Abstract
Purpose
Metallic nanomaterials (MNM) like cobalt oxide (nano-Co3O4) are currently attracting enormous interest owing to their unique size and shape-dependent properties and potential applications in various sectors. The aims of this study were to assess the toxicity of nano-Co3O4 and to propose a risk limit through the estimation of a Predicted No Effect Concentration (PNEC) for this MNM to soil biota.
Materials and methods
For this purpose, a battery of sub-lethal ecotoxicological tests was performed to assess the influence of this MNM on four plant species (endpoints: germination and growth) and two invertebrate species (endpoints: avoidance and reproduction) following standard protocols. Further, biochemical endpoints (acetylcholinesterase [AChE], catalase [CAT], glutathione-S-transferase [GST] activity, and lipid peroxidation [LPO]) were also assessed in Eisenia andrei, one of the invertebrate species tested, in order to contribute for refining the PNEC value.
Results and discussion
The recorded data showed a significant inhibition in the germination of L. lycopersicum and in the growth of Z. mays, even at the lowest concentration tested (269.3 mg kg−1 soildw of nano-Co3O4). Concerning the soil invertebrates, the results showed only significant avoidance (p < 0.05) by E. andrei in the soil contaminated with the highest concentration tested (1000 mg kg−1 soildw of nano-Co3O4), while no significant ecotoxicological effect on reproductive outputs of both species was recorded. However, the data reported for AChE, CAT, GST, and LPO showed significant effects at the range of concentrations tested in E. andrei. Thus, we recorded, the occurrence of oxidative stress and the enhancement of lipid peroxidation, on this invertebrate species.
Conclusions
The data obtained in this study supports the proposal of a PNEC value of 9.1 mg kg−1 soildw for nano-Co3O4 in soil. The integration of data from biochemical endpoints allowed the refinement of the PNEC value and to obtain a more protective threshold.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Andersen CP, King G, Plocher M, Storm M, Pokhrel LR, Johnson MG, Rygiewicz PT (2016) Germination and early plant development of ten plant species exposed to titanium dioxide and cerium oxide nanoparticles. Environ Toxicol Chem 35:2223–2229
Ando M, Kobayashi T, Iijima S, Haruta M (1997) Optical recognition of CO and H2 by use of gas-sensitive Au-Co3O4 composite films. J Mater Chem 7:1779–1783
Antisari LV, Laudicina VA, Gatti A et al (2014) Soil microbial biomass carbon and fatty acid composition of earthworm Lumbricus rubellus after exposure to engineered nanoparticles. Biol Fertil Soils 51:261–269
Asli S, Neumann PM (2009) Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584
Bakkaus E, Gouget B, Gallien JP, Khodja H, Carrot F, Morel JL, Collins R (2005) Concentration and distribution of cobalt in higher plants: the use of micro-PIXE spectroscopy. Nucl Instrum Methods Phys Res B 231:350–356
Baskar V, Nayeem S, Kuppuraj SP et al (2018) Assessment of the effects of metal oxide nanoparticles on the growth, physiology and metabolic responses in in vitro grown eggplant (Solanum melongena). 3 Biotech 8:362
Bouguerra S, Gavina A, Ksibi M, da Graça Rasteiro M, Rocha-Santos T, Pereira R (2016) Ecotoxicity of titanium silicon oxide (TiSiO4) nanomaterial for terrestrial plants and soil invertebrate species. Ecotoxicol Environ Saf 129:291–301
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brami C, Glover AR, Butt KR, Lowe CN (2017) Effects of silver nanoparticles on survival, biomass change and avoidance behaviour of the endogeic earthworm Allolobophora chlorotica. Ecotoxicol Environ Saf 141:64–69
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310
