Paul R. Paquin

The biotic ligand model: a historical overview

During recent years, the biotic ligand model (BLM) has been proposed as a tool to evaluate quantitatively the manner in which water chemistry affects the speciation and biological availability of metals in aquatic systems. This is an important consideration because it is the bioavailability and bioreactivity of metals that control their potential to cause adverse effects. The BLM approach has gained widespread interest amongst the scientific, regulated and regulatory communities because of its potential for use in developing water quality criteria (WQC) and in performing aquatic risk assessments for metals. Specifically, the BLM does this in a way that considers the important influences of site-specific water quality. This journal issue includes papers that describe recent advances with regard to the development of the BLM approach. Here, the current status of the BLM development effort is described in the context of the longer-term history of advances in the understanding of metal interactions in the environment upon which the BLM is based. Early developments in the aquatic chemistry of metals, the physiology of aquatic organisms and aquatic toxicology are reviewed first, and the degree to which each of these disciplines influenced the development of water quality regulations is discussed. The early scientific advances that took place in each of these fields were not well coordinated, making it difficult for regulatory authorities to take full advantage of the potential utility of what had been learned. However, this has now changed, with the BLM serving as a useful interface amongst these scientific disciplines, and within the regulatory arena as well. The more recent events that have led to the present situation are reviewed, and consideration is given to some of the future needs and developments related to the BLM that are envisioned. The research results that are described in the papers found in this journal issue represent a distinct milestone in the ongoing evolution of the BLM approach and, more generally, of approaches to performing ecological assessments for metals in aquatic systems. These papers also establish a benchmark to which future scientific and regulatory developments can be compared. Finally, they demonstrate the importance and usefulness of the concept of bioavailability and of evaluative tools such as the BLM.

Predicting sediment metal toxicity using a sediment biotic ligand model: methodology and initial application

An extension of the simultaneously extracted metals/acid-volatile sulfide (SEM/AVS) procedure is presented that predicts the acute and chronic sediment metals effects concentrations. A biotic ligand model (BLM) and a pore water-sediment partitioning model are used to predict the sediment concentration that is in equilibrium with the biotic ligand effects concentration. This initial application considers only partitioning to sediment particulate organic carbon. This procedure bypasses the need to compute the details of the pore-water chemistry. Remarkably, the median lethal concentration on a sediment organic carbon (OC)-normalized basis, SEM*(x,OC), is essentially unchanged over a wide range of concentrations of pore-water hardness, salinity, dissolved organic carbon, and any other complexing or competing ligands. Only the pore-water pH is important. Both acute and chronic exposures in fresh- and saltwater sediments are compared to predictions for cadmium (Cd), copper (Cu), nickel (Ni), lead (Pb), and zinc (Zn) based on the Daphnia magna BLM. The SEM*(x,OC) concentrations are similar for all the metals except cadmium. For pH = 8, the approximate values (micromol/gOC) are Cd-SEM*(xOC) approximately equal to 100, Cu-SEM*(x,OC) approximately equal to 900, Ni-SEMoc approximately equal to 1,100, Zn-SEM*(x,OC) approximately equal to 1,400, and Pb-SEM*(x,OC) approximately equal to 2,700. This similarity is the explanation for an empirically observed dose-response relationship between SEM and acute and chronic effects concentrations that had been observed previously. This initial application clearly demonstrates that BLMs can be used to predict toxic sediment concentrations without modeling the pore-water chemistry.

Application of the biotic ligand model to predicting zinc toxicity to rainbow trout, fathead minnow, and Daphnia magna

The Biotic Ligand Model has been previously developed to explain and predict the effects of water chemistry on the toxicity of copper, silver, and cadmium. In this paper, we describe the development and application of a biotic ligand model for zinc (Zn BLM). The data used in the development of the Zn BLM includes acute zinc LC50 data for several aquatic organisms including rainbow trout, fathead minnow, and Daphnia magna. Important chemical effects were observed that influenced the measured zinc toxicity for these organisms including the effects of hardness and pH. A significant amount of the historical toxicity data for zinc includes concentrations that exceeded zinc solubility. These data exhibited very different responses to chemical adjustment than data that were within solubility limits. Toxicity data that were within solubility limits showed evidence of both zinc complexation, and zinc-proton competition and could be well described by a chemical equilibrium approach such as that used by the Zn BLM.

