Article pubs.acs.org/est
Sediment Nickel Bioavailability and Toxicity to Estuarine Crustaceans of Contrasting Bioturbative Behaviors − An Evaluation of the SEMAVS Paradigm G. Thomas Chandler,*,†,∥ Christian E. Schlekat,‡,∥ Emily R. Garman,‡,∥ Lijian He,§,∥ Katherine M. Washburn,†,∥ Emily R. Stewart,†,∥ and John L. Ferry§,∥ †
Department of Environmental Health Sciences, Norman J. Arnold School of Public Health, University of South Carolina, Columbia, South Carolina 29208, United States ‡ Nickel Producers Environmental Research Association (NiPERA), 2525 Meridian Parkway, Suite 240, Durham, North Carolina 27713, United States § Department of Chemistry and Biochemistry, University of South Carolina, Columbia, South Carolina 29208, United States S Supporting Information *
ABSTRACT: Robust sediment quality criteria require chemistry and toxicity data predictive of concentrations where population/community response should occur under known geochemical conditions. Understanding kinetic and geochemical effects on toxicant bioavailability is key, and these are influenced by infaunal sediment bioturbation. This study used fine-scale sediment and porewater measurement of contrasting infaunal effects on carbon-normalized SEM-AVS to evaluate safe or potentially toxic nickel concentrations in a high-binding Spartina saltmarsh sediment (4%TOC; 35−45 μmol-S2−·g−1). Two crustaceans producing sharply contrasting bioturbation -- the copepod Amphiascus tenuiremis and amphipod Leptocheirus plumulosus -- were cultured in oxic to anoxic sediments with SEM[Ni]-AVS, TOC, porewater [Ni], and porewater DOC measured weekly. From 180 to 750 μg-Ni·g−1 sediment, amphipod bioturbation reduced [AVS] and enhanced porewater [Ni]. Significant amphipod uptake, mortality, and growthdepression occurred at the higher sediment [Ni] even when [SEM-AVS]/foc suggested acceptable risk. Less bioturbative copepods produced higher AVS and porewater DOC but exhibited net population growth despite porewater [Ni] 1.3−1.7× their aqueous [Ni] LOEC. Copepod aqueous tests with/without dissolved organic matter showed significant aqueous DOC protection, which suggests porewater DOC attenuates sediment Ni toxicity. The SEM[Ni]-AVS relationship was predictive of acceptable risk for copepods at the important population-growth level.
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INTRODUCTION Sediments in low wave-energy estuaries and tidal creeks are typically fine-grained, carbon rich, and supportive of sulfatereducing anaerobic bacteria that produce/release metal-binding sulfides. Organic decomposition releases negatively charged moieties that react with divalent metals and cause direct metal precipitation which reduces organismal aqueous exposure in high ionic-strength environments. A common observation is that particulate and dissolved organic carbon and sulfide released in the sediment biotic zone of high ionic-strength environments attenuate freely dissolved divalent metals [Me2+]1,2 and reduce toxic hazard to benthic infauna.3−5 Sediment metal carbon and sulfide binding or attenuation is thermodynamically driven,6,7 with bioavailability, binding to biotic ligands, and subsequent toxicity (or nontoxicity) to infauna assumed predictable by equilibrium-state partitioning (EqP) models of simultaneously extractable metals [SEM] with acid volatile sulfides [AVS]8,9 and organic carbon.10 Conventional EqP assumes AVS and organic carbon are the dominant controls on divalent metal bioavailability; that toxicity is absent © 2014 American Chemical Society
when weak-acid labile metal molar concentration [SEM] is less than [AVS]; and that risks of metal toxicity increase with the index [SEM-AVS]/foc above a threshold of ∼130 μmol-Me·gC−1.3,4 The sediment biotic ligand model (BLM)10 expanded on the EqP model to predict median lethal concentrations of nickel and other metals across a range of salinities and other sediment porewater characteristics.11 A biotic ligand is any biological receptor(s) where metal coassociation leads to toxicity (sensu the free-ion activity model12,13). This association is influenced in aqueous and porewater phases by competitive cations (e.g., Ca2+, Mg2+), pH, sulfides, chloride, and dissolved organic substances that make the bioavailable sediment metal pool less than the total sediment metal concentration. Metal toxicity to infauna depends on [Me2+] availability at the site(s) of biological uptake (e.g., gill, mucous membranes) versus Received: Revised: Accepted: Published: 12893
