Review article
Fish bioaccumulation and biomarkers in environmental risk assessment: a review

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Abstract

In this review, a wide array of bioaccumulation markers and biomarkers, used to demonstrate exposure to and effects of environmental contaminants, has been discussed in relation to their feasibility in environmental risk assessment (ERA). Fish bioaccumulation markers may be applied in order to elucidate the aquatic behavior of environmental contaminants, as bioconcentrators to identify certain substances with low water levels and to assess exposure of aquatic organisms. Since it is virtually impossible to predict the fate of xenobiotic substances with simple partitioning models, the complexity of bioaccumulation should be considered, including toxicokinetics, metabolism, biota-sediment accumulation factors (BSAFs), organ-specific bioaccumulation and bound residues. Since it remains hard to accurately predict bioaccumulation in fish, even with highly sophisticated models, analyses of tissue levels are required. The most promising fish bioaccumulation markers are body burdens of persistent organic pollutants, like PCBs and DDTs. Since PCDD and PCDF levels in fish tissues are very low as compared with the sediment levels, their value as bioaccumulation markers remains questionable. Easily biodegradable compounds, such as PAHs and chlorinated phenols, do not tend to accumulate in fish tissues in quantities that reflect the exposure. Semipermeable membrane devices (SPMDs) have been successfully used to mimic bioaccumulation of hydrophobic organic substances in aquatic organisms. In order to assess exposure to or effects of environmental pollutants on aquatic ecosystems, the following suite of fish biomarkers may be examined: biotransformation enzymes (phase I and II), oxidative stress parameters, biotransformation products, stress proteins, metallothioneins (MTs), MXR proteins, hematological parameters, immunological parameters, reproductive and endocrine parameters, genotoxic parameters, neuromuscular parameters, physiological, histological and morphological parameters. All fish biomarkers are evaluated for their potential use in ERA programs, based upon six criteria that have been proposed in the present paper. This evaluation demonstrates that phase I enzymes (e.g. hepatic EROD and CYP1A), biotransformation products (e.g. biliary PAH metabolites), reproductive parameters (e.g. plasma VTG) and genotoxic parameters (e.g. hepatic DNA adducts) are currently the most valuable fish biomarkers for ERA. The use of biomonitoring methods in the control strategies for chemical pollution has several advantages over chemical monitoring. Many of the biological measurements form the only way of integrating effects on a large number of individual and interactive processes in aquatic organisms. Moreover, biological and biochemical effects may link the bioavailability of the compounds of interest with their concentration at target organs and intrinsic toxicity. The limitations of biomonitoring, such as confounding factors that are not related to pollution, should be carefully considered when interpreting biomarker data. Based upon this overview there is little doubt that measurements of bioaccumulation and biomarker responses in fish from contaminated sites offer great promises for providing information that can contribute to environmental monitoring programs designed for various aspects of ERA.

Introduction

The environment is continuously loaded with foreign organic chemicals (xenobiotics) released by urban communities and industries. In the 20th century, many thousands of organic trace pollutants, such as polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polycyclic aromatic hydrocarbons (PAHs), polychlorinated dibenzofurans (PCDFs) and dibenzo-p-dioxins (PCDDs) have been produced and, in part, released into the environment. Since the early sixties mankind has become aware of the potential long-term adverse effects of these chemicals in general and their potential risks for aquatic and terrestrial ecosystems in particular. The ultimate sink for many of these contaminants is the aquatic environment, either due to direct discharges or to hydrologic and atmospheric processes (Stegeman and Hahn, 1994). The presence of a xenobiotic compound in a segment of an aquatic ecosystem does not, by itself, indicate injurious effects. Connections must be established between external levels of exposure, internal levels of tissue contamination and early adverse effects. Many of the hydrophobic organic compounds and their metabolites, which contaminate aquatic ecosystems, have yet to be identified and their impact on aquatic life has yet to be determined. Therefore, the exposure, fate and effects of chemical contaminants or pollutants in the aquatic ecosystem have been extensively studied by environmental toxicologists.

