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Animals as Sentinels of Environmental Health Hazards (1991)
Commission on Life Sciences (CLS)

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5 Fish and Other Wildlife as Sentinels Fish and wildlife populations have been dramatically affected by environmental pollutants. One of the best-known examples is the response of wildlife popu- lations to the use of persistent organochlorine pesticides and industrial chemi- cals (e.g., DDT and PCBs). Rachel Carson's 1962 book, Silent Swing, alerted most of the general public to the serious threats that organochlorine com- pounds posed to wildlife, but published research identifying the effects of DDT on wildlife dates back to 1946 (Bishopp, 1946~. A large body of infor- mation already documented acute poisonings that resulted ~ large die-offs of fish, birds, and mammals (Robbing et al., 1951; Carson, 1962; Turtle et al., 1963~. The bulk of the evidence that initially supported the need for a ban on DDT was related to impacts on wildlife, and only later were potential hazards to human health identified. Negative effects on wildlife continue to be used to highlight and reverse the general deterioration of natural environmental caused by chemical pollutants. Demonstrations of adverse effects on wildlife populations are now sufficient grounds for restricting or banning the use of a toxic substance, regardless of human-health considerations. In this manner, in situ studies might now be used to determine the efficacy of cleanup regula- tions aimed at hazardous-waste sites. DESCR1~7VE EPIDEMIOLOGIC STUDIES The literature is replete with reports documenting the presence of residues of environmental contaminants in the tissues of fish, shellfish, and wildlife. Many studies were intended to investigate the suitability of using wildlife as sentinels of environmental hazards to humans. For example, Ohi et al. (1974) determined that pigeons are sensitive monitors of atmospheric lead contami- nation in urban centers. In addition, large volumes of literatures are available on the use of wild animals in surveillance programs for arboviruses and zoo- notic diseases. The following describes investigations of fish and wildlife data 81

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82 ANIMALS AS SENTINELS gathered intentionally for long-term monitoring of environmental contami- nants. National P - ams National Status and Trends Program The National Status and Trends (NS&T) program, sponsored by the Na- tional Oceanographic and Atmospheric Administration (NOAA), has been examining exposure of aquatic organisms to environmental pollutants and effects of exposure at selected aquatic sites in the United States, Canada, and Mexico since 1984. Analytic data form the NS&T program have been used to demonstrate relationships between contaminants in fish liver and high human population densities or extensive industrialization. For example, the 13 highest total-body DDT and metabolite concentrations were found in Cali- fornia fish in the vicinity of a Los Angeles manufacturing facility (Shigenaka, 1987~. The highest concentrations of liver PCBs in the Northeast occurred in Boston Harbor, Mass. (Ernst, 1987~. Two sites on the Pacific Coast~an Diego Harbor, CaliŁ, and Elliot Bay, Wash. produced fish with higher liver PCB concentrations than fish in more pristine sites (Varanasi et al., 1989~. High concentrations of PCB residues appear to be related to population and industrial trends. The NS&T program includes histopathologic evaluations of fish liver, kid- ney, gill, and skin, in addition to measurement of tissue residue concentra- tions. Some types of lesions occur in those target organs of some species more frequently in relatively polluted environments than in pristine areas (Long, 1987~. Many of the lesions resemble those seen after laboratory expo- sure of mammals and fish to similar chemical contaminants. The occurrence of such disorders therefore has been used as a strong indicator of the pollu- tion status of U.S. coastal waters. The Ocean Assessments Division of NOAA reassessed long-term and large- scale geographic trends in the concentrations of PCBs and chlorinated pesti- cides in U.S. coastal and estuarine fish, shellfish, and invertebrate populations with the purpose of reviewing data sources that NOAA staff had identified (NOAA, 1986~. It also examined some data on adjacent marine coastal areas in Canada and Mexico. Its report consists mostly of tabular summaries of investigations or of other reports. The data sets were derived through survey methods, including traditional library searches, a search of the Environmental Protection Agency (EPA) Storet System, and personal communications of team members.

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FISH AND OTHER WILDLIFE AS SENTINELS 83 Data on fish health and its reflection of environmental health are open to interpretation, but many studies have focused on fish as sentinels to define and demonstrate the relationship better. Whether fish tumor epidemics can result in health hazards for humans that consume diseased fish is unknown. Nevertheless, it is reasonable to consider whether human consumption of tissues of fish with liver tumors will result in ingestion of large amounts of carcinogens large enough eventually to induce similar tumors in the consum- ers. Mussel Watch Bivalves, such as mussels and oysters, accumulate many chemicals to con- centrations much higher than those in the ambient water; bioconcentration factors range up to 104 or even 1Os for some chemicals. Bivalves have been used in the Mussel Watch Program (MWP), sponsored originally by EPA (Butler, 1973) and currently by NOAA (Farrington et al., 1983), at selected coastal sites around the United States since 1976. The current MWP is an outgrowth of two previous programs (1965-1972 and 1976-1978) and uses the same sentinel organisms: the blue mussel for the northern Atlantic Coast, the American oyster for the Gulf of Mexico and the middle and southern Atlantic coasts, and the California mussel and blue mussel for the Pacific Coast (in- cluding the coast of Alaska). The bivalves are sampled during the winter months, to avoid problems associated with collecting and analyzing during spawning, when many organisms purify themselves of lipophilic chemical contaminants. Sediments around the mollusks are collected as part of the program. Through the NS&T program, NOAA has been banking specimens from the MWP in the Environmental Specimen Bank Program of the National Institute of Standards and Technology since 1980. Samples of bivalves and sediment are stored in liquid nitrogen (below -llO C). The rationale for a bivalve-sentinel system was based on several factors (Farrington et al., 1983~: (1) bivalves are cosmopolitan, so data from different locations can be compared readily; (2) they are sedentary and therefore are good indicators of pollution in specific areas; (3) they concentrate many chem- icals by factors of 102-105, compared with seawater concentrations; (4) they have little or no detectable activity of enzyme systems that metabolize xeno- biotic materials, so the contamination in their habitat can be assessed rather accurately; (5) most of them have relatively stable local populations extensive enough to be sampled repeatedly and thereby to yield long-term and short- term data on changes in pollution; (6) they survive under conditions of pollu- tion that might severely reduce or eliminate other marine species; and (7) they

