The American public is becoming increasingly aware that the natural environment is fragile. The news media have reported on many instances of environmental changes affecting animal life, often as a result of pollutants from human activities. Recent reports have focused on

These events may be omens that other forms of life, including people, could become threatened if environmental conditions continue to worsen. But how much worse must conditions be before wildlife and human life are in danger? Or are they in danger already? Clearly, better methods are needed to predict the probability of future environmental and health problems based on present evidence. Such information could guide environmental regulators and decision makers in taking actions in time to minimize damage to the environment and human health.

Biological events, such as increases in the populations of pollution-sensitive species in a river or the return of a fish species to a once-polluted stream, can also indicate recovery of an ecosystem. Such information helps scientists determine the extent to which remediation of a contaminated waterway has been successful.

Biological events that provide information about the environment include more, however, than increases and decreases in animal and plant species. A variety of pollutants resulting from human activities can interfere with the normal functioning of an organism, making it less able to grow normally or reproduce successfully in its environment. Short of death, some of the more common but serious effects of environmental stressors on aquatic organisms are changes in behavior, growth, and reproduction. These changes in individual organisms, known as biological indicators (or bioindicators, for short), can eventually result in large-scale changes in biological communities and even ecological systems.

Researchers in the Environmental Sciences Division (ESD) at Oak Ridge National Laboratory are using wildlife species, such as fish and waterfowl, as bioindicators of ecosystem health. Our goal is to develop and improve our capabilities for detecting and predicting the effects of environmental stress on key, or "sentinel," ecological species. This information could lead to appropriate actions that prevent undesirable and irreversible effects in ecological systems such as streams, rivers, and lakes.

At ORNL Mark Greeley, Rhonda Epler, Kai-Lin Lee, Lee Shugart, and I are involved in research to identify biomolecular, biochemical, physiological, and other organism-level responses of aquatic organisms to environmental stressors such as contaminants. ORNL researchers have developed bioindicators of pollutant stress and used these indicators to assess ecological health in creeks, reservoirs, rivers, and marine systems. We have applied this approach to determining biological effects of contaminants in various waterways on or near the Oak Ridge Reservation: East Fork Poplar Creek, White Oak Creek, Mitchell Branch, the Clinch River, and Watts Bar Reservoir. We have studied bioindicators in the Pigeon River and in estuaries in South Carolina, all of which are polluted by pulp and paper mill effluents. We have looked at ecological effects in reservoirs in South Carolina and Georgia, which are contaminated by high levels of PCBs, and in natural lakes at Cape Cod, Massachusetts, which receive underground plumes of contaminants from a nearby military facility.

Early Warnings of Environmental Damage

Bioindicators are useful because they are telltale signs of impending environmental problems. Early effects of pollution initially occur at the lower levels of biological organization. Changes in genes, cells, tissues, body chemical processes, and basic body functions appear before more severe disturbances occur in populations and ecosystems. These biochemical and molecular effects can be detected as changes in enzyme levels, in structure of cell membranes, and in genetic material, or DNA. Changes at these subcellular levels induce a series of structural and functional responses at the next level of biological organization. For example, complex processes such as hormonal regulation, metabolism, and immune system responses can be impaired. These effects may eventually alter the organism's ability to grow, reproduce, or even survive. All these measurable changes serve as bioindicators of pollutant stress. They provide early warnings of environmental damage.

Ultimately, irreversible and detrimental effects may be observed at the population and community level, adversely affecting the health of the entire ecosystem. Dramatic examples of these effects are mass deaths of whales and porpoises along the eastern U.S. and Gulf of Mexico coasts, wholesale shifts in aquatic species and community structure in the Great Lakes of the United States, and biologically dead rivers and reservoirs in Russia. These examples attest to the highly destructive effects of pollutants on the environment.

Examples of Bioindicators

One way a physician can determine the cause of a patient's health problems is to analyze a blood sample. The health of a fish can be determined in a similar way. Analysis of blood from a fish can indicate problems in organ function--a bioindicator. For example, the presence of specific types of enzymes (tranaminases) in fish blood can indicate liver impairment. Just as alcohol can cause liver damage, or cirrhosis, in humans, PCBs and polycyclic aromatic hydrocarbons in the aquatic environment can inflict liver damage in fish, leading to more serious problems.

