Ecotoxicology and ecosystem integrity: The Great Lakes examined Fourth of a four-part series
Ecvroxicology is the study 01 h e fate and effect of toxic agents in ecosystems. In the third part of this series David Hoffman and colleagues reviewed both regulatory and new research developments in assessing chronic and acute effects on wildlife. They highlighted the approaches and problems associated with extrapolation between laboratory and field studies. (See the March 1990 issue, p. 276.) In the second part of this series John Cairns and Donald Mount ad-
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wxiculuyy I several perspectives and callec I L predictive models that address ecc system functioning and resiliencc (See the Februar: 1990 issue p. 154 In th John Basciett0,'Dexter Hinkle colleagues provided an overvi applications of ecotoxi through the various regulat and programs of the EPA. January 1990 issue, p. 10.) U I ~ S S ~ aquallr; U
Hallett J. Harris Paul E. Sager University of Wisconsin-Green Bay Green Bay, WI 5431I - 7001 Henry A. Regier University of Toronto Toronto, ON M5S IAI Canada George R. Francis university of waterloo Waterloo, ON N2L 3GI Canada In developing nations 80% of all illness is attributed to unsafe water supplies, and millions of children under the age of five die annually from water-borne diarrheal disease. By comparison, the
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problem of toxic chemicals in the environment may seem pale at first glance. Environmental contamination with toxic chemicals, however, is not now confined to industrialized nations. Although 80% of agrochemicals are used in developed nations, only 1 % of deaths from acute pesticide poisoning are reported from these countries. It is estimated that approximately 1 million people are poisoned by pesticides each year, and mortality estimates range from 3000 to 20,000 deaths per year (1). Use of pesticides has increased in developing countries because of their rapidly growing populations, demand for food production, and tropical locations conducive to insect pests; 62% of all insecticides are applied in developing countries. The problem of environmental contamination with toxic chemicals, particularly chlorinated hydrocarbons, may well be a less tractable problem than that of water-borne disease. Cause and effect relationships of water-borne disease problems are well understood, solutions are known, and the technologies needed for remediation have been developed. Failure to resolve the problem seems to have more to do with socioeconomic and political constraints than with a dearth of knowledge. In contrast, we know far less about cause and effect of chemical contaminants in the environment. The methodology for evaluating the impact of contaminants is inadequate, and the technology for remediation is poorly developed. The specter of chemical contamination is one of the major environmental issues of this century and likely will remain so during the first several decades of the 2 1st century. Ecotoxicology has thus emerged as a major research area in response to a major social need. It employs both reductionistic science (toxicology) with strong predictive capabilities and holistic science (ecology) with recognizably weak diagnostic and predictive capabilities. This amalgamation is the result of an increasingly broad interest in and concern about the impact of toxic contaminants on ecosystems. In few regions has there been more interest in this problem than in the Great Lakes. Admittedly, current methodologies for protecting human health and the environment are of questionable effectiveness (2). Part of the intractability of the toxics problem in the Great Lakes stems from our limited understanding of the impacts of toxic substances in complex ecosystems. The concept of ecosystem integrity has become central to this issue.