Ecological or environmental risk assessment (ERA) is defined as the procedure by which the likely or actual adverse effects of pollutants and other anthropogenic activities on ecosystems and their components are estimated with a known degree of certainty using scientific methodologies (Depledge and Fossi, 1994). ERA has become increasingly important since environmental scientists as well as the general public have learned that chemicals which are not toxic to humans can have deleterious effects on natural resources which are generally valued, e.g. DDTs jeopardizing predatory birds and fish, death of fish and other aquatic organisms due to acid deposition in poorly buffered lakes which also contributes to the die-back of forests (Bascietto et al., 1990). The risk assessment process can be divided into a scientifically oriented risk analysis and a more politically oriented risk management. Risk analysis is a process, which comprises some or all of the following elements: hazard identification, effect assessment, exposure assessment and risk characterization (Van Leeuwen and Hermens, 1995). Environmental risk management deals with regulatory measures based on risk assessment (Van Leeuwen and Hermens, 1995). Risk management and risk analysis, are closely related but different processes: in risk analysis the risk of a certain situation is determined, whereas risk management examines solutions to the problem. Although ERA is generally performed by predictive methods, the interest in the assessment of pollution that began in the past and may have ongoing consequences in the future is increasing. These so-called retrospective ERAs are primarily concerned with establishing the potential relationship between a pollutant source and an ecological effect caused by exposure of organisms to the pollutant (Suter, 1993).

The ability of various pollutants (and their derivatives) to mutually affect their toxic actions complicates the risk assessment based solely on environmental levels (Calabrese, 1991). Deleterious effects on populations are often difficult to detect in feral organisms since many of these effects tend to manifest only after longer periods of time. When the effect finally becomes clear, the destructive process may have gone beyond the point where it can be reversed by remedial actions or risk reduction. The sequential order of responses to pollutant stress within a biological system is visualized in Fig. 1 (modified from Bayne et al., 1985). Such scenarios have triggered the research to establish early-warning signals, or biomarkers, reflecting the adverse biological responses towards anthropogenic environmental toxins (Bucheli and Fent, 1995). Biomarkers are measurements in body fluids, cells or tissues indicating biochemical or cellular modifications due to the presence and magnitude of toxicants, or of host response (NRC, 1987). Effects at higher hierarchical levels are always preceded by earlier changes in biological processes, allowing the development of early-warning biomarker signals of effects at later response levels (Bayne et al., 1985). In an environmental context, biomarkers offer promise as sensitive indicators demonstrating that toxicants have entered organisms, have been distributed between tissues, and are eliciting a toxic effect at critical targets (McCarthy and Shugart, 1990). In this respect, it is also interesting to study the development and application of sensitive laboratory bioassays, based upon the responses of biomarkers, such as the CYP1A responses in EROD or CALUX assays with hepatoma cell lines (Sawyer and Safe, 1982, Murk et al., 1996). Bioassays offer many advantages for comparing the relative toxicity of specific chemicals or specific effluents. However, toxicity tests also have serious limitations for biological monitoring (BM) because most do not account for the effect of chemical specification in the environment, kinetics and sorption of chemicals to sediment, accumulation through food chains and modes of toxic action which are not readily measured as short-term effects (McCarthy and Shugart, 1990). Depledge and Fossi (1994) suggested the use of biomarkers in toxicity tests as an attempt to link biomarker responses to effects on life-history characteristics (e.g. survival and reproduction), which will provide a further foundation for the use of biomarkers in environmental assessment.

For several reasons, fish species have attracted considerable interest in studies assessing biological and biochemical responses to environmental contaminants (Powers, 1989). Monitoring species should be selected from an exposed community on the basis of their relationship to the assessment endpoint as well as by following some practical considerations (Suter, 1993). For the assessment of the quality of aquatic ecosystems, both criteria are met for numerous species of fish. Fish can be found virtually everywhere in the aquatic environment and they play a major ecological role in the aquatic food-webs because of their function as a carrier of energy from lower to higher trophic levels (Beyer, 1996). The understanding of toxicant uptake, behavior and responses in fish may, therefore, have a high ecological relevance. Most of the general biomarker criteria appear to be directly transferable to certain fish biomarkers (Stegeman et al., 1992). Between different fish species, however, considerable variation in both the basic physiological features and the responsiveness of certain biomarkers towards environmental pollution may become apparent. Despite their limitations, such as a relatively high mobility, fish are generally considered to be the most feasible organisms for pollution monitoring in aquatic systems.