Elevated levels of another bioindicator, urea nitrogen, in fish blood reflect abnormalities in gill function, or respiratory problems. When functioning normally, fish gills as well as kidneys excrete nitrogen-bearing waste products from the body. Fish gills can be damaged by heavy metals--mercury and aluminum--and acidified water. We have found evidence of such effects in fish from the Great South Fork Recreational Area in Tennessee and Kentucky. In this area, drainage from abandoned coal mines contributes both to high levels of heavy metals and to highly acidified surface waters. In the Great Smoky Mountains acid rain can drastically raise the acidity level of mountain streams, periodically killing trout in hatcheries.

As these examples show, bioindicators of pollutant stress range from organ damage responses to increased mortality rates of organisms.

Uses for Bioindicators

The bioindicator approach is not the only method for monitoring possible ecological effects of pollutants. One traditional method is direct measurement of chemical pollutants in streams or in the organisms themselves. Another is the laboratory toxicity test in which the toxicity of a pollutant is determined by the death rate of exposed organisms. Compared to the bioindicator approach, these methods often provide only limited information.

Bioindicators offer several types of rather unique information not available from other methods: (1) early warning of environmental damage; (2) the integrated effect of a variety of environmental stresses on the health of an organism and the population, community, and ecosystem; (3) relationships between the individual responses of exposed organisms to pollution and the effects at the population level; (4) early warning of potential harm to human health based on the responses of wildlife to pollution; and (5) the effectiveness of remediation efforts in decontaminating waterways.

The physiological condition of an animal reflects the combined effects of all its environmental stresses, such as contaminants, unfavorable temperature, suspended sediments, insufficient oxygen, and food shortages. Largemouth bass and striped bass--important sport fish commonly found in reservoirs in East Tennessee reservoirs--are particularly good integrators of environmental stress because they are at the top of the aquatic food chain. Signs of impaired health in fish enable scientists to assess the nature and extent of environmental degradation.

Bioindicators can be used to establish cause-and-effect relationships between different levels of response to pollutants in individual organisms and for the entire population. For example, if a diseased fish is found in a stream, it should be possible to determine not only the cause of the disease but also the potential consequences of that disease for the individual fish and for the population. If the disease kills young fish and impairs reproduction in older fish, then the population may decline or even disappear over time.

Bioindicators and Human Health

For many years, coal miners would place a canary into a newly opened part of the mine to test the toxicity level of gases. If the canary died, the miners knew it was too dangerous to work; if the canary survived, they continued their work. The fate of the canary served as a bioindicator of pollutant toxicity that could threaten human health and possibly cause death.

We have found that bioindicators in the environment can also provide early warning signals of potential human health effects. Several years ago, we were asked by the Environmental Protection Agency to study the health of fish in the Pigeon River. This river was contaminated with chlorine-containing compounds called dioxins and other pollutants, primarily from a nearby paper and pulp mill--the Champion Plant in Canton, North Carolina. Dioxins are produced when elemental chlorine is used to bleach paper. People downstream of the mill expressed concerns about its health effects, such as increased cancer rates, and even filed a lawsuit, which was eventually settled out of court.

When we examined sunfish from the Pigeon River, we found problems with their endocrine, reproductive, and metabolic systems. We detected altered hormone levels, metabolic and nutritional imbalances, and changes in the normal population and community dynamics. We also observed DNA damage and cancerous lesions in these fish. Such effects were attributed to chemicals released from the mill.

In addition, we found that people in the area could have been exposed to contaminants not only by eating fish but also by using water from the Pigeon River to irrigate crops and water livestock. Thus, some of their sources of food may be contaminated with dioxins.

Is there a link between impaired fish health and a potential threat to human health? Recent studies show that dioxin and other environmental chemicals can disrupt the hormonal system by mimicking or inhibiting estrogens in organisms. Estrogens and other hormones are chemical messengers that regulate various processes in the body. Hormones act on parts of the body by sending chemical signals through receptors on or inside cells. This action can be blocked by chemicals that mimic a hormone and attach to its receptors. Because hormones regulate growth and reproduction, it is believed that hormone-disrupting chemicals could interfere with these processes, possibly leading to reproductive and developmental problems in humans.

