Elsevier

Environment International

Volumes 92–93, July–August 2016, Pages 189-201
Environment International

Review article
Saltwater ecotoxicology of Ag, Au, CuO, TiO2, ZnO and C60 engineered nanoparticles: An overview

https://doi.org/10.1016/j.envint.2016.03.041Get rights and content

Highlights

  • We did a review about saltwater effects of nAg, nAu, nCuO, nTiO2, nZnO and C60.

  • Bacteria were generally the less sensitive testing organisms.

  • Microalgae and bivalve molluscs were the most widespread indicators.

  • Toxicity effects in decreasing order: nAu < nZnO < nAg < nCuO < nTiO2 < C60

Abstract

This review paper examined 529 papers reporting experimental nanoecotoxicological original data. Only 126 papers referred to saltwater environments (water column and sediment) including a huge variety of species (n = 51), their relative endpoints and engineered nanoparticles (ENPs) (n = 38). We tried to provide a synthetic overview of the ecotoxicological effects of ENPs from existing data, refining papers on the basis of cross-cutting selection criteria and supporting a “mind the gap” approach stressing on missing data for hazard and risk assessment. After a codified selection procedure, attention was paid to Ag, Au, CuO, TiO2, ZnO and C60 ENPs, evidencing and comparing the observed nanoecotoxicity range of effect. Several criticisms were evidenced: i) some model organisms are overexploited like microalgae and molluscs compared to annelids, echinoderms and fish; ii) underexploited model organisms: mainly bacteria and fish; iii) exposure scenario variability: high species-specific and ENP scenarios including organism life stage and way of administration/spiking of toxicants; iv) scarce comparability between results due to exposure scenario variability; v) micro- and mesocosms substantially unexplored; vi) mixture effects: few examples are available only for ENPs and traditional pollutants; mixtures of ENPs have not been investigated yet; vii) effects of ions and ENPs: nAg, nCuO and nZnO toxicity aetiology is still a matter of discussion; viii) size and morphology effects of ENPs: scarcely investigated, justified and understood. Toxicity results evidenced that: nAu > nZnO > nAg > nCuO > nTiO2 > C60.

Introduction

The manipulation of the matter at the nanoscale (≤ 100 nm) generates engineered nanomaterials (ENMs) with peculiar physico-chemical characteristics (Liu et al., 2014). Recently, the application of nanotechnology in many fields of industrial production has progressively grown, making engineered nanoparticles (ENPs) a new emerging potential category of environmental contaminants (Manzo et al., 2013a). Their innovative and economic potential is threatened by a limited understanding of the related environmental health and safety (EHS) issues. It is commonly accepted that ENPs can be dispersed into the environment during their productive process, use and end-life (Fan et al., 2014), potentially entering the marine compartment and thus posing potential risks for the biota (Hanna et al., 2013).

In the last decade, aquatic ecotoxicity studies about ENP effects grew rapidly, stressing more on freshwater rather than saltwater or terrestrial species (Corsi et al., 2014, Libralato, 2014, Minetto et al., 2014, Libralato et al., 2016, Lofrano et al., 2016, Vale et al., 2016). Saltwater is a complex matrix pushing ahead ENP instability and promoting the rapid formation of agglomerated/precipitated forms (Callegaro et al., 2015). Despite the huge number of papers, their nanoecosafety is still fragmentary, and the comparison of multiple studies can be difficult, since experimental designs and testing conditions are rarely consistent across studies (Salieri et al., 2015). The shrinking time to market of new ENMs drives the need for pressing actions by policymakers and stakeholders that are still slow to arrive. Starting from highly scattered information and considering a special focus on saltwater, this paper will: (i) provide an overview of ENMs ecotoxicological effects from existing data; (ii) refine papers on cross-cutting selection criteria; (iii) support a “mind the gap” approach stressing on missing data supporting hazard and risk assessment.

This review examined 529 papers including original nanoecotoxicological researches embracing freshwater and saltwater environments up to the end of December 2015. Bibliographic search engines were Google Scholar, PubMed, Scopus and Web of Science. Review papers were not considered. Papers investigated aquatic ecotoxicology on 78 ENPs including metals and metalloids (n = 10), metal oxides (n = 33), organics (n = 3), quantum dots (QD) (n = 5) and “others” (n = 27) (Table S1). The “others” category comprised: ALEX (aluminium NPs), C60HxC70Hx, C60OH24, C70, carbon-iron, CD-Se, cotton nanofibers, fluorescent NPs (FNP), fluorescent silica (FS), graphene oxide, hydroxy apatite (HA), L-ALEX (aluminium NPs), Mg(OH)2, Mn-ZnS, Mo/NaO, N-isopropilacrilamide (NIPAM), N-isopropilacrilamide/N-tertbutylacrylamide (NIPAM/BAM), polyethyleneglycol(PEG)-Fe3O4, PEG-QD, polymethylmethacrylate (PMMA), polystyrene, sodium alginate-polyvinylalcohol-ZnO (SA-PVA-ZnO), sodium dodecyl-sulphate/didodecyl-dimethyl ammonium bromide (SDS/DDAB), tricalcium phosphate (TCP), tobramycin polymeric, Zn–Se, zero valent iron (ZVI). An overview of ENP-biological model pair and the list of recorded species are available in Table S1 and Table S2, respectively.

