudeau VL (2017) Neuroendocrine disruption of organizational and activational hormone programming in poikilothermic vertebrates. J Toxicol Environ Health B Crit Rev 20:276–304

    CAS  Google Scholar 

  • Saka M, Tada N, Kamata Y (2013) Application of an amphibian metamorphosis assay to the testing of the chronic toxicity of three rice paddy herbicides: Simetryn, mefenacet and thiobencarb. Ecotoxicol Environ Saf 92:135–143

    CAS  Google Scholar 

  • Shi YB (1999) Amphibian metamorphosis: from morphology to molecular biology. Wiley, New York

    Google Scholar 

  • Shi H, Zhu P, Guo S (2012) Effects of tributyltin on metamorphosis and gonadal differentiation of Xenopus laevis at environmentally relevant concentrations. Toxicol Industrial Health 30:1–7

    Google Scholar 

  • Sparling DW (2016) Ecotoxicology essentials: environmental contaminants and their biological effects on animals and plants. Academic Press, New York

    Google Scholar 

  • Tan SW, Zoeller RT (2007) Integrating basic research on thyroid hormone action into screening & testing programs for thyroid disruptors. Crit Rev Toxicol 37:5–10

    CAS  Google Scholar 

  • Tata JR (1998) Amphibian metamorphosis as a model for studying the developmental actions of thyroid hormone. Cell Res 8:259–272

    CAS  Google Scholar 

  • Tietge JE, Holcombe GW, Flynn KM, Kosian PA, Korte JJ, Anderson LE, Wolf DC, Degitz SJ (2005) Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology. Environ Toxicol Chem 24:926–933

    CAS  Google Scholar 

  • Tietge JE, Degitz SJ, Haselman JT, Butterworth BC, Korte JJ, Lindberg-Livingston KPA, AJ, Burgess EM, Blackshear PE, Hornung MW, (2013) Inhibition of the thyroid hormone pathway in X. laevis by 2-mercaptobenzothiazole. Aquatic Toxicol 126:128–136

    CAS  Google Scholar 

  • van Wyk JH (2013) Thyroid-disrupting activity in the South African aquatic environment. South Africa, Water Research Commission, Pretoria, p 138

    Google Scholar 

  • Wagner N, Wolfram R, Hanka T, Beatrix T, Stefan L (2013) Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environ Toxicol Chem 32(8):1688–1700

    CAS  Google Scholar 

  • Wagner N, Muller H, Viertel B (2017) Effects of a commonly used glyphosate-based herbicide formulation on early developmental stages of two anuran species. Environ Sci Pollut Res Int 24:1495–1508

    CAS  Google Scholar 

  • Yun Z, Kai W, Junxue W, Hongyan Z (2014) Field dissipation and storage stability of glusosinate ammonium and its metabolites in soil. Int J Anal Chem 2014:1–8

    Google Scholar 

  • Zoeller RT (2007) Environmental chemicals impacting the thyroid: targets and consequences. Thyroid 17:811–817

    CAS  Google Scholar 

Download references

Funding

This study was supported by the Water Research Commission, South Africa, Research grant (Grant number K5/1952), as well as the Working for Water Department, Ministry of Water Affairs, South Africa, for the supply of all the herbicides used for this study. We declare that both the Water Research Commission and Working for Water Department, both in South Africa, did not in any way contribute to the design of the experiment, data analysis, as well as report writing and our choice of publication.

Author information

Authors and Affiliations

  1. Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

    Oluwaseun O. Babalola, J. Christoff Truter, Edward Archer & Johannes H. van Wyk

  2. Zoology and Environmental Biology, Lagos State University, Lagos, Nigeria

    Oluwaseun O. Babalola

  3. Department of Microbiology, Stellenbosch University, Stellenbosch, South Africa

    Edward Archer

  4. Department of Paraclinical Sciences, University of Pretoria, Pretoria, South Africa

    J. Christoff Truter

Authors
  1. Oluwaseun O. Babalola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Christoff Truter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward Archer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Johannes H. van Wyk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oluwaseun O. Babalola.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest in financial, relationship, or otherwise.

Ethics Approval

All the use of animals, their housing, breeding and exposure were approved by the Animal Research Ethical Committee of the Stellenbosch University (Approval no-SU-ACUM 12–15).

Appendix

Appendix

See Table 2 .

Table 2 The Gas chromatography analytical results with very low variations compared to the predicted nominal concentrations). The limit of detection was 0.05 μg/L
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Babalola, O.O., Truter, J.C., Archer, E. et al. Exposure Impacts of Environmentally Relevant Concentrations of a Glufosinate Ammonium Herbicide Formulation on Larval Development and Thyroid Histology of Xenopus laevis. Arch Environ Contam Toxicol 80, 717–725 (2021). https://doi.org/10.1007/s00244-020-00758-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-020-00758-3

Keywords

Search

Navigation