the historical basis for ecological risk assessment

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The Historical Basis for Ecological Risk Assessment“ JOANNA BURGER Ecology and Evolution Graduate Program Rutge rs University Piscataway, New Jersey 08855-1 059 and Environmental and Occupational Health Sciences Institute Piscataway, New Jersey 08855-1 179 INTRODUCTION Ecological risk assessment has emerged as a method for evaluating past and future damage to species, populations, communities, and ecosystems from a variety of stressors. Stressors can be natural, such as hurricanes, earthquakes, fire, or pests, or anthropocentric, such as agriculture and forestry, land development, or chemical contamination. In most cases, species and ecosystems are exposed to a combination of stressors, and risk assessment provides a methodology to compare relative risks, and serves as a tool for managers. In this paper, I examine the historical roots of ecological risk assessment. THE ENVIRONMENTAL MOVEMENT The growth of world population, the mass movement of peoples around the world, and the ascendancy of multinational corporations have increased the necessity for concern for protecting natural resources and the environment. Local people no longer have sole responsibility and jurisdiction over their local resources. Subsistence hunting and fishing gives way to a cash economy, followed by exportation of natural resources to distant lands. As Garrett Hardin suggested in his classic Tragedy ofthe Commons, with increased concentration of people in towns and cities comes decreased steward- ship of natural resources, and those who monopolize “common” resources benefit at the expense of the human community.’ The environmental movement has moved forward by fits and starts over the last century. At least six major movements can be easily identified, although the progres- sion of these movements in different countries and in different cultures varies. The general movements are: ( 1) species protection (i.e., the protection of migratory birds); (2) habitat protection (i.e., establishment of parks in the 1920s and the creation of aThis work was partially supported by the Consortium for Risk Evaluation with Stakeholder Participation (CRESP, A1 DE-FCOl-95EW 55084), which is funded by the Department of Energy, NIEHS Grants ES 05022 and ES 05955, the U.S. EnvironmentalProtection Agency, and the Environ- mental and Occupational Health Sciences Institute. 360

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Page 1: The Historical Basis for Ecological Risk Assessment

The Historical Basis for Ecological Risk Assessment“

JOANNA BURGER Ecology and Evolution Graduate Program

Rutge rs University Piscataway, New Jersey 08855-1 059

and Environmental and Occupational Health Sciences Institute

Piscataway, New Jersey 08855-1 179

INTRODUCTION

Ecological risk assessment has emerged as a method for evaluating past and future damage to species, populations, communities, and ecosystems from a variety of stressors. Stressors can be natural, such as hurricanes, earthquakes, fire, or pests, or anthropocentric, such as agriculture and forestry, land development, or chemical contamination. In most cases, species and ecosystems are exposed to a combination of stressors, and risk assessment provides a methodology to compare relative risks, and serves as a tool for managers. In this paper, I examine the historical roots of ecological risk assessment.

THE ENVIRONMENTAL MOVEMENT

The growth of world population, the mass movement of peoples around the world, and the ascendancy of multinational corporations have increased the necessity for concern for protecting natural resources and the environment. Local people no longer have sole responsibility and jurisdiction over their local resources. Subsistence hunting and fishing gives way to a cash economy, followed by exportation of natural resources to distant lands. As Garrett Hardin suggested in his classic Tragedy ofthe Commons, with increased concentration of people in towns and cities comes decreased steward- ship of natural resources, and those who monopolize “common” resources benefit at the expense of the human community.’

The environmental movement has moved forward by fits and starts over the last century. At least six major movements can be easily identified, although the progres- sion of these movements in different countries and in different cultures varies. The general movements are: ( 1) species protection (i.e., the protection of migratory birds); ( 2 ) habitat protection (i.e., establishment of parks in the 1920s and the creation of

aThis work was partially supported by the Consortium for Risk Evaluation with Stakeholder Participation (CRESP, A1 DE-FCOl-95EW 55084), which is funded by the Department of Energy, NIEHS Grants ES 05022 and ES 05955, the U.S. Environmental Protection Agency, and the Environ- mental and Occupational Health Sciences Institute.

