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Adverse Effects of Fullerenes (Nc60) Spiked to Sediments on Lumbriculus Variegatus (Oligochaeta)

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Adverse Effects of Fullerenes (Nc60) Spiked to Sediments on Lumbriculus Variegatus (Oligochaeta) Environmental Pollution 159 (2011) 3750e3756 Contents lists available at ScienceDirect Environmental Pollution journal homepage: www.elsevier.com/locate/envpol Adverse effects of fullerenes (nC60) spiked to sediments on Lumbriculus variegatus (Oligochaeta) K. Pakarinen a,*, E.J. Petersen b, M.T. Leppänen a, J. Akkanen a, J.V.K. Kukkonen a a Department of Biology, University of Eastern Finland, 80101 Joensuu, Finland b Material Measurement Laboratory, National Institute of Standards and Technology, Gaithersburg, MD, USA article info abstract Article history: Effects of fullerene-spiked sediment on a benthic organism, Lumbriculus variegatus (Oligochaeta), were Received 22 March 2011 investigated. Survival, growth, reproduction, and feeding rates were measured to assess possible adverse Received in revised form effects of fullerene agglomerates produced by water stirring and then spiked to a natural sediment. 7 July 2011 L. variegatus were exposed to 10 and 50 mg fullerenes/kg sediment dry mass for 28 d. These concentrations Accepted 13 July 2011 did not impact worm survival or reproduction compared to the control. Feeding activities were slightly decreased for both concentrations indicating fullerenes’ disruptive effect on feeding. Depuration efficiency Keywords: decreased in the high concentration only. Electron and light microscopy and extraction of the worm Carbon nanoparticle Carbon nanotubes fecal pellets revealed fullerene agglomerates in the gut tract but not absorption into gut epithelial cells. fi Ecotoxicity Micrographs also indicated that 16% of the epidermal cuticle bers of the worms were not present in the Nanoecotoxicology 50 mg/kg exposures, which may make worms susceptible to other contaminants. Nanotoxicology Ó 2011 Elsevier Ltd. All rights reserved. 1. Introduction 2009; Isaacson et al., 2009; Brant et al., 2005). High concentrations of cations, especially divalent cations, lead to rapid agglomeration of Carbon nanoparticles (NPs), such as fullerenes (C60), are one of the nC60 and settling out of solution (Chen and Elimelech, 2006), which most promising nanosized materials due to their versatile properties will then make them available to benthic organisms. in electronics, optics, medicine, and cosmetics (Bakry et al., 2007; Studies investigating fullerene toxicity to organisms in the Degiorgi, 1998). Some of these uses, such as cosmetic products, water column have shown mixed results with some studies indi- suggest that they will be directly released to waste waters (Benn et al., cating only minor effects (Fraser et al., 2011; Tervonen et al., 2010), 2011). Increasing manufacturing and use of fullerene-containing while other studies have shown long-term toxic effects such as products may also cause fullerenes to enter the environment either reduced offspring production at a concentration of 2.5 mg/L from production of these products or their use by consumers. Similarly (Tao et al., 2009). However, estimation of toxicity of fullerenes from to other chemicals, there is no reason to assume that manufacturing the current literature is complicated, because many early studies and use of NPs can or will be a perfectly closed system without envi- showed toxic results that were later attributable to THF metabolites ronmental release, and thus the potential ecological risks of fullerenes inadvertently formed in the THF dispersion method (Henry et al., need to be understood. 2007, 2011). Although fullerenes are highly insoluble in water (log Kow ¼ 6.67) In contrast to the numerous studies on the toxic effects of (Jafvert and Kulkarni, 2008), they are modified during mixing in water fullerenes to organisms in the water column, no studies have been to form stable agglomerates of many individual molecules, known as conducted yet on the effects of fullerenes to benthic organisms. These nC60 (Scharff et al., 2004); C60 isthemostcommontypeoffullerenes organisms have important ecological roles in aquatic ecosystems, two and thus the word “fullerene” is used hereafter to indicate C60. of which are as a food source for fish and as decomposers of sediment This ability to be dispersed in water increases fullerenes’ mobility material. Additionally, Oligochaetes have been used as bioindicators in aquatic environments and causes them to be available to aquatic of pollution (Lauritsen et al., 1985). For example, Lumbriculus organisms (Deguchi et al., 2001). However, environmental parame- variegatus hasbeenusedintoxicitytestsfordecades(Bailey and Liu, ters, such as water hardness, ionic strength, pH, and dissolved organic 1980). Survival, growth, and reproduction are the most frequently