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Environmental Effects of DDT Dichlorodiphenyltrichloroethane, better known as DDT, was a potent insecticide when first used in the late 1930s. It had no obvious side effects and was active against many insect pests. As a result, it was extremely widely used, both in the United States and elsewhere. But, as has since happened with so many other chemicals, DDT had unforeseen effects. Those effects resulted from its persistence-one of its initially attractive features. Because of this persistence, DDT was transported from its initial site of application by both biotic and abiotic factors until almost no part of the earth's surface was free of it. Animals in the oceans, lakes, and rivers, on land, and in the air had detectable amounts of DDT in their tissues. The resulting concern led to detailed monitoring, to increased understanding of how chemicals are transported through the environment and how quickly resistance to pesticides can evolve, and to a new aware- ness of how even the most careful scoping of a problem does not guarantee freedom from unpleasant surprises. 358

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Case Study JOHN BUCKLEY, Whitney Point, New York INTRODUCTION DDT (dichlorodiphenyltrichloroethane) was first synthesized in 1874, but its properties as an insecticide were not discovered until 1939. By the early 1940s, the United States was producing large amounts of DDT for control of vectorborne diseases, and its use is credited with saving millions of lives from diseases with insect vectors, such as typhus and malaria. Its use in the United States for agricultural purposes expanded rapidly after World War II, reached a peak of 80 million pounds in 1959, and decreased thereafter until it was terminated by cancellation of its registration in 1972. Approximately 1,350 million pounds of DDT were used in the United States during those 30 years. In addition to domestic use, hundreds of millions of pounds were exported. Public concern over use of DDT became widespread in 1962, when Rachel Carson's Silent Spring was published. As a result of this concern, the pros and cons of DDT use were considered by the President's Science Advisory Committee, whose report, Use of Pesticides, issued in May 1963, recommended an orderly phasing out of DDT over a short period. As early as 1957, the federal government began restricting its own use of DDT, and, beginning in 1967, many registered uses of DDT were can- celed. Finally, on June 14, 1972, after a hearing that generated 9,312 pages of testimony (from 125 experts) and more than 350 documents, the administrator of the Environmental Protection Agency (EPA) announced the cancellation of all remaining uses of DDT on crops. Uses for public health and quarantine purposes were not affected, and export was per- mitted. After appeals by both sides, the Court of Appeals for the District of Columbia ruled on December 13, 1973, that there was "substantive evidence" in the record to support the ban of DDT. The cancellation of DDT was so strongly opposed by some agricultural interests that the 1974 report of the Committee on Appropriations of the House of Representatives (Congressional Record, November 1973, H. 9619) stated: The LEnvironmental Protection] Agency was also directed to initiate a complete and thorough review, based on scientific evidence, of the decision banning the use of DDT. This review of DDT must take into consideration all of the costs and benefits and the importance of protecting the Nation's supply of food and fiber. 359

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360 SELECTED CASE STUDIES The resulting review, DDT: A Review of Scientific and Economic As- pects of the Decision to Ban Its Use as a Pesticide, was published by EPA in July 1975. All data reviewed supported the 1972 findings. ENVIRONMENTAL PROBLEMS The cancellation of DDT was based on its persistence, transport, bio- magnification, and toxic effects and on the absence of benefits of DDT that were not available through less environmentally harmful substances. In the course of research on DDT and its metabolites, many insights into the movement, fate, and effects of pollutants in the environment were developed. DDT was the first pesticide to which rapid and extensive resistance evolved. The earliest field studies were of DDT applied at 5 lb/acre for spruce budworm control. These studies concentrated on acute effects, such as deaths of birds, fish, and insects and other invertebrates. The acute LDso (the dose lethal to 50% of the test organisms) in laboratory mammals varied from 60 mg/kg in dogs to 800 mg/kg in rats. Bioassays of fish, however, revealed LCso values (concentrations in water lethal to 50% of the test organisms in a specified number of hours) of a few parts per billion (ppb). Captive birds had acute LCsoS (concentrations in food lethal to 50% of the test organisms) of 400-1,200 ppm (parts per million) when given in the diet for 5 days (Hill et al., 1975~. Because of the extreme toxicity of DDT to fish, attempts were made to avoid bodies of water in the course of aerial spraying. Avoiding such areas completely was not possible, because more than 50% of the DDT applied typically drifts outside the target area, often onto water. DDT had been in widespread use only a short time before resistance developed in some pest species. The first recognized evidence of resistance to DDT was the failure of house fly control with DDT in southern Italy in 1947 after exceptional success in 1946. Shortly after discovery of resistance to DDT, resistance to other insecticides was observed in the field, but development of resistance was not universally recognized as late as 1956 (Brown and Pal, 19711. Standardized laboratory methods for detection of resistance were worked out under the sponsorship of the World Health Organization. By the time of cancellation of DDT in 1972, more than 200 species of invertebrates were resistant to DDT, cyclodiene, or organophosphorus insecticides; some species were resistant to all three. Resistance in vertebrates is less common, but has been reported to occur in some frogs in Mississippi (Boyd et al., 19631. Resistance has several ramifications in relation to environmental effects. Indirectly, inability to control resistant insects has led to an increase in