Calcagnile P, Italiano I, Anyfantis GC et al (2012) Magnetically driven floating foams for the removal of oil contaminants from water. ACS Nano:5413–5419
Cañas JE, Qi B, Li S, Maul JD, Cox SB, Das S, Green MJ (2011) Acute and reproductive toxicity of nano-sized metal oxides (ZnO and TiO2) to earthworms (Eisenia fetida). J Environ Monit 13:3351–3357
Carpita N, Sabularse D, Montezinos D, Delmer DP (1979) Determination of the pore size of cell walls of living plant cells. Science 205:1144–1147
Castiglione MR, Giorgetti L, Geri C, Cremonini R (2011) The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis L. and Zea mays L. J Nanopart Res 13:2443–2449
Chaney R (1983) Plant uptake of inorganic waste constituents. In: Parr J (ed) land treatment of hazardous wastes. Noyes Data Corporation, Park Ridge, pp 50–76
Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74
Chen G, Vijver MG, Peijnenburg WJGM (2015) Summary and analysis of the currently existing literature data on metal-based nanoparticles published for selected aquatic organisms: applicability for toxicity prediction by (Q) SARs. Altern Lab Anim 43:221–240
Coleman JG, Johnson DR, Stanley JK, Bednar AJ, Weiss CA Jr, Boyd RE, Steevens JA (2010) Assessing the fate and effects of nano aluminum oxide in the terrestrial earthworm, Eisenia fetida. Environ Toxicol Chem 29:1575–1580
Colognato R, Bonelli A, Ponti J, Farina M, Bergamaschi E, Sabbioni E, Migliore L (2008) Comparative genotoxicity of cobalt nanoparticles and ions on human peripheral leukocytes in vitro. Mutagenesis 23:377–382
Coutris C, Hertel-Aas T, Lapied E, Joner EJ, Oughton DH (2012) Bioavailability of cobalt and silver nanoparticles to the earthworm Eisenia fetida. Nanotoxicology 6:186–195
Cundy AB, Hopkinson L, Whitby RLD (2008) Use of iron-based technologies in contaminated land and groundwater remediation: a review. Sci Total Environ 400:42–51
Da Costa JP, Santos PSM, Duarte AC, Rocha-Santos T (2016) (Nano)plastics in the environment—sources, fates and effects. Sci Total Environ 566–567:15–26
De la Rosa G, García-Castañeda C, Vázquez-Núñez E et al (2017) Physiological and biochemical response of plants to engineered NMs: implications on future design. Plant Physiol Biochem 110:226–235
Deng Y, White JC, Xing B (2014) Interactions between engineered nanomaterials and agricultural crops: implications for food safety. J Zhejiang Univ Sci A 15:552–572
Dietz KJ, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16:582–589
Du W, Tan W, Peralta-Videa JR et al (2016) Interaction of metal oxide nanoparticles with higher terrestrial plants: physiological and biochemical aspects. Plant Physiol Biochem 110:210–225
EC (2003) Technical guidance document on risk assessment in support of Commission Directive 93/67/ EEC on risk assessment for new notified substances and Commission Regulation (EC) No. 1488/94 on risk assessment for existing substances. Part II. EUR 20418 EN/2
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
El-Temsah YS, Joner EJ (2010) Impact of Fe and Ag nanoparticles on seed germination and differences in bioavailability during exposure in aqueous suspension and soil. Environ Toxicol 27:42–49
Fu L, Liu ZM, Liu YQ, Han B, Hu P, Cao L, Zhu D (2005) Beaded cobalt oxide nanoparticles along carbon nanotubes: towards more highly integrated electronic devices. Adv Mater 17:217–221
Garcia-Velasco N, Peña-Cearra A, Bilbao E, Zaldibar B, Soto M (2017) Integrative assessment of the effects produced by Ag nanoparticles at different levels of biological complexity in Eisenia fetida maintained in two standard soils (OECD and LUFA 2.3). Chemosphere 181:747–758
Gardea-Torresdey JL, Rico CM, White JC (2014) Trophic transfer, transformation, and impact of engineered nanomaterials in terrestrial environments. Environ Sci Technol 48:2526–2540
