Abstract
The increasing use of silver nanoparticles (AgNPs) in consumer products raises concerns regarding the environmental exposure and impact of AgNPs on natural aquatic environments. Here, we investigated the effects of environmentally relevant AgNP concentrations on the natural plankton communities using in situ enclosures. Using twelve lake enclosures, we tested the hypotheses that AgNP concentration, dosing regimen, and capping agent (poly-vinyl pyrrolidone (PVP) vs. citrate) exhibit differential effects on plankton communities. Each of the following six treatments was replicated twice: control (no AgNPs added), low, medium, and high chronic PVP treatments (PVP-capped AgNPs added continuously, with target nominal concentrations of 4, 16, and 64 μg/L, respectively), citrate treatment (citrate-capped AgNPs added continuously, target nominal concentrations of 64 μg/L), and pulse treatment (64 μg/L PVP-AgNPs added as a single dose). Although Ag accumulated in the phytoplankton, no statistically significant treatment effect was found on phytoplankton community structure or biomass. In contrast, as AgNP exposure rate increased, zooplankton abundance generally increased while biomass and species richness declined. We also observed a shift in the size structure of zooplankton communities in the chronic AgNP treatments. In the pulse treatments, zooplankton abundance and biomass were reduced suggesting short periods of high AgNP concentrations affect zooplankton communities differently than chronic exposures. We found no evidence that capping agent affected AgNP toxicity on either community. Overall, our study demonstrates variable AgNP toxicity between trophic levels with stronger AgNP effects on zooplankton. Such effects on zooplankton are troubling and indicate that AgNP contamination could affect aquatic food webs.
Similar content being viewed by others
References
Angel BM, Batley GE, Jarolimek CV, Rogers NJ (2013) The impact of size on the fate and toxicity of nanoparticulate silver in aquatic systems. Chemosphere 93:359–365
APHA (1992) Standard methods for the examination of water and wastewater. Amer Pub Health Assoc Washington, DC
Asghari S, Johari SA, Lee JH, Kim YS, Jeon YB, Choi HJ, Moon MC, Yu IJ (2012) Toxicity of various silver nanoparticles compared to silver ions in Daphnia magna. J Nanobiotechnology 10:1–11
Baptista MS, Miller RJ, Halewood ER, Hanna SK, Almeida MR, Vasconcelos VM, Keller AA, Lenihan HS (2015) Impacts of silver nanoparticles on a natural estuarine plankton community. Enviro Sci Technol 49:12968–12974
Blakelock GC, Xenopoulos MA, Norman BM, Vincent JL, Frost PC (2016) Effects of silver nanoparticles on bacterioplankton in a boreal lake. Freshwater Biol 61: 2211–2220
Blaser SA, Scheringer M, MacLedo M, Hungerbühler K (2008) Estimation of cumulative aquatic exposure and risk due to silver: Contribution of nano-functionalized plastics and textiles. Sci Total Environ 390:396–409
Blinova I, Niskanen J, Kajankari P, Kanarbik L, Käkinen A, Tenhu H, Penttinen O-P, Kahru A (2013) Toxicity of two types of silver nanoparticles crustaceans Daphnia magna and Thamnocephalus platyurus. Environ Sci Pollut Res 20:3456–3463
Bone AJ, Colman BP, Gondikas AP, Newton KM, Harrold KH, Cory RM, Unrine JM, Klaine SJ, Matson CW, Di Giulio RT (2012) Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of Ag nanoparticles: part 2-toxicity and Ag speciation. Environ Sci Technol 46:6925–6933
Colman BP, Arnaout CL, Anciaux S, Gunsch CK, Hochella MF Jr, Bojeong K, Lowry GV, McGill BM, Reinsch BC, Richardson CJ, Unrine JM, Wright JP, Yin L, Bernhardt ES (2013) Low concentrations of silver nanoparticles in biosolids cause adverse ecosystem responses under realistic field scenario PLOS one doi:10.1371/journal.pone.0057189
Colman BP, Espinasse B, Richardson CJ, Matson CW, Lowry GV, Hunt DE, Wiesner MR, Bernhardt ES (2014) Emerging contaminant or an old toxin in disguise? Silver nanoparticle impacts on ecosystems. Environ Sci Technol 48:5229–5236
