Metal Oxides in Surface Sediment Control Nickel Bioavailability to Benthic Macroinvertebrates.

In aquatic ecosystems, the cycling and toxicity of nickel (Ni) are coupled to other elemental cycles that can limit its bioavailability. Current sediment risk assessment approaches consider acid-volatile sulfide (AVS) as the major binding phase for Ni, but have not yet incorporated ligands that are present in oxic sediments. Our study aimed to assess how metal oxides play a role in Ni bioavailability in surficial sediments exposed to effluent from two mine sites. We coupled spatially explicit sediment geochemistry (i.e., separate oxic and suboxic) to the indigenous macroinvertebrate community structure. Effluent-exposed sites contained high concentrations of sediment Ni and AVS, though roughly 80% less AVS was observed in surface sediments. Iron (Fe) oxide mineral concentrations were elevated in surface sediments and bound a substantial proportion of Ni. Redundancy analysis of the invertebrate community showed surface sediment geochemistry significantly explained shifts in community abundances. Relative abundance of the dominant mayfly (Ephemeridae) was reduced in sites with greater bioavailable Ni, but accounting for Fe oxide-bound Ni greatly decreased variation in effect thresholds between the two mine sites. Our results provide field-based evidence that solid-phase ligands in oxic sediment, most notably Fe oxides, may have a critical role in controlling nickel bioavailability.

Development of a bioavailability-based risk assessment approach for nickel in freshwater sediments.

To assess nickel (Ni) toxicity and behavior in freshwater sediments, a large-scale laboratory and field sediment testing program was conducted. The program used an integrative testing strategy to generate scientifically based threshold values for Ni in sediments and to develop integrated equilibrium partitioning-based bioavailability models for assessing risks of Ni to benthic ecosystems. The sediment testing program was a multi-institutional collaboration that involved extensive laboratory testing, field validation of laboratory findings, characterization of Ni behavior in natural and laboratory conditions, and examination of solid phase Ni speciation in sediments. The laboratory testing initiative was conducted in 3 phases to satisfy the following objectives: 1) evaluate various methods for spiking sediments with Ni to optimize the relevance of sediment Ni exposures; 2) generate reliable ecotoxicity data by conducting standardized chronic ecotoxicity tests using 9 benthic species in sediments with low and high Ni binding capacity; and, 3) examine sediment bioavailability relationships by conducting chronic ecotoxicity testing in sediments that showed broad ranges of acid volatile sulfides, organic C, and Fe. A subset of 6 Ni-spiked sediments was deployed in the field to examine benthic colonization and community effects. The sediment testing program yielded a broad, high quality data set that was used to develop a Species Sensitivity Distribution for benthic organisms in various sediment types, a reasonable worst case predicted no-effect concentration for Ni in sediment (PNECsediment ), and predictive models for bioavailability and toxicity of Ni in freshwater sediments. A bioavailability-based approach was developed using the ecotoxicity data and bioavailability models generated through the research program. The tiered approach can be used to fulfill the outstanding obligations under the European Union (EU) Existing Substances Risk Assessment, EU Registration, Evaluation, Authorisation, and Regulation of Chemicals (REACH), and other global regulatory initiatives. Integr Environ Assess Manag 2016;12:735-746. © 2015 SETAC.

Nickel Partitioning and Toxicity in Sediment during Aging: Variation in Toxicity Related to Stability of Metal Partitioning.

Metals in sediment can be complexed by minerals, partition between solid and aqueous phases, and cause toxicity at high concentrations. We studied how the oxidation of surface sediment that occurs during aging alters the partitioning and toxicity of Ni. Two sediments (Burntwood and Raisin) were amended with Ni, equilibrated, incubated in a flow-through flume, and examined for sediment physicochemistry and toxicity to Hyalella azteca (7 day growth). Through time, the sediment surface (5 mm) was oxidized, acid-volatile sulfide concentrations declined in Raisin sediment, and amorphous Fe oxides increased. Porewater Ni concentrations declined through time but total Ni concentrations in sediment were unchanged, suggesting changes in Ni partitioning through time. Both sediments elicited a toxic dose-response by H. azteca early in the aging process; but only Burntwood, for which Ni was primarily partitioned to Fe oxide minerals, exhibited a consistent dose-response during aging. Low total Ni concentrations (20 mg kg-1) in Raisin sediment reduced H. azteca growth at initiation, but all Ni treatments (up to 3000 mg kg-1) exhibited similar growth after 12 days of aging. The dynamic toxicity observed in Raisin sediment was likely due to the instability of NiS in surface sediments early in the aging process. These data suggest that short-term toxicity assays with homogenized Ni-amended sediment (i.e., standard sediment toxicity tests) may be accurate for sediments where Ni speciation is dominated by oxidized ligands; however, under high-AVS and high-Fe conditions, calculated toxicity thresholds may be overly conservative (here by >100-fold) with respect to natural sediment conditions.

