Effect of silver nanoparticles on marine organisms belonging to different trophic levels
Introduction
Nanotechnology is rapidly expanding with applications in different fields, from electronics to medicine, from remediation to engineering and food industry (Oberdörster et al., 2007, Das et al., 2013, Massarky et al., 2013). Nowadays the products containing silver nanoparticles (Ag-NPs) are increasing, as well as their worldwide diffusion for industrial processes and treatments (Myrzakhanova et al., 2013), due to their importance as antimicrobial agents (Mohan et al., 2007, Zheng et al., 2008) and their particular magnetic, optical, electronic and catalytic properties, that make Ag-NPs suitable for applications in a wide range of fields (Johari et al., 2013). The Woodrow Wilson Database (2011) has listed about 1317 NP-based consumer products currently on the market, 311 of which contain Ag-NPs. Nanotechnology enables the incorporation of these NPs into many daily personal care products, wound dressings, kitchen-ware, children toys, washing machine coatings, wall paints, food packaging and many more (Kim et al., 2007, Sotiriou and Pratsinis, 2010). Moreover 53% of the EPA (Environmental Protection Agency) -registered biocidal silver products likely contain Ag-NPs (Nowack et al., 2011). Such an extensive use and growing production raises questions about Ag-NP safety and environmental toxicity. To date the predicted environmental concentrations (PECs) for Ag-NPs in the environment are at the range of ng L−1 to mg kg−1 (Fabrega et al., 2011a, Reidy et al., 2013) and this value is estimated to be 0.03–0.08 μg L−1 in the water compartment, representing a high potential risk induced by Ag-NPs in the aquatic ecosystem (Mueller and Nowack, 2008). The investigation of Ag-NPs effects in the aquatic ecosystem is very important, since the wide variety of the applications containing Ag-NPs can potentially end up in the aquatic environment and reach the sea during waste disposal (Asharani et al., 2008) as most of NPs do. Ag-NPs may aggregate and/or dissolve in the aquatic environment (Baun et al., 2008), so these processes may alter the fate, transport and toxicity of such NPs (Lowry et al., 2012).
Most of the currently available ecotoxicological data regarding Ag-NPs are limited to freshwater species used in regulatory testing (i.e. OECD, ISO), that represent key environmental organisms, such as algae, crustaceans and fish (Miao et al., 2010, Hoheisel et al., 2012, Kashiwada et al., 2012, Wu and Zhou, 2013). The toxicity of Ag-NPs measured in freshwater depends on the test species (Blinova et al., 2013). For example, Ag-NPs are reported to be toxic for crustaceans at very low concentration (EC50 < 0.1 mg L−1), followed by algae (EC50 = 0.23 mg L−1), but the toxicity to fish is relatively low (EC50 = 7.1 mg L−1, Kahru and Dubourguier, 2010, Ashgari et al., 2012).
On the contrary, the current knowledge on the fate, behavior and ecotoxicity of Ag-NPs in the marine ecosystem is scarce. Recent findings indicate that salinity influences the stability and aggregation of Ag-NPs (Wang et al., 2014), therefore the fate of such NPs is primary to aggregate in the water column, precipitate and accumulate in sediments following release into the marine environment (Keller et al., 2010, Buffet et al., 2013). To date only sparse data on the potential toxicity of Ag-NPs to marine species (e.g. their effects on sea urchin and oyster development, fish and oyster physiology and blue mussel accumulation, Chae et al., 2009, Ringwood et al., 2010, Zuykov et al., 2011, Gambardella et al., 2013, McCarthy et al., 2013) are available.