360

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habitat in the 1930s for ducks and other waterfowl following the dust bowl days); (3) soil conservation in the late 1930s; (4) forest conservation in the 1940s; (5) chemical protection (i.e., regulation and control of pesticides and other chemicals in the late 1960s and early 1970s); and (6) the recent concern that several anthropocentric activities threaten the health of the environment and the structure and function of both natural and man-altered ecosystems. This latter concern has prompted the need for a method to evaluate the importance of the different risks to these systems; leading directly to the need for ecological risk assessment.

In the late 1800s and early 1900s many species of birds were overexploited, and populations declined precipitously. The form of exploitation varied, but included hunting for food, sport, and plumes for the millinery trade. In the height of the fashion, whole terns and shorebirds were put on women’s hats in America and Europe. Many species, particularly colonially nesting birds such as herons, egrets, and terns, were eliminated from some states. This led to a conservation movement to protect migratory birds and to limit hunting of all but game birds, that would be closely monitored and regulated so that hunting pressures did not destroy populations. The Migratory Bird Treaty, signed by Canada, Mexico, and the United States, provided for the protection of all birds that regularly migrated over the borders. It was not passed easily, however, and considerable effort was required by the National Audubon Society, the American Ornithologists’ Union, and several other conservation organiza- tions to persuade the United States to become a signatory.

The deliberate slaughter of animals for food or to collect parts that are valuable for aphrodisiacs, medicine, carvings, or adornments may be largely ended in the United States and Europe, but it continues elsewhere, notably in most of Africa and Asia.’ In general, it is still the largest and scarcest animals that are most heavily e~plo i ted .~

With the immediate threat of avian extinction past in the United States, the emphasis of conservationists and scientists switched to habitat preservation, not only for birds but for all natural resources. National parks and national wildlife refuges were created by the federal government to protect geological beauty, aesthetics, and biological diversity, as well as to create nesting and breeding habitat for valuable game birds and mammals. In the 1930s when much of the West was in the grip of a dust bowl, waterfowl suffered dramatically because there were few prairie potholes where they could reproduce. Agriculture had eliminated most of the postglacial prairie marshes, and only small potholes remained.

In the late 1930s several national wildlife refuges were created by the federal government to protect duck-nesting habitat. Large tracts of land were purchased by the federal government, and diked and filled, by government work programs, with water to produce large prairie marshes. In most cases, this land was originally marshland that had been drained for farming in the late 1800s. Although initially created to protect duck populations, these habitats preserved the biodiversity of many other, nongame animals.

Up until this point, the anthropocentric threats to environmental health were largely from direct disturbance (killing of wildlife) or from habitat loss because of agricultural or suburban development. Farming practices included the use of inorganic compounds for insect control, such as arsenic, but use was low.

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During World War I1 agents of chemical warfare were developed, and many proved to be potent insecticides. Initially chemists developed synthetic insecticides such as compounds of arsenic, copper, lead, manganese, and zinc; pyrethrum from chrysanthemums; and rotenone from leguminous plants from the East Indies. These chemicals had two functions, to enter the body to change reproductive and physiologi- cal processes, and to kill.

When the war ended it was an easy leap to use these chemicals for insect control for agricultural, industrial, and suburban uses. In 1947, only 259,000 pounds of synthetic pesticides were used in the United States; in 1960, this amount had risen 250-fold to 637,660,000 pounds. Two main types of pesticides were in use: chlorinated hydrocarbons such as DDT, chlordane, heptachlor, and dieldrin, and organic phospho- rus insecticides such as malathion and parathion. The organophosphorus compounds are highly toxic to vertebrates as well as to insects, and even today are a cause of considerable human morbidity and occasional mortality. Their impact on vertebrate populations, however, is difficult to assess, since one must track the effects of reducing populations of insects on their predator populations.

