Effects of water temperature on perchlorate toxicity to the thyroid and reproductive system of Oryzias latipes

Highlights

• Perchlorate and high temperature resulted in decrease of T4, but not T3.

• Heat stress aggravated perchlorate-induced thyroid hormone disruption in fish.

• Adverse effects of perchlorate on egg reproduction increased at higher water temperature.

Abstract

Water temperature is expected to increase in many parts of the world due to global climate change. The change in water temperature may affect ecosystems through alterations of the chemical properties or by affecting the susceptibility of organisms. Perchlorate can disrupt thyroid function of an organism by inhibiting iodide uptake. In the present study, the effect of water temperature on perchlorate toxicity was evaluated using Japanese medaka (Oryzias latipes). Pairs of adult medaka fish were exposed to a sublethal concentration of sodium perchlorate (100 mg/L) and a control, at a ‘low’ (26 °C), ‘medium’ (29 °C) or ‘high’ water temperature (33 °C) for seven days. The effects of the water temperature on reproduction, thyroid hormones and cortisol concentrations were determined. Transcription of several genes related to thyroid function and stress were also investigated. Significant down-regulation of thyroid hormone receptor alpha (THR-α) and beta (THR-β) transcripts and up-regulation of deiodinase 2 (DIO2) transcripts were observed in the fish exposed to perchlorate. Thyroxine (T4) concentrations were decreased, while triiodothyronine (T3) levels remained constant following exposure to perchlorate, and this effect became more pronounced under the high water temperature conditions (33 °C). Up-regulation of the DIO2 gene may explain these observations. The total number of spawned eggs decreased slightly as the water temperature increased, and this reduction became significant when fish were exposed to perchlorate. Our observations indicate that exposure to perchlorate could affect thyroid function and overall reproductive fitness, and these effects could be aggravated under high water temperatures.

Introduction

Perchlorate has been used in the manufacture of flares, fireworks, automobile airbags, and rocket propellant. Its widespread use has led to frequent detection of perchlorate in ambient waters worldwide, at levels ranging from 4 to 16 μg/L in the Colorado River in the USA (Strawson et al., 2004), and up to 60 μg/L in the Nakdong River of Korea (Quiñones et al., 2007). Perchlorate has also been detected in bottled water samples at concentrations ranging from 0.04 to 0.29 μg/L with a mean concentration of 0.07 μg/L (Her et al., 2011).

Perchlorate can disrupt thyroid function by interfering with the normal iodine uptake in thyroid follicles via competitive inhibition of the sodium/iodide symporter (McLanahan et al., 2009). Previous studies have also reported that perchlorate can impair thyroid hormone production and increase follicular epithelial cell height, hyperplasia, and hypertrophy in fish (Bradford et al., 2005, Mukhi et al., 2005). Because environmentally relevant concentrations of perchlorate could inhibit thyroid function and normal development of aquatic organisms, the potential impact of this compound in aquatic ecosystems is of growing concern (Goleman et al., 2002, Schmidt et al., 2012).

Thyroid hormones, i.e., thyroxine (T4) and triiodothyronine (T3), play a vital role in the regulation of development, growth, reproduction, and metabolism in vertebrates (Walpita et al., 2009), including teleost fish (Liu et al., 2000). Similar to mammals (Yu et al., 2010), thyroid hormone synthesis of teleosts is also regulated by feedback regulation through the hypothalamus–pituitary–thyroid (HPT) axis. Regulation of thyroid hormone homeostasis involves multiple steps, such as iodine uptake, thyroid hormone synthesis, transport, and deiodination, and binding to thyroid hormone receptors. Therefore, compounds that interact with any of these steps may interrupt the balance of thyroid hormones.

Climate change is one of the important challenges that can affect ecosystem health and chemical safety. Global atmospheric temperature is estimated to rise 1.8–4.0 °C by the end of this century (Noyes et al., 2009), and an increase in water temperature is also predicted (Harvell et al., 2002). The temperatures of Lakes Huron and Ontario in North America, which contain twenty percent of the world׳s total surface freshwater volume, increased by 2.9 °C and 1.6 °C between 1968 and 2002, respectively (Dobiesz and Lester, 2009). Between 1960 and 1990, the temperature of sea water worldwide increased by 0.14±0.04 °C per decade (Casey and Cornillon, 2001).

The change in water temperature may not only modify the chemistry of many pollutants (Schiedek et al., 2007) but may also affect the status of fish populations (Caissie, 2006). In addition, water temperature by itself may act as a stressor, and can possibly induce various physiological changes, including alterations in fish thyroid systems (Eales and Brown, 1993). Plasma T4 degradation and the T4 to T3 conversion were reported to be increased as water temperature increased in rainbow trout (Eales et al., 1982). A change in water temperature may influence the capacity of organisms to respond and react to chemical stressors. However, current understanding on the interaction between water temperature and chemical exposure in fish is still limited.

In the present study, the effect of water temperature on perchlorate toxicity to the thyroid and reproductive system of fish was evaluated. The effects on reproduction, thyroid hormone and cortisol concentrations and transcription of the genes related to thyroid function and stress were investigated in Japanese medaka (Oryzias latipes). The results of this study will help better understand the potential impact of perchlorate on fish under changing environmental conditions and develop management options for this emerging chemical in water.