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&d ANIMALS AS SENTINELS are commercially valuable all over the world so their chemical contamination has public-health implications. National Contaminant Biomonitoring Program Wildlife species have been used as monitors of contamination in many environments. Starlings, mallards, and various fish species have been used since 1965 as indicators of pesticide contamination patterns across the United States. The National Contaminant Biomonitoring Program (NCBP, formerly called the National Pesticides Monitoring Program) of the U.S. Fish and Wildlife Service (FWS) uses free-ranging wildlife to detect trends and magni- tudes of contamination with some persistent pesticides and heavy metals (Ludke et al., 1986~. The wildlife are chosen on the basis of their wide distri- bution, abundance, ease of collection, exposure to the chemicals of interest in specific environmental settings, and tendency to accumulate the chemicals in their tissues. Under the NCBP, fish and bird samples are analyzed for selected persistent organic and inorganic contaminants (particularly organochlorines and heavy metals). The National Fisheries Contaminant Research Center in Columbia, Mo., administers the freshwater-fish portion of the program by preparing instructions, analyzing and archiving samples, and interpreting results. The Patuxent Wildlife Research Center administers the bird portion. All data are computerized and available for epidemiologic studies. Results of the surveys are summarized and distributed within FWS every 2 years. Numerous peer- reviewed scientific articles have been published on the basis of the data through 1985 (e.g., Henderson et al., 1969, 1971, 1972; Ludke and Schmitt, 1980; Schmitt et al., 1981, 1985~. Data have been used to identify temporal and geographic trends in the occurrence of chemical residues so as to improve understanding of the magnitude of existing and potential threats to fish and wildlife resources and to monitor the success of failure of regulatory actions related to environmental contaminants. In addition to revealing trends in contaminant concentrations, the data collected have been used by EPA in identifying exposures to some hazardous substances and hence in regulating the release of some of these substances into the environment. For example, the NCBP has identified specific rivers where fish are highly contaminated with pesticide and PCB residues (Schmitt et al., 1985~; the findings can provide a basis for more-focused risk character- izations of fish-consumers. Some monitoring programs have helped to docu- ment decreases in contamination (Schmitt et al., 1985; Prouty and Bunck, 1986: Bunck et al., 1987) and have provided a basis for broad inferences about

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FISH AND OTHER WILDLIFE AS SENTINELS 85 decreases in risk. Archived samples from a station on the Kanawha River in Winfield, W. Va., were analyzed by EPA for chlorinated dibenzopdioxins to document the historical contamination of that site by a chemical-manufactur- ing facility. The NCBP has shown that removal of persistent chemicals from the mar- ketplace has decreased environmental contaminants to more acceptable con- centrations. The bird and fish surveys have documented the continued wide- spread occurrence of DDT and its metabolites (000 and DOE), even at sites far from known sources. That indicated atmospheric translocation or illegal use of the pesticide. Although the compounds are still present, the concentra- tions and occurrence are declining. However, residues of PCBs have not yet shown consistent declines, despite regulations limiting their use and discharge. One of the most important achievements of the NCBP was the documenta- tion of increasing toxaphene concentrations in lake trout from the upper Great Lakes during the 1970s. Toxaphene is extremely toxic to fish. It was used extensively on cotton in the southern United States to control insect pests, and almost none had been used in the Great Lakes states. With analytic tech- niques that identified the composition of the toxaphene in fish from various parts of the Great Lakes, as well as residues in rainfall, it was eventually concluded that the toxaphene in the Great Lakes was derived from atmo- spheric transport from areas of heavy use in the South and Southwest (Nation- al Wildlife Federation, 1989~. The data were used by EPA to deny renewal of toxaphene registration for most uses. The efficacy of the regulatory actions was demonstrated as toxaphene in Lake Michigan decreased by 50% from 1981 to 1984. Registry of Tumors in Lower Animals The Registry of Tumors in Lower Animals (RTLA), sponsored by the National Cancer Institute at the Smithsonian Institution since 1966, facilitates the study of neoplasms and related disorders in invertebrate and cold-blooded vertebrate animals. To accomplish this mission, the RTLA serves as a speci- men depository, a diagnostic center, a literature resource, and a collaborative research group. Its specimen data base contains 5,300 accessions, two-thirds of which are cold-blooded vertebrates (reptiles, amphibians, fish, etch. The literature data base contains more than 5,000 papers on neoplasms and related diseases in lower animals. Both data bases contain abstracts, and data are computerized by taxonomic nomenclature, habitat and its location, type of disease, organ and cell of origin, diagnosis, disease behavior, and etiology. Neoplasms were described in bivalve mollusks, fish, amphibians, and rep-

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86 ANIMALS AS SENTINELS tiles during the second half of the nineteenth century including a viral lympho- ma in northern pike that remains prevalent in North America and Europe. Important neoplasms discovered in lower animals In the twentieth century included the first neoplasms caused by mutant tumor suppressor genes In more than a dozen neoplasms in fruitflies (Stark and Bridges, 1926, Gateff and Schneiderman, 1969; Gateff, 1978) and in melanoma in platyfish/swordtail hybrids (Haeussler, 1928; Kosswig, 1929; Gordon, 1931~. Other important discoveries included multiple neurofibromas in several species of fish, one of which, the bicolor damselfish, is being studied as a possible model for von Recklinghausen's neurofibromatosis in humans (Schmale et al., 1986~; renal adenocarcinoma in leopard frogs, which provided the earliest evidence that a herpesvirus can be oncogenic (Granoff, 1973~; panzootic liver cancer in hatch- ery rainbow trout, which provided some of the earliest evidence that aflatoxins can be carcinogenic (Rucker et al, 1961; Halver, 1965~; and epizootic liver cancer in 15 species of wild fish clustered in dozens of polluted waterways along the Pacific and Atlantic coasts and among the Great Lakes, which sug- gested that fish can be good sentinels for detecting environmental carcinogens (Harshbarger and Clark, 1990~. Examples of fish from polluted waterways with epizootic liver cancer in- clude English sole from Puget Sound; Seattle, Washington; and Vancouver, British Colombia; winter flounder from Boston Harbor, white sucker from Hamilton Harbor in Lake Ontario; white croaker from Long Beach, Califor- nia; white perch from the Chesapeake and Delaware bays; mummichog from the Elizabeth River, Virginia; brown bullhead from the Black River, Ohio, and many other sites; sauger and walleye from Torch Lake, Upper Peninsula, Michigan; and AtIantic tomcod from the Hudson River. Although v~rtuady all fish cell types appear to have the capacity for neoplastic transformation, liver cancer is the most clearly correlated to a chemical causation and thus is the strongest sentinel for carcinogens in the aquatic environment for the following reasons: · Epidemiologic evidence. Fish with liver cancer are clustered where chemicals are concentrated. · Experimental evidence. Liver cancer results when fish are exposed exper- imentally to chemical carcinogens; other tumors occur occasionally, but liver tumors are consistent. · Physiologic evidence. Fish, like mammals, have a spectrum of cyto- chrome mixed-function oxidases in the liver that metabolize carcinogens to their reactive intermediates and produce DNA adducts. · Other data. No electron microscopic or immunocytochemical evidence demonstrates a virus or other alternative cause. Sediment extracts from sites

