Environmental Pollution 206 (2015) 275e281

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Chronic bisphenol A exposure alters behaviors of zebrafish (Danio rerio) Ju Wang a, 1, Xia Wang b, 1, Can Xiong a, Jian Liu a, Bing Hu c, Lei Zheng a, b, * a

School of Biotechnology and Food Engineering, Hefei University of Technology, Hefei, 230009, China School of Medical Engineering, Hefei University of Technology, Hefei, 230009, China c School of Life Science, University of Science and Technology of China, Hefei, 230027, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 16 December 2014 Received in revised form 5 July 2015 Accepted 14 July 2015 Available online xxx

The adult zebrafish (Danio rerio) were exposed to treated-effluent concentration of bisphenol A (BPA) or 17b-estradiol (E2) for 6 months to evaluate their effects on behavioral characteristics: motor behavior, aggression, group preference, novel tank test and light/dark preference. E2 exposure evidently dampened fish locomotor activity, while BPA exposure had no marked effect. Interestingly, BPA-exposed fish reduced their aggressive behavior compared with control or E2. Both BPA and E2 exposure induced a significant decrease in group preference, as well as a weaker adaptability to new environment, exhibiting lower latency to reach the top, more entries to the top, longer time spent in the top, fewer frequent freezing, and fewer erratic movements. Furthermore, the circadian rhythmicity of light/dark preference was altered by either BPA or E2 exposure. Our results suggest that chronic exposure of treated-effluent concentration BPA or E2 induced various behavioral anomalies in adult fish and enhanced ecological risk to wildlife. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Zebrafish Bisphenol A Behavior

1. Introduction Behavior is a crucial determinant for survival, growth and reproductive success in animals (Gerlai, 2003; Little et al., 1990; Peichel, 2004), which may affect aquatic community compositions and eco-function in adult life (Brodin et al., 2013). For example, motor behavior, aggression, group preference and novel tank test are regarded as the common and easily measured behavioral responses, which correlate to courting display, foraging, escaping from the risky area (Little et al., 1990). Furthermore, the behaviors of animals are initially presumed to be primitive and instinctive which could promote access to resources such as mates, shelter and foraging positions and antipredator defense (Brodin et al., 2013). In addition, the appropriate preference for light or dark environment is vital to the survival of the diurnal/nocturnal animals through affecting fitness of organisms (Gerlai, 2010). Interestingly, our previous study indicated that the choice of light/ dark area can be affected by circadian rhythm in zebrafish (Wang

* Corresponding author. School of Biotechnology and Food Engineering, Hefei University of Technology, Hefei, 230009, China. E-mail addresses: [email protected], [email protected] (L. Zheng). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.envpol.2015.07.015 0269-7491/© 2015 Elsevier Ltd. All rights reserved.

et al., 2014). Consequently, the modification of a wide range of behaviors in male- and female-typical animals can alter the stability of ecosystem through affecting various fitness functions such as growth, reproduction and body maintenance in the whole aquatic environment (Alvarez et al., 2005; McCarthy and Fuiman, 2008). The endocrine disrupting chemicals (EDCs) are an exogenous agent existed widely in environment, which can be accumulated and stored inside animal body (Clotfelter et al., 2004) and plant (Pan et al., 2013). Bisphenol A (BPA), as one of representative EDCs, is composed of two phenol rings and has structural homology with 17b-estradiol(E2), leading to a strong binding to both estrogen receptors (ERs) and estrogen related receptor gamma (ERRg) (Okada et al., 2008; Washington et al., 2001). BPA persists in wastewater effluent through the incomplete polymerization or gradual breakdown of BPA-containing products (Biedermann et al., 2010; Vandenberg et al., 2010; Welshons et al., 2006; Zhang et al., 2013) and can therefore be found at concentrations ranging from nondetectable to 17200 mg/L in treated effluent (Huang et al., 2012; Suzuki et al., 2004; Yamamoto et al., 2001). The evidence has shown that BPA can alter behaviors by participating in the organization of neural circuits that control wide aspects of neuroendocrine, behavioral, and cognitive functions.

