Elsevier

Marine Environmental Research

Volume 111, October 2015, Pages 41-49
Marine Environmental Research

Effect of silver nanoparticles on marine organisms belonging to different trophic levels

https://doi.org/10.1016/j.marenvres.2015.06.001Get rights and content

Highlights

  • Ag-NP effects were investigated in marine species at different trophic levels.

  • Algae, cnidarians, crustaceans and echinoderms were exposed to Ag-NP suspensions.

  • Acute and behavioral end-points were evaluated to detect Ag-NP toxicity.

  • All end-points underlined a dose-dependent effect at any level of the trophic chain.

  • Ag-NPs exposure influenced different trophic levels within the marine ecosystem.

Abstract

Silver nanoparticles (Ag-NPs) are increasingly used in a wide range of consumer products and such an extensive use raises questions about their safety and environmental toxicity. We investigated the potential toxicity of Ag-NPs in the marine ecosystem by analyzing the effects on several organisms belonging to different trophic levels. Algae (Dunaliella tertiolecta, Skeletonema costatum), cnidaria (Aurelia aurita jellyfish), crustaceans (Amphibalanus amphitrite and Artemia salina) and echinoderms (Paracentrotus lividus) were exposed to Ag-NPs and different end-points were evaluated: algal growth, ephyra jellyfish immobilization and frequency of pulsations, crustaceans mortality and swimming behavior, and sea urchin sperm motility. Results showed that all the end-points were able to underline a dose-dependent effect. Jellyfish were the most sensitive species, followed by barnacles, sea urchins, green algae, diatoms and brine shrimps. In conclusion, Ag-NPs exposure can influence different trophic levels within the marine ecosystem.

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).

References (103)

  • C. Gambardella et al.

    Exposure of Paracentrotus lividus male gametes to engineered nanoparticles affects skeletal bio-mineralization processes and larval plasticity

    Aquat. Toxicol.

    (2015)
  • A. Kahru et al.

    From ecotoxicology to nanoecotoxicology

    Toxicology

    (2010)
  • J.S. Kim et al.

    Antimicrobial effects of silver nanoparticles

    Nanomedicine

    (2007)
  • G. Libralato

    The case of Artemia spp. in nanoecotoxicology

    Mar. Environ. Res.

    (2014)
  • M.P. McCarthy et al.

    Tissue specific responses of oysters, Crassostrea virginica, to silver nanoparticles

    Aquat. Toxicol.

    (2013)
  • T. Mesarič et al.

    High surface adsorption properties of carbon-based nanomaterials are responsible for mortality, swimming inhibition, and biochemical responses in Artemia salina larvae

    Aquat. Toxicol.

    (2015)
  • B.S. Nunes et al.

    Use of the genus Artemia in ecotoxicity testing

    Environ. Pollut.

    (2006)
  • S. Pétinay et al.

    Standardisation du développement larvaire de l'oursin, Paracentrotus lividus, pour l'évaluation de la qualité d'une eau de mer

    C.R. Biol.

    (2009)
  • V. Piazza et al.

    A standardization of Amphibalanus (Balanus amphitrite (Crustacea, Cirripedia) larval biomassa for ecotoxicological studies

    Ecotoxicol. Environ. Saf.

    (2012)
  • A.H. Ringwood et al.

    The effects of silver nanoparticles on oysters embryos

    Mar. Environ. Res.

    (2010)
  • L. Siller et al.

    Silver nanoparticle toxicity in sea urchin Paracentrotus lividus

    Environ. Pollut.

    (2013)
  • R. Suwa et al.

    Effects of silver nanocolloids on early life stages of the scleractinian coral Acropora japonica

    Mar. Environ. Res.

    (2014)
  • I. Varò et al.

    Characterisation of cholinestersae and evaluation of the inhibitory potential of chlorpryfos, and dichlorvos to Artemia salina and Artemia parthenogenetica

    Chemosphere

    (2002)
  • G.E. Walsh

    Cell death and inhibition of population growth of marine unicellular algae by pesticides

    Aquat. Toxicol.

    (1983)
  • Y.S. Wong et al.

    Toxicity of marine sediments in Victoria harbor, Hong Kong

    Mar. Pollut. Bull.