Ecosystem integrity During the 1950s and 1960s much
scientific research was directed toward Opinion leaders in the Great Lakes finding practical solutions to severe Basin (9) now use the phrase “ecosysproblems in the natural environment tem approach” as a kind of code to imgenerated by our so-called progressive ply: culture. One consequence of such reapplication of interdisciplinary sciensearch was a series of ecological and tific and scholarly concepts and economic concepts and methods within methods; an overall strategy of incremental utilisystemic understanding of the natural tarianism. Rationality was defined in and cultural whole and the various terms like assimilative capacity, effluparts of the nested ecosystems of the ent quality standards, exposure levels, Great Lakes-St. Lawrence River Babioassay standards, carrying capacity, sin; and maximum sustainable yield, benefitadaptive management, mostly of cost ratio, and marginal cost pricing. people, that would achieve cultural The concept of optimum sustainable and natural integrity within this yield with respect to renewable rebioregion in the contemporary consources was one notable excursion into text in which major unexpected rationality. Another dealt with permisevents abound as a result of cultural sible limits of exposure to radioactive and natural interplay at local to global levels of systemic organizamaterials through a risk analysis. All, however, were reductionist approaches tion. strongly influenced by socioeconomic Thus the term “ecosystem approach,” pressures. which might be expected to relate only The year 1968 may be considered the to a perspective, has come also to enbeginning of the shift away from incre- compass perspective, goal, and methmental utilitarianism and toward more ods. Integrity as a goal thus entered U.S. holistic (ecocentric) views. In 1968 a political process was initiated by Swe- legal documents in the early 1970s. It den within the United Nations that led was invested with objective scientific to the 1972 Stockholm Conference (3). and subjective ethical meanings, as is An international conference was spon- apparent in the proceedings of EPA’s sored by the Conservation Foundation 1975 symposium on integrity of water that indicted conventional exploitive and in other documents (10). Tacitly or development (4). The United Nations explicitly, these objective and subjecEducational, Scientific, and Cultural tive concepts of integrity also are being Organization (UNESCO) convened a applied to uses and abuses of features symposium in Paris that provided the of the Great Lakes-St. Lawrence River basis for the Man and the Biosphere Basin ecosystem other than those adProgram (5). In the United States the dressed directly in the GLWQA: water 1970 National Environmental Policy levels and flows. Now that mandates require the restoAct and the 1972 Federal Water Pollution Control Act Amendments ration and protection of the Great Lakes (FWPCA) contain text consistent with ecosystems, ecologists and toxicolothis reform paradigm. Some of the po- gists (ecotoxicologists) are being challitical implications of the new direc- lenged along several lines: to develop tions were spelled out by L. K. more sensitive means of measuring the Caldwell (who helped to draft the loss (or recovery) of ecosystem integrity; to resolve the problem of extrapoFWPCA) (6-8). The 1978 Great Lakes Water Quality lation of data from standard laboratory Agreement (GLWQA), with its 1987 species to enormously complex ecosysProtocol, proposes an ecosystem ap- tems; and to structure a means of acproach (the perspective) to the integrity counting for the true systemic impact of (goal) of the waters of the Canadian/ a toxicant, including social and ecoAmerican Great Lakes basin system. nomic costs. Neither the perspective nor the goal is specified clearly in the official documents. In addition to a perspective and Understanding complex ecosystems a goal, one would expect to find a stateConcern for extrapolation of data ment of methods (e.g., strategies and from standard laboratory species to tactics). more complex ecosystems has led to Many of the latter are spelled out in multiple species testing; chronic toxicthe 1978 Agreement and 1987 Protoity bioassays; and, more recently, atcol, but not as a comprehensive protempts to develop integrated field, labogram of applied systems analysis and ratory, and mesocosm approaches (2). adaptive management. The 1987 Proto- Yet, as Kitchell et al. (11) point out, col may be perceived as a patchwork “Miniaturization may retain a reprequilt of both reductionistic and holistic sentative physicochemical context for views that places a greater emphasis on studying complex interactions; howthe holistic views than is apparent in the ever, the organisms of interest cannot 1978 GLWQA. be rescaled.” They further note that a Environ. Sci. Technoi., Vol. 24, No. 5,1990 599