matter, strongly impact the agglomeration process (Ma and Bouchard, used endpoints (Leppänen and Kukkonen, 1998a), and bioavailability tests have also been conducted (Leppänen and Kukkonen, 1998a,b,c). fi * Corresponding author. L. variegatus has been identi ed by the U.S. Environmental Protection E-mail address: kukka.tervonen@uef.fi (K. Pakarinen). Agency, OECD, and ASTM as a recommended freshwater organism 0269-7491/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2011.07.014 K. Pakarinen et al. / Environmental Pollution 159 (2011) 3750e3756 3751 for assessing bioaccumulation in sediments (U.S. EPA, 2000; OECD, carbon for L. variegatus (Ristola et al., 1996a,b, 1999; Leppänen and Kukkonen, 2007). One recent study on another Oligochaeta, terrestrial earth- 1998a,b,c), and it was collected from a clean area with concentrations of polycyclic aromatic hydrocarbons and polychlorinated biphenyls that were near or below the worm Lumbricus rubellus, showed that fullerene-spiked soils caused detection limits (Ristola et al., 1996a,b, 1999; Leppänen and Kukkonen, 1998c). a serious population effect by altering mortality and the proportions The total organic carbon percentage, percentage of particles less than 63 mm, dry of juveniles (van der Ploeg et al., 2011). Our hypothesis was mass percentage, and pH were 3.6 Æ 0.1, 57, 13.6 Æ 0.1, and 6.02, respectively; that fullerene may similarly impact benthic species. L. variegatus was uncertainties represent standard deviations of triplicate measurements. chosen as a test benthic species due to its widespread usage in The well-characterized fullerene suspension was spiked to 1000 g wet Lake Höytiäinen sediment at nominal concentrations of 10 and 50 mg/kg sediment ecotoxicology testing as described above and its selective feeding on dry mass, and mixed for 4 h by vigorous stirring by a rotating metal blade. To our fine particulate matter (<63 mm) (Gaskel et al., 2007), the sediment knowledge, there are no measurements of fullerene concentrations in real envi- fraction expected to contain fullerenes that have settled out of the ronmental sediments. While concentrations used in this study are higher than water column. predicted and modeled average concentrations (Boxall et al., 2007; Gottschalk et al., 2009), it is common practice in nanotoxicology studies to test higher concentrations The objective of this study was to assess the extent to which than the expected average environmental concentration to investigate the possible fullerene-spiked sediment may cause adverse effects on L. variegatus. toxic effects in hot spots with substantially elevated concentrations. A lack of an Toourknowledge,thisisthefirst study on L. variegatus or any effect at higher concentrations suggests a lack of an effect at a lower concentration sediment-dwelling organism exposed to fullerenes. We spiked (Petersen et al., 2009). Lastly, the concentration range tested in this study is less than sediments with 10 and 50 mg fullerenes/kg sediment dry mass that recently tested by van der Ploeg et al. (2011) in soils (maximum concentration of 154 mg/kg) to investigate toxic effects to earthworms. Control sediment without and assessed toxicity using the following endpoints: mass change, fullerenes was similarly prepared. After spiking, sediments were stored for 4 d in the reproduction, number of organisms, feeding rates, and morphological dark at 5 C prior to starting the experiment. changes using transmission electron microscopy (TEM). Absorption of Distribution of fullerenes in the sediment size fractions <63 mm and >63 mmwas fullerenes into microvilli was also investigated using TEM. assessed by wet-sieving the spiked sediment and measuring fullerene contents in these fractions (three replicates for both fractions). For fullerene quantification, sediments were dried overnight in an oven at 105 C, and then were pulverized in 2. Materials and methods a mortar. The sediments were then transferred to 50 mL glass vials, homogenized twice in 5 mL 2% NaCl with a probe tip sonicator (Vibra Cell, Sonics & Materials Inc., 2.1. Chemicals Danbury, USA) for 4 min, and then extracted twice to 5 mL toluene by bath soni- cation (Sonorex Super RK 106, Bandelin, Berlin, Germany) for 15 min. Distinct Fullerenes (C , 98%) were purchased from SigmaeAldrich (USA). Artificial 60 toluene phases were formed by centrifugation at 730 G for 1.5 min, the toluene freshwater used to make the fullerene suspensions was prepared by adding phases from the two extractions were combined in separate vials, and analytical grade salts (Baker, Netherlands: CaCl2$2H2O 58.8 mg/L, MgSO4$2H2O þ þ then concentrated to 1 mL using an N-EVAP 112 nitrogen evaporator (Organomation 24.7 mg/L, NaHCO 13.0 mg/L, and KCl 1.2 mg/L; hardness [Ca 2] þ [Mg 2] ¼ 3 Associates Inc., USA). A fullerene-specific peak at 335 nm (UVeVIS spectropho- 0.5 mmol/L) to Millipore-water (at
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