Toxicity assessment of silver nanoparticles in Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) during early life stages Ashkan Banan, Mohammad Reza Kalbassi, Mahmoud Bahmani & Mohammad Ali Yazdani Sadati Environmental Science and Pollution Research ISSN 0944-1344 Volume 23 Number 10 Environ Sci Pollut Res (2016) 23:10139-10144 DOI 10.1007/s11356-016-6239-7
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Author's personal copy Environ Sci Pollut Res (2016) 23:10139–10144 DOI 10.1007/s11356-016-6239-7
RESEARCH ARTICLE
Toxicity assessment of silver nanoparticles in Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) during early life stages 2
Ashkan Banan 1 & Mohammad Reza Kalbassi 1 & Mahmoud Bahmani & Mohammad Ali Yazdani Sadati
2
Received: 28 September 2015 / Accepted: 1 February 2016 / Published online: 12 February 2016 # Springer-Verlag Berlin Heidelberg 2016
Abstract Silver nanoparticles (AgNPs) are widely used in consumer products mainly due to their antimicrobial action. The rapidly increasing use of nanoparticles (NPs) has driven more attention to their possible ecotoxicological effects. In this study, the acute toxicity of colloidal AgNPs was evaluated during the embryonic stage of Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) at concentrations of 0, 0.25, 0.5, 1, 2, 4, and 8 mg/L. Fertilized eggs (75 eggs per replicate) were exposed to aforementioned concentrations for 96 h in triplicate. 96-h LC50 values in Persian sturgeon and starry sturgeon were calculated as 0.163 and 0.158 mg/L, respectively. Furthermore, in starry sturgeon, the short-term effects of AgNPs on the hatching rate, survival rate, and Ag accumulation during early life stages (before active feeding commences) were also analyzed at concentrations of 0, 0.025, 0.05, and 0.1 mg/L of colloidal AgNPs. The highest silver accumulation occurred in larvae exposed to 0.1 mg/L AgNPs; however, the body burden of silver did not alter survival rate, and there were no significant differences among treatments. Based on the obtained results from the acute toxicity exposures, AgNPs induced a concentrationdependent toxicity in both species during early life stages, Responsible editor: Philippe Garrigues * Mohammad Reza Kalbassi
[email protected]
1
Fisheries Department, School of Marine Sciences, Tarbiat Modares University, P.O. Box 46424-356, Noor, Mazandaran, Iran
2
International Sturgeon Research Institute, P.O. Box 41635-3464, Rasht, Gilan, Iran
while complementary studies are suggested for investigating their short-term effects in detail. Keywords Nanoecotoxicology . Colloidal silver nanoparticles . Sturgeons . Silver accumulation . Acute exposure . Short-term exposure
Introduction Nanoparticles (NPs) possess greater reactivity than nonnanoscale materials due to their unique properties including shape, size, surface characteristics, and inner structure. Furthermore, they also exhibit different biological and environmental effects than their micro- and macro-counterparts, and there is evidence to show that manufactured nanoparticles have the potential to cause serious toxic effects obtained from in vitro and in vivo studies (Walker et al. 2008; Griffitt et al. 2013; Johari et al. 2013; Kalbassi et al. 2013; Johari 2014; Johari et al. 2015). Among nanomaterials, silver nanoparticles (AgNPs) are used in industrial and environmental applications due to their antimicrobial properties (Baker et al. 2005; Li et al. 2011; Samberg et al. 2011). About 63 tons of AgNP are annually expected to enter the water bodies on the Earth (Keller et al. 2013) and their expected concentrations in aqueous environments range from 0.03 to 0.32 μm/L (Batley et al. 2013). However, greater concentrations are predicated with greater production and use of nanoparticle-containing products. AgNPs have been used in (1) water purification facilities (Zodrow et al. 2009), (2) nanocomposite films for food packages (Rhim et al. 2006), (3) textile materials (Budama et al. 2013), (4) biosensors for detecting bacterial contamination in drinking water (Sun et al. 2009), and (5) water filters for fungal disinfection during incubational period for rainbow trout
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eggs (Johari et al. 2016). Because many of these nanosilvercontaining products are potential sources that can lead to release of nanoparticles into aquatic environments (Kaegi et al. 2010; Farkas et al. 2011), it is important to understand their impacts on aquatic organisms. The present study examined the acute and short-term effects of colloidal silver nanoparticles on Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus) during the critical period of their life cycle. To date, the majority of the current studies on the toxicity of AgNPs to fish have focused on juvenile and adult stages, with little attention paid to their acute and chronic effects in early life stages of commercial fish. The Caspian Sea, as one of many important water bodies of the world and the habitat of high economic value and internationally important species like sturgeon, is not excluded from this fact. AgNPs are able to induce various toxicities in aquatic organisms: cytotoxicity and genotoxicity (Wise et al. 2010; Nair et al. 2011), alterations in embryonic development (Ringwood et al. 2010; Cho et al. 2013), tissue accumulation, inducing histopathological disorders and alterations in gene expression levels (Griffitt et al. 2012, 2013; Johari et al. 2015; Johari et al. 2016). Given the importance of these species to the Middle East region, we felt that it was considered prudent to evaluate the role of silver nanoparticles on their survivorship and development.