Gavina A, Bouguerra S, Lopes I, Marques CR, Rasteiro MG, Antunes F, Rocha-Santos T, Pereira R (2016) Impact of organic nano-vesicles in soil: the case of sodium dodecyl sulphate/didodecyl dimethylammonium bromide. Sci Total Environ 547:413–421
Ghodake G, Seo YD, Lee DS (2011) Hazardous phytotoxic nature of cobalt and zinc oxide nanoparticles assessed using Allium cepa. J Hazard Mater 186:952–955
Gomes SIL, Caputo G, Pinna N, Scott-Fordsmand JJ, Amorim MJB (2015a) Effect of 10 different TiO2 and ZrO2 (nano)materials on the soil invertebrate Enchytraeus crypticus. Environ Toxicol Chem 34:2409–2416
Gomes SIL, Hansen D, Scott-Fordsmand JJ, Amorim MJB (2015b) Effects of silver nanoparticles to soil invertebrates: oxidative stress biomarkers in Eisenia fetida. Environ Pollut 199:49–55
Gomes AR, Justino C, Rocha-Santos T, Freitas AC, Duarte AC, Pereira R (2017) Review of the ecotoxicological effects of emerging contaminants to soil biota. J Environ Sci Health A 52:992–1007
Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first step in mercapturic acid formation. J Biol Chem 249:7130–7139
Hatami M, Ghorbanpour M, Salehiarjomand H (2014) Nano-anatase TiO2 modulates the germination behavior and seedling vigority of some commercially important medicinal and aromatic plants. J Biol Environ Sci 8:53–59
He X, Fu P, Aker WG, Hwang HM (2018) Toxicity of engineered nanomaterials mediated by nano–bio–eco interactions. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 36:21–42
Heckmann LH, Hovgaard MB, Sutherland DS, Autrup H, Besenbacher F, Scott-Fordsmand JJ (2011) Limit-test toxicity screening of selected inorganic nanoparticles to the earthworm Eisenia fetida. Ecotoxicology 20:226–233
Hu CW, Li M, Cui YB, Li DS, Chen J, Yang LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42:586–591
Hund-Rinke K, Wiechering H (2001) Earthworm avoidance test for soil assessments. J Soils Sediments 1:15–20
ISO (2008) International Organization for Standardization Guideline 17512-1: soil quality—avoidance test for determining the quality of soils and effects of chemicals on behaviour—part 1: test with earthworms (Eisenia fetida and Eisenia andrei). Geneve, Switzerland
ISO (2011) International Organization for Standardization Guideline 17512-2: soil quality—avoidance test for determining the quality of soils and effects of chemicals on behaviour—part 2: test with collembolans (Folsomia candida). Geneve, Switzerland
ISO (2012a) International Organization for Standardization Guideline 11269-2: soil quality—determination of the effects of pollutants on soil flora—part 2: effects of contaminated soil on the emergence and early growth of higher plants. Geneve, Switzerland
ISO (2012b) International Organization for Standardization Guideline 11268-2: soil quality—effects of pollutants on earthworms—part 2: determination of effects on reproduction of Eisenia fetida / Eisenia andrei. Geneve, Switzerland
ISO (2014) International Organization for Standardization Guideline 11267: soil quality—inhibition of reproduction of collembola (Folsomia candida) by soil contaminants. Geneva, Switzerland
Ito A, Shinkai M, Honda H, Kobayashi T (2005) Medical application of functionalized magnetic nanoparticles. J Biosci Bioeng 100:1–11
Jahan S, Alias YB, Bakar AFBA, Bin YI (2018) Toxicity evaluation of ZnO and TiO2 nanomaterials in hydroponic red bean (Vigna angularis) plant: physiology, biochemistry and kinetic transport. J Environ Sci 72:140–152
Jamal A, Rahman MM, Khan SB, Faisal M, Akhtar K, Rub MA, Asiri AM, al-Youbi AO (2012) Cobalt doped antimony oxide nano-particles based chemical sensor and photo-catalyst for environmental pollutants. Appl Surf Sci 261:52–58
Jesmer AH, Velicogna JR, Schwertfeger DM, Scroggins RP, Princz JI (2017) The toxicity of silver to soil organisms exposed to silver nanoparticles and silver nitrate in biosolids-amended field soil. Environ Toxicol Chem 36:2756–2765