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FISH AND OTHER WILDLIFE AS SENTINELS 87 where fish exhibit liver tumors produce liver and skin tumors in fish and mice · e In experiments. Fish develop neoplasms in response to many confirmed mammalian carcin- ogens (NCI, 1984; Couch and Harsbarger, 1985~. Experimental laboratory studies to evaluate the sensitivity of freshwater and brackish-water species to carcinogens showed the freshwater medaka and guppy and, to a lesser extent, the brackish-water sheepshead minnow to be among the most susceptible. When exposed to 1-3 months and held for another 3-9 months, those species expressed a tumor spectrum in up to ten organs or tissues (Cameron, 1988~. In the field, Gardner and Pruell (1988) conducted histopatholog~c studies on four marine species in Quincy Bay, Massachusetts, that are commercially valuable and are consumed by humans: winter flounder, American lobsters, softshell clams, and eastern oysters. They measured the concentrations of selected chemicals in edible flesh and assessed the extent of chemical contami- nation in sediments. They demonstrated histologic abnormalities in the winter flounder and softshell clams in Quincy Bay. The lobsters appeared healthy, but according to commercial fishermen, they had only recently migrated to Quincy Bay. Eastern oysters transplanted to the bay for 40 days developed tumors and ovocystic disease. Neoplastic and non-neoplastic pathologic changes involving various organs and in winter flounder appeared to be relat- ed to chemical contaminants, inasmuch as PCBs, chlorinated pesticides, PAHs, and mercury were concentrated in their habitat. All these animals that display adverse health effects continue to provide data about the status of their envi- ronment and indicate trends in environmental contamination, In addition to signaling potential risks associated with their consumption. Chronic noncommunicative disorders in fish are also useful in environmen- tal monitoring. For example, a vertebral dysplasia experimentally produced in sheepshead minnows by exposure to the herbicide trifluralin (Couch et al, 1979) was confirmed in the field when fish that were exposed to an accidental trifluralin spill in Scotland developed vertebral dysplasia (Wells and Cowan, 19823. Trifural~n induced vertebral dysplasia In fish was later shown to be mediated via the pituitary (Couch, 1984~. Penrose Laboratory of Comparative Pathology The Penrose Laboratory of Comparative Pathology (PLCP) data base contains information on diseases of captive animals for comparison with simi- lar diseases in humans. The data base is at the Philadelphia Zoo and seines primarily Pennsylvania and New Jersey. It has been operational since 1901.

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88 ANIAfALSAS SENTINELS The PLCP data base includes information on species, age, sex, cause of death, and diet from more than 30,000 necropsies of zoo animals and free- ranging wildlife in Pennsylvania and New Jersey. Histologic preparations of diseased and normal tissues from each case are part of the permanent collec- tion of pathologic resource materials. The PLCP has published 272 papers and three books describing the research of its scientific investigators; annual reports summarizing disease information were published from 1901 to 1969. A substantial part of the data base is made up of descriptions of more than 525 malignant cancers that occurred between 1901 and 1988. Data analysis revealed several clusters of particular cancer types that drew suspicion to carcinogenic agents in the environment. For example, a cluster of lung can- cers in seven families of mammals and four families of birds from the Phila- delphia Zoo collection was reported in 1966 (Snyder and Ratcliffe, 1966~. Four squamous cell carcinomas and five adenocarcinomas were reported in mammals, and 13 adenocarcinomas and one undifferentiated carcinoma in birds. Ten of the avian pulmonary adenocarcinomas occurred among ducks and geese between 1943 and 1961. Average longevity of the waterfowl on exhibit had not changed significantly during 1901-1964, so the increased fre- quency of lung cancers could not be attributed to advanced age of the animals. Attention next focused on the possibility of increased amounts of carcinogens in the atmosphere during 1943-1961, because the ducks and geese were housed outdoors, and the mammals with lung cancers had spent the greater part of their lives housed in outdoor enclosures. In addition, an otter that had spent 15 years in an outdoor pool developed lung cancer. In the early 1960s, tough air-pollution control laws were implemented In the Philadelphia area. No lung cancers have been diagnosed in the zoo animals since 1962 (Snyder and Ratcliffe, 1966~. The authors suggest that the animals with lung cancer acted as sentinels of air pollution and that the lack of any new lung cancer cases since 1962 demonstrates the effectiveness of the air-pollution laws. Quarterly Wildlife Mortality Report A quarterly wildlife-mortality report is compiled by the FWS National Wildlife Health Research Center (NWHRC) and published in the Supplement to the Joumal of Midlife Diseases. Information for the quarterly report is provided by the NWHRC staff, FWS contaminant specialists, the Southeastern Cooperative Wildlife Diseases Study (SCWDS), and state disease biologists. Locations of the die-offs, dates, species involved, numbers of animals, and causes of death (if known) are reported. About half the die-offs with known diagnoses have been due to environmental contaminants. Although formal