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Saili et al. (2012) found that BPA led to hyperactivity of larval fish and learning deficits in adult zebrafish. Wang et al. (2013) only reported that BPA exposure altered spontaneous movement, decreased touch response and swimming speed in response to light stimulation in larval zebrafish by inducing axial muscle damage. However, numerous behavioral tasks by chronic BPA exposure are not well known. Behavioral change which could affect dominance hierarchies and alter population stability in the whole aquatic ecosystems has been largely overlooked. The behavioral changes of fish may influence aquatic community compositions and the functioning of aquatic systems. In the present study, we use adult zebrafish (Danio rerio) to evaluate the ecotoxicology in aquatic environment through behaviors (including motor behavior, aggression, group preference, novel tank test and light/dark preference) by mimicking BPA exposure in waste water effluent. 2. Materials and methods 2.1. Animals Subjects were 150 adult (4-6 months-old) zebrafish from wildtype stock (short-fin phenotype), of mixed gender in a 1:1 male: female ratio, obtained from breeding center at University of Science and Technology of China. Zebrafish was housed in the glass tanks in a dedicated “fish” room; each tank (35 cm  20 cm  23 cm, length  width  height) was held 10e15 fish. The water was dechlorinated water which contained some salts, the PH and conductivity were 7.0e8.0 and 1500e1600 ms/cm, respectively. Water temperature was maintained at about 28  C, with a 14 h light/10 h dark cycle (room fluorescent light, 08:00am-22:00pm). They were fed twice per day, at 09:00am and 14:00pm respectively, with freshly hatched brine shrimps. 2.2. Chemical exposures BPA or E2 was added to exposure tanks from stock solutions that were prepared by dissolving 30 mg BPA (98% purity; Chem Service Inc., China) in 3 mL ethanol or dissolving 10 mg E2 (98% purity; Chem Service Inc., China) in 10 mL ethanol. The final concentration of each chemical in experimental tanks was 500 mg/L or 10 mg/L for BPA or E2, respectively. The final concentration of ethanol was 0.005% in BPA or 0.001% in E2. All solutions were changed daily during the exposure periods and animals were kept in the same physical conditions of their home tanks. Before drugs exposure, 150 zebrafish were transferred to tanks in groups of 50 animals per tank. The 2 groups of adult fish were exposed for 6 months to BPA or E2 at concentrations of 500 mg/L or 10 mg/L, respectively. The BPA concentration used in this study was chosen in light of measured concentrations in treated effluent environment (Huang et al., 2012). Despite previous data reported that the lower ethanol concentrations can hardly affect the behavioral parameters of zebrafish (Gerlai, 2003; Wang et al., 2014), the volume of ethanol applied to high exposure tanks was also added to control group to a maximum concentration of 0.005%. 2.3. Behavioral tests The diagram of behavioral devices and the testing parameters of behaviors can refer to Table 1. 2.3.1. Motor behavior To assess motor behavior, the front wall of experimental tank was equally divided into seven segments in vertical direction, and three segments in horizontal direction, so the tank in water area

was consisted of thirty-five equal grids in total. The video recorded the entire number of times that the fish moved from one section into another during observation.

2.3.2. Aggressive behavior In aggressive experiment, the bottom of testing tank was divided into four equal segments by three vertical lines. A mirror was placed inclined at 22.5 to the left lateral wall of the tank (Gerlai, 2003). Fish mirror image appeared closer to it when the experimental fish swam to the left side of the tank. Therefore, fish spent the amount of time in left-most segment was quantified as the intensity of aggressive behavior.

2.3.3. Group preference In the test of group preference, the testing tank was placed in the middle, and both sides of tank were additional tanks (including empty tank and stimulus tank), the stimulus tank held 15 zebrafish as “stimulus fish”. The testing tank was divided into two equal sections with a vertical line in the front wall. The amount of time which the tested fish spent on the side of tank closer to the conspecifics was regarded as group preference or shoal.

2.3.4. Novel tank test Novel tank test was defined by ourselves which reflected the congenital characteristics in swimming behavior of zebrafish. Zebrafish had two behavioral phenomena: erratic movements were defined as sharp changes in direction or velocity and repeated rapid darting behaviors, freezing was defined as a total absence of movement, except for the gills and eyes for 1s or longer. The novel tank was divided into two equal horizontal portions and parameters of these behaviors were recorded: latency to upper half (s), time spent in the upper half (s), number of transitions to the upper half, number of erratic movements, number of freezing bouts and freezing duration (s). Zebrafish were placed individually in the tank. After half a minute habituation period, their behaviors were recorded for 6 min. A video camera with infrared feature was positioned in front of the testing tank to record the behaviors, but the aggressive behavior which was recorded in the above of the tank. The video recordings were later analyzed by recording the behavioral parameters of fish during 6-min observation. 2.3.5. Light/dark preference Zebrafish is a typical diurnal animal, and the appropriate preference for light or dark environment can certainly help them to regulate responses to the social stimulus. To test the light/dark preference, we recorded the proportion of time of fish spent in the dark area as the indicator of the light/dark preference. The detailed apparatus and methods for light/dark preference tests have been described in our previous work (Wang et al., 2014). Briefly, the aquarium consisted of a dark chamber and a light chamber, the dark chamber was covered with matter black paper on all side and the top. 10 L fresh fish water was poured into the experimental tank. Individual zebrafish was placed in the preference tank at 7:30am on day 1 and can swim freely in the entire tank, after a 30 min adaption, the video camera was positioned in the front of the tank and the recording was started from 8:00am on day 1 till 8:00am on day 3 over 48 h. The swimming trajectory of zebrafish were analyzed by fish tracking software which developed by Prof. John Y. Chiang. The experimental room was closed and kept quiet to minimize the interference from the outside, the experimenter was not visible to the fish during the recording.