Crumpton WG, Isenhart TM, Mitchell PD (1992) Nitrate and organic N analyses with second-derivative spectroscopy. Limnol Oceanogr 37:907–913
Culver BA, Boucherle MM, Bean DJ, Fletcher JW (1985) Biomass of freshwater crustacean zooplankton from length-weight regressions. Can J Fish Aquat Sci 42:1380–1396
Dale AL, Lowry GV, Casman EA (2015) Much ado about α: reframing the debate over appropriate fate descriptors in nanoparticle environmental risk modeling. Environ Sci Nano 2:27–32
Das P, Metcalfe CD, Xenopoulos MA (2014) Interactive effects of silver nanoparticles and phosphorus on phytoplankton growth in natural waters. Environ Sci Technol 48:4573–4580
Das P, Xenopoulos MA, Metcalfe CD (2013) Toxicity of silver and titanium dioxide nanoparticle suspensions to the aquatic invertebrate, Daphnia magna. Bull Environ Contam Toxicol 91:76–82
Dash A, Singh AP, Chaudhary BR, Singh SK, Dash D (2012) Effect of silver nanoparticles on growth and eukaryotic green algae. Nano-micro letters 4:158–165
Downing JA, Peters RH (1980) The effects of body size and food concentration on the in situ filtering rate of Sida crystalline. Limnol Oceanogr 25:883–895
Dumont E, Johnson AC, Keller VDJ, Williams RJ (2015) Nano silver and nano zinc-oxide in surface waters – Exposure estimation for Europe at high spatial and temporal resolution. Environ Pollut 196:341–349
Fairchild GW (1980) Movement and microdistribution of Sida crystallina and other littoral microcrustacea. Ecology 62:1341–1352
Findlay DL, Vanni MJ, Paterson M, Mills KH, Kasian SEM, Findlay WJ, Salki AG (2005) Dynamics of a boreal lake ecosystem during a long-term manipulation of top predators. Ecosystems 8:603–618
Fischer JM, Frost TM, Ives AR (2001) Compensatory dynamics in zooplankton community responses to acidification: measurement and mechanisms. Ecol Appl 11:1060–1072
Fulton III RS (1988) Resistance to blue-green algal toxins by Bosmina longirostris. J Plankton Res 10:771–778
Furtado L, Hoque M, Mitrano D, Ranville J, Cheever B, Frost PC, Xenopoulos MA, Hintelmann H, Metcalfe C (2014) The persistence and transformation of silver nanoparticles in littoral lake mesocosms monitored using various analytical techniques. Environ Chem 11:419–430
Furtado LM, Norman BC, Xenopoulos MA, Frost PC, Metcalfe CD, Hintelmann H (2015) Environmental fate of silver nanoparticles in boreal lake ecosystems. Environ Sci Technol 49:8441–8450
Gao J, Youn S, Hovsepyan A, Llaneza VL, Wang Y, Bitton G, Bonzongo J-CJ (2009) Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol 43:3322–3328
Gonzalez A, Loreau M (2009) The causes and consequences of compensatory dynamics in ecological communities. Annu Rev Ecol Evol Syst 40:393–414
Gottschalk F, Scholz W, Nowack B (2010) Probabilistic material flow modeling for assessing the environmental exposure to compounds: methodology and an application to engineered nano-TiO2 particles. Environ Modell Softw 25:320–332
Gottschalk F, Sonderer T, Scholz RW, Nowack B (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, Fullerenes) for different regions. Environ Sci Technol 43:9216–9222
Gray EP, Coleman JG, Bednar AJ, Kennedy AJ, Ranville JF, Higgins CP (2013) Extraction and analysis of silver and gold nanoparticles from biological tissues using single particle inductively coupled plasma mass spectrometry. Environ Sci Technol 47:14315–14323
Griffitt RJ, Luo J, Gao J, Bonzongo J-C, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Tox Chem 27:1972–1978
Handy R, Owen R, Valsami-Jones E (2008) The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology 17:315–325
Hoheisel SM, Diamond S, Mount D (2012) Comparison of nanosilver and ionic silver toxicity in Daphnia magna and Pimephales Promelas. Environ Tox Chem 31:2557–2563
Kahru A, Dubourguier H-C (2010) From ecotoxicology to nanoecotoxicology. Toxicology 269:105–119
Kennedy AJ, Hull MS, Bednar AJ, Goss JD, Gunter JC, Bouldin JL, Vikesland PJ, Stevens JA (2010) Fractionating nanosilver: importance for determining toxicity to aquatic text organisms. Environ Sci Technol 44:9571–9577