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FISH AND OTHER WILDLIFE AS SENTINELS 89 publication of this data base has been in place only since 1987, the NWHRC has records of wildlife mortality dating back to 1978. The SCWDS has similar data going back to 1958, but its earlier information was related primarily to infectious and parasitic diseases of deer. S=ey~R~gio—~ ply Great Lakes The International Joint Commission (UC) was established in the 1970s after the Canada-United States Agreement on Great Lakes Water Quality. The Great Lakes International Surveillance Plan (GLISP) later established routine monitoring of tissue residues in open-lake fish and spot-tail shiners (near-shore fish) for organochlorines and heavy metals. Most of the fish residue work is conducted by the Department of Fisheries and Oceans of Environment Canada. The FWS NCBP also conducts fish, starling, and wa- terfowl residue analyses from the Great Lakes drainage basin. Most of the states bordering the Great Lakes (Minnesota, Wisconsin, Illinois, Indiana, Ohio, Pennsylvania, Michigan, and New York) have their own programs for monitoring water quality in the river drainages and bays of the Lakes. But these studies are not coordinated centrally, and the GLISP publishes biannual reports only of the IJC monitoring efforts. Although the GLISP was established primarily to monitor water quality in the Great Lakes, rather than ecologic effects of contamination, an animal- monitoring system for the Great Lakes was incorporated into it in 1973 after observations of severe reproductive problems in colonial fish-eating birds. Most of this work has been conducted by the Canadian Wildlife Service. The primary species selected for monitoring was the herring gull. That species was considered a good monitor of the overall pollution on a lake-wide basis, and a program was established to measure organochlorine residues in eggs. Later, the effects of chronic exposure to complex mixtures of persistent lipophilic environmental contaminants were also measured eggshell thinning, embryo- toxicity, teratogenicity, genotoxicity, behavioral toxicity, and demographic changes (Fox and Weseloh, 1987~. Similar effects have since been document- ed in cormorants nesting in the Great Lakes as opposed to colonies in nonpol- luted lakes in Canada (Langenberg et al., 1989~. Extensive dose-response data are available on the effects of PCBs and HCBs on reproduction in mink (Aulerich and Ringer, 1977; Hornshaw et al., 1983; Rush et al., 1983), but no public-health agency has used the fact that ingestion of Great Lakes fish by domestic mink impairs reproduction as a

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90 ANIMALS AS SENTINELS basis for characterizing human reproductive risks. Risk characterization for humans is usually conducted by considering data on more conventional labora- tory species (Swain, 1988; National Wildlife Federation, 1989~. Animal senti- nel systems seem to require much more development and validation before they will be used as more than a qualitative underpinning for conventional procedures in human-risk characterization. Chesapeake Bay The Chesapeake Bay program is one of the best examples of a comprehen- sive ecologic monitoring program for an entire estuary. It comprises many small-scale programs, funded and conducted by a plethora of state and federal agencies, and utility-company compliance-monitoring programs. Some of the programs have been in existence for more than 20 years; others are relatively new. Data are acquired and stored by the individual participating agencies, but all the programs are coordinated through the Chesapeake Bay Liaison Office of EPA Region III. A program atlas summarizes all the monitoring programs and lists contacts in the participating agencies (Heasly et al., 1989~. Most of the monitoring stations collect physical and chemical data for use in water-quality analysis. However, biologic monitoring is also done as part of the water-quality program and to track the ecologic health of the ecosystem to see whether fish and wildlife management objectives are being met. Bio- logic monitoring includes bacteria, phytoplankton, zooplankton, submerged aquatic vegetation, emergent vegetation, and animals (from benthic inverte- brates to aquatic and terrestrial macrofauna). Benthic organisms in the Chesapeake Bay and its tributaries are monitored as part of the water-quality programs of New York, Pennsylvania, Maryland, Virginia, West Virginia, and the District of Columbia, and in several electric and pumped storage-station environmental monitoring and compliance pro- grams. Data on benthic taxon identification, abundance, distribution, biomass, and diversity are collected on annual, semiannual, weekly, or daily (summer only) schedules. Of the 18 current programs, 11 were begun in the 1980s, six in the 1970s, and one (for the York River in Virginia) in 1961. There are 25 shellfish and finfish monitoring programs in the Chesapeake Bay estuary. Species numbers, abundance, distribution, and habitat character- istics are recorded by state agencies, electric companies, universities, and federal agencies. Tissue-contaminant sampling programs are also conducted by several states, the FWS NCBP, and in NOAA's NS&T program. Animals targeted for monitoring include oyster, blue crab, yellow perch, river herring, American shad, striped bass, and alosine. General finfish surveys for relative

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FISH AND OTHER WILDLIFE AS SENTINELS 91 abundance and distribution of all taxa also are conducted. Sampling is con- ducted yearly by some stations; others sample daily or weekly in the spring or monthly throughout the winter, spring, or summer. Waterfowl and other birds are monitored in 11 separate programs, includ- ~ng the National Audubon Society Christmas Bird Count and the FWS Breed- ing Bird Survey. The Virginia Department of Game and Inland Fisheries has conducted annual bald eagle surveys since 1977, colonial bird (least tern, great egret, and great blue heron) surveys since 1975, and surveys of osprey breed- ing populations since 1971. The Maryland Department of Natural Resources has been conducting an extensive waterfowl breeding survey every year since 1963, and a smaller program in Pennsylvania has been in effect since 1983. The Susquehanna stream electric-station monitoring program includes a bird component, which has monitored populations of winter and breeding birds on the Susquehanna River and its tributaries since 1971 (except in 1975 and 1976~. None of those programs monitors tissue residues; that is done only through the EWS NCBP. The Virginia Institute of Marine Science at the College of William and Mary provides information on the loggerhead, Kemp's ridley, leatherback, and green turtle populations in the Chesapeake Bay. The monitoring has been conducted during the spring migration every year since 1979 (including an aerial survey since 1982~. Only numbers, distribution, and morphometric measures are gathered routinely; no tissue-residue analysis is performed. However, all dead turtles are necropsied and the causes of their deaths deter- mined, if possible, with toxicosis included in the differential diagnoses. Puget Sound A variety of monitoring efforts have been conducted over the past 2 de- cades to assess the pollution status of Puget Sound. They include the NS&T program, NOAA's Marine Ecosystem Analysis (MESA) project, the Munici- pality of Metropolitan Seattle (METRO) To~ncant Pretreatment Planning Study, and EPA's Puget Sound Estuary Program. Those programs measure contaminant concentrations in tissues of shellfish, fish, and wildlife, including marine mammals. Some of the most comprehensive long-term information on contaminant concentrations in marine mammals has been collected in the Puget Sound area, including data on organochlorine pesticides and heavy metals in fur seals and harbor seals (Anas and Wilson, 1970a,b; Anas, 1974a,b; Calambokidis et al., 1984, 1985~. The data were collected for various purposes, such as a desire to document the need for secondary treatment of sewage sludge, which