Jiang H, Liu F, Yang H, Li Y (2012) Effects of cobalt nanoparticles on human T cells in vitro. Biol Trace Elem Res 146:23–29
Kahru A, Dubourguier HC, Blinova I, Ivask A, Kasemets K (2008) Biotests and biosensors for ecotoxicology of metal oxide nanoparticles: a minireview. Sensors 8:5153–5170
Karami H (2013) Heavy metal removal from water by magnetite nanorods. Chem Eng J 219:209–216
Keeling SM, Stewart RB, Anderson CW, Robinson BH (2003) Nickel and cobalt phytoextraction by the hyperaccumulator Berkheya coddii: implications for polymetallic phytomining and phytoremediation. Int J Phytoremediation 5:235–244
Kim D, Zhang Y, Voit W et al (2001) Superparamagnetic iron oxide nanoparticles for bio-medical applications. Scr Mater 44:1713–1717
Kool PL, Ortiz MD, Van Gestel CAM (2011) Chronic toxicity of ZnO nanoparticles, non-nano ZnO and ZnCl2 to Folsomia candida (Collembola) in relation to bioavailability in soil. Environ Pollut 159:2713–2719
Kwon Y-M, Xia Z, Glyn-Jones S, Beard D, Gill HS, Murray DW (2009) Dose-dependent cytotoxicity of clinically relevant cobalt nanoparticles and ions on macrophages in vitro. Biomed Mater 4:25018
Lachance B, Hamzeh M, Sunahara GI (2013) Environmental fate and ecotoxicology of nanomaterials. In: Malsch I, Emond C (eds) Nanotechnology and human health. CRC Press Taylor & Francis Group, Boca Raton, pp 209–231
Laconte L, Nitin N, Bao G (2005) Magnetic nanoparticle probes. Mater Today 8:32–38
Laurent S, Boutry SMR, Muller RN (2018) Metal oxide particles and their prospects for applications. In: Mahmoudi M, Laurent S (ed) Iron oxide nanoparticles for biomedical applications. Elsevier Ltd., pp 3–42
Lee CW, Mahendra S, Zodrow K, Li D, Tsai YC, Braam J, Alvarez PJJ (2010) Developmental phytotoxicity of metal oxide nanoparticles to Arabidopsis thaliana. Environ Toxicol Chem 29:669–675
Li HF, Gray C, Mico C, Zhao FJ, McGrath SP (2009) Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere 75:979–986
Liang J, Xia X, Zhang W, Zaman WQ, Lin K, Hu S, Lin Z (2017) The biochemical and toxicological responses of earthworm (Eisenia fetida) following exposure to nanoscale zerovalent iron in a soil system. Environ Sci Pollut Res 24:2507–2514
Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 150:243–250
Liu X, Qiu G, Li X (2005) Shape-controlled synthesis and properties of uniform spinel cobalt oxide nanocubes. Nanotechnology 16:3035–3040
Liu X, Zhang S, Quan SX, Christie P (2007) Combined toxicity of cadmium and arsenate to wheat seedlings and plant uptake and antioxidative enzyme responses to cadmium and arsenate co-contamination. Ecotoxicol Environ Saf 68:305–313
Lock K, Becaus S, Criel P, van Eeckhout H, Janssen CR (2004) Ecotoxicity of cobalt to the springtail Folsomia candida. Comp Biochem Physiol C Toxicol Pharmacol 139:195–199
Lowry GV, Gregory KB, Apte SC, Lead JR (2012) Guest comment: transformations of nanomaterials in the environment focus issue. Environ Sci Technol 46:6891–6892
Lu F, Astruc D (2018) Nanomaterials for removal of toxic elements from water. Coord Chem Rev 356:147–164
Ma X, Geiser-lee J, Deng Y, Kolmakov A (2010a) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061
Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Zhao Y, Chai Z (2010b) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78:273–279
Malvern ZetaSizer (2013) Malvern Zetasizer SZ nano series user manual. mano 485, 1.1. United Kingdom
Man L, Niu B, Xu H, Cao B, Wang J (2011) Microwave hydrothermal synthesis of nanoporous cobalt oxides and their gas sensing properties. Mater Res Bull 46:1097–1101
Maurer-Jones MA, Gunsolus IL, Murphy CJ, Haynes CL (2013) Toxicity of engineered nanoparticles in the environment. Anal Chem 85:3036–3049