Kennedy AJ, Hull MS, Diamond S, Chappell M, Bednar AJ, Laird JG, Melby NL, Stevens JS (2015) Gaining a critical mass: A dose metric conversion case study using silver nanoparticles. Environ Sci Technol 49:12490–12499
Lawrence SG, Matley BF, Findlay WJ, Maelver MA, Delbaere IL (1987) Method for estimating dry weight of freshwater planktonic crustaceans from measures of length and shape. Can J Fish Aquat Sci 44:264–274
Levard C, Hotze EM, Colman BP, Dale AL, Truong L, Yang XY, Bone AJ, Brown Jr GE, Tanguay RL, Di Giulio RT, Bernhardt ES, Meyer JN, Wiesner MR, Lowry GV (2012) Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ Sci Technol 47:13440–13448
Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175
Lu W, Senapati D, Wang S, Tovmachenko O, Singh AK, Yu H, Ray PC (2010) Effect of surface coating on the toxicity of silver nanomaterials on human skin keratinocytes. Chem Phys Lett 487:92–96
Malley DF, Lawrence SGL, Maciver MA, Findley WJ (1989) Range of variation in estimates of dry weight for planktonic crustacea and rotifera from temperate North American Lakes. Can Techn Rep Fish Aquat Sci #1666
Maynard DG, Kalra YP (1993) Nitrate and exchangeable ammonium nitrogen. In: Carter MR (ed) Soil Sampling and Methods of Analysis. Lewis Publishers, Florida, pp 28–32
McCauley E (1984). The estimation of the abundance and biomass of zooplankton in samples. In: Downing JA, & Rigler FH (ed) A manual on methods for the assessment of secondary productivity in fresh waters. 2nd edn. Blackwell, Oxford, pp 228–265
McTeer J, Dean AP, White KN, Pittman JK (2014) Bioaccumulation of silver nanoparticles in Daphnia magna from a freshwater algal diet and the impact of phosphate availability. Nanotoxicology 8:305–316
Miao A-J, Luo Z, Chen C-S, Chin W-C, Santschi PH, Quigg A (2010) Intracellular uptake: a possible mechanism for silver engineered nanoparticle toxicity to a freshwater alga Ochromonas danica. PLOS One 5:e15196
Miao A-J, Schwehr KA, Xu C, Zhang S-J, Luo Z, Quigg A, Santschi PH (2009) The algal toxicity of silver engineered nanoparticles and detoxification by exopolymeric substances. Environ Poll 157:3034–3041
Mitrano DM, Barber A, Bednar A, Westerhoff P, Higgins C, Ranville J (2012) Silver nanoparticle characterization using single partial ICP-MS (SP-ICP-MS) and asymmetrical flow field flow fractionation ICP-MS (AF4- ICP-MS). J Anal At Spectrom 27:1131–1142
Musee N (2011) Simulated environmental risk estimation of engineered nanomaterials: A case of cosmetics in Johannesburg city. Hum Exp Toxicol 30:1181–1195
Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak N, Sigg L, Behra R (2008) Toxicity of silver nanoparticles to Chlamydomonas reinhardtii. Environ Sci Technol 42:8959–8964
Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effect of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotox Environ Safe 78:80–85
Pace HE, Rogers NJ, Jarolimek C, Coleman VA, Higgins CP, Ranville JF (2011) Determining transport efficiency for the purpose of counting and sizing nanoparticles via single particle inductively coupled plasma mass spectrometry. Anal Chem 83:9361–9369
Paterson MJ, Podemski CL, Findlay WJ, Findlay DL, Salki AG (2010) The response of zooplankton in a whole-lake experiment on the effects of a cage aquaculture operation for rainbow trout (Oncorhynchus mykiss). Can J Fish Aquatic Sci 67:1852–1861
Petosa AR, Jaisi DP, Quevedo IR, Elimelech M, Tufenkji N (2010) Aggregation and deposition of engineered nanomaterials in aquatic environments: role of physicochemical interactions. Environ Sci Technol 44:6532–6549
Pillai S, Behra R, Nestler H, Suter MJ-F, Sigg L, Schirmer K (2014) Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver. PNAS 111:3490–3495
Pinel-Alloul B, André A, Legendre P, Cardille JA, Patalas K, Salki A (2013) Large-scale geographic patterns of diversity and community structure of pelagic crustacean zooplankton in Canadian lakes. Global Ecol Biogeogr 22:784–795
Prepas EE (1978) Sugar-frosted Daphnia: an improved fixation technique for Cladocera. Limnol Oceanogr 23:557–559
