Toxicity of copper oxide nanoparticles to Neotropical species Ceriodaphnia silvestrii and Hyphessobrycon eques☆
Graphical abstract
Introduction
Copper oxide nanoparticles (CuO NPs) have been applied in several areas due to their excellent thermophysical, catalytic and antibacterial properties (Ebrahimnia-Bajestan et al., 2011; Majumder and Neogi, 2016; Prasad et al., 2016). CuO NPs are widely used in electronics, catalysis, sensors, solar cells, drug delivery, agriculture, food preservation, textiles, paints, coatings and water treatment (Bondarenko et al., 2013; Keller et al., 2017). More specifically, rod-shaped CuO have been demonstrated enhanced properties due to their greater surface to volume ratio compared to the spherical ones (Jia et al., 2015). Inevitably, the increasing production and widespread utilization of CuO NPs lead to their release into the aquatic environment, posing a potential hazard to non-target organisms (Lu et al., 2017; Wu et al., 2017).
Concerns regarding the potential impacts of NPs in the aquatic environments have risen sharply. Although CuO NPs present a low dissolution rate in water, they may cause toxic effects on aquatic organisms (Keller et al., 2017). It is still controversial about what is the major source of toxicity of CuO NPs. Based on the literature, toxicity of CuO NPs may be exerted by particles specific effects (Cronholm et al., 2013; Manusadzianas et al., 2012), by copper ions released from NPs (Jo et al., 2012) or by both particle and ions (Xiao et al., 2015, 1016). The dissolved Cu2+ from CuO NPs can enter the cells through ion channels and active transport. In addition, CuO NPs may interact with cells due to their small size, and cross the cell membranes through ion channels and transporter proteins, endocytosis and/or phagocytosis (Chang et al., 2012). Thus, CuO NPs can cause toxicity by one or more pathways, inducing cell membrane damage, mitochondrial injury, protein denaturation, modification of nucleic acids, cellular damage through reactive oxygen species (ROS) generation, oxidative stress, DNA damage and apoptosis (Hou et al., 2017; Peng et al., 2017; Thit et al., 2017).
Exposure of aquatic organisms to CuO NPs has evidenced the NPs accumulation and trophic transfer through the food chain (Ates et al., 2014, 2015). Aquatic organisms may be in contact with CuO NPs either by direct uptake from water or by dietary intake, which can result in adverse consequences to organisms and ecosystem. Previous studies have reported the effects of CuO NPs on various species, such as bacteria (Bondarenko et al., 2012), cyanobacteria (Lone et al., 2013), algae (Melegari et al., 2013; Zhao et al., 2016), protozoans (Mortimer et al., 2010), cladocerans (Xiao et al., 2015; Wu et al., 2017), fish (Sun et al., 2016; Xu et al., 2017) and aquatic plants (Shi et al., 2011; Zhao et al., 2017). Most data regarding the toxicity of CuO NPs has focused on acute exposure of organisms at relatively high concentrations, which implies little ecological realism. Some studies have investigated the long-term CuO NPs toxicity on cladoceran and fish. Adam et al. (2015) and Rossetto et al. (2014) observed that CuO NPs chronic exposure affected the growth and reproduction of Daphnia magna at different concentrations (>1 mg L−1). Zhao et al. (2011) reported Cyprinus carpio fish growth was inhibited after 30 day sublethal exposure to CuO NPs (100 mg L−1), while Ates et al. (2015) found that CuO NPs induced oxidative stress in Carassius auratus liver and gills after 21 day exposure (1 and 10 mg L−1). However, toxicity data on long-term and chronic effects of CuO NPs at low exposure levels are still insufficient (Hou et al., 2017).
In addition, most toxicity studies on aquatic invertebrates and vertebrates were conducted on standard test species (OECD, 1992; USEPA, 2011), such as the cladocerans D. magna and Ceriodaphia dubia, and fish Danio rerio (zebrafish) and Oncorhynchus mykiss (rainbow trout). Only few studies have investigated the effects of NPs on tropical native species (e.g. Yoo-iam et al., 2014). Toxicological effects of CuO NPs on tropical aquatic organisms are still unknown, representing a risk for biota. Therefore, there is a growing need in obtaining ecotoxicological data under tropical conditions, using native test organisms for the environmental risk assessment of NPs.
