Article pubs.acs.org/est
Particle-Size Dependent Accumulation and Trophic Transfer of Cerium Oxide through a Terrestrial Food Chain Joseph Hawthorne,† Roberto De la Torre Roche,† Baoshan Xing,‡ Lee A. Newman,§ Xingmao Ma,∥ Sanghamitra Majumdar,⊥ Jorge Gardea-Torresdey,⊥ and Jason C. White*,† †
Department of Analytical Chemistry, The Connecticut Agricultural Experiment Station, New Haven, Connecticut 06504, United States ‡ Stockbridge School of Agriculture, University of Massachusetts, Amherst, Massachusetts 01003, United States § Department of Environmental and Forest Biology, SUNY - College of Environmental Science and Forestry, Syracuse, New York 13210 United States ∥ Department of Civil and Environmental Engineering, Southern Illinois University Carbondale, Carbondale, Illinois 62901 United States ⊥ Department of Chemistry, The University of Texas at El Paso, El Paso, Texas 79968 United States S Supporting Information *
ABSTRACT: The accumulation and trophic transfer of nanoparticle (NP) or bulk CeO2 through a terrestrial food chain was evaluated. Zucchini (Cucurbita pepo L.) was planted in soil with 0 or 1228 μg/g bulk or NP CeO2. After 28 d, zucchini tissue Ce content was determined by ICP-MS. Leaf tissue from each treatment was used to feed crickets (Acheta domesticus). After 14 d, crickets were analyzed for Ce content or were fed to wolf spiders (family Lycosidae). NP CeO2 significantly suppressed flower mass relative to control and bulk treatments. The Ce content of zucchini was significantly greater when exposure was in the NP form. The flowers, leaves, stems, and roots of zucchini exposed to bulk CeO2 contained 93.3, 707, 331, and 119 000 ng/g, respectively; NP-exposed plants contained 153, 1510, 479, and 567 000 ng/g, respectively. Crickets fed NP CeO2-exposed zucchini leaves contained significantly more Ce (33.6 ng/g) than did control or bulkexposed insects (15.0−15.2 ng/g). Feces from control, bulk, and NP-exposed crickets contained Ce at 248, 393, and 1010 ng/g, respectively. Spiders that consumed crickets from control or bulk treatments contained nonquantifiable Ce; NP-exposed spiders contained Ce at 5.49 ng/g. These findings show that NP CeO2 accumulates in zucchini at greater levels than equivalent bulk materials and that this greater NP intake results in trophic transfer and possible food chain contamination.
■
INTRODUCTION Nanotechnology will likely achieve a $3 trillion market value by 2020,1 with applications in an impressive array of commercially available products and technologies, including drug delivery and disease treatment approaches, medical devices, electronics, textiles, cosmetics, and agrichemicals.2−5 This widespread use is a function of unique material behavior at the nanometer scale resulting not only from general enhanced reactivity and sizedependent changes in physical/chemical properties but also intentional material assembly and design. It is inevitable that this increasing application of nanotechnology will result in potentially significant release of engineered nanomaterial (NM) into the environment. Unfortunately, our understanding of NM fate and effects in terrestrial and aquatic ecosystems has lagged far behind implementation of the technology. Given the lack of regulatory guidance and requirements for NM use, critical knowledge gaps may remain unanswered in the short to medium term and, as such, judicious use of NM is warranted.6,7 © XXXX American Chemical Society
The agricultural applications of nanotechnology are largely intended to increase food production yields and efficiency, as well as to address resulting waste.2,3,8,9 Several groups have shown that carbon-based NM can enhance crop growth.10−14 Similar enhancements were reported with nanoparticle (NP) forms of Si, ZnO, Ag, and CeO2.15−18 Although such efforts merit significant attention, a general lack of knowledge on NM fate and effects in agro-ecosystems, coupled with an underdeveloped regulatory framework, do raise concern over such approaches. Many groups have reported on the phytotoxicity of engineered NM, including both carbons and metal oxides such as CeO2, to crop species.19−23 Although results regarding the impacts of NM on plant species are somewhat conflicted and Received: August 4, 2014 Revised: October 17, 2014 Accepted: October 23, 2014
A
dx.doi.org/10.1021/es503792f | Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Environmental Science & Technology
Article