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92 ANIMALS AS SENTINELS initiated the METRO program. Unfortunately, that program resulted in a large accumulation of contaminant information with no central location for its archiving and retrieval and no consistent quality-assurance guidelines. A 1-year study of honey bee contamination showed that these insects are effective, sensitive monitors of environmental contaminants over large geo- graphic areas (Bromenshenk et al., 1985~. Sacramento-San loaquin Estuary The Interagency Ecological Study Program of the Sacramento-San Joaquin Estuary was initiated in July 1970 by a memorandum of agreement sided by the California Department of Fish and Game and Department of Water Resources, the U.S. Bureau of Reclamation, and the U.S. Bureau of Sports Fisheries and Wildlife, which now is the FWS (Brown, 1987~. The program was expanded later to include San Francisco Bay with contributions from the U.S. Geological Survey. In 1984, a data-management committee was added, to ensure that the vast amounts of data collected in the various studies were electronically stored in a manner that preserved the data quality and allowed access by participating agencies and other interested individuals and organiza- tions. The agreement requires annual reports summarizing results of the monitoring programs. The memorandum of agreement grew out of a desire to meet environmen- tal requirements regarding fish and wildlife and to design and operate the State Water Project and Federal Central Valley Project so as to minimize detrimental effects on fish and wildlife. The plan includes a water-quality program and a program to monitor fish abundance, movements, and health (including tissue residues of organochlorines, heavy metals, and selected PAHs). The water-quality program evolved from an emphasis on the adverse effects of excessive algal growth in the estuary to a goal of ensuring that por- tions of the delta have enough algae to support fish. The fisheries element includes resident delta fish and oceanic fish, such as striped bass and salmon. Studies of the effects of existing delta fish-rearing facilities on fish populations also are conducted. There are no monitoring studies of the effects of estuar- ine pollution and water-quality changes on terrestrial, semiaquatic, or aquatic wildlife in the delta or San Francisco Bay, other than those performed in the FWS NCBP.

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FISH AND OTHER WILDLIFE AS SENTINELS 93 AAL4LYTIC EPIDEMIOLOGIC STUDIES Many of the animal-monitoring programs just described were established to document spatial and temporal patterns of environmental contamination on local or regional scales. The resulting information has been used to estimate human exposure, through either the food chain or the contaminated environ- ment itself, as well as to monitor exposure of and effects on the animals them- selves. However, wildlife-sentinel systems can be used for many other purpos- es, and several are discussed in detail below. menial Identification of H~dous Aunts Table 1-1 lists some cases in which incidents of poisoning of wild or domes- tic animals provided the first indications of hazards posed by environmental agents. Many other cases could be cited—e.g., arsenic and selenium in domes- tic herbivores; pesticides in crustaceans, fish and birds; acidic pollutants in fish—in which the species first seen to be affected were probably the species most at risk. Table 1-1 focuses on cases in which the observations in animals are thought to have provided warning of potential effects in humans. In some of the cases listed in Table 1-1, it is still uncertain whether the agents pose serious hazards to humans at the concentrations commonly en- countered in the environment; the animals might have been more heavily exposed (e.g., to dioxins) or more susceptible. In the remaining cases in the table, it is now known that the agents pose similar hazards to exposed hu- mans, and the animal data have been important elements in the stepwise procedure of human risk assessment. In most cases, however, it took some time after the initial observation of animal poisonings to identify the causative agents and to confirm their toxicity. During that time, important human exposure or injury had taken place (e.g., involving aflatoxin, dioxins, ergot, mercury, PBBs, and PCBs). In only a few cases were the warnings provided by sentinel animals distinc- tive and decisive enough to trigger control measures before human exposure took place. One such case may be the pesticide Telodrin, whose manufacture was discontinued after serious wildlife damage was reported in association with effluents from early production (Koeman, 1972~. Even then, human poisonings were a factor (eager, 1970~: the decision to discontinue manufac- ture appears to have been influenced by the combination of occupational poisonings with environmental persistence and wildlife toxicity.

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94 ANIA~1LSAS SENTINELS Hazard Identif~oti~ of Hazel Was Another principal way in which animal sentinels have been used to identify environmental hazards is in the screening of complex mixtures of chemicals in the environment. One of the best examples is the investigation of the prevalence of cancers in fish and shellfish living in polluted environments (Brown et al., 1979; Matins et al., 1984, 1988; Murchelano and Wolke, 1985; Becker et al., 1987; O'Connor et al., 1987~. Where the prevalence of certain types of cancers in such species is high, it is reasonable to presume that they have been exposed to combinations of carcinogenic pollutants, even if the specific agents primarily responsible cannot be identified (Matins et al., 1988~. It is then reasonable to infer that human consumers of shellfish from the same waters are be at risk from exposure to accumulated pollutants. It is less clear that human consumers of fish would be at similar risk, because fish can me- tabolize some carcinogenic pollutants and so avoid accumulating them. Some studies have provided information about responses of animals to contamination gradients. End points that have been reported include liver cancer in flounders (Becker et al., 1987; Matins et al., 1988), macrophage function in spot and hogchoker (Weeks and Warinner, 1986), and reduced species diversity in lacustrine and benthic faunas. All those examples yielded exposure-response relationships that are directly applicable only to the species that were studied. Indication of Ohioan ibiEly of C~micab at Hazardaus-Wasfm Sites In less-controlled conditions, wild animals have been used as indicators of the bioavailability of tetrachlorodibenzopdioxin in contaminated terrestrial environments (Fanelli et al., 1980; Young and Shepard, 1982; Bonaccorsi et al., 1984; Heida et al., 1986; Lower et al., 1989). These studies revealed broadly similar patterns between uptake from soil and accumulation from ingestion. However, it is not clear that the results can be used other than qualitatively to infer a potential for human exposure. Wild animals have been used widely to assess the bioavailability of metals, such as lead, from soil and hence to determine patterns of contamination and potential exposure (Wil- liamson and Evans, 1972; Gish and Christensen, 1973; Goldsmith and ScanIon, 1977; Clark, 1979; Ash and Lee, 1980; Hutton and Goodman, 1980; Ohi et al., 1981). In an attempt to determine adverse health effects associated with the Love Canal hazardous-waste site, voles were trapped along and within the fence

