Elsevier

Aquatic Toxicology

Volume 232, March 2021, 105742
Aquatic Toxicology

Effects of salinity on the chronic toxicity of 4-methylbenzylidene camphor (4-MBC) in the marine copepod Tigriopus japonicus

https://doi.org/10.1016/j.aquatox.2021.105742Get rights and content

Highlights

  • Increasing salinity increased the toxicities of 4-MBC in T. japonicus.

  • Increasing salinity increased the uptake and bioconcentration factor of 4-MBC.

  • Increasing salinity exacerbated oxidative stress induced by 4-MBC in T. japonicus.

  • Environmental concentrations of 4-MBC could significantly pose risk to T. japonicus.

Abstract

Organic ultraviolet filters are widely used in personal care products. 4-methylbenzylidene camphor (4-MBC) is one of the most frequently used UV filters. Due to its widespread usage 4-MBC has been detected at high concentrations in offshore waters. Previous toxicological studies have suggested that 4-MBC might induce much higher toxicity in marine organisms than freshwater species. To explore the effects of salinity on 4-MBC toxicity, the marine copepod Tigriopus japonicus was used as the model species, as it plays an important role in marine ecosystems and can be adapted to a wide range of salinity conditions. T. japonicus were adapted to three different salinity conditions (i.e., 20, 30 and 40 ppt) prior to exposure to 0, 1, and 5 μg L−1 4-MBC for multiple generations (F0-F3). Results showed that environmentally relevant concentrations of 4-MBC had toxic effects on T. japonicus and therefore, can pose a significant risk to marine copepods in the natural environment. In addition, increasing salinity levels increased the lethal, developmental and reproductive toxicities of 4-MBC in T. japonicus. This was because that higher salinity levels increased the uptake rate constant and bioconcentration factor of 4-MBC and also further exacerbated the oxidative stress induced by exposure to 4-MBC in T. japonicus. Our study demonstrated that understanding how salinity affects the toxicity of 4-MBC is important for accurate assessment of the risk of 4-MBC in the aquatic environments.

Introduction

Organic ultraviolet filters (UV filters) are a class of compounds that are widely used in various personal care products (PCPs), providing strong oxidative resistance and light stability. These compounds can effectively protect the skin from damage caused by UVB (275−320 nm) and UVA (320−420 nm) ultraviolet radiation (Gasparro, 2000). In addition, UV filters are also commonly used in various products such as building materials, paints, coatings, food packaging materials and textile products, to effectively prevent material from aging and degradation (Fent et al., 2010a). In recent years, due to stratospheric ozone layer depletion and expansion of the ozone hole, the intensity of UV radiation is continually increasing, posing a serious threat to biological and human health. Therefore, the risks associated with increased UV exposure are receiving increasing public attention, leading to rising demand for UV filters and increased production levels accordingly. It has been reported that the global production of UV filters has reached at least 10,000 tons per year, with the volume increasing annually (Gago-Ferrero et al., 2012).

One of the most widely used organic UV filters is 4-methylbenzylidene camphor (4-MBC), an organic camphor derivative (Wahie et al., 2007). 4-MBC has a good absorption effect for ultraviolet rays in the wavelength range of 290−320 nm. Under exposure to UV irradiation, 4-MBC rapidly undergoes a photochemical isomerization reaction and the absorbed radiation is released in the form of heat (Buser et al., 2005). Due to the high levels of usage and production, 4-MBC gradually enters the aquatic environment through direct flushing or sewage discharge. Owing to its strong stability, 4-MBC cannot be completely removed by traditional sewage treatment procedures. Balmer et al. (2005) conducted a sampling survey of inlet and outlet water bodies in 8 local municipal sewage treatment plants in Switzerland and found that the 4-MBC removal efficiency of most sewage treatment plants ranged from 44 %–69 % (Balmer et al., 2005). In addition, it was found that the removal efficiency of 4-MBC is less than 40 % in a sewage treatment plant in Tianjin, China (Li et al., 2007).

4-MBC enters the marine environments via natural freshwater flow from rivers, lakes, and surface runoff. The concentrations of 4-MBC detected in marine water samples collected off the coast of Hong Kong ranged from 173 to 379 ng L−1 (Tsui et al., 2014). In addition, 4-MBC concentrations in the range of 26.6–109.6 ng L−1 were detected in surface seawater collected off the coast of Mallorca in the Mediterranean (Tovar-Sanchez et al., 2013). Recreational activities such as bathing and swimming are also important sources of environmental 4-MBC contamination, causing direct release into local marine ecosystems. It results in relatively higher 4-MBC concentrations during warmer seasons in some coastal areas, such as beaches and other popular scenic spots. For example, up to 1043 ng L−1 of 4-MBC was detected in the coastal waters of Gran Canaria Island during summer (Rodríguez et al., 2015). 4-MBC concentrations also reached 798.7 ng L−1 at Sandvika Beach on the Norwegian coast (Langford and Thomas, 2008).

4-MBC is a lipophilic compound with an octanol-water partition coefficient (log Kow) of 5.02 (Gago-Ferrero et al., 2011) and therefore, tends to accumulate in sediments (Ramos et al., 2015; Pintado-Herrera et al., 2017) and in aquatic organisms (Alonso et al., 2015; Peng et al., 2015). Previous toxicological studies have revealed the endocrine disrupting effects of 4-MBC on mammals. For aquatic vertebrates, 4-MBC exposure has been found to exert estrogenic effects on freshwater zebrafish (Danio Rerio) and medaka (Oryzias latipes) at concentrations above 1 mg L−1 (Inui et al., 2003; Torres et al., 2016). However, in aquatic invertebrates such as fresh water Daphnia magna and Chironomus riparius, or the marine copepod Tigriopus japonicus, 4-MBC induced lethal, developmental and reproductive toxicity at much lower concentrations (e.g., 0.5−800 μg L−1) (Schmitt et al., 2008; Sieratowicz et al., 2011; Ozáez et al., 2013; Chen et al., 2018).