May 28, October October October
2014 6, 2014 14, 2014 14, 2014
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96-well microplates at 6 concentrations (0−150 μg-Ni·L−1) bracketing the nauplius 10-day LC25. [Ni] was measured in triplicate every 72-h by high-resolution ICP-MS at each seawater renewal and removal from microwells. Individuals were observed daily for mortality/development. At adulthood pairs were haphazardly mated/tested in fresh microwells within each treatment for fertility and fecundity. DOC attenuation of lethal and developmental Ni toxicity to copepods was tested in a separate 15-day microplate test31 conducted at the LOEC 120 μg-Ni·L−1 with/without addition of 55 mg-C·L−1 Suwannee River dissolved humic matter (International Humic Substances Society reference material). Baseline seawater [DOC] was set 10× lower at 5 mg-DOC·L−1. Porewater [DOC] in Spartina sediments consistently ranged from 45 to 60 mg-DOC·L−1. Statistical Analysis. All microplate endpoints were compared using nested two-way ANOVA (PROC GLM, SAS Institute, Cary, NC) followed by Dunnett’s or William’s t test a posteriori comparisons to control response (α = 0.05). Where required, faunal count data were transformed to meet requirements for parametric statistical analysis. Cross-microplate responses within treatments were not significantly different for any tests. Only two mating pairs successfully reproduced at 150 μg-Ni·L−1; therefore, that response was assumed “significantly reduced” for the fertility endpoint and excluded from ANOVA. Similarly, one-way ANOVA and a posteriori comparisons were performed for all sediment bioassays (α = 0.05). Copepod Population Growth and Structure. A Lesliematrix four-generation prediction of population growth and stage structure was conducted using a stage-based matrix32,33 of empirical microplate life-table data and life-stage transition probabilities (RAMAS GIS; Applied Biomathematics, Setauket, NY, USA). Female fecundity is based on two hatched clutches. Thus, matrix fecundity is conservative given 8−10 clutches hatch per female reproductive lifetime.34 Predicted population sizes and instantaneous rates of population growth are Table S1, Supporting Information. Sediment Bioassay of Copepods and Amphipods. Sediment weak-acid volatile sulfides (1 N HCl) and simultaneously extractable [Ni] were assayed and reported on a dry mass basis.35 A 10-day rangefinder of 40-day jar milled Nispiked sediments was conducted with L. plumulosus at 175, 635, and 2010 μg-Ni·g-sediment−1. [AVS] was 80, 79, and 10 μmolS2−·g-sediment−1, respectively, by Day 10. Significant amphipod mortality of 67 and 100% occurred at 635 and 2010 μg-Ni·gsediment−1. Copepods showed similar 63 and 100% mortality at these concentrations. Thus, a definitive 28-d lifecycle test was conducted with each species spanning 180 to 750 μg-Ni·gsediment−1, with 4% OC, and 35−45 μmoles-S2−·g-sediment−1. Spartina-marsh sediments (10-kg) from pristine North Inlet, SC, USA (SEM[Ni] = 4.71 ± 0.66 μg-Ni·g−1-sediment) were press sieved at 0.2 mm and homogenized into a 12% solids slurry prior to spiking. Sediments were >95% silt:clay with median diameter 4−5 μm. To ensure nickel association with sediment ligands, test sediments were divided evenly into 12 acid-washed 1-L glass jars, spiked with NiCl2 solution to 180, 260, 370, 525, and 750 μg-Ni·g-sediment−1, nitrogen sealed, and jar-milled in anoxia (25 rpm) for 93 days at 18 ± 0.5C. AVS and SEM[Ni] were measured twice per month per jar to determine when steady state had been reached (i.e., at ∼90 days). An experimental design of six sediment concentrations replicated four times yielded 24 250 mL test beakers (150