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Table 1 The diagram of devices and the testing behavioral parameters. Behaviors

Parameters

References

Motor behaviora

The number of crossing the 35 segments of the tank

Gerlai, 2003

Aggressionb

Relative duration of time (%) in left segment 1

Gerlai, 2003

Group preferencea

Relative duration of time (%) spent by fish near the stimulus fish

Gerlai, 2003

Novel tank test

Latency to upper half (s), time spent in the upper half (s), number of transitions to the upper half, number of erratic movements, number of freezing bouts and freezing duration (s).

Levin et al., 2007; Stewart et al., 2012

Light/dark preference

Proportion of time spent in the dark area (%)

Wang et al., 2014

a b

Diagram of behavioral devices

The front view of experimental tank. The vertical view of experimental tank.

3. Statistical analysis

4.2. Chronic exposure to BPA or E2 affects aggression behavior

All experimental data were analyzed by one-way analysis of variance (ANOVA), followed by post hoc comparisons between the experimental groups. Significance was set at P < 0.05. Data were presented as mean ± SEM.

Responses to the mirror image of an individual conspecific were also significantly changed as a result of BPA or E2 treatment. From Fig. 2, the aggressive behavior was significantly affected by BPA exposure compared with control (F1,18 ¼ 10.67, P < 0.01). Fish exposed to BPA showed less time responding to the mirror stimulus compared to the E2 group (F1,18 ¼ 4.52, P < 0.05). However, no statistically significant difference was detected between E2 exposure groups and the control ((F1,18 ¼ 0.63, P > 0.05).

4. Results 4.1. Chronic exposure to BPA or E2 affects motor behavior Motor behavior of zebrafish, as measured by the number of grid lines when the fish crossed during a 6 min period, was affected by BPA or E2 exposure. As seen from Fig. 1, fish exposed to BPA reduced their locomotor activity slightly compared with the control (F1,18 ¼ 1.18, P ¼ 0.2917). E2 showed serious effects on zebrafish activity (F1,18 ¼ 24.74, P < 0.01), besides, there was no statistically significant difference between BPA and E2 exposure groups (F1,18 ¼ 14.01, P > 0.05).

4.3. Chronic exposure to BPA or E2 affects group preference BPA or E2 exposure also altered group preference of both male and female zebrafish as measured by the total time when fish closed to the shoal per 6 min (F1,20 ¼ 4.75, P < 0.05; F1,20 ¼ 4.44, P < 0.05, respectively) (Fig. 3). Additionally, there was no clear difference between the BPA or E2 exposure groups.

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Fig. 1. The effects of chronic BPA or E2 exposure on locomotion activity behavior in individual adult zebrafish are tested. Statistically significant differences between control and E2 are indicated (*P < 0.05 or **P < 0.01). The sample sizes are as following: control, n ¼ 10; BPA, n ¼ 10; E2, n ¼ 10.

4.4. Chronic exposure to BPA or E2 affects novel tank test Both BPA and E2 can affect the novel tank test of zebrafish (Fig. 4). As seen from Fig. 4A, BPA or E2 exposure resulted in a significantly lower latency to exposure the upper half of the tank compared with control (F1,18 ¼ 9.78, P < 0.01; F1,18 ¼ 35.22, P < 0.01, respectively). Treatment with BPA or E2 increased the number of transitions to the upper portion compared with the control group (F1,18 ¼ 6.04, P < 0.05; F1,18 ¼ 5.88, P < 0.05, respectively) in Fig. 4B. Additionally, in Fig. 4C, chronic administration of BPA or E2 made zebrafish spend more time in the top half of the tank compared with the control group (F1,18 ¼ 26.63, P < 0.01; F1,18 ¼ 16.80, P < 0.01, respectively). Besides, compared with the control group, the BPA or

Fig. 3. The effects of chronic BPA or E2 exposure on group preference in individual adult zebrafish are tested. Statistically significant differences between control and BPA or E2 are indicated (*P < 0.05 or **P < 0.01). n ¼ 11 for each group.

