Annemette Palmqvist

The use and misuse of biomarkers in ecotoxicology

Substantial efforts have been devoted to developing and applying biomarkers for use in ecotoxicology. These efforts have resulted partly from a desire for early warning indicators that respond before measurable effects on individuals and populations occur and partly as an aid to identifying the causes of observed population- and community-level effects. Whereas older biomarkers focused on measures of organism physiology or biochemistry, advances in molecular biology are extending the biomarker philosophy to the level of the genes (i.e., ecotoxicogenomics). However, the extent to which biomarkers are able to provide unambiguous and ecologically relevant indicators of exposure to or effects of toxicants remains highly controversial. In the present paper, we briefly discuss the application of biomarkers in ecotoxicology and ecological risk assessment, and we provide examples of how they have been applied. We conclude that although biomarkers can be helpful for gaining insight regarding the mechanisms causing observed effects of chemicals on whole-organism performance and may, in some cases, provide useful indicators of exposure, individual biomarker responses should not be expected to provide useful predictions of relevant ecological effects--and probably not even predictions of whole-organism effects. Suites of biomarkers are only likely to provide increased predictability if they can be used in a comprehensive mechanistic model that integrates them into a measure of fitness. Until this can be achieved, biomarkers may be useful for hypothesis generation in carefully controlled experiments. However, because the aims of environmental monitoring and ecological risk assessment are to detect and/or predict adverse chemical impacts on populations, communities, and ecosystems, we should be focusing our efforts on improving methods to do this directly. This will involve developing and testing models of appropriate complexity that can describe real-world systems at multiple scales.

Adding Value to Ecological Risk Assessment with Population Modeling

ABSTRACT Current measures used to estimate the risks of toxic chemicals are not relevant to the goals of the environmental protection process, and thus ecological risk assessment (ERA) is not used as extensively as it should be as a basis for cost-effective management of environmental resources. Appropriate population models can provide a powerful basis for expressing ecological risks that better inform the environmental management process and thus that are more likely to be used by managers. Here we provide at least five reasons why population modeling should play an important role in bridging the gap between what we measure and what we want to protect. We then describe six actions needed for its implementation into management-relevant ERA.

Explaining differences between bioaccumulation measurements in laboratory and field data through use of a probabilistic modeling approach.

In the regulatory context, bioaccumulation assessment is often hampered by substantial data uncertainty as well as by the poorly understood differences often observed between results from laboratory and field bioaccumulation studies. Bioaccumulation is a complex, multifaceted process, which calls for accurate error analysis. Yet, attempts to quantify and compare propagation of error in bioaccumulation metrics across species and chemicals are rare. Here, we quantitatively assessed the combined influence of physicochemical, physiological, ecological, and environmental parameters known to affect bioaccumulation for 4 species and 2 chemicals, to assess whether uncertainty in these factors can explain the observed differences among laboratory and field studies. The organisms evaluated in simulations including mayfly larvae, deposit-feeding polychaetes, yellow perch, and little owl represented a range of ecological conditions and biotransformation capacity. The chemicals, pyrene and the polychlorinated biphenyl congener PCB-153, represented medium and highly hydrophobic chemicals with different susceptibilities to biotransformation. An existing state of the art probabilistic bioaccumulation model was improved by accounting for bioavailability and absorption efficiency limitations, due to the presence of black carbon in sediment, and was used for probabilistic modeling of variability and propagation of error. Results showed that at lower trophic levels (mayfly and polychaete), variability in bioaccumulation was mainly driven by sediment exposure, sediment composition and chemical partitioning to sediment components, which was in turn dominated by the influence of black carbon. At higher trophic levels (yellow perch and the little owl), food web structure (i.e., diet composition and abundance) and chemical concentration in the diet became more important particularly for the most persistent compound, PCB-153. These results suggest that variation in bioaccumulation assessment is reduced most by improved identification of food sources as well as by accounting for the chemical bioavailability in food components. Improvements in the accuracy of aqueous exposure appear to be less relevant when applied to moderate to highly hydrophobic compounds, because this route contributes only marginally to total uptake. The determination of chemical bioavailability and the increase in understanding and qualifying the role of sediment components (black carbon, labile organic matter, and the like) on chemical absorption efficiencies has been identified as a key next steps.