In Section 2, general information on different types of biomarkers will be discussed, together with criteria and properties for valid biomarkers in environmental field research. The process of ERA will be elucidated in Section 3. The monitoring of aquatic pollution, which is the most important aspect of the ERA process with respect to biomarkers, will be discussed in Section 4. The processes governing the bioaccumulation of organic trace pollutants in fish, as well as the use of fish as a bioconcentrator to identify certain substances with low water levels will be reviewed in Section 5. Biota-sediment accumulation data will be presented and discussed with regard to the potential use of fish body burdens in the assessment of exposure to various groups of organic pollutants. In Section 6 an overview will be presented of virtually all fish biomarkers (biological and biochemical parameters) that have been used in order to assess exposure to and effects of environmental contaminants. Emphasis will be placed on the biochemical responses to organic trace pollutants, and the feasibility of these markers as early-warning signals for environmental hazards. An extensive summary with the overall conclusions of this review will be presented in Section 7, and the perspectives will be given in the final Section 8.

The scope of this review will be to give an overview of fish bioaccumulation and biomarker studies and to discuss the advantages and limitations of applying these parameters in the assessment of environmental risks in aquatic ecosystems. At present, ERA processes are mainly based upon the determination and prediction of contaminant levels in the various ecosystem compartments, and upon comparison of these concentrations with legislative threshold values or environmental safety standards. However, there is a growing awareness that focusing on chemical data alone is insufficient to reliably assess the potential risks of the complex mixture of contaminants in the aquatic environment. There is an increasing trend to use the behavior of pollutants (bioavailability, bioaccumulation, and biotransformation) as well as pollution-induced biological and biochemical effects on aquatic organisms to evaluate or predict the impact of chemicals on aquatic ecosystems. Emphasis in this review will, therefore, be placed on the use of bioaccumulation and biomarker responses in fish as monitoring tools for the assessment of the risks and hazards of environmental pollutants for the aquatic ecosystem, as well as on its limitations.

Section snippets

Biomarkers

Several definitions have been given for the term ‘biomarker’, which is generally used in a broad sense to include almost any measurement reflecting an interaction between a biological system and a potential hazard, which may be chemical, physical or biological (WHO, 1993). A biomarker is defined as a change in a biological response (ranging from molecular through cellular and physiological responses to behavioral changes) which can be related to exposure to or toxic effects of environmental

Environmental or ecological risk assessment (ERA)

Risk assessment can be defined as the process of assessing magnitudes and probabilities to the adverse effects of human activities or natural catastrophes (Suter, 1993). The development of risk assessment has been driven by the need to allocate scarce resources to estimate human-related risks (Power and McCarty, 1997). Risk assessment clearly separates the scientific process of estimating the magnitude and probability of effects (risk analysis) from the process of choosing among alternatives

Monitoring aquatic pollution

Monitoring is a repetitive observation for defined purposes of one or more chemical or biological elements according to a prearranged schedule over time and space, using comparable and standardized methods (according to the definition of the United Nations Environmental Program (UNEP)). This last step in the risk management process, which is most relevant with respect to biomarkers, may serve a number of purposes: the control function to verify the effectiveness of risk reduction or to ensure

Fish bioaccumulation markers and ERA

Exposure assessment has to provide information on steady-state concentrations of potentially toxic xenobiotics in a selected environmental compartment. Methods for assessing exposure to a chemical fall into two categories (WHO, 1993):

  • measurement of levels of chemical agents and their metabolites and/or derivatives in cells, tissues, body fluids or excreta, i.e. BAM;

  • measurement of biological responses such as cytogenetic and reversible physiological changes in the exposed individuals, i.e. BEM,

Fish biomarkers and ERA

It is virtually impossible to monitor all contaminants of anthropogenic (predominantly halogenated hydrocarbons) and natural origin (heavy metals and most PAHs) which form a potential threat to the environment. In order to assess the overall quality of the aquatic environment, however, a more promising approach is to examine biochemical responses reflecting the potential of contaminants to impair physiological processes in the exposed organisms (McCarthy and Shugart, 1990). BEM by determining

Summary and conclusions

In the preceding chapters a wide array of bioaccumulation markers and biomarkers, which can be or are being used to demonstrate exposure to and effects of environmental contaminants, have been discussed. Based upon the data presented in this review, there is little doubt that measurement of bioaccumulation and biomarker responses in organisms from contaminated sites offers great promises for providing information that can contribute to environmental monitoring programs designed for

Perspectives

McCarthy (1990) proposed a research plan for focusing and coordinating resources necessary to develop and implement a biomarker-based environmental monitoring program, consisting of five major tasks:

  • Task I: preliminary survey: proof of the principle. The primary objective of this research is to compare the qualitative pattern and quantitative responses of a suite of biomarkers in sentinel species from sites polluted with specific types of contaminants, compared with the responses of organisms

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