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Cellular and physiological measures of pollution effect
Marine Pollution Bulletin, Vol. 16, No. 4, pp. 127-129, 1985 Printed in Great Britain
0025-326X/85 $3.00+0.00 Pergamon Press Ltd.
Cellular and Physiological Measures of Pollution Effect B. L. BAYNE NERC, Institute for Marine Environmental Research, Prospect Place, The Hoe, Plymouth, Devon PL1 3DH, UK
The importance of techniques capable of measuring the biological effects of pollution is stated very well in the 'Comprehensive Plan' of the IOC Global Investigation of Pollution in the Marine Environment (GIPME). This plan, first published by IOC in 1976, proposes a systematic four-stage approach to the determination of the extent of marine pollution; the third stage, called Pollution Assessment, involves the conversion of chemical base-line and mass-balance information into knowledge of biological impact and it is not until the assessment of biological effects is satisfactory that the fourth and final stage of the Plan, consideration of the need for Regulatory Action, can be made effective. Indeed, the very term 'pollution' is now recognized as expressing biological features of the response of environmental systems to contamination. This need for convincing measures of biological response to physical and chemical disturbance has been recognized for some years and has, needless to say, prompted a great deal of research. Biological systems function at many levels in an hierarchy of organized states 'from the cell to the community' and the quest for measures of response to disturbance has proceeded at all such levels. In this Special Issue of the Marine Pollution Bulletin we have chosen to concentrate attention on cellular and physiological processes, for a number of reasons. Research into the responses of such processes to chemical contamination has been particularly active, resulting in a large body of fundamental information that may be used to provide an integrated appreciation of the biochemical and physiological 'condition' of an organism at one point in time. Responses at these levels in the biological hierarchy occur over short time-scales, from minutes to days, and they may be surprisingly sensitive. As a result of these, and other, considerations, there is a growing corpus of experience in evaluating measures of biochemical and physiological response in the natural environment, as potential monitors of pollution impact (Martin, and Lack & Johnson, this issue). Finally, and by no means least, studies of cellular processes come closest to tackling the features of animals and plants which are most intimately responsive to the contaminants in the environment. However, this emphasis is certainly not meant to imply
that these measures should take precedence over measures of population- or community-level response. The ultimate concern must be for the long-term effects of contamination on the form and function of marine ecosystems. Identifying this concern immediately recognizes a major ignorance, however viz. the meaning of the concept of stability as applied to ecosystems, its important components and the role of individual organisms and populations in contributing to ecosystem performance and to the resilience of complex ecological systems when faced with disturbance. These are all problems that currently challenge the ecologists (ConneU & Sousa, 1983). Whatever the outcome of this research, we can be certain that any thorough evaluation of the biological effects of contamination must contain objective statements on the responses of individual organisms, if only because it is at this level that the most immediate and quantifiable link between chemical stimulus and biological response is to be found. In adopting any particular suite of sub-lethal response measures for biological effects assessment (and it is certainly to be recommended that more than one measurement be included in any such programme) certain important criteria should be borne in mind (GESAMP, 1979). These criteria have most recently been reviewed by Bayne et al. (1985); two are selected for brief discussion here in order to suggest both the strengths and the possible weaknesses of currently available techniques. One strength of the cellular and physiological procedures that are discussed in more detail in this issue concerns their inter-relatedness. As an example, it is quite clear that within marine molluscs the lysosomal system of the cells serves as an important site for accumulation and sequestration of contaminants entering the animal (Viarengo, this issue). The capacity of the cell to sequester (and so to 'detoxify') material in this way is, however, limited. Contaminating compounds above a certain concentration will eventually confer damage on the lysosomal membranes, with toxic consequences to the cell due, at least in part, to the destabilization of overall lysosomal function (Moore, this issue). The cumulative result of these cellular events is an increase in protein turnover which, if sufficiently large, may alter the metabolic 127
Marine Pollution Bulletin
nitrogen quotient (or O:N ratio) of the animal and reduce its scope for growth (Widdows, this issue). This coupling of responses at the biochemical, cytological and physiological levels confers some confidence on their use as an integrated toxicological index of pollutant effect. Perhaps the greatest potential weakness in the application of these techniques in biological effects monitoring concerns their variability. Variability in biochemical and physiogical responses may be due to many causes, but most significant in the present context are seasonal changes, both endogenous and exogenous, the multivariate nature of these responses (i.e. their sensitivity to many environmental stimuli, both natural and anthropogenic) and differences between individuals, possibly of a genetic origin. The seasonality that is inherent both in the environment and in many biological processes must be accounted for in sampling and experimental design. Different responses will vary in their