McShane H, Sarrazin M, Whalen JK, Hendershot WH, Sunahara GI (2012) Reproductive and behavioral responses of earthworms exposed to nano-sized titanium dioxide in soil. Environ Toxicol Chem 31:184–193
Nair PMG, Chung IM (2014) Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignificaion, and molecular level changes. Environ Sci Pollut Res 21:12709–12722
NanoComposix (2015) Guidelines for dynamic light scattering measurement and analysis, available at: https://cdn.shopify.com/s/files/1/0257/8237/files/nanoComposix_Guidelines_for_DLS_Measurements_and_Analysis.pdf
Nowack B, Ranville JF, Diamond S, Gallego-Urrea JA, Metcalfe C, Rose J, Horne N, Koelmans AA, Klaine SJ (2012) Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ Toxicol Chem 31:50–59. https://doi.org/10.1002/etc.726
Nowack B, Bornhöft N, Ding Y, Riediker M, Jiménez AS, Sun T, van Tongeren M, Wohlleben W (2015) The flows of engineered nanomaterials from production, use, and disposal to the environment. In: Viana M (ed) Indoor and outdoor nanoparticles, determinants of release and exposure scenarios. Springer International Publishing, Cham, pp 209–231
OECD (1984) Organization for Economic Cooperation and Development. Terrestrial plants, growth test. Guideline for testing of chemicals. 208. Paris, France www.oecd.org/chemicalsafety/testing/33653757.pdf
Pandey BK, Shahi AK, Srivastava N, Kumar G, Gopal R (2015) Synthesis and cytogenetic effect of magnetic nanoparticles. Adv Mater Lett 6:954–960
Pankhurst QA, Connolly J, Jones SK, Dobson J (2003) Applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys 36:R167–R181
Papis E, Rossi F, Raspanti M, Dalle-Donne I, Colombo G, Milzani A, Bernardini G, Gornati R (2009) Engineered cobalt oxide nanoparticles readily enter cells. Toxicol Lett 189:253–259
Parkes LM, Hodgson R, Lu LT, Tung LD, Robinson I, Fernig DG, Thanh NTK (2008) Cobalt nanoparticles as a novel magnetic resonance contrast agent—relaxivities at 1.5 and 3 Tesla. Contrast Media Mol Imaging 3:150–156
Ponti J, Sabbioni E, Munaro B, Broggi F, Marmorato P, Franchini F, Colognato R, Rossi F (2009) Genotoxicity and morphological transformation induced by cobalt nanoparticles and cobalt chloride: an in vitro study in Balb/3T3 mouse fibroblasts. Mutagenesis 24:439–445
Pulicharla R, Brar SK, Verma M et al (2015) Behavior and fate of natural and engineered nanomaterials in soils. In: Brar SK, Zhang TC, Verma M et al (eds) Nanomaterials in the environment. American Society of Civil Engineers, Reston, pp 291–314
Rajput VD, Minkina T, Sushkova S, Tsitsuashvili V, Mandzhieva S, Gorovtsov A, Nevidomskyaya D, Gromakova N (2018a) Effect of nanoparticles on crops and soil microbial communities. J Soils Sediments 18:2179–2187
Rajput VD, Minkina T, Suskova S, Mandzhieva S, Tsitsuashvili V, Chapligin V, Fedorenko A (2018b) Effects of copper nanoparticles (CuO NPs) on crop plants: a mini review. BioNanoScience 8:36–42
Rault M, Mazzia C, Capowiez Y (2007) Tissue distribution and characterization of cholinesterase activity in six earthworm species. Comp Biochem Physiol B Biochem Mol Biol 147:340–346
Ray PC, Yu H, Fu PP (2009) Toxicity and environmental risks of nanomaterials: challenges and future needs. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27:1–35
Rizwan M, Ali S, Qayyum MF et al (2017) Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: a critical review. J Hazard Mater 322:2–16
Rutnakornpituk M, Baranauskas VV, Riffle JS et al (2002) Polysiloxane fluid dispersions of cobalt nanoparticles in silica spheres for use in ophthalmic applications. Eur Cells Mater 3:102–105
Serag MF, Kaji N, Habuchi S, Bianco A, Baba Y (2013) Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers. RSC Adv 3:4856
