Elsevier

Chemosphere

Volume 243, March 2020, 125288
Chemosphere

Effect of triadimefon and its metabolite on adult amphibians Xenopus laevis

https://doi.org/10.1016/j.chemosphere.2019.125288Get rights and content

Highlights

  • Triadimefon and its metabolite potentially affected X. laevis by endocrine-disrupting.

  • 2. Different levels of triadimenol exerted distinct effect on swimming activity.

  • There were sex differences on the antioxidant enzyme activity.

  • Triadimefon produced more effects on liver pathology than triadimenol.

  • There were sex differences on liver histology and thyroid hormone.

Abstract

The decrease in the population of amphibians all over the world has raised concerns. Adult X. laevis frogs were exposed to 0, 1 and 10 mg/L triadimefon and triadimenol. After 14 or 28 days exposure, we collected male and female specimens to study swimming activity, lactic dehydrogenase (LDH) and antioxidant enzyme activity in blood samples, histopathology of liver and thyroid tissue, thyroid hormone levels and thyroid hormone-related gene expression levels in brains. Our results showed that triadimefon and triadimenol could affect the swimming activity of frogs and that this was distinct at different levels of triadimenol. Moreover, triadimefon and triadimenol exposure produced a greater effect on superoxide dismutase (SOD) in females than in males, which was reverse to the finding for glutathione S-transferase (GST) and catalase (CAT). After 28 days exposure, triadimefon produced more toxic effects on the liver than observed for triadimenol. Besides this, triadimefon and triadimenol exposure exerted a greater effect on liver histology and thyroid hormone levels in male frogs than in the females. Our results also found that the expression of genes related to thyroid hormone in brains depended on the exposure level and time, as well as the sex of the treated individual. This study shed light on the relationships between the toxicity of metabolite products and their parent compounds and provided further understanding of the risk of pesticide use on amphibians.

Introduction

The world-wide decrease in the population of amphibians is of significant concern. In 2008, the International Union for Conservation of Nature (IUCN) Red List of Threatened Animals revealed that 32% of the over 6200 species of amphibians are either threatened or endangered and that one-third of amphibians are in decline (Houlahan and Findlay, 2003). This decline was attributed to exposure to pollution, including pesticides (Gibbons et al., 2000), which likely flow into amphibian habitats by runoff and aerial drift (Dabrowski et al., 2002). Moreover, some habitats are situated in agricultural sites where pesticides were applied, often during larval breeding and development periods (Mann et al., 2009). Therefore, it is imperative to assess the risk that pesticides pose to amphibian survival.

One such pollutant, Triadimefon [1-(4-chlorophenoxy)-3,3-dimethyl-1-(1H-1,2,4-triazol-1-yl)-2-butanone] is a 1,2,4-triazole fungicide with excellent antifungal activity. Triadimefon (Fig. 1) is metabolized to the more active triadimenol, [β-(4-chlorophenoxy)-R-(1,1-dimethylethyl)-1H-1,2,4-triazole-1-ethanol], which is also an agricultural fungicide (Huston et al., 1999). Once triadimefon reaches water, however, it becomes stable; in water with a pH of 3.0, 6.0, or 9.0, almost 95% of the compound remained after 28 weeks (Garrison et al., 2011). In water-samples collected in southern Sweden during May–September 1992–1996, Triadimenol was found in concentrations up to 3 μg/L (Kreuger, 1998). The estimated expected environmental concentration (EEC) for triadimefon is 41 μg/L (Zhang et al., 2018).

In general, the pesticide parent compound is more toxic to biota than its metabolite product. However, when a metabolite product has higher mobility compared to the parent, the less toxic pesticide metabolite product may still potentially produce an adverse impact on the environment (Kolpin et al., 2001). Thus, it is vital to assess the risk of pesticide metabolite products to the environment. The LC50 for the technical formulation of triadimefon in rainbow trout, bluegill sunfish, and goldfish are 14, 11, and 10 mg/L, respectively (Garrison et al., 2011). The United States Environmental Protection Agency classifies triadimenol as moderately toxic, similar to the toxicity of triadimefon for rainbow trout and bluegill, with LC50s of 19 and 15 mg/L, respectively (Kenneke et al., 2009). Their strong fungicidal effect is a result of the inhibition of cytochrome (CYP) P-450 dependent C14 demethylation of lanosterol, an intermediate in ergosterol biosynthesis (Konwick et al., 2006). Thus, triadimefon and triadimenol also have the potential to produce endocrine-related side effects in wildlife and humans, especially amphibians, whose entire development and growth are regulated by thyroid hormone. Consequently, it is important to assess the influence of triadimefon and triadimenol on amphibians.

Amphibian species are susceptible to contaminants in wastewater discharged from agricultural fields, industrial and household areas, some of which can influence development (Qin et al., 2003; Hayes et al., 2010). Xenopus laevis is a reliable experimental amphibian organism, which is easy to maintain under laboratory conditions, has permeable skin and displays high sensitivity to environmental chemicals. A previous study showed that triadimefon and triadimenol could inhibit metamorphic development of tadpoles, with triadimefon exerting a more inhibitory effect than triadimefon at high levels (10 mg/L) (Zhang et al., 2018). However, to date there has been only a few studies comparing the toxicological effects of triadimefon and triadimenol on adult X. laevis.

In our study, we monitored the biological effects on X. laevis adults exposed to 0, 1 and 10 mg/L triadimefon and triadimenol. After 14 and 28 days exposure, we collected male and female specimens to study swimming activity, LDH and antioxidant enzyme activity in blood, histopathology of the liver and thyroid, thyroid hormone levels and brain tissue expression levels of genes related to thyroid hormone. We aimed to explore the effect of triadimefon and its metabolism on frogs and provide further understanding of the risk of pesticide use to amphibian populations.

Section snippets

Chemicals and Xenopus laevis

Analytical grade triadimefon (>98.0%) and triadimenol (>99.0%) chemicals were sourced from Jiangsu Seven Continent Green Chemical. Tadpoles of X. laevis were purchased from the State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-environmental Sciences, and raised in 5 L tanks filled with charcoal-filtered tap water. The laboratory growth conditions used were 12 h light/12 h dark cycle at 24 ± 1 °C. We used the Nieuwkoop and Faber system to determine the

Swimming activity

As we can see from Fig. 1, swimming activity in frogs exposed to chemicals was lower than that in the acetone treated control, with the exception of the 10 mg/L triadimenol treatment group at 14 and 28 days. The decrease in activity may result in increased predation rates (Bridges, 1997). However, tadpoles spending too much time resting may not acquire adequate resources for development and growth.

There were some reports that tadpoles exposed to sublethal levels of chemical contaminants exhibit

Conclusion

Altogether, triadimefon and triadimenol were found to affect the swimming activity of frogs. At histological levels, triadimefon produced more toxic effects than triadimenol. Interestingly, the triadimefon and triadimenol exposure were noted to have sex-linked differences in antioxidant enzyme activities, liver histology, thyroid hormone levels and thyroid hormone-related gene expression in brain tissue. Based on the results for gene expression levels, we inferred that the toxicological action

Declaration of competing interest

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled.

Acknowledgment

This work was supported by fund from the National Natural Science Foundation of China (Contract Grant number: 21577171) and National Key Research and Development Program of China (2016YFD0200202).

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