E2 exposure decreased the amount of erratic movement performed by zebrafish (F1,18 ¼ 7.67, P < 0.05; F1,18 ¼ 5.44, P < 0.01, respectively) (Fig. 4D). From Fig. 4E and F, the amount and duration time of freezing were also decreased in response to the E2 exposure group (F1,18 ¼ 40.09, P < 0.01; F1,18 ¼ 13.78, P < 0.01, respectively), but no statistically significant difference was detected between BPA exposure group and the control group (P > 0.05). 4.5. Chronic exposure to BPA or E2 affects light/dark preference As seen from Fig. 5, the control group displayed the circadianlike trend of light/dark preference in 2 days with the dark preference increased initially from morning (29.62%, 8:00am) to midnight (74.06%, 2:00am), and subsequently decreased till next morning (43.53%, 8:00am). Compared with the control, zebrafish from BPA or E2 exposure altered the circadian trend of light/dark preference. Although the proportion of dark preference in BPA group was slightly higher than control at 8:00am on day 1 (29.62% vs 39.81%, P > 0.05), there was a significant difference between the control and BPA group at 2:00am on day 2 (74.06% vs 55.56%, P < 0.05). The mean proportion of time spent in the dark area for the E2 exposure group was higher than the control, for example, the mean proportion of dark preference was a significant difference between the control and E2 group at 8:00am on day 1 (29.62% vs 50%, P < 0.01), but there was no difference at 2:00am on day 2 (74.06% vs 81.48%, P > 0.05). 5. Discussion

Fig. 2. The effects of chronic BPA or E2 exposure on aggressive behavior in individual adult zebrafish are tested. Statistically significant differences between control and BPA or E2 are indicated (*P < 0.05 or **P < 0.01). The sample sizes are as following: control, n ¼ 10; BPA, n ¼ 10; E2, n ¼ 10.

BPA is a primary ingredient to manufacture polycarbonate plastic and epoxy resin, and widely used as an intermediate in the production of numerous consumer products including polycarbonate bottle, resin-lined cans and some dental sealants. However, the incomplete polymerization or gradual breakdown of BPAcontaining products results in potential leaching of BPA into food or water (Biedermann et al., 2010; Liao and Kannan, 2013; Welshons et al., 2006). BPA can be found at concentrations ranging from 0.04 to 370,000 ng/L in water (Huang et al., 2012), and even can attain hundreds of thousands of ng/L in some industrial waste waters from the industrial park (Fukazawa et al., 2001). The

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Fig. 4. Novel tank test effects of chronic BPA and E2 exposure (500 mg/L or 10 mg/L for 6 month, respectively) in individual adult zebrafish (5 male and 5 female) tested in the novel tank test during 6 min *P < 0.05 or **P < 0.01. n ¼ 10 for each group.

purpose of this work is to assess whether and how low dose of BPA based on the concentration of treated effluent affects key behaviors of aquatic organisms with chronic exposure in ecotoxicological research. The individuals' behavioral traits of motor behavior, aggression, group preference and light/dark preference were tested by adult zebrafish with 6 months BPA or E2 exposure. Motor behavior is regarded as one of the most common and easily measured behavioral responses that correlate to the physiological

capacity of fish because it can generate and coordinate the locomotive energy required for basic functions such as migration or escaping predators (Little et al., 1990). One example of the importance of motor behavior for rainbow trout is maintaining position against flowing water while feeding (Little et al., 1990). Fish exposed to the BPA reduce their locomotor activity slightly, while E2 can seriously decrease the activity compared with the control (Fig. 1). BPA exposure cannot cause serious motor deficits like E2 does, the reason may be that the concentration of BPA is

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Fig. 5. Plot of the proportion of time spent in the dark area at each time of day in zebrafish in different drugs exposure (control (closed diamonds), BPA (closed squares), E2 (closed triangle)). n ¼ 9 for each group.