The aim of this study was to evaluate the toxicity of rod-shaped CuO NPs to Neotropical species Ceriodaphnia silvestrii and Hyphessobrycon eques. Rod-shaped CuO NPs were selected due to their wide application and different way of interacting with a biological system since the particle shape seems to have effects on biological responses (Misra et al., 2014; Venkataraman et al., 2011). In addition, we also compared the toxicity of CuO NPs and CuCl2.2H2O on these species to investigate the contribution of particles and cupper ions to the CuO NPs toxicity. C. silvestrii (Cladocera) has a wide geographic distribution in South America; a short life cycle and is easy to maintain in laboratory conditions; and belongs to one of the most sensitive group of species for a variety of contaminants (Fonseca and Rocha, 2004; Mansano et al., 2016). Hyphessobrycon eques (Characidae) is a Neotropical fish widely distributed in South America, especially in regions with pH levels between 6.5 and 7.0, temperature between 26 °C and 28 °C; and due to its peculiar body coloration, it is highly appreciated as an aquarium fish (Aguinaga et al., 2014; Fujimoto et al., 2013). The toxicity of CuO NPs and CuCl2 to C. silvestrii and H. eques was evaluated through lethal and sublethal exposure: for cladoceran, the endpoints immobility, reproduction, feeding rates and reactive oxygen species (ROS) generation were investigated, while for fish the mortality, ROS generation, apoptosis and necrosis induction and uptake in the gill cells were assessed. We also evaluated the sensitivity of these species compared to other species through species sensitivity distribution curves and discussed the importance of using native species in risk assessments.
Section snippets
Synthesis and characterization of CuO NPs
CuO nanoparticles were synthesized by modification of a previous method (Misra et al., 2014). For this, 335 μL of glacial acetic acid were added to 100 mL of a 0.02 M CuSO4.5H2O aqueous solution. The system was heated to 100 °C followed by a rapid addition of 0.45 g NaOH under vigorous stirring. After 15 min, the system was cooled to room temperature and the black precipitated was washed in ultrapure water by centrifugation. The particles were then resuspended in solution containing 1% m/v of
Characterization of CuO NPs
The characterization of CuO NPs by X-ray diffraction (XRD) is shown in Fig. 1A. The characteristic peaks corresponding to (−111), (111), (−202), (202), (−311), and (220) planes are located at 2θ = 35.57°, 38.74°, 48.76°, 58.35°, 66.28° and 68.13°, respectively. They correspond to CuO monoclinic phase by comparison with the Joint Committee on Powder Diffraction Standards (JCPDS) card files no. 48–1548. The absence of peaks related to Cu2O3, Cu2O, and Cu confirmed the formation of single-phase
Discussion
The results regarding the dynamics of the NPs showed a very small dissolved copper fraction (<1%) from CuO NPs in exposure suspensions. Different authors confirmed this low dissolution value from Cu NPs. Griffitt et al. (2007, 2008) reported that ion release from Cu NPs was <0.1% and Misra et al. (2014) verified that copper fraction released from rod-shaped CuO NPs was 1.1%. Previous findings also revealed that different shaped NPs release distinct amounts of ions in the testing medium, where
Conclusions on the potential risks of CuO NPs
Currently, few studies have reported on the concentrations of Cu NPs present in aquatic environment (e.g. Chio et al., 2012). The predicted environmental concentration (PEC) for Cu NPs in some receiving waters was 60 μg L−1 with a 95% confidence interval of 10–920 μg L−1 (Chio et al., 2012). Given these predicted concentrations in some aquatic systems, Cu NPs may represent potential risks for some species of cladocerans and fish in natural systems (Fig. 7). According to the PEC values, all the
Conflicts of interest
The authors declare no conflicts of interest.
Acknowledgments
This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (Proc. No.150395/2016-7) and the Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (Proc. No. 2017/03165-1). We thank Brazilian Nanotechnology National Laboratory - LNNano/CNPEM/MCTIC (Campinas, SP, Brazil) for the use of TEM. We thank the Analytical Chemistry Laboratory - CENA/USP (Piracicaba, SP, Brazil) for the use of ICP-OES.
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