Ag-NPs cause a significant decrease in marine biofilm volume and biomass (Fabrega et al., 2011b), inhibit the photosynthetic performance of green algae (Oukarroum et al., 2012) and induce mortality and a cyst hatching decrease in brine shrimp (Arulvasu et al., 2014). As a contribution to this field, the effects of Ag-NPs on environmental relevant marine test species belonging to different trophic levels have been examined in the present paper. In order to obtain a comprehensive assessment of Ag-NP effects on seawater column organisms, toxicity testing was carried out across a battery of six species belonging to different trophic levels (primary producers and consumers), including algae (Skeletonema costatum and Dunaliella tertiolecta), cnidaria (Aurelia aurita), crustaceans (Artemia salina and Amphibaanus amphitrite) and echinoderms (Paracentrotus lividus). The diatom S. costatum, the green alga D. tertiolecta, the sea urchin P. lividus, the brine shrimp A. salina and the barnacle A. amphitrite were selected because they are established model species in standardized toxicity tests, ecotoxicological studies and in ecological risk assessment (Wong et al., 1995, UNI EN ISO, 2000, ASTM, 2004, Faimali et al., 2006, Losso et al., 2007, Pane et al., 2008, Dineshrama et al., 2009, Pétinay et al., 2009, Garaventa et al., 2010, Piazza et al., 2012).
In addition, the jellyfish A. aurita was used in this work since it has been recently proposed as a very new, sensitive and innovative model organism in ecotoxicological studies. Besides occupying a key evolutionary position as basal metazoan (Faimali et al., 2014, Costa et al., 2015), cnidarians are important components of marine food webs both as major consumers of zooplankton (Riisgård et al., 2007) and preys (Cardona et al., 2012, Titelman et al., 2006). Moreover, increasing evidence has shown that jellyfish have an influence on microbial food webs, through direct and indirect effects, and are important regulators of marine biogeochemical fluxes (Turk et al., 2008).
Therefore, the aim of this study was to expand knowledge on the effects of Ag-NPs on the marine ecosystem, by analyzing different end-points, such as algal growth, jellyfish immobility and frequency of pulsation, crustacean mortality and swimming behavior, and sea urchin sperm motility.
Section snippets
Ag NPs characterization
Ag NPs were obtained from Polytech Inc. (Germany) as a 1000 ppm suspension of metallic silver in deionized water, with a nominal particle size provided by the producer in the range of 1–10 nm. Ag-NPs were suspended in 0.22 μm filtered natural seawater (FNSW, supplied from the Aquarium of Genova (Italy, pH 8.27; Salinity 36.9‰) and sampled at few miles from the Ligurian Sea coast) to obtain a concentration of 1 mg mL−1 according to Gambardella et al. (2013), before bringing them to the different
Ag-NP characterization
The mean average of Ag concentration as determined by ICP-OES was 974 ± 4 mg L−1, and therefore it substantially confirmed the nominal concentration reported by the commercial company (100 mg L−1).
Toxicity tests
IC50, LC50 and EC50 values are reported in Table 2. It was not possible to calculate the median concentration for both A. aurita ephyra investigated end-points and crustacean swimming speed alteration (with the exception of 2 4h SSA of A. salina) because they resulted to be lower than the lowest
Discussion
The purpose of this study was to investigate the potential toxicity of Ag-NPs in the marine ecosystem by analyzing effects on invertebrates belonging to different trophic chain levels. The ecotoxicological bioassays performed and the evaluated end-points gave substantially similar results namely that a toxic effect of such NPs is evident. The potential risk of Ag-NP exposure to the selected taxonomic groups is added to that already reported for the exposure to other NPs across primary
Conclusions
Our results showed that Ag-NPs exposure resulted to be toxic to all the tested organisms in a dose-dependent manner suggesting that this kind of metal NPs may affect different trophic levels within the marine ecosystem. Furthermore, selected organisms showed different level of sensitivity to Ag-NPs and A. aurita ephyrae and A. amphitrite nauplii proved to be the most sensitive ones. On the basis of these results it is possible to provide the following species-sensitivity increasing sequence:
Acknowledgments
The authors would like to gratefully acknowledge RITMARE Flagship Project, a National Research Programme funded by the Italian Ministry of University and Research (MIUR).
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