    (1995)
  • H. Alyuruk et al.

    A video tracking based improvement of acute toxicity test on Artemia salina

    Mar. Freshw. Behav. Physiol.

    (2013)
  • C. Amiard-Triquet

    Behavioral disturbances: the missing link between sub-organismal and supra-organismal responses to stress? Prospects based on aquatic research

    Hum. Ecol. Risk Assess.

    (2009)
  • APAT IRSA CNR 8070

    Metodo di valutazione della tossicità acuta con Artemia sp

    (2003)
  • C. Arulvasu et al.

    Toxicity effect of silver nanoparticles in brine shrimp Artemia

    Sci. World J.

    (2014)
  • P.V. Asharani et al.

    Toxicity of silver nanoparticles in zebrafish models

    Nanotechnology

    (2008)
  • S. Ashgari et al.

    Toxicity of various silver nanoparticles to silver ions in Daphnia magna

    J. Nanobiotechnology

    (2012)
  • ASTM, E1563-98

    Standard Guide for Conducting Static Acute Toxicity Tests with Echinoid Embryos

    (2004)
  • M. Ates et al.

    Comparative evaluation of impact of Zn and ZnO nanoparticles on brine shrimp (Artemia salina) larvae: effects of particle size and solubility on toxicity

    Environ. Sci. Process. Impacts

    (2013)
  • A. Baun et al.

    Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing

    Ecotoxicology

    (2008)
  • A.A. Becaro et al.

    Toxicity of PVA-stabilized silver nanoparticles to algae and microcrustaceans

    Environ. Nanotechnol. Monit. Manag.

    (2014)
  • C. Blaise et al.

    Ecotoxicity of selected nanomaterials to aquatic organisms

    Environ. Toxicol.

    (2008)
  • I. Blinova et al.

    Toxicity of two types of silver nanoparticles to aquatic crustaceans Daphnia magna and Thamnocephalus platyurus

    Environ. Sci. Pollut. Res.

    (2013)
  • L. Braydich-Stolle et al.

    In vitro cytotoxicity of nanoparticles in mammalian germline stem cells

    Toxicol. Sci.

    (2005)
  • L.M. Browning et al.

    Silver nanoparticles incite size- and dose-dependent developmental phenotypes and nanotoxicity in zebrafish embryos

    Chem. Res. Toxicol.

    (2013)
  • L. Cardona et al.

    Massive consumption of gelatinous plankton by Mediterranean apex predators

    Plos One

    (2012)
  • C. Castellini et al.

    Long-term effects of silver nanoparticles on reproductive ability of rabbit buck

    Syst. Biol. Reprod. Med.

    (2014)
  • T. Cerdevall et al.

    Food chain transport of nanoparticles affect behaviour and fat metabolism in fish

    Plos One

    (2012)
  • E. Costa et al.

    Effect of neurotoxic compounds on ephyrae of Aurelia aurita jellyfish

    Hydrobiologia

    (2015)
  • R. D'Adamo et al.

    The effect of floods on sediment contamination in a microtidal coastal lagoon: the Lagoon of Lesina, Italy

    Archiv. Environ. Contam. Toxicol.

    (2014)
  • P. Das et al.

    Toxicity of silver and titanium dioxide nanoparticle suspensions to the aquatic invertebrate, Daphnia magna

    Bull. Environ. Contam. Toxicol.

    (2013)
  • R. Dineshrama et al.

    Biofouling studies on nanoparticle-based metal oxide coatings on glass coupons exposed to marine environment

    Colloids Surf. B: Biointerf.

    (2009)
  • A. Fabbrocini et al.

    Gamete and embryos of sea urchins (P. lividus Lmk 1816) reared in confined conditions: their use in toxicity bioassays

    Chem. Ecol.

    (2011)
  • M. Faimali et al.

    Swimming speed alteration of larvae of Balanus amphitrite as behavioural endpoint for laboratory toxicological bioassays

    Mar. Biol.

    (2006)
  • M. Faimali et al.

    Produzione ed allevamento di larve di Cirripedi: Balanus amphitrite come specie modello

  • C. Falugi et al.

    Dose dependent effects of silver nanoparticles on reproduction and development of different biological models

    EQA

    (2012)
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