[Me2+] scavenging by carbon and other competing nonbiological ligands.11,13 These biotic-ligand:metal (BLM) relationships are measurable, predictable, and useful for sediment risk management when sulfide and carbon(organic) concentrations are known;10,11,14 and they have been applied for prediction of nontoxic “safe” and toxic sediment metal concentrations via the SEM-AVS3,4 and related BLM paradigms.5,9,11 The SEM-AVS relationship has many demonstrated benefits for freshwater sediment criteria establishment; but various uncertainties need resolution to improve its use for risk assessment in well-buffered, high ionic-strength seawater. For example, in Spartina alternif lora estuaries of the USA, sediment sulfide and organic carbon vary seasonally but commonly range from 9 to 120 μmol-S2−·g−1 sediment15−17 and 2−10% carbon, which is sufficiently high to attenuate μg- to mg-Me·g−1 in the anoxic phase. However, the anoxic phase is converted repeatedly in these systems to an oxidized state by infaunal burrowing/pumping and constant sediment turnover at cm to meter scales. On the USA Gulf and East coasts, the most abundant infaunal crustaceans are amphipods and copepods. Meiobenthic copepods (e.g., Amphiascus tenuiremis) are only 1−10 μg each but occur at >10 5 individuals per m 2 seafloor.18−20 Meiobenthos turn over ≤20-g carbon·m−2 per year18 and generate extensive burrow networks with enhanced sediment porosity to the depth of the sediment redox layer.21 Burrowing amphipods (e.g., Leptocheirus plumulosus) in contrast are 100−500× larger, more sessile, but deepen the oxic:anoxic boundary 2−4× by pumping bottom water vigorously (60 mL·h−1·amphipod−1) into U-shaped burrows in the top 2 cm of sediments.22,23 Given how widespread infaunal-driven sediment bioturbation is in estuarine/marine systems, it has been unclear if EqP-based toxicity relationships determined for freshwater organisms are applicable to and protective of marine organisms. We tested this question through a series of estuarine sediment bioassays with concurrent fine-scale measurement of AVS, SEMNi, particulate and dissolved organic carbon, and porewater-Ni for two similarly sensitive but ecologically different estuarine crustaceans − Leptocheirus plumulosus (a strongly bioturbative burrow-dwelling deposit-feeding amphipod common in S. alternif lora estuaries24) and Amphiascus tenuiremis (a free-burrowing, sediment-ingesting meiobenthic copepod also common in S. alternif lora estuaries). For each species, sulfide and organic carbon relationships to porewater [Ni] bioavailability/bioaccumulation were measured, with Ni safety:toxicity assessed relative to SEM-AVS3,4 and BLM11 predictions.
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EXPERIMENTAL SECTION Test Species. Under laboratory conditions (15S; 25 °C), the L. plumulosus lifecycle spans 40 days, with higher salinities and lower temperatures extending the lifecycle period.25−27 Useful for our study, L. plumulosus has similar aqueous sensitivity to metals as A. tenuiremis, and it is easily reared in sediment culture.28 A. tenuiremis is culturable in sediments or aqueous-only media allowing both sediment and seawater-only bioassays.29−31 It passes through naupliar, copepodite, and adult life-stages in 15−17 days at 25S:23 °C.30,31 Copepod Aqueous Nickel and Nickel:DOC Microplate Bioassays. Bioassays followed protocols of ASTM E2317-04. Hatched A. tenuiremis nauplii (30, 220 μg-Ni·L−1 even in the presence of high sediment sulfide and OC (i.e., at [SEM-AVS]/foc > −600 μmol-Ni·g-C−1; Table 1.A). Porewater [Ni] was more variable microcore-to-microcore within and across same-treatment test vessels than was SEMNi and usually more concentrated in shallow sediments (0−1.5 cm) than deep for the strong bioturbator L. plumulosus (Figure 2.A; Day 28). For the copepod sediments, mean porewater [Ni] was less variable and ranged from 47 to 200 μg-Ni·L−1 across treatments through Day 28 (Figure 2.B). At depth, copepod porewater [Ni] was on average ∼20 μg·L−1 lower in each treatment regardless of SEM[Ni]. Amphipod shallow mean porewater [Ni] ranged more broadly from 53 to 255 μg-Ni·L−1 across treatments; but in four of five declined much more sharply with depth by 42.5 ± 7.6% on average. Ni Body Burdens in Amphipods and Copepods Reared in Ni-Sediments. For both