sensitivity to particular environmental variables; most physiological effects have a low specificity in this context, providing instead a general measure of animal health. Some biochemical processes, however, offer a greater degree of specificity of response, often indicating the effect of a particular type of contaminant (Livingstone, this issue). Simple doseresponse relationships are not to be anticipated, especially where contaminating inputs are complex and diverse, and interactions between contaminants both in the environment and in the animal certainly occur; nevertheless, there are grounds for expecting that particular aspects of the cell's biochemical machinery will respond predominantly to specific contaminants so suggesting causative agents for monitoring purposes. Variability due to differences betweeen individuals is something we know little about. However, there are suggestions from current research that the extent of this variability may itself provide information on the extent of environmental stress. Future studies might best avoid the temptation of
128
seeking only to know the mean response and take note, as well, of the variance, as a possible index of incipient damage. The papers in this Special Issue demonstrate the richness in current research effort into the toxicological aspects of cellular and physiological processes in marine invertebrates, the growing application of these research results to real environmental problems, and the developing dialogue between the chemists and the biologists which is so essential for a true understanding of pollution damage (Nelson & Donkin, this issue). There is a conscious emphasis on mussels and other molluscs, both to provide a unifying theme to the issue and to reflect the global importance of these organisms in environmental monitoring programmes. I can imagine a companion issue with its emphasis on population and community responses to contamination and which might also reflect the growing awareness of how to relate effects on individual animals to potential population damage. There is certainly an area of responsibility here for the biologists viz. to provide the methodology for an integration across all levels of the biological hierarchy and so to progress towards convincing and quantitative assessments of pollution impact in the marine environment. The articles in this issue indicate some of the promise of current toxicological studies on individual organisms in contributing to this objective. Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M., Moore, M. N., Stebbing, A. R. D. & Widdows, J. (1985). The Effects of Stress and Pollution on Marine Animals. Praeger Special Studies, New York. 384 pp. Connell, J. H. & Sousa, W. P. (1983). On the evidence needed to judge ecological stability or persistence. Amer. Natur. 121, 789-824. GESAMP (1979). Working group on monitoring biological variables related to marine pollution. UNESCO, GESAMP Report No. 12. IOC (1976). A comprehensive plan for the global investigation of pollution in the marine environment and baseline study guidelines. UNESCO, IOC Technical Series No. 14.
0025-326X/85 $3.00+0.00 Pergamon Press Ltd.
Cellular and Physiological Measures of Pollution Effect B. L. BAYNE NERC, Institute for Marine Environmental Research, Prospect Place, The Hoe, Plymouth, Devon PL1 3DH, UK
The importance of techniques capable of measuring the biological effects of pollution is stated very well in the 'Comprehensive Plan' of the IOC Global Investigation of Pollution in the Marine Environment (GIPME). This plan, first published by IOC in 1976, proposes a systematic four-stage approach to the determination of the extent of marine pollution; the third stage, called Pollution Assessment, involves the conversion of chemical base-line and mass-balance information into knowledge of biological impact and it is not until the assessment of biological effects is satisfactory that the fourth and final stage of the Plan, consideration of the need for Regulatory Action, can be made effective. Indeed, the very term 'pollution' is now recognized as expressing biological features of the response of environmental systems to contamination. This need for convincing measures of biological response to physical and chemical disturbance has been recognized for some years and has, needless to say, prompted a great deal of research. Biological systems function at many levels in an hierarchy of organized states 'from the cell to the community' and the quest for measures of response to disturbance has proceeded at all such levels. In this Special Issue of the Marine Pollution Bulletin we have chosen to concentrate attention on cellular and physiological processes, for a number of reasons. Research into the responses of such processes to chemical contamination has been particularly active, resulting in a large body of fundamental information that may be used to provide an integrated appreciation of the biochemical and physiological 'condition' of an organism at one point in time. Responses at these levels in the biological hierarchy occur over short time-scales, from minutes to days, and they may be surprisingly sensitive. As a result of these, and other, considerations, there is a growing corpus of experience in evaluating measures of biochemical and physiological response in the natural environment, as potential monitors of pollution impact (Martin, and Lack & Johnson, this issue). Finally, and by no means least, studies of cellular processes come closest to tackling the features of animals and plants which are most intimately responsive to the contaminants in the environment. However, this emphasis is certainly not meant to imply