The relative abundance of studies for ENP was reported in Fig. 1. The attention was mainly focused on metal oxides (65%) and then on metals and metalloids (20%), organics (8%), QD (2%) and others (5%). The most investigated ENPs were: TiO2 (31%), Ag (12%), ZnO (11%), CuO (6%), C60 (5%), Au (3%), CeO2 (3%) and carbon nanotubes (3%).

Focusing on saltwater species, the statistics drastically changed. Only 126 papers (24%) accounted for saltwater nanoecotoxicology including 38 ENPs. They were grouped as metal oxides (n = 20), metals and metalloids (n = 5), organics (n = 3), QD (n = 2) and others (n = 6). A detailed overview of ENP-biological model pair and the list of ENPs relative abundance are available in Table S3, and Fig. 2 (considering saltwater species).

The consistency of data showed to vary according to the exposure scenario making their interpretation very case specific. Various ENPs were tested on several species and endpoints increasing the responses within and between each ENP category and group of organisms (Kahru and Dubourguier, 2010). Nanotoxicity/nanosafety data are increasing day-by-day, but the importance to regulators is often unclear or unproven mainly because their extreme case specific outlook (Minetto et al., 2014). Selected ENPs were considered after a skimming process including (i) the ENPs studied with a frequency ≥ 5%; (ii) the presence of analytical concentrations; (iii) the presence of detailed experimental design including organism exposure conditions, ENP characterization and/or dispersion methods; and (iv) the compliance with quality assurance and quality control procedures. Six ENPs met these criteria (nAg, nAu, nCuO, nTiO2, nZnO and C60) and were investigated within this review.

Section snippets

Ecotoxicity of ENPs

An overview concerning the ecotoxicity effects on saltwater species of nAg, nAu, nCuO, nTiO2, nZnO and C60 was proposed in Table S4. For each ENP, toxicity data were classified according to the taxonomy of biological models. The ENP administration/exposure conditions and uptake were also specified. The reviewed papers not cited in this review, thus not meeting the above-mentioned criteria, were listed in Supplementary materials (Table S5) with the relative references.

Discussion

Data revision highlighted how it is still difficult determining a clear framework about nanoecosafety to saltwater organisms. Information appeared fragmentary and incomplete, and sometimes with a profile of limited ecological significance. From Table S6, it can be observed that i) nevertheless non-ecologically relevant exposure concentrations were taken into consideration (sometimes up to several hundreds of mg/L or mg/kg depending on ENP and its way of exposure - water or sediment), frequently

References (85)

  • E.A. Fairbairn et al.

    Metal oxide nanomaterials in seawater: linking physicochemical characteristics with biological response in sea urchin development

    J. Hazard. Mater.

    (2011)
  • R. Fan et al.

    Effects of nano-TiO2 on the agronomically-relevant Rhizobium-legume symbiosis

    Sci. Total Environ.

    (2014)
  • J. Farkas et al.

    The impact of TiO2 nanoparticles on uptake and toxicity of benzo(a)pyrene in the blue mussel (Mytilus edulis)

    Sci. Total Environ.

    (2015)
  • G. Frenzilli et al.

    Effects of in vitro exposure to titanium dioxide on DNA integrity of bottlenose dolphin (Tursiops truncatus) fibroblasts and leukocytes

    Mar. Environ. Res.

    (2014)
  • C. Gambardella et al.

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

    Mar. Environ. Res.

    (2015)
  • J. García-Alonso et al.

    Toxicity and accumulation of silver nanoparticles during development of the marine polychaete Platynereis dumerilii

    Sci. Total Environ.

    (2014)
  • C.A. García-Negrete et al.

    Behaviour of Au-citrate nanoparticles in seawater and accumulation in bivalves at environmentally relevant concentrations

    Environ. Pollut.

    (2013)
  • T. Gomes et al.

    Genotoxicity of copper oxide and silver nanoparticles in the mussel Mytilus galloprovincialis

    Mar. Environ. Res.

    (2013)
  • T. Gomes et al.

    Accumulation and toxicity of copper oxide nanoparticles in the digestive gland of Mytilus galloprovincialis

    Aquat. Toxicol.

    (2012)
  • T. Gomes et al.

