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Human-induced changes in the environment have had adverse effects on both wild and domestic animals. Damage to agricultural livestock, poultry, pets, and other domestic animals has occasionally been severe, with important eccnom- ic consequences (Lillie 1970). Cainage to wild birds, fish, and mammals has decreased the aesthetic and recreational value of the environment, ard this in turn has had consid- erable economic impact (L. Stickel 1975). In ecological terms, effects on populations of one species may have con- sequences for other elements in biological communities that interact with the affected organisms. In addition to their intrinsic importance, effects on wild or domestic animals iray occasionally provide corroborative evidence or warnings of potential risks to humans. Fesearch on effects on domestic animals and wildlife must develop the same lines of evidence needed to evaluate human health hazards. Specifically, closely coordinated studies are needed to assess the health status of animal populations in the field before, during, and after pollu- tion episodes of short cr long duration; to measure expo- sures of animals to agents suspected of causing any effects observed; to test the effects of the same agents on animals under controlled laboratory conditions; and to elucidate the metabolic and ecological mechanisms cf effects. Effec- tive study cf the impacts of environmental contaminants on animals requires integrated multidisciplinary research. Large gaps remain ir our understanding of effects of environmental contaminants on animals. Much cf the published research has been done in response to particu- lar problems or specific needs for regulatory action, and lacks both the breadth and the depth required to support wider extrapolations or more fundamental prin- ciples. Furthermore, the state cf knowledge is differ- ent for domestic and wild animals. The biology and physiology of most economically signifi- cant livestock, pets, and other domestic animals have been

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studied extensively. Relatively detailed knowledge is available on toxic effects of some air pollutants, such as fluoride and arsenic, and of certain water contaminants, such as nitrate, that have had important impacts on live- stock (Lillie 1970, NRC 1972). The nutritional and health effects of both excessive and insufficient ingestion of many ether trace elements have also been well documented, chiefly from the perspective of improving animal production. Inves- tigations of effects of environmental contaminants have been relatively uncommon, except in cases of substantial and ob- vious injury to livestock. Very little is known yet about, for example, the effects on domestic animals of common urban air pollutants like ozone and other photochemical oxidants (Lillie 1970). Many farms and feedlots lie within heavily polluted airsheds (such as the San Eernardino-Riverside basin), and it is important to know whether such environ- mental conditions have had significant 'effects on the health or productivity cf livestock. There are a number of striking and well-documented examples of effects of environmental contaminants on wild- life, such as eggshell thinning in fish-eating birds due to chlorinated hydrocarbon pesticides in the food chain. In general, however, information on actual or potential effects of contaminants on wildlife is far from complete. Relatively little is kncwn of the physiological responses of wild species of terrestrial and aquatic vertebrates and invertebrates to potential environmental hazards. Unlike domestic animals, most wildlife organisms must continuously interact in demanding ways with their surroundings (to find food or a mate, to avoid predators, and so on) . For wiId- life , therefore, subtle effects, such as changes in repro- ductive success or behavior, may have consequences for popu- lations that are as important as, or more important than, mortality or overt toxicity. A great deal of field and laboratory research on wildlife has been conducted both on relatively easily observed acute effects and on chronic, more subtle repro- ductive or. behavioral impacts. Investigations have con- centrated on organisms with important eccnomic signifi- cance, such as agricultural pests, pollinators, shell- fish, commercial food and game fish, and the food chain organisms on which the latter depend. Effects on wild birds and mammals have been studied less intensively, although these effects have received much public atten- tion. Eespite the substantial information base available, knowledge of effects on wildlife is far from adequate (W. Stickel 1975). One fundamental problem is the enor- mous number of contaminants that are widespread in the environment, and the vast array cf species that may be - 65 -

