Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology
Suppression and recovery of reproductive behavior induced by early life exposure to mercury in zebrafish
Graphical abstract
Introduction
Metals are a major class of pollutants in the water environment that can negatively affect the health of aquatic organisms. Among the metals, mercury (Hg) is of particular concern because of its considerable toxicity to aquatic organisms even at low concentrations (Vieira et al., 2009). Anthropogenic activities such as industry and agriculture, together with natural sources such as volcanic eruptions, have released large amounts of Hg into the water environment (Monteiro et al., 2013). In the aquatic system, fish accumulate Hg from surrounding water and other organisms via the food chain transfer, which in turn induces histopathological changes and disturbs metabolic processes and endocrine status (Zhang et al., 2016a, Zhang et al., 2016b; Sun et al., 2018).
For animals that undergo sexual reproduction, reproductive behavior is one of the most key events during the life cycle. Normal reproductive behavior is essential to maintain the size and age structure of the population (Weis et al., 2001), and altered reproductive behavior can be act as an ecologically relevant biomarker of endocrine dysfunction caused by contaminants (Sandheinrich and Miller, 2006). In teleost fish, a series of special sexual behaviors occurs during gamete release and fusion, such as nesting, courtship, chasing, mating, egg release, and/or sperm release (Munakata and Kobayashi, 2010). These behaviors can be performed in an innate manner after attaining puberty and are influenced by various environmental factors such as depth gradient, temperature, and contaminants (Sessa et al., 2008; Lorenzi et al., 2016; Schram and Steele, 2016). If any of these behaviors are blocked, normal patterns of reproductive behavior may be disrupted and ultimately impair reproductive success. Reproductive behavior is regulated by physiological and endocrine processes. Several hormones and neuropeptides play key roles in regulating the occurrence of reproductive behavior of fish, such as gonadotropin-releasing hormone (GnRH), gonadotropin-inhibitory hormone (GnIH), and kisspeptin (Munakata and Kobayashi, 2010; Parhar et al., 2016). The GnRH system can mediate reproductive behaviors by regulating neuroendocrine, while GnIH and kisspeptin can inhibit and stimulate the secretion of gonadotropins as well as the activity of GnRH, respectively (Zhao et al., 2014; Parhar et al., 2016; Li et al., 2017). Therefore, the disturbance of these endocrine hormones and neuropeptides is closely associated with changes in reproductive behavior.
In fish, early life stages (embryo-larva) are particularly sensitive to contamination, and the short-term toxicity test at early life stages is particularly important for assessing the long-term effects of pollutants on fish. In addition, this test does not require exposure throughout the life cycle, which can be performed in a more cost- and labor- efficient manner (Arcand-Hoy and Benson, 1998). Previous studies have demonstrated that behaviors of fish can be affected by Hg exposure, showing aberrant swimming behavior and depression of predation or predator avoidance performance (Zhou and Weis, 1998; Ho et al., 2013; Harayashiki et al., 2018). Moreover, Hg-induced reproductive impairment and its underlying mechanism have been widely studied in fish (Crump and Trudeau, 2009; Guchhait et al., 2018). It is unclear whether the reproductive behavior of adult fish is affected by early life exposure to Hg2+ and whether this effect can be recovered in offspring.
Zebrafish (Danio rerio) is one of the excellent models for toxicology studies. The main objective of this study was to investigate the effects of short-term exposure of zebrafish to Hg2+ during early life stages on reproductive behavior in adulthood and the next generation. Zebrafish embryos were exposed to 0.6, 3, or 15 μg·L−1 Hg2+ for 5 days, and then grown-out in clean water until 120 days. The survival and growth of fish and the accumulation of Hg in brains were determined. The reproductive behavior was videotaped and typical parameters of sexual behavior were examined. Furthermore, expressions of genes encoding neuropeptides and hormones related to reproductive behavior were detected. In addition, these parameters were also examined in the F1 generation to determine whether they could be recovered.
Section snippets
Chemical and exposure doses
Mercuric chloride (HgCl2, purity ≥99.5%) was purchased from Sinopharm Group Corporation (Shanghai, China). Stock solutions were prepared in double-distilled water, from which small aliquots were added to dechlorinated water in order to achieve the desired concentrations of 0 (control), 0.6, 3, or 15 μg·L−1 Hg2+. The actual concentration of total Hg (tHg) for each treatment were 0.06 ± 0.01, 0.54 ± 0.05, 2.50 ± 0.27 and 13.43 ± 0.53 μg·L−1, respectively. These concentrations were selected based
Survival and growth
In the F0 generation, exposure to 15 μg·L−1 Hg2+ during early life stages reduced fish survival (Fig. 1A) and the body length and mass of adult males and females (Fig. 1B and C). In the F1 generation, exposure of F0 individuals to Hg2+ during early life stages did not significantly affect survival and growth of fish (Fig. 1D, E, and F).