The biotic ligand model: a model of the acute toxicity of metals to aquatic life

Abstract The United States Environmental Protection Agency (USEPA) has established nationally applicable water quality criteria (WQC) for metals that are designed to be protective of aquatic life. However, in some instances these criteria may be over-protective as a result of natural, site-specific differences in water quality characteristics. These differences affect metal speciation and bioavailability, fundamental considerations in assessing toxicity. Laboratory studies completed during recent years have advanced the current understanding of metal chemistry in aquatic systems, including the formation of organic and inorganic metal complexes and sorption to particulate organic matter. Parallel investigations have led to an improved understanding of the physiological basis of why metals are toxic to aquatic organisms. These studies have, in combination, led to an improved understanding of how site-specific water chemistry affects bioavailability, and how metals exert toxicity at the organism site of action, at the biotic ligand in the context of the model to be described. The biotic ligand model provides a quantitative framework for assessing metal toxicity over a range of hardness, pH and dissolved organic carbon (DOC) levels. The chemical equilibrium sub-model incorporates metal-biotic ligand interactions to compute metal accumulation at the site of action (e.g., the gill of a fish) as a function of water quality. The toxicity sub-model uses this computed accumulation level as the basis for successfully predicting observed variations in toxicity associated with changes in water quality. The results highlight the potential utility of this approach to provide an alternative means of developing site-specific permit limits and WQC. The ability of the model framework to quantitatively assess the effects of hardness, pH and DOC on toxicity, in comparison to current WQC for metals that typically vary with hardness alone, is a significant advance in understanding how site-specific conditions affect the toxicity of metals.

Utility of Tissue Residues for Predicting Effects of Metals on Aquatic Organisms

As part of a SETAC Pellston Workshop, we evaluated the potential use of metal tissue residues for predicting effects in aquatic organisms. This evaluation included consideration of different conceptual models and then development of several case studies on how tissue residues might be applied for metals, assessing the strengths and weaknesses of these different approaches. We further developed a new conceptual model in which metal tissue concentrations from metal-accumulating organisms (principally invertebrates) that are relatively insensitive to metal toxicity could be used as predictors of effects in metal-sensitive taxa that typically do not accumulate metals to a significant degree. Overall, we conclude that the use of tissue residue assessment for metals other than organometals has not led to the development of a generalized approach as in the case of organic substances. Species-specific and site-specific approaches have been developed for one or more metals (e.g., Ni). The use of gill tissue residues within the biotic ligand model is another successful application. Aquatic organisms contain a diverse array of homeostatic mechanisms that are both metal- and species-specific. As a result, use of whole-body measurements (and often specific organs) for metals does not lead to a defensible position regarding risk to the organism. Rather, we suggest that in the short term, with sufficient validation, species- and site-specific approaches for metals can be developed. In the longer term it may be possible to use metal-accumulating species to predict toxicity to metal-sensitive species with appropriate field validation.

Critical tissue copper residues for marine bivalve (Mytilus galloprovincialis) and echinoderm (Strongylocentrotus purpuratus) embryonic development: Conceptual, regulatory and environmental implications

Critical tissue copper (Cu) residues associated with adverse effects on embryo-larval development were determined for the Mediterranean mussel (Mytilus galloprovincialis) and purple sea urchin (Strongylocentrotus purpuratus) following laboratory exposure to Cu-spiked seawater collected from San Diego Bay, California, USA. Whole body no-observed-effect-residues (NOER) were similar, with means of 21 and 23 microg g(-1) dw, for M. galloprovincialis and S. purpuratus, respectively. Mean whole body median effect residues (ER50) were 49 and 142 microg g(-1) dw for M. galloprovincialis and S. purpuratus, respectively. The difference in ER50s between species was reduced to a factor of <2 when expressed as soft tissue residues. Coefficients of variation among whole body-ER50s were 3-fold lower than median waterborne effect concentrations (EC50) for both species exposed to samples varying in water quality characteristics. This suggests that tissue concentrations were a better predictor of toxicity than water concentrations. The CBRs described herein do not differentiate between the internal Cu concentrations that are metabolically available and those that are accumulated and then detoxified. They do appear, however, to be well enough related to the level of accumulation at the site of action of toxicity that they serve as useful surrogates for the copper concentration that affects embryonic development of the species tested. Results presented have potentially important implications for a variety of monitoring and assessment strategies. These include regulatory approaches for deriving saltwater ambient water quality criteria for Cu, contributions towards the development of a saltwater biotic ligand model, the conceptual approach of using CBRs, and ecological risk assessment.