Materials and methods Preparation of silver nanoparticles The colloidal AgNPs, type L (commercial name: Nanocid), purchased from Nano Nasb Pars Co. (Tehran, Iran), were synthesized using a novel process involving the photo-assisted reduction of Ag+ to metallic NPs, registered under United States Patent Application No. 20090013825 (Nia 2011). Briefly, 4.5 g of LABS (Linear Alkyl Benzene Suffocate) was dissolved in 95 mL of distilled water and then added to a solution containing 0.32 g of silver nitrate. After mixing thoroughly, the addition of 0.2 g of a hydrazine solution (0.03 M) formed a yellowish silver colloidal solution. According to information provided by the manufacturer, the product was a water-based colloidal suspension containing 4000 mg/L spherical silver nanoparticles (average size 16.6 nm). The stock solution was stored in a dark room at 25 °C and used within 25 days. The physicochemical properties of the colloidal product were characterized previously (Salari Joo et al. 2013) using inductively coupled plasmaatomic emission spectroscopy (ICP-AES, Model: 3410 ARL, Switzerland) (the resulting silver concentration was 3980 mg/L), dynamic light scattering (DLS) (the average silver hydrodynamic diameter was 54.8 nm), transmission electron microscopy (TEM) (the AgNPs observed by TEM were
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spherical in shape, with a maximum diameter of 129 nm; 65.14 % of the particles had diameters between 1 and 13 nm (2.28 % of the particles had diameters more than 100 nm) and the CMD (count median diameter) for the particles was 6.47 nm). Broodstock and artificial breeding Spawning sturgeon of both species were captured in the southwestern part of the Caspian Sea, particularly from fish landing sites in Behshahr (Mazandaran Province, Iran) and transported to Shahid Rajaei Breeding, Rearing and Re-stocking Center (Sari, Mazandaran Province) (latitude 36°37′ N, longitude 53°05′ E) from January to March, 2014. The fish were maintained in concrete tanks with a water temperature of 18 ± 1.5 °C, an oxygen content of >5 mg/L and a pH of 7.6 to 7.9. Maturation was induced by injecting 5–10 μg/kg of luteinizing hormone-releasing hormone agonist (LHRH-A2) (Aramli et al. 2014). Semen and egg collection from matured fish were conducted as described by Amini et al. (2012). These fertilized eggs were used for the present study. Exposure conditions A specific exposure system was designed to conduct the acute and short-term toxicity exposures. Nine-L glass tanks were divided into three compartments by two glass walls that were cemented into the larger tank with silicon. A standing mesh tray was placed in each compartment (replicate), and the fertilized eggs, after de-adhesion and water absorption at 2 h post fertilization (hpf), were placed on the trays. Water temperature, dissolved oxygen, and pH were measured daily throughout the experiments (Table 1). The exposures were conducted based on semi-static exposure and re-dosing every 24 h. During the study period before the eggs hatched, 1 mg/L formaldehyde was added to water once per day after water exchange to prevent fungal infections. The experimental design is depicted in Fig. 1. Acute toxicity exposures Based on similar studies, a total of eight treatments, seven AgNP concentrations (nominal values of 0.125, 0.25, 0.5, 1, 2, 4, and 8 mg/L) in addition to a no-dose freshwater control, were included for both species (Cho et al. 2013; Johari et al. 2013). Seventy-five fertilized eggs per compartment/replicate Table 1 Selected physicochemical characteristics of water used in acute and short-term exposures (mean ± standard deviation) Parameter
Temperature (°C)
Dissolved oxygen (mg/L)
pH
Mean
20 ± 1
7.9 ± 0.4
8 ± 0.3
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Fig. 1 Toxicity exposure experimental design. a Acute exposures in Persian sturgeon and starry sturgeon and b short-term exposure in starry sturgeon
were exposed to the aforementioned concentrations at the same time until 96 hpf and in triplicate. Mortality percentage (any disruptions in embryonic development process including disruptions in cell segmentation, organogenesis, and hatch were recorded as mortality) at 24, 48, 72, and 96 hpf was measured as described by Dettlaff et al. (1992).
sampling for silver accumulation measurement took place before the onset of the first larval active feeding. Hatching (80 hpf) and survival rates (8 dpf) were also measured.