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FISH AND OTHER WILDLIFE AS SENTINELS 95 surrounding the canal, in an area across the street from the fence, and in a reference area 0.~2 km from the canal. After adjustment for ages, mortality was higher in the voles from the area along and within the fence than in the other groups. Liver and adrenal weights in females and seminal vesicle weights in males were significantly lower than those in voles outside the im- mediate Love Canal vicinity (Rowley et al., 1983~. The white-footed mouse, another ubiquitous North American rodent, was used to assess the genotoxic hazards of an EPA Superfund waste site in Cam- den County, NJ. (Tice et al., 1988~. Animals were trapped on the site and at a nearby control site. Laboratory-reared white-footed mice were included in the study as a second control. The frequency of bone marrow micronucleated polychromatic erythrocytes was significantly higher in animals collected at the waste site than in control animals; bone marrow mitotic index and percentage polychromatic erythrocytes in peripheral blood were significantly lower among the animals. No significant difference was detected in average generation time, sister-chromatic exchange frequency, or percentage of metaphase cells containing chromosomal damage. The authors concluded that white-footed mice can be used to detect hazardous concentrations of genotoxic and cytotox- ic pollutants in the environment. Wavers y Ming Most of the monitoring programs in large bodies of water such as Puget Sound, the Great Lakes, or the Sacramento-San Joaquin Delta—were estab- lished principally to measure water quality and to document the success of remediation efforts. In such programs, fish and shellfish have been used only as monitors of tissue residue buildup of persistent compounds that are bio- available. Using animals to monitor the health of the ecosystem—that is, to look at effects of pollution, as well as potential exposure to it has recently been considered but has not yet been widely adopted into monitoring pro- grams. The International Joint Commission is considering such monitoring in the Great Lakes basin, and several studies have recently been funded by the Interagency Ecological Studies Program for the Sacramento-San Joaquin Estuary. Agricultural drainwater has been shown to be an important nonpoint source of pollution of wetlands and catchment basins. Attention was focused on the issue after observations of embryo deaths and deformities in shorebirds and waterfowl at the Kesterson Reservoir in California (Ohlendorf, 1989~. Later work identified selenium as the primary contaminant and arsenic and boron as contributors (Ohlendorf, 1989~. Those elements occur naturally in

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96 ANIMALS AS SENTINELS the soil of the surrounding farmlands and are leached out during irrigation. Drainwater is collected in canals and disposed of ~ evaporation ponds and natural marshes, which harbor large numbers of birds. A dose-response relationship between selenium contamination of food or water and embryo toxicity or immunotoxicity has been determined experimentally in laboratory studies (Heinz et al., 1987, 1988; Ohlendorf, 1989; Fairbrother and Fowles, in press) and through field observations (Skorupa, 1989~. It has been possible to establish a criterion value for selenium contaminations in water that would protect wildlife, as well as fish, shellfish, and humans (Skorupa, 1989~. Indicators of Air Pollution Many instances of illness and death in game animals, free-ranging horses, birds, and bees downwind from smelters or exposed to other sources of air- borne pollutants have been reported (Newman, 1975; Bromenshenk et al., 1985), but there are no systematic uses of wildlife as sentinels of air pollution. Risk ton of Species Under S - y Shortly after the introduction of organochlorine pesticides (e.g., DDT, heptachlor, endrin, aldrin, and dieldrin) in the 1940s and 1950s, dead birds were commonly observed in treated areas (Rudd and Genelly, 1956; Turtle et al., 1963; Nisbet, 1989~. For example, dead birds were found in fields sprayed with DDT at more than 5 lb/acre, and the density and reproduction of forest birds decreased when the trees were sprayed at 2 lb/acre each year (Rudd and Genelly, 1956; Carson, 1962~. More alarming, abrupt decreases in num- bers of peregrine falcons, bald eagles, ospreys, Cooper's hawks, and brown pelicans in the United States were noted from the mid-19SOs to the late 1960s (Hickey, 1968~. The population declines were determined to be the result of reproductive decreases due to breeding delays, failure to lay eggs, and, most notably, drastic thinning and weakening of eggshells; the latter had led to breakage and decreased hatchability (Peakall, 1970~. The geographic pattern of deaths and reproductive failures in affected species, combined with high concentrations of organochlorine pesticides and their metabolites (e.g., DDE) in body tissues or egg yolks, proved that the agricultural chemicals were the cause of the population declines. On June 14, 1972, the cancellation of all remaining uses of DDT on crops was announced by EPA Administrator Ruck- leshaus (Federal Register, June 14, 1972~. Since the ban, eggshell quality and reproduction in the affected species have improved, and population sizes have