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at risk. Another important lack is knowledge of mecha- nisms that exist within wildlife populations that iray offset or compensate for effects of pollution. Some basic problems common tc research on both domestic and wild animals have limited the usefulness of much of the available information for estimating risks. Vulnerability to most effects differs sharply and unpredictably anong species; even within a species, effects can vary with such characteristics as age, sex, nutritional condition, and seasonal or reproductive state (V. Stickel 1975). Some contaminants are ingested or absorbed directly by animals, while others are^ accumulated by plants or other organisms in food chains. Toxic effects may appear only in animals at higher levels of the food web, scmetimes well removed in space and tiire from sources of pollution. Indirect impacts may occur in some populations through ecological interactions (such as decreased availability of prey or pollinators) rather than through direct toxicity. One very important area in which mere information is reeded is the combined effects on animals of multiple pcl- lutarts and ether environmental or physiological stresses. Many studies of the toxicity of mixtures of agents have been done in the laboratory, primarily with aquatic organisms, and interactions between some pesticides and physiological stresses (such as hunger) have been examined in some birds and fish (w. Stickel 1975). In general, however, not enough is known to estimate the risk involved in simultaneous cr sequential exposures to multiple contaminants that are likely to occur in the ambient environment. To achieve the capability to predict and prevent effects cn domestic animals and wildlife, some broad principles of chemical ecology must be developed. Unifying concepts are needed to understand and predict species differences, tc assess the risks of mixtures of pollutants, and to resolve ether currently unanswerable questions. Such a structure cf knowledge should be built up through well-conceived, coordinated interdisciplinary research. Some critical pro- grams to develop needed information are described in the recommendations that follow. - 66 -

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EPIDEMIOLOGY OF DOMESTIC ANIMALS yej.Uance programs to environirer.t- 3llY^causgd_diseases_of .domestic Agricultural livestock, pets, animals in zoos, and small birds and animals -that commonly share human habi- tats are exposed to many of the same risks of environmen- tally induced diseases as people are. Specific functional effects, causative agents, and rcutes of exposure may be similar to or different from those experienced by man, but the end results — death, degererative disease, cancer, birth defects, mutations, or behavioral abnormalities — may be much the same for a great many species. Effects in animals with relatively short lifespans may, in some cases, serve as early warnings of potential chronic effects in humans, and animal epidemiolcgical data might provide corroborative evidence of patterns of diseases in man. Ir many other instances, the suffering and economic damage that environmental agents cause in animal populations are important in themselves, regardless cf implications for human health. Some notable pollution-related outbreaks cf disease in domestic animals include fluorosis in cattle and sheep grazing in the vicinity of phosphate or aluminum pro- cessing operations (NRC 1974) , ard toxic effects of feed contaminated with'polybrcminated biphenyls in farm animals in Michigan (Isleib and Whitehead 1975). It is very likely that there are many additional distinctive (if less obvious) environment-linked patterns in the incidence of diseases of domestic animals, but unless attempts are made to find them, they may go unnoticed. Studies should be undertaken to look for such patterns, and when they are identified additional tests should be pursued, including collection of tissue sam- ples, toxicological experiments, and clinical veterinary studies, Capabilities for conducting animal epidemiology are relatively limited at present. Most states maintain regis- tries of diseases of livestock, and registries of tumors in pets have been proposed in some areas, but no systematic effort to organize such a surveillance program has been made. The opportunity exists, ir. connection with human epid-eroiological studies that are likely to be undertaken in the next several years (see Chapter 4) , to include information on nonhurnan species exposed to the same envi- ronments (Shimkin 197U, Doll 1976). Additional studies - 67 -