taxa, nickel accumulated to tissues from sediments in dose-dependent fashion (Figure 2.C−D). Copepods accumulated 10-fold higher nickel (e.g., 388 μg-Ni·gtissue−1 at 300 μg-Ni·g-sediment−1) than amphipods (e.g., 36 μg-Ni·g−1 at 300 μg-Ni·g-sediments−1) at the same sediment concentration. The small size (i.e., higher surface area; 102−103 times lower mass)37 of copepods relative to amphipods may explain them achieving closer equilibration to sediment concentrations in the 28-d exposure. Nickel also may be more readily excreted by Leptocheirus than by Amphiascus; but elimination kinetics are unknown for either species. Leptocheirus’ burrowing habit (Figure S1.B, Supporting Information) with constant irrigation by overlying seawater−and a correspondingly lower porewater [Ni] exposure within burrows−also likely contributed to a lower tissue [Ni] burden. Amphipod and Copepod Response to Sediment Nickel. At the SEMNi concentrations tested − and tested at 4% OC and [AVS] of 35−45 μmol S2−. g-sediment−1 − little nickel toxicity 12898
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to L. plumulosus, and despite copepod population densities 5− 10× higher, copepod bioturbative effects on sediments were comparatively small. Copepod survival was unaffected at any sediment Ni concentration. In fact a statistically significant increase in juvenile-stage copepodite production (1.9×) was seen at 2.4 μmoles Ni (140 μg-Ni·g-sediment−1; SEM-AVS/foc = −850). For copepods, the SEM-AVS relationship was a better predictor of nontoxicity (“safety”) than direct comparisons of sediment porewater [Ni] to copepod dose response under similar aqueous-only exposures. Sediment porewater [Ni] at 11.4 and 13.2 μmol-Ni·g-sediment−1 (i.e., [SEM[Ni] − AVS]/foc = −500 to −600) exceeded the aqueous LOECmortality by 1.3 to 1.7× (Figure 2.B); yet no significant toxicity was observed, and populations reproduced well even at these high concentrations. This lack of toxicity may have been due to porewater DOC attenuation of bioaccumulation/toxicity at the measured 40−55 mg-C·L−1porewater (sensu Figure 1.E,F). For amphipod tests, and contrary to predictions of EqP models, sediments were toxic at [SEM[Ni] − AVS]/foc values ≥ −577. Porewater Ni at this and higher sediment concentrations was 222 and 256 μg-Ni·L−1 and matched or exceeded the L. plumulosus 10-d LC50 of 216 μg-Ni· L−1. Even though EqP models did not predict the toxicity seen in long-term amphipod tests, by day 28 the [SEM-AVS]/foc values in 0−1.5 cm deep sediments of the two toxic treatments were near zero (−25 to +56), compared to −570 in 1.5−3 cm deep sediments (Table 1.A). Shallow sediments did approach, and one slightly exceeded, the more conservative EqP ’no toxicity’ threshold (i.e., SEM-AVS = 0).4,5 In sum, for these common and representative marine crustaceans, the equilibrium partitioning model based on [SEM-AVS]/f OC4 was quite protective of A. tenuiremis in nickel-equilibrated aged sediments up to the highest 676 μg-Ni· g-sediment−1 level but not protective of the similarly sensitive amphipod L. plumulosus. The EqP model estimates thresholds for nickel toxicity (and other metals) when sediment acid volatile sulfide, SEM, and organic carbon concentrations are known.5,11 It predicts increasing occurrence of toxicity as these indices increase above certain thresholds that are indicative of bioavailable and toxic metal concentrations. The sediment BLM11 predicts that, at 25S salinity, nickel contaminated sediments with [SEM-AVS]/foc values of 2000 to 2050 μmolNi·g−1 organic carbon will be lethal to 50% of benthic organisms. In our initial testing of an acute 10-day exposure of L. plumulosus to 30-day rather than 90-day jar-milled sediments (i.e., SEM[Ni] = 13.2 μmoles, [S2−] = 28.5 μmoles, and organic carbon = 4%), SEM-AVS/foc was −383 and was associated with 67% amphipod mortality. A shorter exposure time would have predicted a weaker response than for a 28-d test; and a negative [SEMNi-AVS]/foc would predict no toxicity -- but neither event was observed. Porewater [Ni] was measured in this acute test and was above the L. plumulosus aqueous [Ni] LC50 at 237 ± 46.4 μg-Ni·L−1 with DOC of 62 ± 0.4 mg-C·L−1porewater. These porewater values were similar to 28-day [Ni] for amphipod shallow sediments in the highest 11 μmol-Ni·g-sediment−1 treatment (Figure 2.A). Recently, Besser et al. showed that chronic Ni toxicity to freshwater invertebrates in eight sediment types was primarily a function of AVS concentration.14 Sediments varied in [AVS], total organic carbon, and cation exchange capacity. Of these parameters, AVS explained the most intraspecies variance in toxic response for the amphipods Hyalella azteca and Gammarus pulex and the mayfly Hexagenia sp.14 Vangheluwe