Validation study of the acute biotic ligand model for silver

An important final step in development of an acute biotic ligand model for silver is to validate predictive capabilities of the biotic ligand model developed for fish and invertebrates. To accomplish this, eight natural waters, collected from across North America, were characterized with respect to ionic composition, pH, dissolved organic carbon, and sulfide. Tests were conducted with the cladoceran Ceriodaphnia dubia (48-h static) and the fish Pimephales promelas (96-h static renewal) to determine the concentrations causing lethality to 50% of the organisms (LC50s) for silver in each of these waters. Overall, the biotic ligand model adequately predicted silver toxicity to C. dubia; however, in some cases, predicted LC50 values exceeded measured values. The accuracy of the biotic ligand model predictions was less convincing for silver toxicity to P. promelas with pronounced problems in low-ionic strength waters. Another issue was the use of acclimated organisms in toxicity studies because the biotic ligand model has been developed with the use of a mix of studies with acclimated and nonacclimated test organisms of varying ages and sizes. To evaluate whether effects of acclimation to test waters influence biotic ligand model predictions, a subset of the natural waters were also tested with P. promelas that had been acclimated to the natural water for 7 d before testing. These experiments revealed no differences in toxicity between acclimated and nonacclimated P. promelas. To determine the influence of organism size, which has been previously correlated to Na(+) turnover and acute silver toxicity across multiple species, Na(+) and Cl(-) influx rates were measured in P. promelas of different sizes. Our results show that Na(+) and Cl(-) influx rates were inversely related to fish mass and positively correlated with silver sensitivity.

Evaluating the role of ion composition on the toxicity of copper to Ceriodaphnia dubia in very hard waters.

The mitigating effect of increasing hardness on metal toxicity is reflected in water quality criteria in the United States over the range of 25-400 mgl(-1) (as CaCO(3)). However, waters in the arid west of the US frequently exceed 400 mgl(-1) hardness, and the applicability of hardness-toxicity relationships in these waters is unknown. Acute toxicity tests with Ceriodaphnia dubia were conducted at hardness levels ranging from approximately 300 to 1,200 mgl(-1) using reconstituted waters that mimic two natural waters with elevated hardness: (1) alkaline desert southwest streams (Las Vegas Wash, NV), and (2) low alkalinity waters from a CaSO(4)-treated mining effluent in Colorado. The moderately-alkaline EPA synthetic hard water was also included for comparison. Copper toxicity did not consistently vary as a function of hardness, but likely as a function of other water quality characteristics (e.g., alkalinity or other correlated factors). The hardness equations used in regulatory criteria, therefore, may not provide an accurate level of protection against copper toxicity in all types of very hard waters. However, the mechanistic Biotic ligand model generally predicted copper toxicity within +/-2X of observed EC(50) values, and thus may be more useful than hardness for modifying water quality criteria.

The Challenges of Hazard Identification and Classification of Insoluble Metals and Metal Substances for the Aquatic Environment

The OECD is currently harmonizing procedures for aquatic hazard identification of substances. Such a system already exists in Europe where it is recognized that special consideration must be given to sparingly soluble metals and metal compounds (SSMMCs) because standard hazard testing procedures designed for organic chemicals do not accommodate the characteristics of SSMMCs. Current aquatic hazard identification procedures are based on persistence, bioaccumulation, and toxicity (PBT) measurements. Persistence measurements typically used for organic substances (biodegradation) do not apply to metals. Alternative measurements such as complexation and precipitation are more appropriate. Metal bioaccumulation is important in terms of nutritional sufficiency and potential food chain transfer and toxicity. Unlike organic substances, metal bioaccumulation potential cannot be estimated using log octanol-water partition coefficients. Further, bioaccumulation and bioconcentration factors are often inversely related to exposure concentration for most metals and organisms, and hence are not reliable predictors of chronic toxicity or food chain accumulation. Metal toxicity is due predominately to the free metal ion in solution. In order to assess the toxicity of SSMMCs, the rate and extent of transformation to a soluble form must be measured.

Tissue‐based risk assessment of cyclic volatile methyl siloxanes

Cyclic volatile methyl siloxanes (cVMS) are important consumer materials that are used in personal care products and industrial applications. These compounds have gained increased attention in recent years following the implementation of chemical legislation programs worldwide. Industry-wide research programs are being conducted to characterize the persistence, bioaccumulation, and toxicity (PBT) properties of cVMS materials. As part of this larger effort, a tissue-based risk assessment was performed to further inform the regulatory decision-making process. Measured tissue concentrations of cVMS compounds in fish and benthic invertebrates are compared with critical target lipid body burdens (CTLBBs) as estimated with the target lipid model (TLM) to evaluate risk. Acute and chronic toxicity data for cVMS compounds are compared with data for nonpolar organic chemicals to validate application of the TLM in this effort. The analysis was extended to estimate the contribution from metabolites to the overall cVMS-derived tissue residues using a food chain model calibrated to laboratory and field data. Concentrations of cVMS materials in biota from several trophic levels (e.g., invertebrates, fish) are well below the estimated CTLBBs associated with acute and chronic effects. This analysis, when combined with the limited biomagnification potential for cVMS compounds that was observed in the field, suggests that there is little risk of adverse effects from cVMS materials under present-day emission levels.