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ENVIRONMENTAL EFFECTS OF DDT 361 entomological research to find alternative methods of control. Generally referred to as IPM (integrated pest management), these methods depend on greater understanding of the life history and ecology of the pest, and they result in much more selective control. Pesticides are used in most applications of IPM, but only sparingly and in combination with other methods, so that there is less contamination of the environment. In the mid-19SOs, massive spraying programs were undertaken to save the American elm by killing the elm bark beetle, which spread the imported Dutch elm disease fungus from tree to tree. Robin mortality was wide- spread, and robins dying with tremors characteristic of DDT poisoning were commonly seen in treated areas. Dying robins appeared not only at the time of spraying, but also in the following spring before additional spraying. Chemical analyses showed that soils in these areas contained DDT at up to 18 ppm, and earthworms that fed on the leaves in the soils contained DDT at 53-204 ppm. Dead robins that had fed on the worms had up to 3 mg of DDT in their tissues (Barker 19581. Tests for residues in forest soils revealed that DDT disappeared slowly (Woodwell, 19611. Here was unequivocal evidence of the persistence of DDT and of the movement and concentration of DDT through a terrestrial food chain. Also during the mid-19SOs, dichlorodiphenyldichloroethane* (000, also called tetrachlorodiphenylethane, or TDE) was applied to Clear Lake, California, to control gnats. Initial concentrations of 0.02 ppm in water yielded DDD residues of 10 ppm in plankton, 903 ppm in the fat of plankton-eating fish, 2,690 ppm in the fat of predatory fish, and 2,134 ppm in the fat of grebes that fed on fish (Hunt and Bischoff, 19601. In the late l950s, the first indication of worldwide spread of DDT residue was observed. It was discovered (Buckley, 1979) that shark liver contained detectable amounts of DDT and its metabolites. This dis- covery was so surprising that it was not believed. The initial presumption was that the sample analyzed had been inadvertently contaminated; but a second sample, taken with precautions to avoid contamination, also contained DDT residues. Because DDT was not applied to the oceans, it appeared that the residue in shark liver had to be a naturally occurring substance, but residue analysis of pre-DDT shark liver oil detected no DDT. Finally, it was assumed that the DDT must have been accidentally dumped into the ocean and that the shark liver contamination was local. Residue analysis showed at least small amounts of DDT widely distributed in sharks and other marine fish, thus requiring us to acknowledge long-range movement of DDT and biological magnification of these residues. Laboratory studies confirmed the bioaccumulation. Later analyses of tissues from penguins, skuas, and seals from the *000 was used directly as an insecticide, but also formed by metabolism of DDT.

