Low level of polystyrene microplastics decreases early developmental toxicity of phenanthrene on marine medaka (Oryzias melastigma)

https://doi.org/10.1016/j.jhazmat.2019.121586Get rights and content

Highlights

  • Microplastics (MPs, 10 μm) accumulated on the chorion, but did not enter the embryo.

  • High levels of MPs (20 and 200 μg/L) inhibited hatching and growth of marine medaka.

  • High levels of MPs did not alter the toxicity of phenanthrene (Phe).

  • Low level of MPs (2 μg/L) decreased the teratogenicity and lethality of Phe.

  • Combined exposure to MPs and Phe may lead to a decrease of marine fish population.

Abstract

Microplastics (MPs) have become global environmental concern. However, the effects of environmental concentrations of MPs, singly or in combination with organic pollutants, on the early development of marine fish remain unclear. In this study, fertilized eggs of marine medaka (Oryzias melastigma) were exposed to polystyrene MPs (0, 2, 20, 200 μg/L) and/or phenanthrene (Phe, 50 μg/L) for 28 days. The results revealed that MPs were accumulated on the chorion and ingested by larvae from 2 days post-hatching. High levels of MPs (20 and 200 μg/L) decreased the hatchability, delayed the hatching time, and suppressed the growth, whereas Phe inhibited hatching and caused malformations in larvae. The presence of MPs at 20 and 200 μg/L did not alter the toxicity of Phe. By contrast, combined exposure to 2 μg/L MPs and Phe increased the hatchability by 25.8%, decreased malformation and mortality rates, and restored Phe-induced abnormal expressions of cardiac development-related genes. The reduced early developmental toxicity could be attributed to the decreased bioavailability and bioaccumulation of Phe by the low level of MPs. These findings contradicted the view that MPs would aggravate the toxicity of organic pollutants, and future studies are warranted to elucidate the ecological risks of marine MPs.

Introduction

Plastic waste, which continually accumulates in the oceans, has become a global concern owing to its potential impacts on the marine ecosystems and human health (Galloway and Lewis, 2016). Large plastics break down into microplastics (MPs, <5 mm) via mechanical and biological degradation (Besseling et al., 2013). MPs have become the main form of plastic waste and are ubiquitous throughout the oceans (Obbard et al., 2014). For example, the abundances of MPs in surface waters of the Jade system (southern North Sea) and sediments of the South Yellow Sea (China) accounted for 1700 items/L (Dubaish and Liebezeit, 2013) and 4205 items/kg dry weight (Wang et al., 2019), respectively. Due to their small size, MPs can be easily ingested by zooplankton (Setälä et al., 2014), mollusks (Sussarellu et al., 2016), and fish (Rainieri et al., 2018). It was reported that the ingestion of MPs caused severe histological changes in the intestinal tissues of European sea bass (Dicentrarchus labrax) (Pedà et al., 2016) and hampered the feeding activity of Lugworm (Arenicola marina). Moreover, MPs can absorb a substantial amount of persistent organic pollutants (POPs) due to their large surface area (Rainieri et al., 2018; Teuten et al., 2007). Concentrations of polycyclic aromatic hydrocarbons (PAHs) and polychlorinated biphenyls (PCBs) accumulated on plastic particles ranged from 27 to 980 ng/g and 39 to 1200 ng/g (Rios et al., 2007), which were approximately 106 times higher than those in the surrounding seawater (Lohmann, 2017). Phenanthrene (Phe), one of the most common PAHs, has been frequently detected in the marine MPs and its concentration was as high as 2.38 μg/g (Zhang et al., 2015). As vectors for environmental contaminants, MPs are generally assumed to increase the translocation and accumulation of POPs in marine organisms, thereby enhancing their toxic effects on these living organisms (Granby et al., 2018).