Short-term toxicity exposure in starry sturgeon
Larvae that remained alive and healthy after the exposure were killed then evaluated for Ag content. Whole larvae were first dried and ground into powder by a freeze dryer (Operon, FDU-7012, South Korea). Then, amounts of 0.2-g sample were digested with 6 ml 65 % HNO3 and 4 ml 30 % H2O2 at 150 °C using a microwave digestion system (Milestone MLS-1200, Leutenkirch, Germany). Following a cooling to room temperature, the digested samples were diluted with distilled water. The analysis was performed by inductively coupled plasma optical spectrometry (ICP-OES) (Jarić et al. 2011).
Based on the obtained results from the acute toxicity exposures, a total of four treatments in triplicate were included for the short-term exposure, three AgNP concentrations (nominal values of 0.025, 0.05, and 0.1 mg/L) in addition to a no-dose freshwater control (50 fertilized starry sturgeon eggs at 2 hpf per replicate). The exposure duration was 8 days so that 0.351
0.35
0.337
0.3 100
0.25 0.2
0.163
0.158
0.15 0.1
LC10
95
LC50
90
LC90 0.076
0.074
0.05
%
AgNP Concentration mg/L
0.4
AgNP tissue burden quantification
85 80 75
0
Persian Sturgeon
Starry Sturgeon
Fig. 2 Comparison of 96-h lethal concentration values of colloidal AgNP in embryos of Persian sturgeon (Acipenser persicus) and starry sturgeon (Acipenser stellatus)
70
0
0.025 0.05 AgNP concentration (mg/L)
0.1
Fig. 3 Hatching rate of starry sturgeon embryos after exposure to different concentrations of AgNPs
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significant. Analysis of variance (one-way ANOVA) tests were applied to the short-term treatments. Data were plotted using Excel (version 2013, Microsoft Corporation, WA, USA).
95
%
90 85 80 75 70
0
0.025 0.05 AgNP Concentration (mg/L)
0.1
Fig. 4 Survival rate of starry sturgeon larvae after 8 days of exposure to different concentrations of AgNPs
Concentration of Ag (µg/g)
Acute toxicity LC50 values after 96 h of exposure in Persian sturgeon and starry sturgeon were calculated as 0.163 and 0.158 mg/L, respectively (Fig. 2). LC10 and LC90 values were determined as 0.076 and 0.351 in Persian sturgeon and 0.074 and 0.337 in starry sturgeon. The obtained results indicated that during the last 24 h and with the onset of hatch, lower concentrations of AgNP also created lethal effects.
0.25 0.2 0.15 0.1 0.05 0
Results
Short-term toxicity in starry sturgeon 0.025
0.05
AgNP Concentration (mg/L)
0.1
Fig. 5 Silver accumulation in starry sturgeon larvae after 8 days of exposure to different concentrations of AgNPs
Statistical analysis Based on the obtained results from the acute toxicity exposures, the average 96-h median lethal concentrations of AgNPs were calculated for the studied species during their embryonic stage by EPA Probit analysis (Probit analysis program, version 1.5.; WEST, Cheyenne, WY, USA). Values are presented as means ± SE. Statistical analysis was conducted using SPSS (version 16, SPSS Chicago, IL, USA) and differences of P < 0.05 were considered to be statistically Table 2 LC50 values of AgNP in different life stages of a few freshwater teleosts
The short-term exposure results showed that the average hatching rate of control, 0.025, 0.05, and 0.1 mg/L treatments were 91.33 ± 3.2, 88.67 ± 1.7, 87.33 ± 1.76, and 84.67 ± 3.53, respectively, and their average survival rates were 86 ± 1.15, 85.33 ± 4.06, 83.33 ± 1.76, and 77.33 ± 2.91. Statistical analysis of the obtained results from the short-term exposure indicated that there are no significant differences among the studied treatments concerning the hatching and survival rates (P > 0.05). However, by increasing the AgNP concentration, hatching and survival rates decreased (Figs. 3 and 4). The ICP-OES data indicate that Ag accumulation in 0.1 mg/L treatment (0.19 ± 0.02 μg/g) is higher than other treatments (0.15 ± 0.02 μg/g in 0.025 mg/L AgNP and 0.14 ± 0.01 μg/g in 0.05 mg/L AgNP) (P > 0.05) (Fig. 5).