Integrating Population Modeling into Ecological Risk Assessment

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Environmentally sensitive life‐cycle traits have low elasticity: implications for theory and practice

The relationships between population growth rate and the life-cycle traits contributing to it are nonlinear and variable. This has made it difficult for ecologists to consistently predict changes in population dynamics from observations on changes in life-cycle traits. We show that traits having a high sensitivity to chemical toxicants tend to have a low elasticity, meaning that changes in them have a relatively low impact on population growth rate, compared to other life-cycle traits. This makes evolutionary sense in that there should be selection against variability in population growth rate. In particular, we found that fecundity was generally more sensitive to chemical stress than was juvenile or adult survival or time to first reproduction, whereas fecundity typically had a lower elasticity than the other life-cycle traits. Similar relationships have been recorded in field populations for a wide range of taxa, but the conclusions were necessarily more tentative because stochastic effects and confounding variables could not be excluded. Better knowledge of these relationships can be used to optimize population management and protection strategies and to increase understanding of the drivers of population dynamics.

Biotransformation and genotoxicity of fluoranthene in the deposit-feeding polychaete Capitella sp. I.

Polycyclic aromatic hydrocarbons, such as fluoranthene (Flu), are of environmental concern because of their persistence, toxicity, and mutagenic properties. In this study we examined the genotoxicity of Flu to Capitella sp. I using the comet assay. We assessed patterns of DNA damage as a function of uptake route and as a function of exposure and depuration time and related levels of DNA damage to published information on Flu-metabolite formation. Exposure to approximately 30 microg Flu/g dry-weight sediment or 50 microg Flu/L seawater resulted in significant DNA damage. The degree of DNA damage was time dependent during both exposure and depuration, and although exposure route had no effect on the maximum degree of DNA damage occurring, it did influence the time course of damage. Levels of damage declined despite continued exposure to Flu, providing evidence for the induction of one or more DNA repair mechanisms. Comparison with Flu-metabolite profiles suggests that DNA damage is associated with the production of aqueous metabolites. The transitory nature of the DNA damage and repair process may contribute important insights into the mechanisms of toxicant effects at the molecular level but limits the usefulness of such endpoints as biomarkers of exposure or effect in ecotoxicological studies.

Uptake, depuration, and toxicity of dissolved and sediment‐bound fluoranthene in the polychaete, Capitella sp. I

Deposit-feeders may be important in facilitating the removal of organic contaminants from bulk sediment. The relationship between uptake route (water vs sediment), depuration and toxicity was investigated in the deposit-feeding polychaete Capitella species I. Individual worms were exposed either to dissolved (i.e., < 0.45 micron) fluoranthene (FLU) (water-only treatment [WO]), or both to dissolved and sediment-bound FLU (porewater and sediment [PWS] treatment). The porewater concentration of dissolved FLU in PWS was set approximately equal to the dissolved concentration in WO (0, 50 micrograms FLU l-1). Fluoranthene marginally affected growth in WO worms (6 d exposure) but not in PWS worms (5 d exposure). The final body-burdens in PWS and WO worms were 141.2 and 99.5 micrograms total FLU equivalents (g dry wt worm)-1, respectively. Sediment-bound FLU was calculated to contribute at least 30% and up to as much as 91% of the total amount taken up by PWS worms. Water-only treatment worms retained all of the FLU during the subsequent depuration (4 d), whereas PWS worms decreased both the weight-specific (t1/2 = 0.95 d) and the total-body burden (t1/2 = 7.8 d), suggesting both active excretion and dilution of FLU body burden as a result of growth. Thus, our results indicate that the sediment-associated pool is an important route of uptake in Capitella sp. I, and that such deposit feeders may be important for remobilization of sediment-associated contaminants, such as fluoranthene.