extensive preliminary testing that we felt was likely to yield measurable negative responses in both similarly sensitive crustaceans. Future testing at higher [Ni] and/or lower organic carbon content would be useful in this regard. Environmental Relevance. A large body of literature describes physical:chemical alterations of marine sediment structure and oxic:anoxic boundaries by macro- and meiobenthos;21,38−43 but far fewer data exist showing bioturbation effects on sediment metal release to porewaters and enhanced bioavailability.44−48 In our study, significant L. plumulosus nickel toxicity (mortality and growth depression) was seen at (SEMAVS)/foc values of −600 to 50 μmol-Ni·g-C−1, and well below, for example, predicted no effect levels of ∼100−150 μmol [Ni]excess·g−1 C from equilibrium partitioning models.3,4,10 This departure from EqP predictions may partially be explained by L. plumulosus incessant burrowing and sediment ingesting ecology (Figure S1.B, Supporting Information) which mobilizes porewater nickel. In the topmost sediment layer (0−1.5 cm), L. plumulosus bioturbation significantly enhanced porewater [Ni] in four of five sediment treatments by 1.6−2.2-fold and also sharply reduced [S2−] by 2.4−9.7-fold compared to deeper 2− 3.0 cm sediments. L. plumulosus created visibly oxidized microhorizons around burrow walls that may have pushed nickel porewater bioavailability to toxic levels in the highest treatments. Consequently, overlying [Ni] was 43 and 91% higher in amphipod test waters than in copepod waters on days 14 and 21 (31.6 ± 8.7 and 50.5 ± 14.5 μg-Ni·L−1 respectively, but still far below aqueous toxic thresholds). With the onset of amphipod mortality, this difference dissipated by Day 28 to a consistent overlying water range of 18−23 μg-Ni·L−1 across all treatments. Similar bioturbation-enhanced nickel availability and toxicity (ostensibly from reduced AVS) has been observed in freshwater systems for the similarly bioturbative burrow-irrigating mayfly Hexagenia sp.,14 which in turn prompted its recommended use as a conservative (precautionary) species for sediment Ni toxicity prediction.44 Porewater DOC was not measured in shallow versus deep sediments in our study; but sampling at the 1.5−3 cm depth on days 14 and 28 still showed amphipod sediments had consistently and significantly lower porewater [DOC] than the much less bioturbated copepod sediments [i.e., Day 0prefauna = 67 (±16.8) mg-DOC·L−1; Days-14, 28amphipod = 42.4 (±4.7), 33.6 (±6.6) mg-DOC; Days-14, 28copepod = 50.8 (±5.2), 44.9 (±6.8) mg-DOC·L−1]. Thus, DOC protections from nickel toxicity likely were reduced for amphipods by bioturbative DOC loss from porewater. Meiofaunal bioturbation is much more subtle and driven by population density rather than animal size; e.g., by extensive tube building or burrowing (submm scales), and changes to sediment granulometry through mucus secretions, cocoon making, or fecal pelletization at high densities. 21,42,49 Amphiascus tenuiremis, like most free-burrowing copepods, is strongly oxygen dependent and does not build and irrigate sessile burrows or tubes.40,50 It constantly burrows up and down to the limit of the oxidized sediment boundary. Copepod burrows were not seen below 1 cm depth in this experiment -most were visible from 0 to 5 mm (Figure S1.A). In contrast to amphipods, copepod burrowing and sediment ingestion in the 0−1 cm sediment horizon exerted little effect on shallow porewater [Ni] compared to deeper sediments; but [S2−]shallow was consistently 1.2 to 3.5 times less than in deeper sediments and most likely lower from increased sediment porosity and oxygen infusion as reproducing populations increased. Relative 12899