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of livestock in rural areas might also b€ useful. Neither all the required techniques for detecting environmentally induced diseases in aninals nor the marpcwer needed to mount an effective nationwide prcgram in this field is yet available. A pilot program might be carried out instead in a small number of carefully selected areas as part of studies of human disease patterns in the same locations. If this approach fulfills its apparent promise, it should receive a higher priority in the future. TOXICCLOGICAL STUDIES The physiology, toxicology, and pharmacology of wild and domestic birds, mammals-, fish, and other organisms differ considerably from those of man or of the standard laboratory animal surrogates for man. Advances in toxi- cological methods for evaluating risks to human health should be paralleled by the development cf increasingly sensitive techniques for detecting effects in other species. Many available methods are adequate only for measuring acute effects of high exposures; a number of more sensitive tests exist, but have beer employed with relatively few species. Most of the impcrtant chronic effects of low-level environmental pollution are likely to be insidious. Experimental methods are needed that can detect mutations, effects on behavior or reproduc- tive processes, and subtle or subclinical disease condi- tions that may make the organism more susceptible to other environmental hazards, such as predation, pathogens, or adverse weather. Some sensitive tcxicological methods have been adapted to test for low-level tcxicity in wildlife; for example, behavioral changes have keen observed in fish and birds in response to pollutants (Warner et al. 1966, Anderson 1971, Heinz 1976) . Emphasis should be placed both on extension of emerging techniques to other important wildlife species, and on increasing understanding of the biological and ecological meaning of observed effects. Determination of the ecological significance of behav- ioral and other subtle effects or animals requires labora- tory studies that go beyond single species and examine interactions typical of the ecological community, Fesearch is needed to advance conceptual models and techniques for experimental study in this area. Initial efforts should - 68 -

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be directed toward developing lakcratory tests for effects cn population interactions, which might then be verified in the field. The research would need to be multidisci- plinary, coordinating physiological, tcxicoloqical, and behavioral studies with the sorts of investigations of effects at the community and ecosystem level that are described in Chapter 7. It is important to examine effects cf pollutants on animals of varied taxonomic groups and habits under dif- ferent seasonal and physiological conditions. Research on effects of combinations of chemicals, administered concurrently and consecutively, deserves high priority. For tcxicological studies to be most useful for evalu- ating effects in the field, it is essential to examine the influence of as many of the relevant variables as possible under controlled conditions. FIELD STUDIES OK WILDIIFE li§13_investiga.tions_shcuid_be_ carried oai_iHIiiEillg Jily it h . exjer imjnt al dYnamicsx_behaviorx_and_rej:roductive succe§s_gf_wildlif e lii t ed_§nvir onm €nt§ . To test the significance in the life of the crganism cf any effects revealed by laboratory tcxicological tests, it is necessary to study wildlife populations in the field. Laboratory and field studies must he closely coordinated, so that ecologists and tcxicologists can make comparable observations on the same species. While laboratory studies are concerned with the re- sponses cf small, confined populations cf animals, field studies must deal with effects or larger, free-living populations. Behavioral, reproductive, cr other chronic effects may lead to changes in the size, age structure, cr spatial distribution cf populations. Field research often requires many years for full evaluation of such effects, because biological processes may allow popula- tions to respond to or compensate for adverse conditions. Disease, competitior, predation, the weather, and in- herent characteristics of the population contribute to natu- ral fluctuations in population density, and other factors unrelated tc polluticn may have adverse effects on wildlife, If effects of pollutants are to be distinguished from those due to other causes, field research must be closely tied to both laboratory tests and investigations of mechanisms. - 69 -

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MECHANISMS OF ACTION Increased research cn the Ehysiglogisal The elucidation of biological mechanisms of action is arcther critical element in urderstanding effects on wild and domestic animals. Information of this sort can be obtained by study of the metabolism and pharmacology of chemicals in organisms and by examination of ecologi- cal processes such as bioaccumulation, fcod chain trans- fer, and degradation of pollutants. Such knowledge is needed to develop principles for defining, for example, the physiological basis of differences among species, the nature of interactions among pollutants or among pollutants and ether stresses, and the relationships between effects on a given organism and those on others at different levels of a food web. Such general princi- ples are essential for the prediction of ecological effects from limited data on the biological activity of a substance. A second valuable result of research on mechanisms is knowledge of the physiological correlates of effects on behavior, reproduction, or other important functions; such knowledge can lead to accurate, sensitive, and simple bio- assays for effects. Increased understanding of the mech- anisms of toxicity might also provide a basis for the use cf some specific wild or domestic animals as "sentinels" to provide early warnings of potential environmental haz- ards to man, or to other wild or domestic species. INSTITUTIONAL AFRANGEKEKTS Fesearch on effects of environmental contaminants or various animal species is being conducted in many govern- ment agencies and universities. Studies of effects on livestock and other domestic animals have been conducted or supported by the Eepartment of Agriculture (USDA), many state agricultural research programs, the animal producing industry, scme health agencies, and university scientists in several disciplines. Research on effects on wildlife is being done by or for the Department of the Interior (Fish and Wildlife Service), the Department of Ccmmerce (the National Marine Fisheries Service, in NOAA), USDA, EPA, EPCA, MIEHS, and seme state agencies. Additional contributions have come from a number cf universities, and NSF has supported investigations in this field. - 70 -