not high enough to disrupt the axonal growth of primary and secondary motor neurons in zebrafish (Wang et al., 2013), and E2 is associated with the defect of neurobehavioral development which may seriously affect the activity (Hamad et al., 2007). The decreased locomotor performances can increase lethargy in the shoal of fish. Aggression has extended the whole animal kingdom, and most animal species use aggression to establish dominance hierarchies with dominant individuals chasing (Basquill and Grant, 1998) and biting subordinate individuals in order to compete for food or mates. Levels of aggressiveness are related to territory ownership (Whoriskey and FitzGerald, 1994), territory size (van den Assem, 1967) and reproductive success. Zebrafish exposed to BPA shows less aggressive to the mirror stimulus compared to the control. Similar results have been observed after exposure to the other EDCs, such as nonylphenol (NP) (Xia et al., 2010) and ethinyloestradiol exposure (Bell, 2001). The mechanisms of the decreased aggression by BPA exposure associate with the regulation of testosterone and 11-ketotestosterone (Villars, 1983), inhibiting the binding of native androgens to androgen receptor or downregulation of the androgen production via BPA acts as an androgen receptor antagonist in male zebrafish (Bell, 2001; Bonefeld-Jorgensen et al., 2007; Lee et al., 2003; Sohoni and Sumpter, 1998; Xu et al., 2010). The effects of BPA or E2 on the behavior of individual animals influence the dynamics of fish populations in aquatic environments. Group preference is essential for all shoaling teleosts, and shoaling behavior can associate with foraging, spawning security, predator recognition (Pitcher, 1986). Zebrafish is a shoal species and exhibits group preference (Spence et al., 2008), shoaling behavior appears to be innate and commences soon after hatching (Engeszer et al., 2007), and fish rear in isolation quickly form shoals when they are placed together (Kerr, 1962). Shoaling behavior has many advantages for zebrafish. For example, shoal can provide a defense against predators, enhance the ability of the fish to find their own prey or mate and increase foraging success. In our results, group preference was significantly affected by BPA or E2 exposure for both male and female zebrafish compared with the control group. Similar results are found in rainbow trout (Ward et al., 2006) and killifish (Ward et al., 2008) after exposure to nonyphenol. The mechanism of group preference associate with dopaminergic system by the change of the level of dopamine, DOPAC, serotonin and 5HIAA, respectively (Scerbina et al., 2012). BPA or E2 exposure decreased the group preference which could affect dopaminergic system. Zebrafish may suffer from increased predation, decreased food acquisition and decreased the chance of reproduction if the

properties of a shoal were broken down as a result of exposure to BPA or E2. To assess more directly ecological effects of BPA and E2 exposure, we measured individual novel tank test, which are initially presumed to be primitive and instinctive (de Perera, 2004; Laland et al., 2003). Individuals spend the majority of time at the bottom when introduced into a novel condition and then expand their position of swimming to the higher portions of the tested tank (Levin et al., 2007). However, chronic BPA or E2 exposure can alter these behaviors of individuals, with lower latency to reach the top, more entries to the top, longer time spent in the top, lower and fewer frequent freezing, as well as reduced erratic movements. These findings suggest that zebrafish with BPA or E2 exposure is probably weaker adaptability to the novel environment, which may increase predation risk. Naturally, fish had the preference in light or dark area, and the appropriate preference was vital to the survival of fish, moreover, our previous research indicated that circadian clock could affect the light/dark preference of zebrafish (Wang et al., 2014). In our present results, the circadian trend of light/dark preference was significantly affected by BPA or E2 exposure compared with the control group (Fig. 5). The less obvious preference may associate with down-regulated of clock genes expression via BPA or E2 exposure in the pituitary, brain, muscle, and skin in fish (Rhee et al., 2014). BPA or E2 exposure may affect circulating pineal 5-hydroxytryptaming (5-HT) levels (Ho et al., 1985; Weber et al., 2015). As seen from Fig. 5, fish lack of sensitive to the variation from day to night by the modification of light/dark preference through BPA or E2 exposure, because circadian rhythm can alter intensity of social behavior and direct locomotor activity (Weber and Spieler, 1994; Pankseep et al., 2008). The locomotor activity may influence the proportion of dark preference in BPA and E2 group. This environmentally relevant concentration of BPA affects zebrafish behaviors is alarming, considering the extensive BPA products that are found in waters worldwide. It should also be emphasized that BPA has direct effect on zebrafish behavior which allocate to various fitness functions such as growth, reproduction and body maintenance. Our results highlight ecologically important effects, previously underappreciated effects of BPA that enters aquatic ecosystems, and calls for new attention to examine the full environmental impact of BPA residues. 6. Conclusions The research demonstrated that chronic exposure of treatedeffluent concentration BPA or E2 could be able to induce various

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Chronic bisphenol A exposure alters behaviors of zebrafish (Danio rerio).

The adult zebrafish (Danio rerio) were exposed to treated-effluent concentration of bisphenol A (BPA) or 17β-estradiol (E2) for 6 months to evaluate t...
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