Concentrations of tHg in brain
In the F0 generation, compared with the control, greater concentrations of tHg were observed in brains of adult females exposed to 15 μg·L−1 Hg2+, and in brains
Discussion
Reproductive toxicity is one of the most sensitive and crucial toxic endpoints of contaminations, and reproductive behavior is an obligatory component of successful breeding. Disruption of normal patterns of reproductive behavior can impair the reproductive output and consequently population dynamics (Oshima et al., 2003). Although previous studies have reported negative effects of exposure to Hg on fish reproduction, such as impairment of gonadal histology, disturbance of hormones balance,
Conclusions
The present study showed that early life exposure of zebrafish to Hg2+ suppressed subsequent reproductive behavior in adulthood, manifested by lessened courtship activities of males and apparent avoidance of the spawning area by both males and females, which resulted in lesser spawning and fertilization. Interference with the transcription of genes encoding neuropeptides and hormones related to reproduction might be responsible for diminished sexual behavior and reduced reproductive outcomes.
Declaration of competing interest
The authors declare no conflict of interest.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31901183), the Basic Research and Frontier Exploration Project of Chongqing (cstc2018jcyjAX0123), and the Science and Technology Research Program of Chongqing Municipal Education Commission (KJQN201900512).
References (50)
- et al.
Disrupted reproductive behavior in unexposed female zebrafish (Danio rerio) paired with males exposed to low concentrations of 17α-ethinylestradiol (EE2)
Aquat. Toxicol.
(2015) - et al.
Mercury levels in surface waters of the Carson River-Lahontan reservoir system, Nevada: influence of historic mining activities
Environ. Pollut.
(1996) - et al.
Exposure of rainbow trout milt to mercury and cadmium alters sperm motility parameters and reproductive success
Aquat. Toxicol.
(2010) - et al.
Molecular mechanism of mercury-induced reproductive impairments in banded gourami, Trichogaster fasciata
Gen. Comp. Endocrinol.
(2018) - et al.
Effects of oral exposure to inorganic mercury on the feeding behaviour and biochemical markers in yellowfin bream (Acanthopagrus australis)
Mar. Environ. Res.
(2018) - et al.
Effects of in vitro exposure of mercury on sperm quality and fertility of tropical fish Cyprinus carpio L. Egypt
J. Aquat. Res.
(2019) - et al.
Total mercury, methylmercury and selenium in mercury polluted areas in the province Guizhou, China
Sci. Total Environ.
(2003) - et al.
Environmentally relevant exposure of 17α-ethinylestradiol impairs spawning and reproductive behavior in the brackish medaka Oryzias melastigma
Mar. Pollut. Bull.
(2014) - et al.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method
Methods
(2001) - et al.
Endocrine control of sexual behavior in teleost fish
Gen. Comp. Endocrinol.
(2010)
Suppression of sexual behavior in male Japanese medaka (Oryzias latipes) exposed to 17β-estradiol
Chemosphere
Selenium and mercury have a synergistic negative effect on fish reproduction
Aquat. Toxicol.
Methylmercury-induced changes in gene transcription associated with neuroendocrine disruption in largemouth bass (Micropterus salmoides)
Gen. Comp. Endocrinol.
Maternally transferred mercury in wild largemouth bass, Micropterus salmoides
Environ. Pollut.
Developmental selenomethionine and methylmercury exposures affect zebrafish learning
Neurotoxicol. Teratol.
Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour
Chemosphere
Impairment of reproduction of adult zebrafish (Danio rerio) by binary mixtures of environmentally relevant concentrations of triclocarban and inorganic mercury
Ecotoxicol. Environ. Safe.
Tributyltin impaired reproductive success in female zebrafish through disrupting oogenesis, reproductive behaviors and serotonin synthesis
Aquat. Toxicol.
Inhibitory effect of cadmium exposure on digestive activity, antioxidant capacity and immune defense in the intestine of yellow catfish (Pelteobagrus fulvidraco)
Comp. Biochem. Physiol. C Toxicol. Pharmacol.
Trans-generational transmission of neurobehavioral impairments produced by developmental methylmercury exposure in zebrafish (Danio rerio)
Neurotoxicol. Teratol.
Endocrine regulation of fish reproduction
Exposure to mercuric chloride induces developmental damage, oxidative stress and immunotoxicity in zebrafish embryos-larvae
Aquat. Toxicol.
Reproductive toxicity of inorganic mercury exposure in adult zebrafish: histological damage, oxidative stress, and alterations of sex hormone and gene expression in the hypothalamic-pituitary-gonadal axis
Aquat. Toxicol.
Swimming behavior and predator avoidance in three populations of Fundulus heteroclitus larvae after embryonic and/or larval exposure to methylmercury
Aquat. Toxicol.
Fish reproduction: an ecologically relevant indicator of endocrine disruption
Environ. Toxicol. Chem.
Cited by (0)
- 1
These authors contributed equally to this work.