    Differential protein expression in mussels Mytilus galloprovincialis exposed to nano and ionic Ag

    Aquat. Toxicol.

    (2013)
  • S.K. Hanna et al.

    Accumulation and toxicity of metal oxide nanoparticles in a soft-sediment estuarine amphipod

    Aquat. Toxicol.

    (2013)
  • W. Hu et al.

    Toxicity of copper oxide nanoparticles in the blue mussel, Mytilus edulis: a redox proteomic investigation

    Chemosphere

    (2014)
  • B.D. Johnson et al.

    Cellular responses of eastern oysters, Crassostrea virginica, to titanium dioxide nanoparticles

    Marine environmental research

    (2015)
  • A. Kahru et al.

    From ecotoxicology to nanoecotoxicology

    Toxicology

    (2010)
  • G. Libralato

    The case of Artemia spp. in nanoecotoxicology

    Mar. Environ. Res.

    (2014)
  • G. Libralato et al.

    Phytotoxicity of bulk, micro- and nano-sized iron in three plant species

    Ecotoxicol. Environ. Saf.

    (2016)
  • G. Libralato et al.

    Embryotoxicity of TiO2 nanoparticles to Mytilus galloprovincialis (Lmk)

    Mar. Environ. Res.

    (2013)
  • Y. Liu et al.

    Nanoparticles in wastewaters: hazards, fate and remediation

    Powder Technol.

    (2014)
  • G. Lofrano et al.

    Polymer functionalized nanocomposites for metals removal from water and wastewater: an overview

    Water Res.

    (2016)
  • M. Maisano et al.

    Developmental abnormalities and neurotoxicological effects of CuO NPs on the black sea urchin Arbacia lixula by embryotoxicity assay

    Mar. Environ. Res.

    (2015)
  • S. Manzo et al.

    Toxic effects of ZnO nanoparticles towards marine algae Dunaliella tertiolecta

    Sci. Total Environ.

    (2013)
  • B.F. Marques et al.

    Toxicological effects induced by the nanomaterials fullerene and nanosilver in the polychaeta Laeonereis acuta (Nereididae) and in the bacteria communities living at their surface

    Mar. Environ. Res.

    (2013)
  • A.-J. Miao et al.

    The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances

    Environ. Pollut.

    (2009)
  • D. Minetto et al.

    Ecotoxicity of engineered TiO2 nanoparticles to saltwater organisms: an overview

    Environ. Int.

    (2014)
  • M.O. Montes et al.

    Uptake, accumulation, and biotransformation of metal oxide nanoparticles by a marine suspension-feeder

    J. Hazard. Mater.

    (2012)
  • E.B. Muller et al.

    Impact of engineered zinc oxide nanoparticles on the energy budgets of Mytilus galloprovincialis

    J. Sea Res.

    (2014)
  • A. Oukarroum et al.

    Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta

    Ecotoxicol. Environ. Saf.

    (2012)
  • J.-F. Pan et al.

    Size dependent bioaccumulation and ecotoxicity of gold nanoparticles in an endobenthic invertebrate: the tellinid clam Scrobicularia plana

    Environ. Pollut.

    (2012)
  • J. Park et al.

    Effect of salinity on acute copper and zinc toxicity to Tigriopus japonicus: the difference between metal ions and nanoparticles

    Mar. Pollut. Bull.

    (2014)
  • X. Peng et al.

    Effect of morphology of ZnO nanostructures on their toxicity to marine algae

    Aquat. Toxicol.

    (2011)
  • C.H. Pham et al.

    Biomarker gene response in male medaka (Oryzias latipes) chronically exposed to silver nanoparticle

    Ecotoxicol. Environ. Saf.

    (2012)
  • A.L.d.O.F. Rossetto et al.

    Comparative evaluation of acute and chronic toxicities of CuO nanoparticles and bulk using Daphnia magna and Vibrio fischeri

    Science of The Total Environment

    (2014)
  • Cited by (103)

    • Toxicity assessment of TiO<inf>2</inf>-conjugated Carbon-based nanohybrid material on a freshwater bioindicator cladoceran, Daphnia magna

      2022, Aquatic Toxicology
      Citation Excerpt :

      A wide range of such materials are currently being considered and investigated (e.g., carbon nanotubes, titanium dioxide (TiO2)) as potential photocatalysts in water treatment (Lu et al., 2016). Amongst these NMs, the metal-oxide-semiconductor, TiO2, appears to be the most promising and most abundant NP in water (Minetto et al., 2016). The production of nanohybrids (NHs) consisting of metal-oxide NPs and carbon-based nanomaterials (C-NMs) has increased and attracted defined research interest because NHs can be applied to improve the surface area, multifunctional properties and catalytic efficiency of photocatalytic NPs (Baek et al., 2020).

    View all citing articles on Scopus
    View full text