NP CeO2 solutions were dispersed with a probe sonic dismembrator at 30% amplitude for 2 min. The bulk CeO2 solutions were sonicated for 1 h on a bath sonicator (Fisher Scientific, FS-220) so as to avoid NP formation. Two hundred g of a Cheshire fine sandy loam (69.4% sand, 22.0% silt, 8,6% clay; 4.3% organic matter; pH 5.9 [water]; cation exchange capacity 18.6 cmol/kg) and 12 g of dry vermiculite (approximately 80 mL) were then slowly added to each solution-containing beaker and the contents were mixed manually in an attempt to achieve homogeneity. The final CeO2 concentrations were 0 or 1228 μg/g (Ce at 1000 μg/g). This concentration may be high but it is comparable to that of other published studies21,23 and was selected based on the lack of knowledge concerning the magnitude of Ce trophic transfer. In addition, several high-concentration exposure scenarios do exist, including accidental release and long-term accumulation in soil. A single C. pepo seedling was gently planted in each beaker and the plants were incubated in a growth room under ambient and supplemental fluorescent lighting (60 μE/m2/sec) at approximately 22−28 °C. The plants were top watered as needed with the Hoagland’s Solution described above for a 28d growth period. Plants were grown in successive “plantings” of approximately 30 replicates to provide adequate tissues at the appropriate time for insect feeding studies. Exposure Assay: Arthropods. Fifteen hundred medium size crickets (3 weeks old) were ordered from Fluker Farms (Port Allen, LA) and were sorted by groups of 12−15 individuals into 9.5 × 5 × 3.5 inch polylactide hinged loaf containers (Food Service Warehouse, Greenwood Village, CO). A short (7 cm) cardboard tube was added to each container as is typical for rearing these insects; each container served as an individual replicate. There were 22, 22, and 38 control, bulk, and NP CeO2 replicates, respectively. During an initial 5-day pre-exposure period, crickets were sustained on “orange cube cricket diet” and gelatinous “Cricket Quencher with Calcium” (Fluker’s). At the onset of exposure, one-half of a fresh zucchini leaf from plants grown in soil containing 0 or 1228 μg/g NP or bulk CeO2 was added to the each replicate container each day for a 14-day exposure period. A modest amount of quencher was also added to maintain adequate moisture in the container. During the 14-day exposure, cricket feces were collected from select replicate containers of each treatment. At the end of the exposure, most crickets were euthanized and stored in a freezer (−4 °C) until digestion. A small number of crickets were retained for the arachnid feeding trial. Several dozen adult wolf spiders were ordered from Carolina Biological Supply (Burlington, NC) and sorted into individual 9.5 × 5 × 3.5 inch polylactide hinged loaf containers amended with approximately 2 cm of cedar shavings. Spiders were maintained without food for 48 h to ensure cricket consumption upon feeding. Individual crickets that were fed leaves exposed to 0 or 1228 μg/g bulk or NP CeO2 were added to replicate spider containers at a rate of approximately one cricket per day. During the 7-day exposure period, the number of crickets consumed was recorded for individual spider replicates. As a control to monitor possible decreases in Ce content during this 7-day exposure, crickets were maintained under equivalent conditions for control, bulk, and NP treatments but instead of being fed to the spiders, the insects were subject to ICP-MS analysis as described below. No significant decreases in cricket Ce content were observed during the 7-d spider feeding trial (data not shown). After
likely driven by particle-, species-, and concentration-specific interactions, the literature is growing quickly and a robust data set is being developed. The potential bioaccumulation and trophic transfer of NM within terrestrial and specifically agricultural food chains is almost completely unknown. This lack of information is troublesome given the potential for an uncharacterized route of human exposure. Several studies have reported varying extents of NM trophic transfer in relatively simple aquatic systems24−28 but reports with terrestrial species are highly limited. Judy et al.29,30 described significant biomagnification of NP Au from tomato (Lycopersicon esculentum) and tobacco (Nicotiana tabacum) to tobacco hornworm (Manduca sexta). However, a separate soil-based study with earthworms (Eisenia fetida) and juvenile bullfrogs (Rana catesbeina) yielded 100-fold decreases in NP Au content at each trophic level.31 Although these findings only focus on one NP and are clearly far from definitive, the results do demonstrate potential NM trophic transfer in terrestrial food chains. The goal of the current study was to evaluate the particle-size dependent transfer of a widely used engineered NM, the rare earth element (REE) CeO2, and its bulk oxide equivalent from soil to an agricultural crop species. Nanoceria was chosen as the global production approaches 10 000 tons, with uses in fuels, paints, and catalytic converters. As such, the presence of nanoceria in wastewater treatment is likely, which could result in contamination of applied biosolids onto agricultural fields that results in crop exposure.32,33 In addition, the subsequent trophic transfer of the plant-accumulated CeO2 to herbivorous and subsequently, carnivorous species, was also measured.
■
EXPERIMENTAL SECTION Analytes and Plants. Cerium oxide in bulk (99.9%) and NP (99.99%,