The combined toxicity of MPs and organic pollutants on marine organisms has gained immense interest. Jeong et al. (2018) found that MPs enhanced the toxicity of tetrabromodiphenyl ether and triclosan on the oxidative stress-induced damages of monogonont rotifer (Brachionus koreanus). Similarly, Rochman et al. (2013) reported that a mixture of polyethylene microspheres and polybrominated diphenyls caused severe liver toxicity and pathological damage in zebrafish (Danio rerio). On the other hand, Guven et al. (2018) revealed that MPs did not increase the adverse effects of pyrene on the predation ability and feeding rate of juvenile barramundi (Lates calcarifer), which was in agreement with the combined effects of MPs and 4-n-nonylphenol/Phe on plankton (Beiras and Tato, 2019; Ma et al., 2016). Lin et al. (2019) reported that polystyrene nanoparticles at low concentrations could decrease the toxicity of PCBs in Daphnia magna by reducing free PCBs concentration in the water. We speculate that the exposure level of MPs may be an important factor to influence the combined toxicology of MPs and organic pollutants.

Fish are effective bioindicators of contaminants in the aquatic environment and have been widely used in the toxicity studies of MPs. Current studies usually adopted freshwater adult fish as the test organisms (Ding et al., 2018; Jin et al., 2018). In contrast, the early life stages are more sensitive to toxicants than the adults (Mohammed, 2013); in particular, the development of heart, one of the first organs to become functional during organogenesis, is extremely susceptible to environmental stresses (Hicken et al., 2011). Phe, a typical tricyclic PAH compound, has strong toxic effects on aquatic organisms and it can cause malformations during early development (Mu et al., 2014). For instances, 200 μg/L Phe caused serious heart malformations, prolonged the embryo incubation time, and increased the mortality of marine medaka (Oryzias melastigma) (Mu et al., 2014). Similarly, exposure to Phe (>1 μg/L) could cause arrhythmia and abnormal cardiac morphology in zebrafish embryos (Zhang et al., 2013). Recently, Pitt et al. (2018) reported that polystyrene nanoparticles (100 μg/L) induced obvious bradycardia in zebrafish embryos, suggesting that MPs may damage the heart function in larval fish. Considering the high adsorption of Phe on MPs, their combined toxicity effects on early development of marine fish merit attention.

Therefore, in the present study, we selected polystyrene microspheres (PS-MPs, 10 μm) and Phe as model MPs and PAHs to evaluate their single and combined effects on early development of marine medaka, a model organism used marine ecotoxicity studies. Firstly, the accumulation of MPs in embryos and larvae, and the effects of MPs alone on egg hatching and larval development were investigated to verify whether MPs could negatively impact early development of marine fish. Thereafter, the combined toxicity of MPs and Phe at environmental concentrations was compared to Phe single exposure by assessing heart development, hatching performance, and malformations as the endpoints. This study may provide a baseline information for evaluating the ecological effects of MPs on marine fish.

Section snippets

MPs and chemicals

Polystyrene was a commonly detected type of plastics in the ocean, and MPs in small size accounted for a high proportion of microplastic amount in the marine environment (Wang et al., 2019). Therefore, this study chose polystyrene microspheres with a particle size of 10 μm as the model MPs. Cross-linked monodisperse polystyrene microspheres (10 μm, water 1:1 emulsion, 2.5% (w/v), Fig. S1) and fluorescently labeled polystyrene microspheres (10 μm, 467/526 nm excitation/emission, water 1:1

Accumulation of MPs in fertilized eggs and larvae

Fluorescence was observed on the surface of embryos and it gradually increased with prolonged exposure (Fig. 1A), and eventually reached a plateau during 5–10 dpf (Fig. 1D). The newly hatched larvae revealed no fluorescence; however, strong fluorescence was observed on the egg shells (Figs. 1B and S5A, B) and in larvae from 2 dph. Moreover, the fluorescence particles were excreted at 3 dph (13 dpf), and strong fluorescence was found in the feces (Figs. 1C and S5C, D).

Concentrations of MPs in seawater

At the embryo stage (10

Discussion

The present study found that both MPs and Phe impacted the early development of marine medaka, and 2 μg/L MPs reduced the Phe-induced heart damage, deformity, and mortality in marine medaka, suggesting that low level of MPs could alleviate the toxicity of Phe on early development of marine fish. It was reported that polystyrene MPs >50 nm could not enter zebrafish embryos (Bisesi et al., 2014). Our results revealed that MPs were adsorbed on the egg shells, but they were not observed in newly

Acknowledgements

We wish to thank two anonymous reviewers for their constructive comments that improved the manuscript. This research was supported by Central Public-interest Scientific Institution Basal Research, CAFS & Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, P. R. China (NO. 2019HY-XKQ01) and Fundamental Research Funds for the Central Universities (201964025).

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