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FISH AND OTHER WILDLIFE AS SENTINELS 97 generally recovered (Anderson et al., 1975; Grier et al., 1977; Grier, 1982; Cade et al., 1988; Wiemeyer et al., 1984~. Another important example of risk characterization of wildlife is the deter- mination that oil spills pose a potential risk to fish and wildlife. That determi- nation led to the inclusion of wildlife monitoring and damage assessment plans in Coast Guard regulations governing the transport and shipment of petro- leum products. A major consideration underlying the regulations was the risk posed to wildlife (including seabirds, marine mammals, and sea turtles) by spilled oil. Many of the species at risk are monitored regularly, although detection of effects of spilled oil is only one of several purposes of such moni- toring (Ainley and Boekelheide, 1990~. Yet another example of protection of monitored species as the primary reason for risk-management action is the adoption of U.S. Department of the Interior regulations to restrict the use of lead shot in waterfowl hunting areas (DOI, 1976~. That action was taken after extensive documentation of lead poisoning in waterfowl (Bellrose, 1959) and, more recently, in the endangered bald eagle (Reichel et al., 1984~. Dose-Response Relationships Animal sentinel systems that use free-ranging animals have not often been applied to clarify dose-response relationships, mainly because quantitative information on doses and exposures of sentinel animals is rarely available. The major exception is a series of studies of effects of DDE on eggshell-thin- ning and reproductive success in wild birds. The studies yielded the ranges of dose (measured as DDE concentration in eggs) in various species and information on the shape of the dose-response curves (Blus et al., 1972; Fyfe et al., 1988; Nisbet, 1988~. Anton of Julian Food Chad Many national, regional, and local programs are designed to monitor hu- man exposure to contaminants in the food chain by sampling fish, game, or other nonmarketed food animals (Schmitt et al., 1985, Bunck et al., 1987~. Calculation of intakes from contamination measurements is not always straightforward, however. Contamination in wild animals often varies widely, and concentrations in animals as sampled in the field can differ systematically from those in animals consumed after preparation and cooking (Humphrey, 1976~. Human consumption of fish and game animals is extremely variable

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98 ANIMALS AS SENTINELS and poorly documented. Careful attention to sample design and population characterization is needed, if studies of this kind are to identify the most highly exposed individuals and groups and provide reliable estimates of their exposure. Data are collected each year on harvested waterfowl, game, and fur-bearing animals, primarily for determining the impact of hunting on species popula- tions and setting harvest limits for the following year. However, some risk estimates are being made in connection with consumption of wildlife, especial- ly fish, found in contaminated waters (National Wildlife Federation, 1989~. Those animals provide some indication that health effects are being amplified in a sentinel population before they develop in humans. For example, rein- deer in the arctic and other foraging animals have been sentinels of radioactiv- ity that resulted from the April 1986 nuclear-reactor accident in Chernobyl, Ukraine, USSR, by virtue of the radioactivity in their flesh and milk. The reindeer provide continuous data on radioactivity in northern Sweden; the data have been used to regulate human exposure. Food-monitoring programs are in effect monitoring animals that are acting as sentinels of environmental contamination. For example, fish (brown trout, lake trout, salmon, yellow perch, and walleye pike) in Lake Michigan provide data on pesticides (DDT, dieldrin, and chlordane) and PCBs in the lake. Those sentinels provide information that is useful in determining not only the impact of contaminants on the food supply, but the potential for human expo- sure and health risks. A study by the National Wildlife Federation (1989) calculated human exposure to contaminants in fish from the Great Lakes; these exposure calculations were used to derive estimates of risks of cancer and noncancer health effects. Many regulatory actions have been taken to limit human consumption of contaminated animals that are used as sentinels. Perhaps the most frequent of these actions is restrictions on the taking of shellfish based on magnitudes of contamination with fecal coliform bacteria, metals or other pollutants, or paralytic shellfish toxin. Shellfish are continuously monitored for those con- taminants around most coasts of the United States, and together the monitor- ing programs probably constitute the largest set of animal sentinel systems in current operation and the most direct use of animal sentinel systems in risk management. Local bans on fishing or advisories to limit fish consumption have been promulgated in a number of places (especially around the Great Lakes and on other inland waters) where fish are contaminated with pesti- cides, PCBs, or mercury. A well-known example was the closing of the lower James River to fishing and shellfishing after contamination with kepone (chlordecone) from a plant in Hopewell, Virginia, during the mid-1970s. In laboratory exposures, kepone causes scoliosis in fish (Couch et al., 1977~.

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FISH AND OTHER WILDLIFE AS SENTINELS 99 Selection of those actions usually was based on data from fish-monitoring programs and on faction levels. developed by the U.S. Food and DrugAdminis- tration. The action levels themselves were selected to limit human risks, but in most cases involved consideration of other factors as well. IN SITU STUDIES Fish Bioassays of in situ caged fish have been used effectively for many years to detect the presence of toxic chemicals in lakes and streams. Fish held in tanks have been used for continuous monitoring of the quality of wastewater dis- charges from industrial plants. Caged-fish toxicity bioassays have included investigations of fish mortality related to field applications of pesticides (Jack- son, 1960), effluent discharges from pulp and paper mills (Ziebell et al., 1970) and chemical-manufacturing plants (Kimerle et al., 1986), and metal releases from mining-waste sites (Davies and Woodling, 1980~. Because caged-fish bioassays have become so well accepted in the monitoring of water pollution, the Department of the Interior has adopted them as one method of evaluating the effects of hazardous waste on wild fish populations (DOI, 1987~. Caged fish have also been used in carcinogenicity bioassays (Grizzle et al., 1988~. PI Planarians are potentially useful for in situ water-testing and might prove to be the optimal organism for water-quality bioassay. In a cooperative effort between the United States and West Germany (Deutsch Norm., 1986), re- searchers are using freshwater free-living triclads (also called planarians, turbellarians, and platyhelminths) as sensitive aquatic organisms to detect water pollutants. They are particularly sensitive to heavy metals (Kenk, 1976~. In contaminated water, planarians generally die before fish. They exhibit a sublethal array of acute neurotoxic signs that can be recognized by a min~mal- ly trained observer for example, screw shape, convulsions, hyperkinesis, vom- iting (with pharynx protruding), roll shape, banana shape, and pharynx out or Belly up.~ Planarians are more cost-effective, need less testing time, and are more sensitive to pollutants than are traditional laboratory species (Brigham, 1981; Barndt and Bohn, 1985~; their use also requires minimal equipment.