The chlorinated hydrocarbons had the advantage of lower vertebrate toxicity (though far from innocuous), but even low-level exposures results in bioaccumulation through the food chains such that top predatory species could accumulate relatively high levels, particularly in their adipose tissue. Moreover, unlike the organophospho- rus compounds, these insecticides biodegrade very slowly, so the accumulation in food chains can have far-reaching effects. The most severe effects are those on reproduction, which ultimately results in reduced population sizes.

As early as 1950 the Federal Food and Drug Administration recognized that it was “extremely likely” that the potential hazards from chemicals such as DDT were underestimated. The modem environmental era, however, can be traced to Rachel Carson’s Silent Spring4 which clearly and eloquently forced us to face the conse- quences of the unthinking, unrestricted, and unregulated use of chemicals. Her interest was on the role of pesticides on bird and other wildlife populations. Her message was simple: unless we do something, we will one day wake up to a silent spring, for there will be no more birds to sing.

Even then, her emphasis was on direct toxicity of pesticides to birds, but by 1970, the effects of bioaccumulation of chlorinated hydrocarbons on the reproduction of birds that survived acute toxicity was recognized. Entire populations of eagles, peregrine falcons (Falco peregrinus), and pelicans (Pelecanus occidentatis) were eliminated.5,6 Within a few years, the direct effects on populations decreased, but we began to see indirect effects from this same class of compound that function as endocrine disruptors. The consequences on populations and communities are as severe, but they are less o b v i o ~ s . ~

Although many dismissed Carson’s message as that of hysteria, gradually people began to notice that, indeed, there were fewer birds, frogs, insects, and butterflies. Within only a few years, stimulated by a wide coalition of organizations in addition to conservation ones, the country as a whole demanded environmental protection. It was not a matter of a few environmental or conservation groups, but middle America wanted to see protection of our air and water. Environmental protection became a national priority, not a partisan issue. Environmental protection was a broad mandate that included protection for human health, nature, and wildlife.

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Many of the current issues that affect environmental management are fraught with a lack of basic information on the status and trends of the particular environment being considered.8 This has led to calls for monitoring programs to assess changes in a variety of populations, communities, and chemicals.

LAWS GOVERNING ENVIRONMENTAL ASSESSMENT

With the groundswell of concern for the environment there was a national mandate, at least in the United States and many other Western countries, for laws and agencies that would develop legislation and regulations that would protect our environment. The concern was bipartisan and central to political thought, rather than being considered at one end of a continuum.

The first step was the creation of the US. Council on Environmental Quality in the late 1960s. Its function was to analyze and coordinate federal environmental policy. The problem with the council was that it had no authority and was only advisory, reporting directly to the president. The council, composed of 35 -40 people, was placed in the Office of the President. Its main contribution was to write a “toxic substances” report that laid the groundwork for the Toxic Substances Control Act (TSCA). The report noted that the rate of use of toxic chemicals was increasing, that many posed a hazard, and that they were inadequately controlled.

This led directly to the formation of the Environmental Protection Agency in 1970, under President Richard M. Nixon. William Ruckelshaus was the first adminis- trator, and he recognized that there was a public outcry for environmental protection. His initial assumptions were that (1) if the government set standards, polluters would comply; (2) we know who the bad polluters are; (3) we know the levels that cause adverse environmental and health effects, and (4) environmental protection can be accomplished at a reasonable cost, and in a reasonable time frame. It took him just three months in office to question these assumptions.

Ruckelshaus believed that he must establish the credibility of the agency, demon- strate a willingness of the federal government to act, and set out some achievable goals. He had a total work force of only about 1500 people, very small for a federal agency. Surprisingly, in these early days, much of the agenda of the environmental movement was embraced by the EPA, certainly very different from present-day reality when environmental groups are often at odds with EPA.