Species (stage)
Exposure duration (h)
LC50
Reference
Acipenser persicus (embryo) Acipenser stellatus (embryo) Oncorhynchus mykiss (embryo) Oncorhynchus mykiss (larva) Oncorhynchus mykiss (juvenile) Hypophthalmichthys molitrix (adult) Carassius auratus (adult) Oryzias latipes (embryo) Oryzias latipes (embryo) Oryzias latipes (adult) Oryzias latipes (adult)
96 96 96 96 96 96 96 96 96 48 96
0.163 0.158 0.25 0.71 2.16 66.4 83.9 0.84 1.39 1.03 0.0346
Present research Present research Johari et al. (2013) Johari et al. (2013) Johari et al. (2013) Jahanbakhshi et al. (2012) Jahanbakhshi et al. (2012) Cho et al. (2013) Kashiwada et al. (2012) Wu et al. (2010) Chae et al. (2009)
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Discussion In this study, the acute and short-term effects of colloidal silver nanoparticles on Persian sturgeon (A. persicus) and starry sturgeon (A. stellatus) were studied during the critical period of their life cycle. Based on European guidelines (EC 2008), Directive 67/548/EEC (EC 1999), colloidal nanoparticulate silver exposure to embryonic Persian sturgeon and starry sturgeon can be considered as highly toxic. This result is consistent with a number of studies focusing on different species (Table 2) and the toxicity of the particles is consistent across them, with the sensitivity of sturgeon embryos to AgNPs being slightly more sensitive than other species. Results from the short-term exposure after 8 days and hatching and survival rates suggested a concentrationdependent decrease (Figs. 3 and 4) which is in accordance with the obtained results by Cho et al. (2013), however they were nonsignificant in the present study. It was shown that particles with 34.9 to 42,000 nm in diameter can enter the chorion layer of medaka eggs and accumulate there in the form of oil droplets and during embryonic development, particularly, particles of 39.4 nm moved into the yolk and gallbladder (Kashiwada et al. 2012). In an experiment using a fluorescent probe, Lee et al. (2007) reported that AgNPs (5–46 nm) enter zebrafish chorion pores via diffusion and can block chorion pore canals which may create severe damage during embryonic development. Present study findings are in accordance with this hypothesis so that by increasing AgNP concentrations, hatching and survival rates decreased. Asharani et al. (2011) compared the toxicity of silver, gold, and platinum nanoparticles in zebrafish embryo and investigated metal accumulation in the hatched larvae where a concentration-dependent increase was observed for each metal nanoparticle. Quantification of silver accumulation in the larvae collected at the end of short-term exposure did not support concentration-dependent trend obtained by Asharani et al. (2011). The measured silver accumulation in 0.05 mg/L AgNP treatment showed a slight decrease compared to 0.025 mg/L AgNP treatment. Overall, silver nanoparticles may create harmful effects like organ failure in the exposed larvae because of their long-term deposition inside the larva body (Asharani et al. 2011). In conclusion, a more detailed understanding of the effect and fate of NPs to aquatic ecosystems is crucial for ensuring biosafety in commercial development of nanotechnology. This study, to the best of our knowledge, is the first report of an exposure to AgNP in sturgeon. Here, an efficient method for determining the toxicity of AgNPs in sturgeon was proposed. Our results show that short-term exposure to nonfatal concentrations of AgNP can result in significant larva body accumulation and more attention should be paid to nanomaterial waste disposal and also in vivo applications of
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nanoparticles due to possible indirect human exposure through fish consumption. Also, complementary studies for understanding the mechanism and extent of AgNP effects on sturgeon egg and larva are suggested, investigating molecular impacts to histological alterations. Acknowledgments Financial support for the present study was provided by grants from the Tarbiat Modares University and the Iran Nanotechnology Initiative Council. The authors would like to acknowledge Prof. Alan Kolok, Jonathan Ali, and Krystal Herrmann for their support.
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