that these measures should take precedence over measures of population- or community-level response. The ultimate concern must be for the long-term effects of contamination on the form and function of marine ecosystems. Identifying this concern immediately recognizes a major ignorance, however viz. the meaning of the concept of stability as applied to ecosystems, its important components and the role of individual organisms and populations in contributing to ecosystem performance and to the resilience of complex ecological systems when faced with disturbance. These are all problems that currently challenge the ecologists (ConneU & Sousa, 1983). Whatever the outcome of this research, we can be certain that any thorough evaluation of the biological effects of contamination must contain objective statements on the responses of individual organisms, if only because it is at this level that the most immediate and quantifiable link between chemical stimulus and biological response is to be found. In adopting any particular suite of sub-lethal response measures for biological effects assessment (and it is certainly to be recommended that more than one measurement be included in any such programme) certain important criteria should be borne in mind (GESAMP, 1979). These criteria have most recently been reviewed by Bayne et al. (1985); two are selected for brief discussion here in order to suggest both the strengths and the possible weaknesses of currently available techniques. One strength of the cellular and physiological procedures that are discussed in more detail in this issue concerns their inter-relatedness. As an example, it is quite clear that within marine molluscs the lysosomal system of the cells serves as an important site for accumulation and sequestration of contaminants entering the animal (Viarengo, this issue). The capacity of the cell to sequester (and so to 'detoxify') material in this way is, however, limited. Contaminating compounds above a certain concentration will eventually confer damage on the lysosomal membranes, with toxic consequences to the cell due, at least in part, to the destabilization of overall lysosomal function (Moore, this issue). The cumulative result of these cellular events is an increase in protein turnover which, if sufficiently large, may alter the metabolic 127
Marine Pollution Bulletin
nitrogen quotient (or O:N ratio) of the animal and reduce its scope for growth (Widdows, this issue). This coupling of responses at the biochemical, cytological and physiological levels confers some confidence on their use as an integrated toxicological index of pollutant effect. Perhaps the greatest potential weakness in the application of these techniques in biological effects monitoring concerns their variability. Variability in biochemical and physiogical responses may be due to many causes, but most significant in the present context are seasonal changes, both endogenous and exogenous, the multivariate nature of these responses (i.e. their sensitivity to many environmental stimuli, both natural and anthropogenic) and differences between individuals, possibly of a genetic origin. The seasonality that is inherent both in the environment and in many biological processes must be accounted for in sampling and experimental design. Different responses will vary in their sensitivity to particular environmental variables; most physiological effects have a low specificity in this context, providing instead a general measure of animal health. Some biochemical processes, however, offer a greater degree of specificity of response, often indicating the effect of a particular type of contaminant (Livingstone, this issue). Simple doseresponse relationships are not to be anticipated, especially where contaminating inputs are complex and diverse, and interactions between contaminants both in the environment and in the animal certainly occur; nevertheless, there are grounds for expecting that particular aspects of the cell's biochemical machinery will respond predominantly to specific contaminants so suggesting causative agents for monitoring purposes. Variability due to differences betweeen individuals is something we know little about. However, there are suggestions from current research that the extent of this variability may itself provide information on the extent of environmental stress. Future studies might best avoid the temptation of
128
seeking only to know the mean response and take note, as well, of the variance, as a possible index of incipient damage. The papers in this Special Issue demonstrate the richness in current research effort into the toxicological aspects of cellular and physiological processes in marine invertebrates, the growing application of these research results to real environmental problems, and the developing dialogue between the chemists and the biologists which is so essential for a true understanding of pollution damage (Nelson & Donkin, this issue). There is a conscious emphasis on mussels and other molluscs, both to provide a unifying theme to the issue and to reflect the global importance of these organisms in environmental monitoring programmes. I can imagine a companion issue with its emphasis on population and community responses to contamination and which might also reflect the growing awareness of how to relate effects on individual animals to potential population damage. There is certainly an area of responsibility here for the biologists viz. to provide the methodology for an integration across all levels of the biological hierarchy and so to progress towards convincing and quantitative assessments of pollution impact in the marine environment. The articles in this issue indicate some of the promise of current toxicological studies on individual organisms in contributing to this objective. Bayne, B. L., Brown, D. A., Burns, K., Dixon, D. R., Ivanovici, A., Livingstone, D. R., Lowe, D. M., Moore, M. N., Stebbing, A. R. D. & Widdows, J. (1985). The Effects of Stress and Pollution on Marine Animals. Praeger Special Studies, New York. 384 pp. Connell, J. H. & Sousa, W. P. (1983). On the evidence needed to judge ecological stability or persistence. Amer. Natur. 121, 789-824. GESAMP (1979). Working group on monitoring biological variables related to marine pollution. UNESCO, GESAMP Report No. 12. IOC (1976). A comprehensive plan for the global investigation of pollution in the marine environment and baseline study guidelines. UNESCO, IOC Technical Series No. 14.