potential resolution may be to perform manipulative experiments in a series of different-sized enclosures to develop scaling rules for extrapolation to lakes and reservoirs. Current methods for toxicity testing also fail to deal with ecosystem complexity resulting from multiple causality and synergy of multiple stresses acting within the ecosystem simultaneously. Large aquatic ecosystems, particularly in near-shore areas (12), are frequently subject to a battery of human interactions. For example, researchers and resource managers have judged that no fewer than 18 stresses (Figure 1) may be acting on Green Bay, Lake Michigan (13). It is then useful to know which stresses are most strongly interactive and consequently influential in the ecosystem. So-called stress ecology seeks to understand the separate and joint effects of various kinds of interventions by humans (as well as natural phenomena) in the ecosystem (14, 15). Stress ecology and graph theory have been used to assess the health of the Green Bay ecosystem. We currently believe that three stresses-excess nutrients, toxics (polychlorinated biphenyls [PCBs]), and suspended solids and sediments-acting in an additive or synergistic fashion, are primarily responsible for the loss of integrity in the Green Bay ecosystem (12). Figure 2 summarizes the inferred complex relationships between a large number of species populations and certain abiotic variables of the environment. The ecosystem is being maintained in its present state (or being further degraded) by a number of relatively unconstrained positive feedback mechanisms, Suspended particles play an important role in the Green Bay system, as they do in other Great Lakes ecosystems. The movements, repeated resuspension, and ultimate sedimentation of these particles are critically important to the transport and ultimate disposal of toxic contaminants. PCBs, which are major contaminants in the Green BayFox River system, are a case in point. The degree to which a contaminant attaches to a particle depends both on the physicochemical properties of the contaminant and on the type of particle involved. PCBs are easily attached to organic-rich particulate matter. Depending on the type of PCB, 60-75% of the total load appears to be associated with suspended particles (16). The adsorption of PCBs on phytoplankton provides a direct route into the food chain and leads to the contamination of fishes and other animals at the top of the food web (Figure 2). The effects of contaminant loading therefore can be modified by a number of factors 600
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such as wind direction and force, the million of PCBs). number of top predators (piscivores), Although this effort will undoubtedly herbivore biomass, macrophyte abun- reveal much needed information about dance, and availability of phosphorus. the fate of toxicants in large-scale Frankly, it is difficult to see how a aquatic systems, it will reveal nothing meaningful effluent standard can be set per se about toxic effects on the ecosysthat will protect, or in this case restore, tem. Our contention here, following integrity to the Green Bay ecosystem. Schindler's observations (19), is that We suggest that toxicity testing of efflu- toxicity at the ecosystem level can only ent will give little guidance for achiev- be assessed by investigations of particing ecosystem integrity, particularly ular ecosystem properties (20). Some since approximately 80% of the PCBs of these properties (e.g ., sedimentation discharged to Green Bay are believed to rates, input-output measures, residence come from the sediments (J. R. Sul- times) will be investigated as part of the livan, Wisconsin Department of Natu- Mass Balance Study, whereas others ral Resources, personal communica- (e.g ., trophic structure, connectivity, tion, March 1988). carbon transfer efficiency) will not. The complexity and intractability of One of the greatest challenges for ecosystems as exemplified by Green toxicologists and ecologists is to deBay are a major reason for the difficulty velop a means of predicting true ecoof dealing with toxic contamination of system effects of persistent toxicants. ecosystems. Mathematical modeling of State-variable models now being used chemical fate is at present the preferred require considerable aggregation of approach to this difficulty (17). system components before mathematiOne useful modeling approach inte- cal modeling of the system dynamics grates data on physicochemical proper- can be carried out. Frost et al. (21) ties of the toxicant with hydrodynamic point out that there can be distinct adand aerodynamic transport models. vantages to aggregation but that errors The EPA Great Lakes National Pro- can arise through improper aggregation gram Office has initiated an unprece- or neglect of components. An alternative way to learn more dented effort to deal with toxicants in Green Bay by developing a mass bal- about toxicity at the community and ance model for PCBs and three other ecosystem level is the potential use of toxicants (18). individual-based (organism) models. This mass balance model is intended Because toxicity is expressed and meato permit the prediction of PCB levels sured at the level of the organism but in three species of fish based on a ultimately may be manifest at the popuknown reduction of PCB loading to the lation, community, or ecosystem level, system. The end-point is predicated on it may be reasonable to employ orgathe allowable limit of human consump- nism-based simulation models. These tion of contaminated fish (2 parts per models that reflect the outcome of inter-
actions between individuals in a population or between species in a community (22) may greatly improve predictive capabilities regarding toxicity because they do not merely lump individuals, as do the presently used state-variable models. In any case, model development and refinement have some distance to go before it is possible to accurately predict effects of toxic compound dosages in biota or humans. Furthermore, our current understanding of complex ecosystems limits our potential of prediction at that level.