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In general, roles and responsibilities for research among the many agencies involved have been reasonably well defined and separated, but improved coordination is still needed in some areas, such as effects on aquatic organisms. The research recommended here can prcbably be accom- plished best, at least in terms cf federal involvement, vdthin long-term research programs in agencies with the greatest interest and expertise in appropriate areas: USDA for livestock and ether domestic animals, and EOI and NCAA for fish and wildlife, Some cf the basic bio- logical research might be done within or be supported by certain offices of NIH, especially NIEHS, and in univer- sities. As in most environmental research, irteragency coor- dination is important; in particular, research in other agencies should draw upon EPA's knowledge of the current cr likely state of the environmert and potential impacts cf new technologies, and EPA should be irade aware early of any problems that might have important impacts on domestic or wild animals. A substantial amount of research manpower and resources will prcbably need to be devoted to standardized toxicolog- ical tests on domestic animals and wildlife to develop information for regulatory decisions, work of this sort (beyond that required of industry) ought to be performed by EPA, possibly through contracts with qualified private institutions. Short-term research of this sort is essen- tial; however, many of the information needs identified in this chapter will be met only through sustained efforts that may require five tc ten years to produce answers. - 71 -

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Anderson, J,M. (1971) Assessment of the effects of pollu- tants on physiology and behavior. Proceedings of the Poyal Society (London) B177:307-320. Coll, R. (1976) Epidemiology of cancer: Current perspectives. American Journal of Epidemiology 104(4) :396-404. Heinz, G. (1976) Methylmercury: Second-year feeding effects cn mallard reproduction and duckling behavior. Journal cf Wildlife Management 40(1):82-90. Isleib, D.R. and G. L. Vihitehead (1975) Polybrominated biphenyls: An agricultural incident and its conse- quences. I. The agricultural effects of exposure. Pages 47-55, Proceedings of the 9th Annual Conference cn Trace Substances in Environmental Health, edited by D.E. Hemphill. Columbia, Mo.: University of Missouri. Lillie, R.J. (1970) Air Pollutants Affecting the Performance cf Domestic Animals. A Literature Review. Agricultural Handbook No. 380. Washington, D.C.: U.S. Department of Agriculture. National Research Council (1972) Water Quality Criteria of 1972. A Report of the Committee on Vater Quality Criteria, Environmental Studies Board, National Academy cf Sciences, at the request cf and funded by the U.S. Envircnmental Protection Agency. EFA-R3-73-033. Washington, D.C. : U.S. Government Printing Office; PB-236 191. Springfield, Va.: National Technical Information Service. National Research Council (1974) Effects of Fluorides in Animals. Committee on Animal Nutrition, Board on Agricultural and Renewable Resources, Commission on Natural Resources. Washington, D.C.: National Academy of Sciences. Shimkin, M.E. (1974) Upon man and beast—adventures in cancer epidemiology; Presidental address. Cancer Research 34:1525-1535. - 72 -

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Stickel, I. (1975) Testimony. Pages 176-189, Costs and Effects of Chronic Exposure to Lew-Level Pollutants in the Environment. Hearings before the Subcommittee en the Environment and the Atmosphere, Committee on Science and Technology, U.S. Congress, House. 94th Congress, 1st Session. Stickel, Vs. (1975) Seme effects cf pollutants. Pages 25-74, Ecological Toxicology Research, edited by A.D. Mclntyre and C.F. Mills. New York: Plenum Press. Warner, P.E., K.K. Peterson, and L. Eorgiian (1966) Eehavioural pathology in fish: A quantitative study cf sublethal pesticide toxication. Journal of Applied Ecology 3 (Supplement: Pesticides in the Environment and their Effects on Wildlife, edited by N.W. Moore):223-247. - 73 -