Biotransformation of dissolved and sediment-bound fluoranthene in the polychaete, Capitella sp. I.

Polycyclic aromatic hydrocarbons (PAHs) are widely distributed in the marine environment and have physicochemical properties that make them likely to bioaccumulate. The main purpose of this study was to investigate fluoranthene (FLU) uptake, biotransformation and elimination in the deposit-feeding polychaete Capitella sp. I exposed via different routes. Individual worms were exposed to either dissolved FLU or to both dissolved and sediment-bound FLU. The 14C-FLU was used as a tracer to determine the amounts of unmetabolized FLU (parent), water-soluble (aqueous)- and water-insoluble (polar) FLU metabolites and FLU residues (unextractable fraction) in sediment, water, and worm tissue. Capitella was capable of accumulating and biotransforming FLU regardless of route of exposure, thus suggesting that biotransformation activity is not restricted to gut tissues. Although both feeding and nonfeeding worms were able to biotransform FLU extensively, feeding worms eliminated/transformed parent FLU faster than both aqueous and polar FLU metabolites after transfer to clean conditions, whereas nonfeeding worms barely excreted FLU in any form. The high biotransformation capability of Capitella sp. I. along with the dependency of elimination on exposure route, demonstrates the potential importance of these processes in controlling the fate and effects of PAH and possibly other organic toxicants in contaminated marine sediments.

Chronic toxicity of silver nanoparticles to Daphnia magna under different feeding conditions.

Despite substantial information on the acute toxicity of silver nanoparticles (AgNP) to aquatic organisms, little is known about their potential chronic effects and the applicability of current test guidelines for testing nanomaterials. The purpose of this study was to study the influence of food availability on toxicity. This was done through a series of Daphnia magna 21-day reproduction tests (OECD 211) using 30 nm citric acid stabilized AgNP aimed at studying the influence of food abundance on the reproductive toxicity of AgNP in D. magna. The experiments were carried out as static renewal tests with exposure concentrations from 10 to 50 μg Ag/L, and test animals were fed green algae Pseudokirchneriella subcapitata in low and high food treatments. The endpoints recorded were survival, growth of parent animals and number of live neonates produced. Detrimental effects of AgNP on survival, growth and reproduction were observed in concentrations higher than 10 μg Ag/L, whereas the animals exposed to 10 μg Ag/L had larger body length and produced more offspring than controls at both food treatments. High food treatment resulted in higher animal survival, growth and reproduction compared to result found for low food treatment.

Stakeholders' Perspective on Ecological Modeling in Environmental Risk Assessment of Pesticides : Challenges and Opportunities

The article closely examines the role of mechanistic effect models (e.g., population models) in the European environmental risk assessment (ERA) of pesticides. We studied perspectives of three stakeholder groups on population modeling in ERA of pesticides. Forty-three in-depth, semi-structured interviews were conducted with stakeholders from regulatory authorities, industry, and academia all over Europe. The key informant approach was employed in recruiting our participants. They were first identified as key stakeholders in the field and then sampled by means of a purposive sampling, where each stakeholder identified as important by others was interviewed and asked to suggest another potential participant for our study. Our results show that participants, although having different institutional backgrounds often presented similar perspectives and concerns about modeling. Analysis of repeating ideas and keywords revealed that all stakeholders had very high and often contradicting expectations from models. Still, all three groups expected effect models to become integrated in future ERA of pesticides. Main hopes associated with effect models were to reduce the amount of expensive and complex testing and field monitoring, both at the product development stage, and as an aid to develop mitigation measures. Our analysis suggests that, although the needs of stakeholders often overlapped, subtle differences and lack of trust hinder the process of introducing mechanistic effect models into ERA.