Elsevier

Chemosphere

Volume 80, Issue 9, August 2010, Pages 1095-1100
Chemosphere

Acute effects of triclosan, diclofenac and carbamazepine on feeding performance of Japanese medaka fish (Oryzias latipes)

https://doi.org/10.1016/j.chemosphere.2010.04.073Get rights and content

Abstract

The toxicity of three pharmaceutical and personal care products (PPCPs) – carbamazepine (CBMZ), diclofenac (DCF), and triclosan (TCS) – was examined by measuring their effects on feeding behavior and swimming speed of adult Japanese medaka fish (Oryzias latipes). Medaka were exposed to 6.15 mg L−1 CBMZ, 1.0 mg L−1 DCF, 0.17 mg L−1 TCS, or no PPCP (control) for 9 d. Fish behaviors were monitored during days 5–9 of the exposure period. Feeding behavior (time to eat midge larvae, TE) and swimming speed (SS) of individual exposed and control fish were tracked in two dimensions, using an automated system with a digital charge-coupled device camera. As a result, feeding behavior was affected by exposure to CBMZ and DCF, while SS was altered by exposure to CBMZ and TCS. Thus, TCS, DCF and CBMZ appear to affect fish behaviors through different mechanisms. Overall, the results suggest that behavioral changes may provide a sensitive indicator for assessing the toxicity of PPCPs to aquatic organisms.

Introduction

Pharmaceuticals and personal care products (PPCPs) have recently been identified as potentially toxic chemicals in aquatic environments (Laura Martín-Díaz et al., 2009). Triclosan (TCS), diclofenac (DCF), and carbamazepine (CBMZ) are among the most frequently detected PPCPs worldwide (Kolpin et al., 2002, Ferrari et al., 2003). TCS is widely used as an antibacterial agent in many personal care products such as soaps, detergents, toothpastes, disinfectants, cosmetics and pharmaceuticals (Ying and Kookana, 2007), and its widespread use has been shown to pose a potential risk to aquatic organisms (Dussault et al., 2008). DCF is an anti-inflammatory drug with large production volumes. CBMZ is an antiepileptic drug, and its environmental persistence raises concerns about potential effects on non-target organisms (Zaremba et al., 2006). The maximum environmentally detected concentrations of these PPCPs in waste water treatment plant (WWTP) effluents were 0.269 mg L−1 TCS in Spain (Mezcua et al., 2004), 0.006 mg L−1 CBMZ and 0.002 mg L−1 DCF in Germany (Ternes, 1998). Assessing the human risk posed by PPCPs in water is a high priority; however, the impacts of these chemicals on aquatic organisms and communities are also important (Bendz et al., 2005, Dove, 2006). Our previous studies evaluated the acute toxicity of TCS, DCF and CBMZ to adult and embryos of medaka fish, and concluded that TCS and DCF may pose ecological risks to aquatic organisms (Nassef et al., 2009, Nassef et al., 2010).

Although acute lethality tests are useful for generating guidelines to protect against physiological death (i.e., mortality) of aquatic animals, these tests ignore “ecological death,” i.e., the inability to function in an ecological context when normal behaviors are altered. Such effects may occur at much lower toxicant exposures, even if animals are not overtly harmed by a contaminant. Indeed, environmental impacts in natural ecosystems often occur at concentrations well below those causing significant mortality (Jensen and Bro-Rasmussen, 1992, Cabrera et al., 1998, Norris et al., 1999, Gaworecki and Klaine, 2008). A better understanding of the toxicological effects of contaminants can be achieved by examining behavioral changes and determining how they relate to effects at other levels (Scott and Sloman, 2004). Behavioral alterations can provide estimates of endpoints for sublethal toxicity, and serve as a tool for environmental risk assessment and analysis of toxicological impact (Andrew et al., 2004).

Appropriate feeding is essential for growth and reproduction of most aquatic animals, including fish (Volkoff and Wyatt, 2009). The ability to capture prey could be impacted by prolonged exposure to low concentrations of contaminants, including PPCPs (De Lange et al., 2006, Kristen and Stephen, 2008). Swimming performance is closely related to food capture (Zeng et al., 2009), and is considered to be a primary determinant of survival in many species of fish and other aquatic animals (Jones and Hill, 1974, Taylor and McPhail, 1986). For example, De Lange et al. (2006) observed reduced locomotion in Gammarus pulex exposed to CBMZ (1–1000 ng L–1 for 1.5 h) and speculated that the reduction may interfere with feeding behavior.

Japanese medaka have been used in previous studies of basic fish biology and behavior, as well as toxicology, and the species has been proposed by the Organization for Economic Cooperation and Development for use as the standard fish for toxicology tests (Bendz et al., 2005, Organization for Economic Cooperation and Development (OECD),, 1999). Our previous research showed that exposure of medaka to sublethal concentrations of 17β-estradiol impaired sexual behavior and decreased reproductive success (Oshima et al., 2003). Significant changes in swimming speed were observed in medaka exposed to cyanide or aldicarb (Kang et al., 2009). Although previous studies used medaka to examine the accumulation and toxicity of anthropogenic chemicals, there is limited information on behavioral effects. Even though the neurotoxicity of PPCPs has been characterized in non-target species (Gao and Chuang, 1992, Gokcimen et al., 2007), the effects on behavior of aquatic organisms have not been well studied. The goal of the present study was to investigate the effects of sublethal concentrations of two pharmaceuticals (CBMZ and DCF) and one personal care product (TCS) on the behavior of Japanese medaka (Oryzias latipes). Based on ecological relevance, feeding behavior and swimming performance of medaka were chosen as indicators of TCS, DCF and CBMZ toxicity to aquatic animals.

Section snippets

Test chemicals

TCS (>98.0% purity), DCF (>98.0% purity), CBMZ (>97.0% purity) and dimethyl sulfoxide (DMSO, >99.0% purity) were obtained from Wako Pure Chemical Industries Ltd. (Tokyo, Japan). Stock solutions (1.7 mg mL–1 TCS, 1.0 mg mL–1 DCF, and 6.15 mg mL–1 CBMZ) were prepared by dissolving pure chemicals in DMSO, and stored prior to use. Treatment solutions were prepared by mixing appropriate amounts of stock solutions with 1 L of artificial seawater (0.01% salinity). PPCP concentrations in treatment solutions

Results

Exposure to TCS had no significant effect on time to eat the midge larva (TE) by medaka, but did significantly decrease mean swimming speed (SS) on days 6 and 8 (Fig. 2). Conversely, exposure to DCF increased TE in exposed fish compared to controls (Fig. 3A); on days 8 and 9, most of the medaka did not eat the larvae at all and the number of fish did not eat ML was four and five fish, respectively. However, exposure to DCF had no significant effect on SS (Fig. 3B). Similarly to DCF, exposure to

Discussion

Results of the present study clearly showed that feeding behavior of medaka was affected by exposure to DCF and CBMZ at concentrations of 1.0 and 6.15 mg L–1, respectively, but not by exposure to TCS at 0.17 mg L–1. On the other hand, swimming speed was affected by exposure to TCS and CBMZ, but not by exposure to DCF. Thus, the mechanisms of the behavioral effects appear to be different for each chemical.

The observed effects of exposure to TCS, DCF and CBMZ on SS of medaka are similar to effects on

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