The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach

https://doi.org/10.1016/S0048-9697(99)00499-4Get rights and content

Abstract

Within the frame of the 2nd Iberian Congress of Environmental Contamination and Toxicology (University of the Basque Country, Leioa, June 1998) a workshop was held about the use of biomarkers in marine pollution monitoring. Among others, the following biomarkers received special attention: metallothionein induction, acetylcholinesterase inhibition, cytochrome P450 system induction, imposex, lysosomal enlargement and lysosomal membrane destabilisation, and peroxisome proliferation. These biomarkers can be used to evaluate exposure to and effect of different contaminants (metals, organic xenobiotics and organometallic compounds) and they can be measured using different methodological approaches (biochemistry, cytochemistry, immunochemical methods based on the use of biotechnology). Before the application of a set of biomarkers in pollution monitoring programmes, well-defined protocols of Quality Assurance have to be established to allow adequate comparison of results. It is also necessary to include analysis of standard reference materials and to obtain detailed knowledge of basal values and seasonal variations of the biomarkers in various species, as well as to integrate the information obtained with the different biomarkers. Marine bivalve molluscs such as mussels are appropriate sentinel species for most of the biomarkers proposed except for the induction of the cytochrome P450 system, which should be measured in fish, and the degree of imposex, which is a biomarker of exposure to TBT specifically measured in certain gastropod molluscs. As a result of the workshop, a battery of biomarkers of contaminant exposure and effects are proposed that could be incorporated into programmes monitoring the quality of the coastal environment in the Iberian Peninsula. These measures would be undertaken in conjunction with chemical measures of contaminant burdens in selected sentinel species.

Introduction

In recent years, levels of contaminants in the marine environment have increased as a consequence of anthropogenic activities. The diminishing of water and sediment quality can involve a decrease in natural resources. For this reason there is an increasing need to develop methods for the identification, estimation, comparative assessment and management of the risks posed by chemical pollutant discharges to the environment and natural resources. As recognised in the last years by international organisations and environmental agencies, risk assessment can not be solely based on chemical analysis of environmental samples because this approach does not provide any indication of deleterious effects of contaminants on the biota. Therefore, the measurement of the biological effects of pollutants has become of major importance for the assessment of the quality of the environment (Bayne, 1989, Gray, 1992).

Recently, the use of biological markers or biomarkers measured at the molecular or cellular level have been proposed as sensitive ‘early warning’ tools for biological effect measurement in environmental quality assessment (McCarthy and Shugart, 1990). The selected biomarkers should indicate that the organism has been exposed to pollutants (exposure biomarkers) and/or the magnitude of the organism’s response to the pollutant (effect biomarkers or biomarkers of stress). One of the most important features of molecular/cellular biomarkers is that they have the potential to anticipate changes at higher levels of biological organisation, i.e. population, community or ecosystem. Thus these ‘early warning’ biomarkers can be used in a predictive way, allowing the initiation of bioremediation strategies before irreversible environmental damage of ecological consequences occurs. Biomarkers are then defined as short-term indicators of long-term biological effects.

Recently the biomarker approach has been incorporated into several pollution monitoring programmes in Europe and the USA (e.g. the North Sea Task Force Monitoring Master Plan and the NOAA’s National Status and Trends Program). Likewise, different methods for biological effect measurement have been evaluated in a series of practical workshops organised by the International Council for the Exploration of the Sea (ICES) and the Intergovernmental Oceanographic Commission (IOC), such as those in the North Sea (Stebbing and Dethlefsen, 1992). The United Nations Environment Programme has funded a biomonitoring programme in the Mediterranean Sea including a variety of biomarkers (UNEP, 1997, and see below). Recently, biomarkers have also been included in the Joint Monitoring Programme of the OSPAR convention where Portugal and Spain are members.

In the Iberian Peninsula there has been no attempt to perform a periodical monitoring programme of pollution effects on the coastal environments. In Spain, only chemical monitoring has been performed on a regular basis using bivalve molluscs and other indicator species since 1986 (Porte and Albaigés, 1993, Solé et al., 1994). The Spanish Institute of Oceanography (IEO) is currently in charge of chemical monitoring along the Spanish coast. In Portugal only chemical monitoring has been performed, under the responsibility of the Portuguese Ministry for the Environment, in order to fulfil the obligations under the ICES and OSPAR Conventions. Apart from chemical monitoring, individual research groups have been involved in recent years in applying the biomarker approach to measure the effects of pollution in selected coastal areas of the Iberian Peninsula. In the following sections we describe some of the biomarkers used and overview the results obtained in different case studies along the coastal environments of the Iberian Peninsula. This information was presented and discussed thoroughly in the Workshop on Biomarkers held during the 2nd Iberian Congress on Environmental Contamination and Toxicology (University of the Basque Country, Leioa, June 1998). The aims of the workshop were to discuss the usefulness and problems associated with the biomarker approach and to prepare a report with suggestions of biomarkers and sentinel species adequate to detect the effects of pollution in littoral and coastal zones of the Iberian Peninsula. Potential areas for future research on the use of biomarkers in marine pollution monitoring were also identified.