4-MBC can cause species-specific toxicity in aquatic invertebrates. In addition, salinity likely plays a role in 4-MBC induced toxicity, as there are obvious differences between the toxicity of 4-MBC to freshwater species and marine species. For example, the acute LC50 (72 h) of 4-MBC was 92 μg L−1 in the coastal copepod Tigriopus japonicus (Chen et al., 2018), which was 6- to 8-fold lower than in the freshwater crustacean Daphnia magna (LC50 of 560−800 μg L−1) (Fent et al., 2010b; Sieratowicz et al., 2011). The results of a one generation life-cycle test showed that the LOEC of reproductive toxicity was 1 μg L−1 4-MBC in marine T. japonicus (Chen et al., 2018), while reduced reproduction rate and body length were observed in freshwater D. magna exposed to the LOEC of 50 μg L−1 (Fent et al., 2010a). Moreover, the 4-MBC LC50 in the marine fish Solea senegalensis was more than ten-fold lower than in the freshwater fish Danio rerio (Li et al., 2016; Araujo et al., 2018). Overall, the results of these studies suggest that 4-MBC may be more toxic to marine organisms than freshwater species, with these differences potentially due to interspecies variation, while it is also likely that salinity affects the toxicity of 4-MBC.

In aquatic organisms, adaptation to salinity ensures normal growth, reproduction rates and affects population distribution, which is also an energy costing process (Devreker et al., 2009). Previous studies have indicated that changes in salinity affect the toxicity of some heavy metals and organic pollutants (Janssen et al., 2003; Kwok and Leung, 2005; Church et al., 2017). Salinity is considered to be a key variable affecting the bioavailability and toxicity of metals, with salinity often weakening the interaction between the metals and bio-ligands. In addition, salinity can increase complexation between chlorides and metals, resulting in a decrease in the concentration of free metal ions and reducing the bioavailability of metals (Janssen et al., 2003; Church et al., 2017; DeForest et al., 2017). However, there are relatively few studies available on the effects of salinity on organic pollutant toxicity and only a few pollutants have been investigated, such as perfluorinated compounds, tributyltin and polychlorinated biphenyls (Jeon et al., 2010a; Kwok and Leung, 2005). The toxicities of some of these organic pollutants have been found to increase with higher salinity levels, while some pollutants exhibited reduced toxicity. Moreover, the underlying mechanisms responsible for these varying responses remain unclear.

In the present study, to investigate the effects of salinity on the chronic toxicity of 4-MBC, T. japonicus was used as the model species, as it can be adapted to a wide range of salinity conditions (Kowk and Leung, 2005; Hagiwara et al., 1995). In addition, the effects of salinity on the bioconcentration of 4-MBC and the transcription of genes related to oxidative stress, apoptosis and ecdysis were also investigated to help establish the potential mechanisms of how salinity affects the toxicity of 4-MBC.

Section snippets

Chemicals and reagents

4-MBC was purchased from the Tokyo Chemical Industry Co. (Tokyo, Japan). 4-MBC- d4 was used as an internal standard for analysis and was purchased from CDN Isotopes Inc. (Pointe-Claire, Canada). The organic solvents methyl alcohol, dichloromethane and acetonitrile, which were used for sample extraction and LC–MS/MS analysis, were purchased from Tedia Inc. (Fairfield, Ohio, USA). All other reagents were purchased from Sigma-Aldrich Chemical Co. (St. Louis, Missouri, USA).

Copepod maintenance

T. japonicus was

Effects of salinity on T. japonicus

After acclimation, T. japonicus were continually cultivated under three different salinity conditions (20, 30 and 40 ppt) for four generations (F0-F3). Results showed that with the absence of 4-MBC, T. japonicus exhibited altered survival rates due to variation in salinity conditions in the F0 generation, although this effect was not significant (Fig. 3A). Particularly, the mortality frequently occurred during the Nsingle bondC phase (nauplii to copepodite) under all three salinities, and no obvious

Discussion

In the present study, all salinity groups (20, 30 and 40 ppt) exhibited high survival rates without 4-MBC exposure (Fig. 3). Previous studies also showed that T. japonicus can adapt well to varying salinity conditions (Raisuddin et al., 2007; Kowk and Leung, 2005). Minor mortality occurred only in the N-C (nauplii to copepodite) phase in the F0 generation, suggesting that N-C stage is a sensitive period in the whole developmental process. It has been reported that juveniles may not tolerate the

Conclusions

Toxicity tests using the marine copepod model species T. japonicus showed that environmentally relevant concentrations of 4-MBC could pose a significant risk to marine copepods, threatening the stability of marine ecosystems. In addition, increasing salinity levels resulted in an increase in the lethal, developmental and reproductive toxicity of 4-MBC in T. japonicus. The mechanism of effect of salinity on 4-MBC toxicity was explored, indicating that higher salinity levels increased the uptake

CRediT authorship contribution statement

Haizheng Hong: Conceptualization, Funding acquisition, Investigation, Methodology, Supervision, Writing - original draft, Writing - review & editing. Jiaxin Wang: Investigation, Formal analysis. Dalin Shi: Conceptualization, Supervision, Resouces, Writing - origianl draft, Writing - review & editing.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (No. 41676094). Dr. Qiaoguo Tan, Miss Yunchen Zhao and Miss Yawen Chen were acknowledged for their assistance in data analysis and figure plotting.

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