At about the same time, there were a number of laws passed that directly regulated different aspects of the environment (TABLE 1). From the perspective of ecological risk assessment, the most important of these was the National Environmental Policy Act (NEPA, 1969) which requires the analysis and disclosure of the effects of any human-induced (anthropogenic) factors, including chemicals; and requires the prediction of all consequences of an action or chemical. This led to the requirement for environmental impact assessments (EIS) that were to be performed uniformly in all states.

Environmental impact assessments were to be multidisciplinary approaches to understanding consequences and impacts of actions or chemicals. The intent was to provide information so that decision makers could balance effects against other factors such as economic development. This landmark legislation required that the consequences of human actions would be considered in environmental decisions.

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TABLE 1. Major Legislation for Protection of the Environment'

Year Legislation

1910 1916 1947

1965 1969 1970 1972 1973 1974 1976 1976 1977 1977 1980

1982 1983 1986

Federal Insecticide Act Migratory Bird Treaty Federal Insecticide, Fungicide and Rodenticide Act (FIFRA) (major changes and

Water Quality Act National Environmental Policy Act (NEPA) Clean Air Act Marine Protection, Research, and Sanctuaries Act Federal Water Pollution Control Act Safe Drinking Water Act Resource Conservation and Recovery Act (RCRA) Toxic Substances Control Act (TSCA) Wetlands Protection Executive Order Surface Mining Control and Reclamation Act Comprehensive Environmental Response, Compensation and Liability Act

Nuclear Waste Policy Act Endangered Species Act Superfund Amendment Reauthorization Act (SARA)

additions relevant to ecological risk were made in 1972 and 1978)

(CERCLNSuperfund Act)

" After Openchow~ki~~ and Cairns.2

There are several difficulties with the environmental impact assessment process, however, including an emphasis on cataloging species and on endangered species, no requirement for experts, no consistency among approaches or methods used, no consistency in end points, no requirement for consideration of uncertainties, and no requirement for evaluating the correctness of conclusions.9~'0 Also, monitoring after the action or exposure is conspicuously absent." One never knew or had to know whether an EIS was correct. This means when making future decisions, it is impossible for the manager o r regulator to know whether past mitigations or restorations were successful. I"

In some ways, the role of science has been unclear in the EIS process, and it is possible for people with little biological training to conduct these, based IargeIy on endangered and threatened plant and animal lists. Community- and ecosystem-level effects were completely ignored. Protection of the environment or evaluation of the effects of hazards has not been adequately served by this process.

The role of risk in EIS, has also been largely ignored." Despite the large number of laws, regulations, programs, and agencies devoted to environmental protection, many national environmental goals have not been met, and many large-scale environ- mental problems remain.'* This is partly the result of the fragmentary nature of environmental policy, laws, and tools. The emergence of ecological risk assessment provides another powerful tool to address the fragmentary and evaluative nature of environmental problems.

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BISECTING FIELDS

Several fields have been involved with evaluating the effects of physical, biologi- cal, and chemical stressors on organisms, populations, communities, and ecosystems, including ecology, ecotoxicology, and wildlife and land management. Ecology mainly concentrated on understanding the structure and function of ecosystems and their component parts. Although ecologists primarily study natural systems, they also examine systems perturbed by man. Often understanding how organisms and ecosys- tems respond to natural disturbances such as fire and hurricanes can provide models for understanding at least the physical perturbations caused by man. Recently the subfield of restoration ecology has developed to help people understand how to restore damaged ecosystems to functioning systems that provide ecological service^.'^-'^ The emphasis on understanding changes in biodiversity is fundamental to examining the effects of humans on biological diversity.'6,17

Ecotoxicology has been concentrating on understanding the effects of toxic chemi- cals on organisms, largely in laboratory settings.'* Thus ecotoxicologists have been able to examine carefully the effect of dose and exposure on organisms, but frequently they work on only a few species of organisms that can be maintained in a laboratory setting. Moreover, they often concentrate only on establishing lethal doses or the no- observed-effect level (NOEL), without considering subtle behavioral and behavioral effects that may be significant in the ~ i l d . ' ~ , * ~ The results of such laboratory studies can be extrapolated to the field; however, this assumption is seldom tested. More recently, ecotoxicologists have recognized the importance of developing predictive models that address ecosystem function and resiliency, particularly for hazardous- waste