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100 ANIMALS AS SENTINELS 5~ The Institute of Wildlife and Environmental Toxicology at Clemson Univer- sity is using starlings for in situ testing for the Navy at Naval Air Station (NAS) Whidbey Island, Wash., to assess the potential bioavailability of toxic materials in and around this site, to assess their impact on wildlife, and to evaluate risks associated with remediation of waste sites, especially National Priorities List (NPL) sites (NAS Whidbey Island has been nominated for addition to the NPL3 (Johnston and Kendall, 1990~. Much of the area is forest, grassland, and marsh that provide habitat for upland game birds, water- fowl, various mammals, and the endangered peregrine falcon and bald eagle. Beaches and bays around NAS Whidbey Island are popular fishing and shell- fish-gathering areas. Past disposal sites might have contaminated lowland areas, and the accumulation of persistent and bioaccumulating pollutants in the food chain could affect higher-order predators and humans. Starlings are attracted to the area by placement of artificial nest boxes. That makes possi- ble ready examination of nesting birds for mortality, reproductive impairments, or other signs of physiologic malfunction, such as depressed delta-aminolevu- linic acid dehydratase due to lead exposure, mixed-function oxygenates in liver or embryos, brain cholinesterase activity, and immunologic functions (Hoffman et al., 1990~. The results of the study will be important for demonstrating the usefulness of starlings as a sentinel of the toxicants at a hazardous-waste site. E0hwom~s Several species of earthworms are used in laboratory toxicity tests of envi- ronmental chemicals. The night crawler is the species of choice (FDA, 1987~. Earthworms have been selected as key indicator organisms for ecotoxicologic testing of industrial chemicals by the European Economic Community, the U.N. Food and Agriculture Organization (Edwards, 1983), and the EPA (per- sonal communication, C. Callahan, EPA Environmental Research Laboratory, Corvallis, Oreg., 1989~. Earthworms are true soil dwellers, live in arable fields and woodland areas, and are very sensitive to chemical insult. The redworm and the manure worm inhabit manure heaps, compost piles, and sludge-dry~ng beds and are less sensitive than earthworms to toxic chemicals. All three species concentrate some compounds, such as organochlorine insecticides (Edwards and Thomp- son, 1973) and heavy metals (Edwards, 1983), in their tissues. Bioaccumula- tion of chemicals from the soil makes earthworms good candidate species for in situ monitoring studies, as well as for traditional laboratory bioassays. Earthworms are also large, easy to handle, and readily bred in the laboratory.

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FISH AND OTHER WILDLIFE AS SENTINELS 101 Numerous studies have tested the short- and long-term effects of pesticides on native earthworm populations (e.g., Barker, 1982; Korschgen, 1970~. In situ studies are conducted by placing buckets of laboratory-reared worms at ha~ardous-waste sites (personal communication, C. Callahan, EPA Environ- mental Research Laboratory, Conallis, Oreg., 1989) or areas where contami- nated dredge material has been deposited (Stafford et al., 1987~. The buckets are filled with soil from the site and partially buried at the study area. At various times after their placement at the site, the death rate of the worms is observed, and various tissues are analyzed for the concentrations of chemical contaminants. Comparisons of sediment concentrations with earthworm body burdens have confirmed that laboratory-reared earthworms accumulated as many chemicals and heavy metals and were as sensitive when placed in the field as when contaminated soil was brought into the laboratory for exposure of earthworms under controlled conditions. Preliminary studies also showed that earthworms collected from the site had reduced immunologic functions, as measured by E-rosette formation and macrophage function (Rodriguez et al., 1989; Fitzpatrick et al., 1990~. Honey Bees Honey bee colonies have been used as in situ monitors of air and water pollution in the Puget Sound area (Bromenshenk et al., 1985) and around ha~rdous-waste sites in Montana (personal communication, J. Bromenshenk, University of Montana, 1990~. Bees are particularly well suited for use as in situ sentinels. Hives of various sizes can be moved easily to within or near an area of concern. Once in place, the bees become contaminated either through foraging activities, in which they are exposed to contaminated pollen or water, or by forced-air circulation and evaporative cooling used to control hive tem- perature and humidity. Environmental contaminants might be reflected In the bees themselves or in hive components, including wax, pollen, and honey (Bromenshenk et al., 1985~. Honey bees can be used to monitor pollution distribution over large geographic areas by either intentional placement of hives or use of the vast network of commercial beekeepers. SUAML4RY The use of fish, shellfish, and other wildlife species in coordinated environ- mental monitoring programs can be a valuable, cost-effective mechanism for assessing the bioavailability of environmental contaminants. The few pro-

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ld2 ANIMALS AS SENTINELS grams that have been in place for a long time (e.g., Mussel Watch and the NCBP) have been able to differentiate areas of high pollution and have shown substantial reduction in contaminant loads after restriction of the use of par- ticular chemicals. Those programs have the advantage of using animals that are in direct contact with an environment in question. They have been suc- cessful at providing information both about the state of the habitat and eco- logic consequences to the species themselves and about potential human- health risks. In addition, fish, shellfish, and wildlife are part of the human food chain and thus are sources of contamination in themselves. Therefore, monitoring free-ranging animals is important in food-safety concerns as well. The study of cancer in fish and amphibians not only would provide new insights into the origins of human cancers, but would provide numerous other benefits, because these animals would serve as sentinels of environmental contaminants and as models for studying neoplasia and basic mechanisms in oncology. Despite the obvious advantages of monitoring animals that live in an envi- ronment in question, substantial difficulties are associated with designing and executing such monitoring programs. Techniques for analyzing chemical residues in tissues from a wide variety of species are more difficult and less developed and standardized than similar techniques for less-complex matrices (e.g., the water column). Logistically, it often is difficult and expensive to sample appropriate species, particularly those whose populations have been reduced by exposure to hazardous substances. Animal-welfare issues are important and can pose substantial obstacles in any monitoring programs that involve large vertebrate species. Consequently, most of the current monitoring programs have been restricted to fish and shellfish (the NCBP is an excep- tion). Of the many biomarkers that have been studied for fish and shellfish, histopathology is the most reliable followed perhaps by DNA abducts. Among others being investigated are the induction of hepatic mixed function onuses, increase in macrophage aggregates, activation of oncogenes, teratosis, chemi- cal load in tissues, reproduction impairment, immune response impairment, induction of heat shock proteins, sister chromatic exchange, changes in bio- mass, erythrocyte micronuclei assay, and acute toxicity (McCarthy and Shu- gart, 1990~.

Representative terms from entire chapter:

environmental contaminants