Singh R, Nalwa HS (2011) Medical applications of nanoparticles in biological imaging, cell labeling, antimicrobial agents, and anticancer nanodrugs. J Biomed Nanotechnol 7:489–503
Srivastava N (2015) Interaction of cobalt nanoparticles with plants: a cytogenetical aspect. J Exp Nanosci 10:769–776
Tepfer M, Taylor IE (1981) The permeability of plant cell walls as measured by gel filtration chromatography. Science 213:761–763
Tjong SC, Chen H (2004) Nanocrystalline materials and coatings. Mater Sci Eng R Rep 45:1–88
Trujillo-Reyes J, Peralta-Videa JR, Gardea-Torresdey JL (2014) Supported and unsupported nanomaterials for water and soil remediation: are they a useful solution for worldwide pollution? J Hazard Mater 280:487–503
Wahid F, Khan T, Shehzad A, Ul-Islam M, Kim YY (2014) Interaction of nanomaterials with cells and their medical applications. J Nanosci Nanotechnol 14:744–754
Wang J, Wang W (2014) Significance of physicochemical and uptake kinetics in controlling the toxicity of metallic nanomaterials to aquatic organisms. J Zhejiang Univ A 15:573–592
Wang GX, Chen Y, Konstantinov K, Yao J, Ahn JH, Liu HK, Dou SX (2002) Nanosize cobalt oxides as anode materials for lithium-ion batteries. J Alloys Compd 340:L5–L10
Wang K, Xu JJ, Chen HY (2005) A novel glucose biosensor based on the nanoscaled cobalt phthalocyanine-glucose oxidase biocomposite. Biosens Bioelectron 20:1388–1396
Wang Z, Zhao J, Li F, Gao D, Xing B (2009) Adsorption and inhibition of acetylcholinesterase by different nanoparticles. Chemosphere 77:67–73
Wierzbicka MS, Obidzińska J (1998) The effect of lead on seed imbibition and germination in different plant species. Plant Sci 137:155–171
Wild E, Jones KC (2009) Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. Environ Sci Technol 43:5290–5294
Wu SG, Huang L, Head J et al (2012a) Phytotoxicity of metal oxide nanoparticles is related to both dissolved metals ions and adsorption of particles on seed surfaces. J Pet Environ Biotechnol 3:2–6
Wu HB, Chen JS, Hng HH, Lou XWD (2012b) 182 nanostructured metal oxide-based materials as advanced anodes for lithium-ion batteries. Nanoscale 4:2526–2542
Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 158:122–132
Yang M, Jiang J, Yang Y, Chen X, Shen G, Yu R (2006) Carbon nanotube/cobalt hexacyanoferrate nanoparticle-biopolymer system for the fabrication of biosensors. Biosens Bioelectron 21:1791–1797
Yang Z, Chen J, Dou R, Gao X, Mao C, Wang L (2015) Assessment of the phytotoxicity of metal oxide nanoparticles on two crop plants, maize (Zea mays L.) and rice (Oryza sativa L.). Int J Environ Res Public Health 12:15100–15109
Zhou Z-Y, Tian N, Li J-T, Broadwell I, Sun SG (2011) Nanomaterials of high surface energy with exceptional properties in catalysis and energy storage. Chem Soc Rev 40:4167–4185
Ziccardi L, Mcardle M, Lowney Y (2008) The ecological effects of nanomaterials: a focus on aquatic life. Nano 3:251–255
Funding
This research is part of the project REALISE (PTDC/AAC-AMB/120697/2010) funded by the Portuguese Government (Program Ciência – Inovação 2010) and by the European Social Fund – COMPETE. Sirine Bouguerra was supported by an investigator fellowship (Ref. PTDC/AAC-AMB/120697/2010) from the project. Ana Gavina was also supported by a Ph.D. Grant (Ref. SFRH/BD/94902/2013) from FCT – Foundation for Science and Technology. This research was also partially supported by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020.
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Bouguerra, S., Gavina, A., da Graça Rasteiro, M. et al. Effects of cobalt oxide nanomaterial on plants and soil invertebrates at different levels of biological organization. J Soils Sediments 19, 3018–3034 (2019). https://doi.org/10.1007/s11368-019-02285-8
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DOI: https://doi.org/10.1007/s11368-019-02285-8