Macroinvertebrate responses to nickel in multisystem exposures.

Metals introduced to sediments undergo a variety of complexation and partitioning changes that affect metal bioavailability. Using simultaneously extracted metal (SEM)/acid volatile sulfide (AVS) and organic carbon (f(OC)) models, the authors examined nickel (Ni) toxicity and bioavailability in 2 field studies (using streamside mesocosm and in situ colonization) and 1 laboratory study. The streamside mesocosm experiments indicated that benthic communities (Ephemeroptera, abundance, and taxa richness) responded negatively to increasing SEM(Ni) /AVS and (SEM(Ni) -AVS)/f(OC) models. In the in situ colonization study, taxa richness, abundance, and Ephemeroptera, Plecoptera, and Trichoptera (EPT) taxa decreased with increasing SEM(Ni) and SEM(Ni)/AVS values. Nickel-spiked sediments were tested in the laboratory with indigenous field-collected mayflies (Anthopotamus verticis, Isonychia spp., and Stenonema spp) and a beetle (Psephenus herricki), and with laboratory-cultured Hyalella azteca and Chironomus dilutus. The amphipod H. azteca was the most sensitive organism tested, and the mayflies Anthopotamus verticis and Stenonema spp. were the most sensitive indigenous organisms to Ni-spiked sediments. These studies help discern which factors are important in determining Ni toxicity and bioavailability at the individual, population, and community levels.

Nickel toxicity to benthic organisms: The role of dissolved organic carbon, suspended solids, and route of exposure.

Nickel bioavailability is reduced in the presence of dissolved organic carbon (DOC), suspended solids (TSS), and other complexing ligands; however, no studies have examined the relative importance of Ni exposure through different compartments (water, sediment, food). Hyalella azteca and Lymnaea stagnalis were exposed to Ni-amended water, sediment, and food, either separately or in combination. Both organisms experienced survival and growth effects in several Ni compartment tests. The DOC amendments attenuated L. stagnalis Ni effects (survival, growth, and (62)Ni bioaccumulation), and presence of TSS exposures demonstrated both protective and synergistic effects on H. azteca and L. stagnalis. (62)Ni trophic transfer from food to H. azteca and L. stagnalis was negligible; however, bioaccumulating (62)Ni was attributed to (62)Ni-water ((62)Ni flux from food), (62)Ni-TSS, and (62)Ni-food. Overall, H. azteca and L. stagnalis Ni compartment toxicity increased in the following order: Ni-water >> Ni-sediment >> Ni-all (water, sediment, food) >> Ni-food.

Copper and nickel partitioning with nanoscale goethite under variable aquatic conditions.

Metal contaminated sediments can be toxic to aquatic organisms and are common in human-dominated ecosystems, which results in metals being a leading cause of ecosystem impairment. Bioavailability of metals is influenced by their affinity for dissolved and solid-phase ligands, including iron (Fe) oxyhydroxides, which have been hypothesized to reduce metal toxicity in sediments. The authors examined the adsorption kinetics of copper (Cu) and nickel (Ni) with goethite (α-FeOOH) and characterized the influences of solute metal concentration, pH, ionic strength, and humate concentration on steady-state partitioning of the metals with goethite under conditions representative of natural aquatic environments. Copper and Ni readily adsorbed to goethite, and steady-state partitioning was achieved within 2 h. Although ionic strength had no effect on metal partitioning, adsorption of Cu and Ni to goethite was enhanced by alkaline pH and reduced by competition with humate. Because distribution coefficient (KD ) values for Cu and Ni from the present study are comparable to values measured in natural systems, the authors hypothesize that goethite may contribute significantly to the adsorption of both Ni and Cu to particles in the environment. The authors suggest that incorporating binding by Fe oxides in metal bioavailability models should be a priority for improving risk assessment of metal-contaminated oxic sediments.

Nickel phase partitioning and toxicity in field-deployed sediments.

The pool of bioavailable metal in sediments can be much smaller than total metal concentration due to complexation and precipitation with ligands. Metal bioavailability and toxicity in sediment is often predicted from models of simultaneous extracted metal and acid volatile sulfide (SEM-AVS); however, studies of the applicability of these models for Ni-contaminated sediments have been conducted primarily in laboratory settings. We investigated the utility of the SEM-AVS models under field conditions: Five lotic sediments with a range of sulfide and organic carbon contents were amended with four concentrations of Ni, deployed in streams for eight weeks, and examined for colonizing macroinvertebrates. After four weeks, colonizing macroinvertebrates showed a strong negative response to the Ni-treated sediments and SEM-AVS models of bioavailability differentiated between toxic and nontoxic conditions. By Week 8, relationships deteriorated between colonizing macroinvertebrates and SEM-AVS model predictions. Total Ni in the sediment did not change through time; however, Ni partitioning shifted from being dominated by organic cabon at deployment to associations with Fe and Mn. Combined geochemical and toxicity results suggest that Fe and Mn oxides in surface sediments resulted in Ni being less available to biota. This implies that current SEM-AVS models may overestimate bioavailable Ni in sediments with oxic surface layers and sufficient Fe and Mn.