Assessing ecosystem integrity Assuming that problems of prediction may be overcome, how might we ensure the restoration and maintenance of ecosystem integrity? We must first identify useful measures of ecosystem integrity. Should they be structural or functional characteristics, or perhaps a combination of both? Certainly, measures of ecosystem integrity must go beyond the organism or species population level, for it is at
higher levels of integration that ecosystem properties emerge. Ecosystem phenomena such as nutrient cycling, energy flux, and biomagnification are aggregates of phenomena at the lower levels of organization (22). Some species may serve as useful integrative indicators (23). Much time and effort has been expended in the identification of key species. Unfortunately, by the time we see effects of a toxicant at this level, we have missed the early diagnosis of the problem, and ecosystem integrity has already been debased. Schindler (I 9) argues quite convincingly that “in most aquatic ecosystems, sensitive indicators of stress include life table parameters of sensitive, short-lived species and changes in community resulting from elimination of keystone predators.” In addition, he believes that neither short-term acute toxicity studies nor measurements of ecosystem level processes (e.g., phytoplankton production or nutrient cycling) are sufficientlysensitive to detect the early stages of ecosystem stress.
The loss or change in population numbers of some of the more sensitive species may be compensated for by increases in other more tolerant species that have similar roles in the ecosystem. Hence the goal of integrity may be easier to define than the diagnosis of it. Karr and colleagues (24), for example, suggest that inherent potential stability, capacity for self-repair, and minimal external management are all reasonable features of integrity for biological systems. What is needed are working definitions of integrity and identification of key ecosystem parameters for assessing and diagnosing early ecosystem degradation or for monitoring restoration of degraded ecosystems. Karr and Dudley (25) and Schaeffer and colleagues (IS) provide some interesting beginnings to these ends. From our vantage point, it is unthinkable to experimentally toxify largescale ecosystems with persistent contaminants to detect early signs of system degradation. The alternative is to remove the toxicants from existing
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contaminated systems and look for the “trailing edge” effect of reduced contaminants. The Great Lakes already represent large-scale ecosystem manipulation (26). (In 1981 the Water Quality Board of the International Joint Commission established “Areas of Concern” based on environmental quality data from all media-sediment, biota, and water. Fortytwo areas in need of remediation have been identified.) Is it possible to use selected ecosystems of the Great Lakes to test hypotheses of toxicity by reducing toxic loading while purposefully holding all other anthropogenic stresses relatively constant? We don’t know, but we suggest that of the 42 Areas of Concern in the Great Lakes there may be candidates for such an undertaking. Ideally, we wish to see decontamination effects first in long-lived top predators (K species) (27). Satisfying as that may be, we also will need to look for effects within the complex of shortlived species (r species) if we are to learn something about detecting early threats to system integrity. Some experience with the Green Bay ecosystem and Saginaw Bay suggests that such a response of r species can be detected (EL Rubio, M.S. thesis, University of Wisconsin-Green Bay, 1987; 28). It seems clear that ecotoxicology as a conceptual and practical field of study must focus more attention on ecosystem processes to fully address the societal impact of toxic chemicals in our environment.
The goal of a sustainable society Issues of ecotoxicology must be viewed in the context of society. Toxic contaminant problems arise as the cumulative consequences of various polluting activities, and they similarly affect various social groups. Some impacts arise from more obvious ecosystem responses such as the biomagnification of toxics in fish via the food web, which affects sportsmen and commercial enterprises. Other effects are more complex; for example, where should we place contaminated dredge spoils? It is possible in principle, and to some degree in practice, to estimate the economic consequences of these impacts on a community in terms of lost tourism and shipping revenues, bankrupted businesses, or lowered property values. Degraded ecosystems, such as Green Bay and other Areas of Concern in the Great Lakes, reflect a historic allocation of resources toward those users and beneficiaries who were not dependent on maintaining high environmental quality or sensitive biota. Ecosystem rehabilitation strategies seek a realloca602