Rana S, Samanta S, Bhattacharya S, Al-Khaled K, Gosawami A, Chattopadhyay J (2015) The effect of nanoparticles on plankton dynamics: a mathematical model. Biosystems 127:28–41
Rosen RA (1981) Length-dry weight relationships of some freshwater zooplankton. J Freshwater Ecol 1:225–229
Sakamoto M, Chang KH, Hanazato T (2005) Differential sensitivity of a predacious cladoceran (Leptodora) and its prey (the cladoceran Bosmina) to the insecticide carbaryl: results of acute toxicity tests. Bull Environ Contam Toxicol 75:28–33
Sterner RW, Schulz KL (1998) Zooplankton nutrition: recent progress and a reality check. Aquatic Ecology 32:261–279
Stevenson LM, Dickon H, Klanjscek T, Keller AA, McCauley E, Nisbet RM (2013) Environmental feedbacks and engineered nanoparticles: mitigation of silver nanoparticle toxicity to Chlamydomonas reinhardtii by algal-produced organic compounds. PLOS ONE 8:e74456
Tejamaya M, Romer I, Merrifield RC, Lead JR (2012) Stability of citrate, PVP, and PEG coated silver nanoparticles in ecotoxicology media. Environ Sci Technol 46:7011–7017
Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M (2010) An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: A systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 408:999–1006
Unrine JM, Colman BP, Bone AJ, Gondikas AP, Matson CW (2012) Biotic and abiotic interaction in aquatic microcosms determine fate and toxicity of Ag nanoparticles. Part 1. Aggregation and dissolution. Environ Sci Technol 43:6015–6024
Vinebrooke RD, Schindler DW, Findlay DL, Turner MA, Paterson M, Mills KH (2003) Trophic dependence of ecosystem resistance and species compensation in experimentally acidified Lake 302S (Canada). Ecosystems 6:101–113
Xenopoulos MA, Leavitt PR, Schindler DW (2009) Ecosystem regulation of boreal lake phytoplankton by ultraviolet radiation. Can J Fish Aquat Sci 66:2002–2010
Yan ND, Girard R, Heneberry JH, Keller WB, Gunn JM, Dillon PJ (2004) Recovery of copepod, but not cladoceran zooplankton from severe and chronic effects of multiple stressors. Ecol Lett 7:452–460
Yan ND, Strus R (1980) Crustacean zooplankton communities of acidic, metal-contaminated lakes near Sudbury, Ontario Can J Fish Aquat Sci 37:2282–2293
Zhao C-M, Wang W-X (2010) Biokinetic uptake and efflux of silver nanoparticles in Daphnia magna. Environ Sci Technol 44:7699–7704
Zhao C-M, Wang W-X (2011) Comparison of acute and chronic toxicity of silver nanoparticles and silver nitrate to Daphnia magna. Environ Tox Chem 30:885–892
Acknowledgements
This research was funded by Canada’s Natural Sciences and Engineering Research Council Strategic Project grant awarded to Trent University, with additional support from Environment Canada, the IISD-Experimental lakes Area and the Provinces of Ontario and Manitoba. We thank Graham Blakelock, Lindsay Furtado, Jonathan Martin, and Nicole Novodvorský for their assistance in the field and laboratory. We thank Chris Metcalfe and Holger Hintelmann for all the insightful discussions throughout this project. In addition, we thank the scientists and staff at the Experimental Lakes Area for their support, guidance and knowledge throughout this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
This research was funded by Canada’s Natural Sciences and Engineering Research Council Strategic Project grant awarded to Trent University, with additional support from Environment Canada, the IISD-Experimental lakes Area and the Provinces of Ontario and Manitoba. All authors declare that they have no conflict of interest. This article does not contain any studies with vertebrate animals performed by any of the authors.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Vincent, J.L., Paterson, M.J., Norman, B.C. et al. Chronic and pulse exposure effects of silver nanoparticles on natural lake phytoplankton and zooplankton. Ecotoxicology 26, 502–515 (2017). https://doi.org/10.1007/s10646-017-1781-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-017-1781-8