Field measurement of nickel sediment toxicity: role of acid volatile sulfide.

A field experiment was performed in four freshwater systems to assess the effects of Ni on the benthic macroinvertebrate communities. Sediments were collected from the sites (in Belgium, Germany, and Italy), spiked with Ni, and returned to the respective field sites. The colonization process of the benthic communities was monitored during a nine-month period. Nickel effect on the benthos was also assessed in the context of equilibrium partitioning model based on acid volatile sulfides (AVS) and simultaneously extracted metals (SEM). Benthic communities were not affected at (SEM - AVS) ≤ 0.4 µmol/g, (SEM - AVS)/fraction of organic carbon (f(OC)) < 21 µmol/g organic carbon (OC). Sediments with (SEM - AVS) > 2 µmol/g, (SEM - AVS)/f(OC) > 700 µmol/g OC resulted in clear adverse effects. Uncertainty about the presence and absence of Ni toxicity occurred at (SEM - AVS) and (SEM - AVS)/f(OC) between 0.4 to 2 µmol/g and 21 to 700 µmol/g OC, respectively. The results of our study also indicate that when applying the SEM:AVS concept for predicting metal toxicity in the field study, stressors other than sediment characteristics (e.g., sorption capacity), such as environmental disturbances, should be considered, and the results should be carefully interpreted.

Effects of suspended solids and dissolved organic carbon on nickel toxicity.

Nickel (Ni) is a common and potentially toxic heavy metal in many fluvial ecosystems. We examined the potentially competitive and complementary roles of suspended sediment and a dissolved organic ligand, humate, in affecting the partitioning and toxicity of Ni to a model organism, Daphnia magna, in both batch and stream-recirculating flume (SRF) tests. Sediments included a fine-grained deposit, montmorillonite, and kaolinite. Survival of D. magna was unaffected by the range of suspended solids used in the present study (8-249 mg/L). However, exposure to suspended solids that were amended with Ni had a deleterious effect on test organism survival, which is attributed to partitioning of Ni into the aqueous phase. At comparable levels of dissolved Ni, survival of D. magna was reduced in tests with Ni-amended suspended solids compared to Ni-only aqueous exposures, suggesting potentiation between these two aquatic contaminants. Addition of humate attenuated toxicity to D. magna in both Ni-only and Ni-amended suspended sediment exposures. These results indicate that organic ligands and suspended solids have important functions in affecting the bioavailability and toxicity of Ni to aquatic organisms and should be incorporated into predictive models to protect ecosystem quality.

Laboratory and field validation of multiple molecular biomarkers of contaminant exposure in rainbow trout (Oncorhynchus mykiss).

Novel primers for three different genes (CYP1A1, vitellogenin, and metallothionein) for use in reverse transcription-polymerase chain reaction (RT-PCR) were developed and tested in laboratory flow-through experiments using model compounds benzo[a]pyrene, estradiol, and cadmium. Field validations of the molecular biomarkers were performed using 8-d or 48-h in situ, cagedexposure of juvenile rainbow trout (Oncorhynchus mykiss). Expression levels of genetranscription(messengerRNA [mRNA]) were monitored in gill and liver tissue after exposure at sites downstream of a known source of creosote contamination in the Little Scioto River (Marion, OH, USA) and metals and hydrocarbon contamination in Dick's Creek (Middletown, OH, USA). Significant increases of liver cytochrome P4501A1 gene (CYP1A1) and vitellogenin were measured in both streams at sites downstream of contaminant sources. Significant increases of gill CYP1A1 were also observed. Significant increases of gill and livermetallothionein occurred in Dick's Creek. A sample of gill tissue taken from each fish prior to placement in the Little Scioto River provided a pre-exposure control measurement for each individual. Expression of CYP1A1 and vitellogenin in trout at both streams indicated that exposure to bioavailable hydrocarbons and endocrine-disrupting compounds had taken place. Previous to this study, estrogenic compounds had not been detected in the Little Scioto River. Metallothionein expression confirmed the presence of metals in Dick's Creek. These results suggest a mixed contaminant environment that poses physiological hazard to existing teleost populations. Multiple molecular biomarkers provided a sensitive, physiologically based method of determining contaminant presence and bioavailability to aquatic organisms.