Microplastic does not magnify the acute effect of PAH pyrene on predatory performance of a tropical fish (Lates calcarifer)
Introduction
The coastal zones are productive areas of high biodiversity and provide important forage and spawning grounds for fish stocks. Further they house a significant part of the global aquaculture production (FAO, 2016). However, the increasing human population and activities in the coastal areas lead to large quantities of nutrients and pollutants are discharged and incorporated in organic matter (Halpern et al., 2008, Halpern et al., 2015). Microplastics are of increasing importance as pollutants and pose a risk to aquatic environments due to their ubiquity, their long residence times, and their susceptibility to be ingested by biota (Barnes et al., 2009; Andrady, 2011; Li et al., 2016a, Li et al., 2016b). Jambeck et al. (2015) has calculated that approximately 12 million tons of plastics are dumped to the sea annually. The South China Sea is one of the most biologically diverse ecosystems (Liu, 2013), but it is also one of the most plastic polluted regions since the surrounding countries dump 2.36–6.30 million tons of plastic, accounting for 50% of total plastic dumping to the world ocean annually (Jambeck et al., 2015; Lebreton et al., 2017). Numerous studies have focused on the bioavailability of microplastic particles originating either from direct release of plastic particles or being the result of fragmentation of larger items (Lusher, 2015), and recent studies have documented plastic particles in >50% of marine fish collected from the South China Sea (Rochman et al., 2015). Also, mussels collected along the coastal water of China contained microplastic (Li et al., 2016a, Li et al., 2016b). Despite the growing concern about potential effects of plastic litter on marine and coastal environments worldwide (Galgani et al., 2013; UNEP and GRID-Arendal, 2016), no study has yet investigated possible effects of microplastics on the fish from the South China Sea.
Besides the possible direct impacts of microplastics on marine environment, there is a growing concern that plastic particles could act as vector for transport of hydrophobic contaminants into organisms and food webs (Teuten et al., 2007, Teuten et al., 2009; Rochman et al., 2013a, Rochman et al., 2013b; Ziccardi et al., 2016; Endo and Koelmans, 2016). In the marine environment, hydrophobic components, such as polycyclic aromatic hydrocarbons (PAHs), could rapidly bind to suspended particles, including microplastics (e.g. Teuten et al., 2007). A common PAH in the marine environment is pyrene (Kucklick et al., 1997; Luo et al., 2006; Xu et al., 2007) and concentrations up to 0.58 μg L−1 have been reported in the coastal areas (Reddy and Quinn, 2001). Sources of pyrene can be of natural origin, but in the coastal marine environment the major fraction originates from anthropogenic activities such as urban runoff, wastewater effluents, industrial outfalls, atmospheric deposition, and spills and leaks during the transport and production of fossil fuels (Latimer and Zheng, 2003). Pyrene has documented lethal and sub-lethal effects, such as a lowered feeding rate, oxygen uptake, growth rate, development time or reproductive output (Lotufo, 1997; Almeda et al., 2013; Barata et al., 2005; Incardona et al., 2012). The vector effect of microplastic is based on the binding affinities of hydrophobic contaminants as PAHs to plastic particles in the hydrophilic pelagic because of their natural binding affinities. However, once inside an organism the conditions in the gastrointestinal might facilitate desorption of the hydrophobic contaminant rendering the contaminant available for toxic effects (Rochman, 2016; Teuten et al., 2007).
Several fish species using the coastal areas for breeding are sensitive to such ecotoxicological impacts from e.g. PAHs and microplastic (Oliveira et al., 2012; Lechner et al., 2014; Steer et al., 2017; Vendel et al., 2017). Both fish larvae and juveniles have been found to ingest microplastic particles (Steer et al., 2017; Oliveira et al., 2013; Karami et al., 2017), and individuals exposed to microplastics and PAHs in combination have shown impaired swimming performance, e.g. for common goby juveniles (Oliveira et al., 2012) and for pufferfish larvae (Itoyama et al., 2017).