Wildlife and land management are fields that deal with the practical aspects of managing resources, presumably to the benefit of both the exploited populations and for humans in general. To maintain suitable populations for exploitation, it is necessary to understand the factors that control these populations, and the effects that perturba- tions have on the system. A recent dialog between wildlife management biologists and toxicologists promised fruitful results in modeling effects of chemicals on popula- tions .23

All three of these disciplines have been examining the effects of anthropogenic forces on organisms, populations, communities, and ecosystems; but they have done so largely in isolation." Moreover, the levels of study have varied: ecologists have studied the whole continuum from organisms to ecosystems and the landscape; ecotoxicologists have largely concentrated on effects on the individual (similar to human health considerations); and wildlife and land managers have largely concen- trated on exploitable lands and organisms.

At the same time that these three disciplines were examining the effects of physical, biological, and chemical stressors on ecological systems, human health risk assessors were developing paradigms and methodologies to assess the risk from various factors (usually chemicals) on various human health end points, particularly c a n ~ e r . ~ ~ , ~ ~

Recently, ecologists and environmentalists have been evaluating the possibility of using the human health risk assessment paradigm for ecological systems. The human health risk assessment paradigm, formalized by the National Research Coun-

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366 ANNALS NEW YORK ACADEMY OF SCIENCES

ci1,24,?5 consists of four phases: hazard identification, dose-response analysis, exposure assessment, and risk characterization.

EMERGENCE OF ECOLOGICAL RISK ASSESSMENT

For a variety of reasons, there is a clear public mandate for the maintenance of environmental “health.”2628 Although there is debate about the nature of ecological systems, and whether the health paradigm is useful, the public clearly is interested in examining the effects of physical, biological, and chemical hazards on ecosystems and their component parts (see references 29 and 30). Moreover, most people, both experts and the general public, can agree on what clearly constitutes an unhealthy ecosystem and one that is no longer providing ecological services.

Ecological risk assessment has emerged as a useful method for examining the effects of perturbations on ecosystem^.^"^^^-^^ Perturbations can be natural and anthro- pogenic, or both. Ecological risk assessment can be used for single species or local natural communities, as well as for regional and landscape problem^.'"^^^ It can deal with chemical pollutants, biotechnology introductions, or proposed developments.

Over the last several years, the four phases of human risk assessment have been modified substantially for ecological risk assessment.’2~25~’1~’5~38 The primary modifications have included the addition of a more detailed initial problem-formula- tion phase, a recognition that dose-response data may not be available for most organisms and most ecosystem functions, and a formalization of the importance of a dialog between scientists and managers in all phases. Lack of dose-response data, however, does not mean a lack of hazard and response data. Two current models for ecological risk assessment are shown in FIGURES 1 and 2.

More recently, Burger and Hande13’ have suggested that restoration evaluation should be added as an important component of risk characterization. They added this component because there is a very real need to provide a science-based mechanism for evaluating the risks among sites. For example, one pressing problem facing Western countries today is how to deal with nuclear wastes4’ Indeed, the international community and United Nations consider these substantive issues for worldwide cooperation and agreement.

The money required for the cleanup of all hazardous-waste sites to residential standards is exorbitant, and some relative ranking is required, both for the sites that will be cleaned up, and for the level of clean up. One way to do this is to evaluate the time, cost, and energy required to restore the degraded systems to functioning ecosystems that provide the ecological services desired for that site. Ecological risk assessment and restoration ecology provide tools for this task.