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362 SELECTED CASE STUDIES Antarctic and fur seals from the Pribiloff Islands in the Bering Sea con- firmed the occurrence of DDT and its metabolites far from any area where it had been applied. DDT was truly ubiquitous (Anas and Wilson, 1970; Sladen et al., 19661. The degree of bioconcentration of DDT from the environment into living tissues and of residues from prey to predator was so striking as to be almost unbelievable (U.S. EPA, 19751: Experimental data showed that DDT can be biologically concentrated by a variety of aquatic organisms at all trophic levels. Phytoplankton, the dominant oceanic vegetation and primary food source for marine animals, concentrates DDT from seawater into its cell membranes. Water-fleas (Daphnia), a food source for many freshwater fish species, accumulated 9.0 ppm in tissues after three days exposure to 80 pptr (parts per trillions. This represents a bioconcentration factor of 112,500 times the exposure level. Rainbow trout exposed to 1.0 ppm DDT (wet weight) in food and 10 pptr in water for 84 days contained 2.3 ppm as whole body residues. Exposure to food alone resulted in residues of 1.8 ppm (a concentration factor of 1.8 X) and exposure to water alone yielded residues of 0.72 ppm (a concentration factor of 72,000 X). In fish fed 1 mg/kg DDT/day, 73% of the DDT residues were present 90 days after the fish were transferred to clean food. DDT is not equally toxic to all species of animals. Control programs for arthropods have sometimes resulted in increased pest damage, because predators of a pest were eliminated by DDT. For example, DDT appli- cations in apple orchards eliminated populations of predaceous ladybird beetles, so that red-mite populations formerly controlled by the ladybird beetles reached outbreak proportions. This particular mite is not suscep- tible to DDT and was hardly influenced directly by the DDT that killed the beetles (Helle, 19651. In other cases, less susceptible populations have flourished after control programs, presumably because of reduction in competition as a result of elimination or reduction of more susceptible species. Cope (1961) reported that, after treatment of 72,000 acres of the Yellowstone River watershed, the total numbers of invertebrates had re- covered within a year, but the species composition was still altered. Ple- copterans and ephemopterans were reduced, but trichopterans and dipterans occurred at higher numbers at the end of the year. In some cases, selective toxicity has resulted in reductions of species that are normally used as food by valued predators. Ide (1967), in studies of the effects of DDT applied at 0.5 lb/acre in the forested watershed of the Mirimachi River in New Brunswick, observed that fewer insect species emerged in streams affected by DDT, and that those most severely reduced were the large ones, such as caddie flies, on which salmon mainly feed. Recovery of stream fauna required up to 4 years.

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ENVIRONMENTAL EFFECTS OF DDT 363 Studies carried out at the Patuxent Wildlife Research Center demon- strated that stored residues of DDT could be mobilized during weight loss, and this resulted in mortality after exposure to DDT had stopped (Van Velzen et al., 1972~. These studies provide a basis for understanding the cause of some of the delayed mortality observed in the field. During the 1960s, more subtle effects of DDT and its metabolites were discovered. The striking eggshell thinning in some predatory birds such as bald eagles, ospreys, peregrine falcons, and pelicans was clearly the cause of decreases in their populations. Eggshells of the affected species collected before 1945 were found to be noticeably thicker than those collected in the late 1940s and later (Anderson and Hickey, 1972~. It was hypothesized that this eggshell thinning resulted in decreased reproductive success, and field studies of the brown pelican supported the hypothesis (Risebrough et al., 19711. Laboratory studies confirmed that thinning of shells occurred in mallards (Davison and Sell, 1974), American kestrels (Peakall et al., 1973), and ring doves (Haegele and Hudson, 1973) when dichlorodiphenyldichloroethylene (DDE) was incorporated in the diet of these birds. Since the cancellation of DDT in 1972, there has been a marked decrease of DDT residues in brown pelicans and improved re- production in those pelicans on the Pacific, Gulf, and Atlantic coasts and in ospreys in the eastern United States (U.S. EPA, 19751. DDT alters the behavior of some fish, and some of the changes are clearly detrimental to the welfare of the species. Atlantic salmon Parr, for example, select water temperatures below those to which they are accli- mated when exposed to DDT at 10 ppb or less and temperatures higher than acclimation temperature when exposed to DDT at 10-100 ppb. Fur- thermore, exposed salmon are less active than control fish. Rainbow trout select higher than acclimation temperatures and exhibit high-temperature shock followed by death (Javaid, 1972a). KEY ISSUES By 1970, it was evident that DDT residues were everywhere and that reducing the residues would require huge reductions in the use of DDT. Contamination of fish used for human food beyond the contamination limit approved by the Food and Drug Administration (FDA) occurred widely, especially in freshwater fish. Residues also appeared in many meats and dairy products. Surveys of human fat revealed virtually universal contamination by DDT, and residues in human milk gave rise to concern over the desirability of breastfeeding. That DDT residues appeared far from where DDT had been applied and lasted for years or even decades suggested that most uses would have to stop; control of application sites