Section snippets

Metallothionein induction

Metals are among the major contaminants reaching the marine environment. Their levels have been increasing over the last decades as a result of technological development. The exposure of marine organisms to certain metals can lead to alterations of several biochemical processes that have the potential to be used as biomarkers of exposure and therefore as ‘early warning’ signals of the presence of these particular contaminants. It is generally accepted that toxicity will manifest itself at the

Application of the biomarker approach in the Med Pol monitoring programme

Several of the biomarkers mentioned in the above section have been applied in a pollution monitoring programme of the Mediterranean Sea (Med Pol, UNEP, 1997). Recently a Med Pol II Programme was carried out with the aim of evaluating the toxic effects of the pollutants on the marine organisms along the Mediterranean coast.

The Med Pol II Mediterranean Biomonitoring Programme was planned following the establishment of some important general criteria to standardise field/laboratory activities in

Conclusions

From the practical cases discussed above it becomes clear that there is a need to plan and develop a multidisciplinary monitoring programme to assess environmental pollution in the Iberian Peninsula, particularly on the Atlantic coast. The Mediterranean coast has received more attention and has been included in the Med Pol monitoring programme, which attempts to assess environmental pollution in the Mediterranean Sea as a whole.

Besides the sampling stations where chemical monitoring is carried

Acknowledgements

This collaborative effort has been possible thanks to the funding of CICYT (Spanish Ministry of Education and Culture) through a Special Action (ref AMB98-1330-E). Work in the laboratory of MP Cajaraville has been funded by projects AMB96-0523 (CICYT), UPV 076.310-EC219/97 (University of the Basque Country) and PL97-3827 (EU FAIR Programme). The work in the laboratory of C. Porte and A. Viarengo was partially supported by the CE-BIOMAR project refs. EV5V-CT94-0550 and ENV4-CT96-0300.

References (121)

  • M. Etxeberria et al.

    Changes in digestive cell lysosomal structure in mussels as biomarkers of environmental stress in the Urdaibai estuary (Biscay Coast, Iberian Peninsula)

    Mar Pollut Bull

    (1995)
  • J.W. Farrington et al.

    ICES/IOC intercomparison exercise on the determination of petroleum hydrocarbons in biological tissues (mussel homogenate)

    Mar Pollut Bull

    (1988)
  • E.D. Goldberg

    The mussel watch — a first step in global marine monitoring

    Mar Pollut Bull

    (1975)
  • J.S. Gray

    Biological and ecological effects of marine pollutants and their detection

    Mar Pollut Bull

    (1992)
  • C. Habig et al.

    Comparative properties of channel catfish (Ictalurus punctatus) and blue crab (Callinectes sapidus) acetylcholinesterases

    Comp Biochem Physiol

    (1988)
  • A. Köhler

    Lysosomal perturbations in fish liver as indicators for toxic effects of environmental pollution

    Comp Biochem Physiol

    (1991)
  • P.K. Krishnakumar et al.

    Cytochemical responses in the digestive tissue of Mytilus edulis complex exposed to microencapsulated PAHs or PCBs

    Comp Biochem Physiol

    (1997)
  • D.M. Lowe et al.

    Effects of oil on digestive cells in mussels: quantitative alterations in cellular and lysosomal structure

    Aquat Toxicol

    (1981)
  • I. Marigómez et al.

    Structural changes in the digestive lysosomal system of sentinel mussels as biomarkers of environmental stress in mussel-watch programmes

    Comp Biochem Physiol

    (1996)
  • M.N. Moore

    Cellular responses to pollutants

    Mar Pollut Bull

    (1985)
  • Y. Morcillo et al.

    Monitoring of organotin compounds and their effects in molluscs from the Catalan Coast (NW Mediterranean)

    Trends Anal Chem

    (1998)
  • Y. Morcillo et al.

    Effects of tributyltin on the Phase I testosterone metabolism and steroid titres of the clam Ruditapes decussata

    Aquat Toxicol

    (1998)
  • B.M. Nilsen et al.