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tion in favor of the more sensitive beneficial uses and values. The basic issue is one of equity. It will be perceived in terms of the distribution of benefits and costs that are associated with these shifts in a community. Perceptions of the situation influence the response of the affected groups, and this in turn leads to efforts to mobilize the political will needed to solve the perceived problems. Ecotoxicological analyses have a major role to play in documenting the conditions of degraded ecosystems. They can point to some of the causes and possible technical solutions. As rehabilitation proposals are made, they too would likely be subject to benefit-cost analyses, risk assessments, or environmental impact studies, all promoted to help ensure “rational decision making.” However, such proposals can contribute in this way only on the condition that the basic processes for decision making are perceived by all concerned to be legitimate and fair. If not, the analytical techniques and those who use them risk falling under considerable public distrust. Analysts may then be perceived as deliberately attempting to mystify the questions that ought to be asked, obscuring who actually pays the social and environmental costs and who benefits, and disguising disputes that are really based on fundamentally different values. Benefit-cost analyses and risk assessments already have fallen into considerable disrepute because of their perceived use as political tactics. The call for refined mass balance studies of toxics in the environment instead of source reductions toward “zero discharge” can easily be perceived the same way. This kind of situation might be avoided by focusing less on details of the techniques and more on the social context within which they are being applied. Because many of the groups and organizations interested in the environment have conflicting values and agendas, trust, distrust, and cooperation have important bearings on the successful implementation of strategies for restoring ecosystem integrity and ultimately for attaining a more sustainable society. For example, rehabilitation and the search for sustainability are social learning processes; no one organization or professional specialty can achieve this goal alone. In addition, the number of agencies, organizations, and other groups (“actors” or “stakeholders” in sociological terms) who would have to be involved even for relatively localized efforts can be impressively large. The remedial action planning process for Green Bay involved 25 actors. For the 2160-hectare Hamilton Harbor on
the west end of Lake Ontario, the remedial action planning process involves consultations with at least 48 stakeholder groups, including 21 governmental bodies at five different levels of hierarchical authority. If rehabilitation and a sustainable society require major changes in underlying beliefs and values (moving from a technocentric to an ecocentric position), intergroup tension could rise to levels that are not easily manageable. Assuming sustainability is a goal to be sought, what might it imply? Some basic principles to foster the search for ecological sustainability have been articulated in the World Conservation Strategy (1980), and others have been articulated in some proposals for enacting an environmental Bill of Rights. As summarized and extended by the 1987 report (29) of the World Commission on Environment and Development (the Brundtland Commission), the principles for sustainability are listed in the box. In a recent review by the Rawson Academy of Aquatic Science (Ottawa) of nine bilateral agreements between the United States and Canada pertaining to the Great Lakes, one of the main perceived weaknesses was identified as follows: “For the most part, principles of international law and those principles derived from bilateral agreements attempt to define the outer limits of behavior that remain internationally acceptable rather than the achievement of long-term goals, such as joint stewardship over shared resources, intergenerational equity, or maintenance of environmental or ecosystemic integrity. ” Ecotoxicology has much to do with ecosystems integrity, particularly since it has been cast in the framework of both a reductionistic and a holistic science. The challenges for a successful merger of these particular views will require a greater concerted effort than is presently being given either by scientists or by political leaders.
References (1) World Resources 1988-89; World Resources Institute and International Institute for Environment and Development; World Resources 1988-89; Basic Books: New York, 1988. (2) Bascietto, J. et al. Environ. Sci. Technol. 1990,24, 10-15. (3) “Report of the United Nations Conference on the Human Environment, June 516, 1972”; United Nations: New York, 1973; AlCONF.48/14/REV. 1. (4) The Careless Technology: Ecology and International Development; Farver, M. T.; Miltom, J. I?, Eds.; Natural History Press: Garden City, NJ, 1972. ( 5 ) United Nations Educational, Scientific, and Cultural Organization and Food and Agriculture Organization; Conservation and Rational Use of the Environment; U.N. Economic and Social Council: New York, 1968; E14458.