With the ending of the Cold War, the nearly 40 Department of Energy sites in the United States that manufactured nuclear weapons and thereby became repositories of chemical and nuclear wastes (as well as countless other federal and contractor facilities that were involved) are slated for cleanup. The task is daunting in terms of time, money, and energy, and critical management decisions are required regarding which sites to clean up, when and how to clean them up, and what the criteria are for a clean site.

The problem of evaluating degraded and contaminated sites is even more critical in some Eastern Block nations, because there were few environmental controls.

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Ecologicll Risk Assessment 1

1 I I I

I * I - - - - - - -A RiskManagemeat k--------’

FIGURE 1. Ecological risk assessment paradigm as proposed by the EPA.”

Massive amounts of industrial, oil, and nuclear wastes currently render large tracts of land unusable. The international community, as well as national agencies, will have to determine which problems are the most acute and pose the greatest risk to ecosystems and humans.

Ecological risk assessment will also be useful for evaluating physical damage caused by natural events such as fires, hurricanes, and tornadoes, and by anthropogenic events such as clear-cutting, water diversion, development, and the introduction of exotic (or bioengineered) species.

CONCLUSIONS

Ecological risk assessment has a special role in the decisions required in the next century; with human populations increasing and resources decreasing, there is an even greater need to make choices about the risks of chemicals and other perturbations to our fragile environment. Some of these choices will result in mitigation or cleanup, some may dictate habitat management, while others may involve little or no interven-

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1

Discvsaion with Risk Asssaror Md Ria MM.w

L I I

u

Relationship

I I

I

FIGURE 2. Ecological risk assessment paradigm as proposed by the NRCZ5 and modified by Burger'" and Burger and Handel."

tion. These choices must have a sound scientific basis, and ecological risk assessment can provide this basis. Risk assessments for different degraded habitats can be used in the process of triaging which sites to clean up or mitigate.

Each of our current state and federal agencies, and our environmental laws, have responsibility for some fragment of environmental protection or management.* This often results in a great deal of regulation without improvement in overall environmen- tal q~al i ty .~ ' Ecological risk assessment has the potential of overcoming the fragmented nature of environmental assessment by examining all the factors that affect environ- mental "health," and by providing scientific data to make difficult management choices. Ecological risk assessment can be used in a landscape context to help make the best available decision when there are management options. It takes into account long-term changes that transcend the traditional 70-year lifetime.42

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One key advantage of ecological risk assessment is that it provides a uniform methodology for evaluating the magnitude and probability of adverse effects of both natural and anthropogenic catastrophes, and of evaluating a range of diverse hazards such as chemicals, physical disruptions, and hunting and fishing (plus many, many others4’). By using a common methodology, we can compare risks, leading to sound management decisions (i.e., leadu). Further, ecological risk assessment provides the opportunity for stakeholder participation in the initial scoping of the problem, and in the final risk characterization stage.

Although the ecological risk assessment process itself is science-based, a variety of stakeholders, including the government and the private sector, can influence both the types of risk assessments to be conducted, and the valuation of these assessments. Stakeholders can broaden or narrow the future land-use scenarios that risk assessors can incorporate. Risk assessment provides a way for expert knowledge to be used objectively to determine the risk of a hazard, while allowing for continuous stakeholder participation. Risk assessment is thus an iterative process, with risk assessors evaluat- ing the hazards, while managers, regulators, and the general public can influence the selection of assessments and their ultimate valuation.

Ecological risk assessment is a fitting next step to the environmental movement of the twentieth century, because it provides a common method for evaluating the wide range of environmental problems that led directly to our environmental protection laws. The assessment process can be used for single stressors, or a combination, and for different types such as chemical, physical, and biological.

ACKNOWLEDGMENTS

I thank S. Bartell, L. Barnthouse, K. Cooper, B. D. Goldstein, M. Gochfeld, M. Greenberg, J. Ehrenfeld, M. Lee, J. Moore, S. Norton, D. Policansky, C. Powers, M. Robson, C. Safina, and D. Wartenberg for valuable discussions about ecological risk and the environmental movement.

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