Estrogens are known to play critical roles in the development of breast cancer. In fact, hormones are believed to be indirectly responsible for 40% of all cancers in women. Thus, the recent rise in environmental chemicals, including estrogenlike compounds, has increased exposure of body tissues to estrogen, possibly accounting for the 1% annual increase in U.S. breast cancer deaths since the 1940s.

We found evidence of altered sexual development--possible sex changes, impaired gonad development, and reduced steroid hormone concentrations--in fish taken from the upper and most contaminated section of the Pigeon River. Interestingly, breast cancer incidences are higher in the two counties downstream of the paper mill than in surrounding counties. There is only about a 1 in 500 probability that the observed incidences of breast cancer in these two counties are due to random chance alone. This example suggests that bioindicators could provide a reliable early warning that human health may be potentially endangered by increasing levels of environmental pollution.

In a project coordinated with Andy Gilman of the Great Lakes Health Effects Program, we are examining the implications of ecosystem health indicators for human health. We are using data supplied by Gilman to write a paper on this subject. In the Great Lakes area in the late 1980s, Theodora Colborn, a zoologist with the World Wildlife Fund, discovered problems with the offspring of 16 predator species, including fish, birds, reptiles, and mammals. Many of the young failed to survive to adulthood or to reproduce. These animals experienced these problems apparently because their parents ate fish from the Great Lakes, which were contaminated with hormone-disrupting chemicals. These wildlife species provide one of the first models for the transfer of hormone-disrupting chemicals from one generation to the next.

Such responses in wildlife can provide models for predicting responses of humans to the same environmental pollutants. However, it is difficult to prove that declines in wildlife populations are attributable to certain suspect chemicals. It is even more difficult to prove that these chemicals are affecting human fertility in the United States. These difficulties can be addressed only through multidisciplinary research linking ecological, wildlife, human, and laboratory animal research and by building bridges among the human, veterinary, and environmental health sciences.

Environmental Restoration

Since 1942 research and production activities on the Oak Ridge Reservation have resulted in occasional spills or discharges of hazardous materials, including radioactive cesium, PCBs, and mercury into various waterways. Recent environmental laws and regulations such as the Clean Water Act; the Resource Conservation and Recovery Act, and the Comprehensive Environmental Response, Compensation, and Liability Act impose limits on releases of these materials and require that these materials be properly treated, recovered, and isolated from the environment. They also require cleaning up waterways and land contaminated by discharges of hazardous materials.

In the Biological Monitoring and Abatement Program directed by Jim Loar of ESD, bioindicators are being used to evaluate the short-term and long-term effectiveness of remedial actions on aquatic systems receiving discharges from ORNL, the Oak Ridge Y-12 Plant, and the Oak Ridge K-25 Site. These remedial actions are being taken to comply with environmental regulations.

Biological indicator studies on East Fork Poplar Creek since 1986 have shown marked improvements in the health of fish populations in the stream at several levels of biological organization. In fact, several pollution-sensitive species of fish that have been missing from the creek for years are now beginning to flourish there.

Bioindicators are also being used to evaluate both the need for and potential effectiveness of remedial actions on the Oak Ridge Reservation. The reservation has been a source of pollutants to off-site waterways--Poplar Creek, the Clinch River, and Watts Bar Reservoir. As part of the Clinch River Environmental Restoration Project directed by Bob Cook of ESD, we are assessing the health of important wildlife species, such as several fish species (largemouth bass, bluegill, catfish, and striped bass) and waterfowl (blue herons and ducks) living in or near these waterways. In addition, the levels of contaminants--PCBs, heavy metals, and radionuclides--are being measured in animals (by ESD's Marshall Adams and Mark Bevelhimer), sediments (by ESD's Dan Levine), and the water (by ESD's Clell Ford) of the Watts Bar system.

An unusual aspect of this project is that both the bioindicators and contaminant data will be used for human health and ecological risk assessments (by ESD's Glenn Suter and Larry Barnthouse). These assessments will guide regulators in determining the extent of environmental restoration required in the Clinch River-Watts Bar system. Additional bioindicator and contaminant data will be obtained later from this system to determine the effectiveness of any reservation-wide cleanup.

Bioindicators are an excellent tool for monitoring the health of biological populations, assessing the potential hazards of environmental pollution to human health, determining if industry is complying with regulations, and evaluating the effectiveness of remedial actions.

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