A fundamental right to an environment adequate for human health An obligation to maintain ecosystem cal diversity, and the sustainable use of living natural resources and ecosystems Mandatory environmental assessments for any activities significantly affecting the environment or use of a natural resource Prior notification, access, and due process for anyone likely to be
Paul E. Sager is Cofrin Professor of environmental studies in the Department of ~ ” w ~ ~ ~ ~ -
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ceived a Ph. D. in zoologyfrom the University of Wisconsin-Madison. He has been active in research on eutrophication and phytoplankton ecology of the waters of Green Bay, Lake Michigan, for many years. He has served on advisory committees in the development of the Green Bay Remedial Action Plan. Caldwell, L. K. Nut. Res. J. 1970, IO, 203-2 1. Woodwell, G. M. The Integrity of Water; Proceedings of a Symposium March 1012, 1975; Washington, DC; Government Institutes Inc.: Rockville, MD, 1977, pp. 141-48. Jorling, T. In The Integrity of Water; Ballentine, R. K.; Guarraia, L. J., Eds.; Symposium convened by U . S. Environmental Protection Agency, March 10- 12, 1975, Washington, DC, 1977; U.S. Government Printing Office: Washington, DC, 1977; 055-001-01068-1, pp. 9-14. (9) “Report of the Science Advisory Board, International Joint Commission”; Great Lakes Regional Office: Windsor, ON, 1989. “The Integrity of Water”; Proceedings of a symposium March 10-12, 1975, Washington, DC, U. S. Environmental Protection Agency; Government Institutes Inc: Rockville, MD, 1977. Kitchell, J. F. et al. In Complex Znteractions in Lake Communities; Carpenter, S. R., Ed.; Springer-Verlag, New York, 1987; pp. 263-80. Harris, H. J. et al. Ambio 1988, 17, 11220. Harris, H. J. et al. “Green Bay in the Future-A Rehabilitation Prospectus” ; Great Lakes Fishery Commission: Ann Arbor, MI, 1982; Technical Report No. 38. Rapport, D. J.; Regier, H. A.; Hutchinson, T. C. Am. Nut. 1985, 125, 627-40. Schaeffer, D. J.; Herricks, E. E.; Kerster, H. W. Environ. Manag. 1988, 12, 445-55. Smith, P. L. et al. Oceanus 1988,31, 1220. Breck, J. E.; Bartell, S. M. In Taxic Contaminants and Ecosystem Health: A Great Lakes Focus; Evans, M. S., Ed.; Wiley: New York, 1988. “EPA Green Bay Mass Balance Study Plan”; U.S. Environmental Protection Agency Great Lakes National Program Office: Chicago, 1989. Schindler, D. W. Can. J. Fish Aquat. Sci. 1987,44 (Suppl. l), 6-25. Harris, H. J. et al. Environ. Manag. 1987, 11, 619-25. Frost, T. M. et al. In Complex Znteractions in Lake Communities; Carpenter, S. R. Ed.; Springer-Verlag: New York, 1987; pp. 229-58. Huston, M.; DeAngeli’s D.; Post, W. Bioscience 1988, 38, 682-91.
(23) “Report to the International Joint Commission”; Ryder, R. A.; Edwards, C. J., Eds.; Great Lakes Regional Office: Windsor, ON, 1985. (24) Karr, J. R. et al. Illinois Nut. Hist. Surv. Spec. Publ. 5, 1986; p. 28. (25) Karr, J. R.; Dudley, D. R. Environ. Manag. 1981,5, 55-68. (26) Ragotzkie, R. A. Rrhandlungen Znternationale Vereinigung Limnologie 1988,23, 259-365. (27) Kubiak, T. J. et al. Arch. Environ. Contam. Toxicol. 1989, 18, 706-27. (28) McNaught, D. C. et al. “PCBs in Saginaw Bay: Development of Functional Indices to Estimate Inhibition of Ecosystem Fluxes”; Report to U.S. Environmental Protection Agency, 1984; EPA600/3-84-008. (29) Our Common Future; World Commission on Environment and Development; Oxford University Press: New York, 1987.
Hallett J . Harris is Herbert Fisk Johnson Professor of environmental studies at the Universityof Wisconsin-Green Bay. He received a Ph.D. in zoology from Iowa State University. From 1978 to I986 he coordinated a major research efort on Green Bay, Lake Michigan, as part of the University of Wisconsin Sea Grant Institute, funded by the National Oceanic and Atmospheric Administration and the state of Wisconsin. He is currently working with the EPA Great Lakes Program Ofice in the application of large-scale models to determine the fate of PCBs and other toxic substances in the Green Bay ecosystem.
Henry A. Regier was educated at Queen’s University in Ontario and received a Ph. D. from Cornell University. He is a specialist in fish andJisheries in an interdisciplinary, comparative context. He is currently professor of zoology at the University of Toronto and serves as a commissioner of the Great Lakes Water Quality Agreement, to the International Joint Commission.
George R. Francis has university degrees in ecology from the universities of Toronto and British Columbia, in political economy fiom McGill, and in resourceplanning and management from Michigan. He has served as a consultant in a number of countries on development assistance projects, and is interested in interdisciplinary environmental education and the preservation of nature. He has served as scientiJic adviser to the two Great Lakes commissions. Environ. Sci. Technol., Vol. 24, No. 5,1990 603
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