    Monoclonal and polyclonal antibodies against fish vitellogenin for use in pollution monitoring

    Mar Environ Res

    (1998)
  • T.P. O’Connor

    Trends in chemical concentrations in mussels and oysters collected along the US coast from 1986 to 1993

    Mar Environ Res

    (1996)
  • B. Ozretic et al.

    Esterase heterogeneity in mussel Mytilus galloprovincialis: effects of organophosphate and carbamate pesticides in vitro

    Comp Biochem Physiol

    (1992)
  • C. Porte et al.

    Responses of mixed-function oxygenase and antioxidase enzyme system of Mytilus galloprovincialis to organic pollution

    Comp Biochem Physiol

    (1991)
  • Ph. Quevauviller et al.

    Organotins in sediments and mussels from the Sado estuarine system (Portugal)

    Environ Pollut

    (1989)
  • J.K. Reddy et al.

    Oxidative DNA damage caused by persistent peroxisome proliferation: its role in hepatocarcinogenesis

    Mutat Res

    (1989)
  • F. Regoli et al.

    Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki

    Aquat Toxicol

    (1998)
  • R. Barreiro et al.

    Respuesta a la contaminación por TBT en individuos transplantados de Nucella lapillus (L.) desde zonas poco contaminadas a los puertos de Ferrol y A Coruña

    Cuad Inv Biol

    (1998)
  • B.L. Bayne

    Measuring the biological effect of pollution: the mussel watch approach

    Water Sci Technol

    (1989)
  • M.J. Bebianno et al.

    Metallothionein induction in Mytilus edulis exposed to cadmium

    Mar Biol

    (1991)
  • M.J. Bebianno et al.

    Cadmium metabolism in the clam Ruditapes decussata: the role of metallothioneins

    Aquat Toxicol

    (1993)
  • M.J. Bebianno et al.

    Involvement of metallothionein in cadmium accumulation and elimination in the clam Ruditapes decussata

    Bull Environ Contam Toxicol

    (1994)
  • D.W. Beyers et al.

    Acetylcholinesterase inhibition in federally endangered Colorado squawfish exposed to carbaryl and malathion

    Environ Toxicol Chem

    (1994)
  • J. Blasco et al.

    Acid and alkaline phosphatase activities in the clam Ruditapes philippinarum

    Mar Biol

    (1993)
  • G. Bocquené et al.

    Acetylcholinesterase activity in the common prawn (Palaemon serratus) contaminated by carbaryl and phosalone

    Ecotoxicol Environ Saf

    (1991)
  • T. Burgeot et al.

    Bioindicators of pollutant exposure in the northwestern Mediterranean Sea

    Mar Ecol Prog Ser

    (1996)
  • M.S. Cairns et al.

    Brain cholinesterase activity of bobwhite acutely exposed to chlorpyrifos

    Environ Toxicol Chem

    (1991)
  • M.P. Cajaraville et al.

    Automated measurement of lysosomal structure alterations in oocytes of mussels exposed to petroleum hydrocarbons

    Arch Environ Contam Toxicol

    (1991)
  • M.P. Cajaraville et al.

    Peroxisomes in digestive gland cells of the mussel Mytilus galloprovincialis Lmk. Biochemical, ultrastructural and immunocytochemical characterization

    Eur J Cell Biol

    (1992)
  • M.P. Cajaraville et al.

    Cellular biomarkers as useful tools in the biological monitoring of environmental pollution: molluscan digestive lysosomes

  • M.P. Cajaraville et al.

    Detection, control and monitoring of pollution using early warning cellular biomarkers: conventional and innovative approaches based on biotechnology

    Cuad Inv Biol

    (1998)
  • J.L. Casterline et al.

    The distribution and binding of cadmium in oyster, soybean and rat liver and kidney

    Arch Environ Contam Toxicol

    (1975)
  • M.R. Coelho et al.

    Imposex in neogastropod snails from southern Portugal

    Cuad Inv Biol

    (1998)
  • K.E. Day et al.

    Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides

    Aquat Toxicol

    (1990)
  • S.J. de Mora

    Tributyltin: case study of an environmental contaminant. Cambridge Environmental Chemistry Series

    (1996)
  • M.H. Depledge

    The rational basis for the use of biomarkers as ecotoxicological tools

  • C.J. Driver et al.

    Routes of uptake and their relative contribution to the toxicologic response of northern bobwhite (Colinus virginianus) to an organophosphate pesticide

    Environ Toxicol Chem

    (1991)
  • A. El Hamdani et al.

    Imposex in prosobranch molluscs: an indicator of TBT pollution in the Valencian coasts (Spain, Western Mediterranean)

    Cuad Inv Biol

    (1998)
  • Cited by (0)

    View full text