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et al. proposed the use of such empirically measured bioavailability/toxicity relationships as an alternative to the one-tailed SEM-AVS relationship, which predicts the absence of toxicity but not its occurrence.44 This approach may be particularly important for assessing Ni risks to diverse benthic communities as toxicity has been observed for Hexagenia sp. under conditions where the EqP model would have predicted no toxicity. Similarly, in our study, the aqueous Ni response equivalence between these related crustaceans, but sharp contrasts for sediment Ni, makes a broader generalization about management of divalent metal toxicity in sediments difficult in the context of present SEM-AVS concepts. By design, the EqP model includes no consideration of animal:sediment relationships, but these may influence bioavailable metal pools in sulfide:carbon-rich sediments.3,4,51−53 Further studies of the importance of porewater DOC quantity (and quality) to metal bioavailability (sensu5) might alleviate some limitations of EqP if measured and incorporated into predictive toxicity models. At highest sediment Ni concentrations, porewater DOC appeared to offer little protection to the amphipod model; but DOC clearly was attenuative of nickel toxicity to copepods. Centimeter-scale differences in porewater and sediment-associated nickel concentrations occurred for both species which suggests faunal ecology should not be overlooked when determining metal hazards and risks for sediment infauna. For freshwater sediments in the European Union, an empirically based regression approach to developing sediment quality guidelines has been developed that includes careful determination of bioavailability relationships for multiple sediment features and for multiple test fauna that have different effects on sediment structure.44 Regression approaches are a robust and logical next step for predicting if toxicity will occur in sediment systems when toxicant concentration(s) and important binding ligands are known. More simplistic geochemically based “safe levels” risk assessment applied without consideration of the strong and unique effects of fauna on sediment structure will likely be misplaced and inappropriate for protection of species that affect bioavailability through ecology. On the other hand, ubiquitous and abundant small infauna like the meiobenthos produce comparatively less dramatic change to sediment structure and geochemistry than large infauna and may be better suited to generalized protection schemes employing concurrent measurements of sediment metal geochemistries and [Me2+] attenuating ligands. Clearly a limitation of the sediment studies presented here is the use of only one sediment type (high binding) with one carbon level, one iron concentration, and one salinity. More diverse manipulation of ligand content (carbon, sulfur, iron:manganese), salinity, and other potentially toxic metals into mixture would provide more broadly useful information for sediment quality guideline development protective of both large and small infauna of marine sediments.
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AUTHOR INFORMATION
Corresponding Author
*Phone: 803-777-5008. Fax: 803-777-4783. E-mail: tchandler@ sc.edu. Author Contributions ∥
The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. All authors contributed equally to the work. Funding
Nickel Producers Environmental Research Association (NiPERA). Notes
The authors declare no competing financial interest.
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REFERENCES
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ASSOCIATED CONTENT
S Supporting Information *
Nickel Leslie-matrix results, bioturbation photos, sediment AVS:SEM values, amphipod growth, and copepod clutch sizes are provided. This material is available free of charge via the Internet at http://pubs.acs.org. 12900
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dx.doi.org/10.1021/es5025977 | Environ. Sci. Technol. 2014, 48, 12893−12901