Due to the high sorption capacity, plastics debris tends to become associated with persistent organic pollutants present in marine environment (Lee et al., 2014). Thus, there is great concern whether there will be a bioaccumulation of absorbed toxic chemicals in marine organisms as a consequence of plastic debris ingestion (Rochman, 2013, Rochman, 2016). Sorption potential of several mass-produced plastic polymers has been demonstrated by long-term (12 months) field studies (Rochman et al., 2012; Rochman, 2013). Among other plastic polymers, polystyrene stands out having a high potential as sink for PAHs in marine environment (Rochman et al., 2013b). PAHs are widespread organic pollutants in the marine environment, and are known to exert carcinogenic, mutagenic and toxic effects (Douben, 2003). PAHs have been known to modulate the immune responses of fishes and as a consequence increased disease susceptibility of these (Collier et al., 2014). Moreover, occurrence of hepatic neoplasms and toxicopathic liver lesions in wild fish has also linked with exposure to PAHs (Collier et al., 2014). Due to their ability to disrupt endocrine function and toxic – mutagenic effects on germ cells, PAHs are known to cause reproductive impairment (Collier et al., 2014). Adverse effects of PAH exposure in the early stages of larval development such as heart defects and phototoxicity in cells-tissues have also been reported (Collier et al., 2014). In addition, exposure to PAHs adversely affects the feeding rate and growth in fish (Palanikumar et al., 2013). Among PAHs, pyrene has previously been reported to cause adverse effects on grazing and total reproductive output of copepod species (Lotufo, 1997; Jensen et al., 2008; Nørregaard et al., 2014; Krause et al., 2017). Several studies have demonstrated that fish ingested single and mixtures of chemicals including microplastic with absorbed PAHs (Oliveira et al., 2013; Rochman et al., 2013a).
In the Southeast Asia, the barramundi (Lates calcarifer), also known as the Asian seabass or giant sea perch is an important fish species both in its natural environment and in aquaculture (FAO, 2017). It migrates into brackish waters to breed, which could be at river mouths, in the lower reaches of estuaries, or around coastal headlands (FAO, 2017). In those areas, fish larvae develop into juveniles, remaining in coastal areas for several months (FAO, 2017), in areas where they are at risk of being exposed to both microplastic and oil substances (Vikas and Dwarakish, 2015).
In the present study, we examined the single and interactive effects of microplastic and pyrene, as an important PAH, on the swimming behaviour and predatory performance of juvenile barramundi. We hypothesized that i) pyrene would impact the predatory performance and swimming behaviour; ii) the presence of plastic particles would lead to lower feeding rate on natural prey; and iii) the presence of both plastic and pyrene would more seriously impact fish foraging due to a negative synergistic effect of exposure to two stressors.
Section snippets
Ethical issues
Laboratory handling of larvae were carried out according to the legal and ethical requirements of European regulations. O. Guven is accredited (Experimental animal usage certificate-Category B) to carry out animal experimentation. At the end of the experiments, we killed the fish immediately in ethanol (96%) and stored in Eppendorf tubes (volume of 1.5 mL) for later examination.
Study species
Juveniles of the barramundi (Lates calcarifer) (18+ days post hatch) were purchased from a local hatchery located in
Dose-effect experiment
There were no signs of immobilization or mortality observed in the seawater controls (100% survival and swimming). In the acetone control no mortality was observed, but about 10% fish were immobilized. The experiments were conducted over two days, with 100 nM pyrene concentration included at both days to test for differences between the two experimental days. No difference was found between the two days (two-sample t-test: p = 0.51) and data from the two days were combined. For barramundi
Discussion
In the present study, we investigated the immediate single and interactive effects of MP and pyrene on predatory performance of juvenile barramundi, a voracious fish predator with an important ecological role in tropical coastal marine ecosystems and further of aquaculture value (Ribeiro and Qin, 2015). While the effects of pyrene on the predatory performance of the barramundi juveniles were strong, there were no apparent single effects of microplastic and the presence of microplastic did not
Acknowledgements
O. Guven was supported by the Scientific and Technical Research Council of Turkey (TUBITAK) under the BIDEB 2219-International Postdoctoral Research Scholarship Program. We highly acknowledge the support of Nha Trang University and Institute of Aquaculture and Pham Quoc Hung, Doan Xuan Nam, Nha Trang University and Nguyen Ngoc Lam, Doan Nhu Hai and Truong Sy Hai Trinh, Institute of Oceanography, Nha Trang for assisting us during the experiment. Dr. Frank Rigét is acknowledged for statistical
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