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364 SELECTED CASE STUDIES and care in application would not be enough to reduce environmental residues substantially. The low cost of DDT, its relatively low toxicity to mammals (including humans), and its persistence made its continued use highly desirable for public health vector control programs. Although concern for its toxicity is greater now than when DDT was first used in the United States (FDA workers are said to have attested to its harmlessness by putting a spoonful in their coffee), there is still no clinical or epidemiological evidence of damage to man from approved uses of DDT, despite its demonstrated tumorigenicity in mice. ECOLOGICAL APPROACHES TO THE ENVIRONMENTAL PROBLEMS ASSOCIATED WITH DDT Ecologists first became concerned about ecological effects of DDT when it began to be used for control of forest insects, especially when applied from aircraft over hundreds of thousands of acres. The earliest studies consisted of field observations of treated areas. Mortality at the time of treatment or shortly thereafter was the criterion of the effect of treatment. These first field observations revealed some mortality of birds and fish in streams in treated areas and massive mortality of stream insects. For example, it was noted in one study that cutthroat and brook trout stomachs contained 99% crayfish after spraying, compared with none before, pre- sumably because of the almost complete elimination of their insect food (Adams et al., 19491. An experimental area was treated annually for 4 years with DDT, and breeding bird populations were studied. Three species decreased substantially, but no changes were detected in 23 others (Rob- bins et al., 1951~. Studies during the early 1950s, principally in the laboratory, continued to concentrate on acute effects of DDT. In the late 1950s, the Dutch elm disease control program resulted in insights into food-chain transfer and accumulation of toxic materials in terrestrial environments. Studies of DDT (and other chlorinated organic pesticides) thereafter regularly looked for phenomena associated with food-chain accumulations. The general belief among toxicologists had been that metabolism of toxic substances invariably decreased their toxicity, but it was discovered that some me- tabolites of DDT, especially DDE, were more persistent and in some cases more active biologically than the original compound. This discovery laid the groundwork for research that eventually explained the decline of a number of bird species through eggshell thinning. Pesticide-wildlife studies also led to insights into repopulation by song- birds of areas from which birds were removed. A study by Robbins and

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ENVIRONMENTAL EFFECTS OF DDT 365 colleagues demonstrated that, if half or more of the songbirds were re- moved from a 40-acre tract of bottomland forest in Maryland during the early part of the nesting season, they were replaced within a few days, as judged by counts of singing males before and after the removal (U.S. FWS, 19631. By the early 1960s, it had become evident that many freshwater sport and commercial fish were becoming so contaminated with DDT and its metabolites (and with other chlorinated hydrocarbons) that they were not suitable for human food. Concentrations were sometimes high enough to impair fish reproduction. For example, lake trout from Lake George, New York, produced eggs containing DDT and metabolites at 2.9 ppm or more; these eggs hatched, but the fry died (Burdick et al., 19641. USES OF ECOLOGICAL KNOWLEDGE AND UNDERSTANDING Valued Ecosystem Components No formal effort was made to identify valued ecosystem components, although it was the effects on valued ecosystem components that eventually resulted in eliminating the use of DDT in the United States. Among these effects were the decrease in songbird populations caused by massive con- trol programs, such as those for spruce budworms in forests and Dutch elm disease in suburban areas; the declines in sport fish, such as lake trout in Lake George, caused by blackfly control programs; the contamination of fish and game desired as human food to a point greater than that permitted in domestic animals used for food; and the decline of avian predators at the top of food chains, particularly aquatic ones. Importance of the Impacts Probably of greatest importance were the drastic population decreases over large regions or continents of bird species at the top of their food chains. Some of these decreases such as those of the osprey, brown pelican, peregrine falcon, and bald eagle resulted in the extirpation of the species over vast areas of the United States and were grounds for legitimate concern over total extinction of these species. Boundaries of the Problem Effects of DDT in the ecosystem were at first perceived to be local and restricted to areas where DDT was applied, but findings from studies of DDT kept expanding the boundaries of the problem. Eventually, it was

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366 SELECTED CASE STUDIES recognized that DDT residues appeared throughout the world. Studies were conducted, often cooperatively with scientists in other nations, to elucidate the problems wherever they existed, e.g., raptor decline in Eu- rope and residue appearance in the Arctic and Antarctic and in marine environments throughout the Northern Hemisphere. Actions by the United States to resolve the problems, however, were restricted to the control of DDT within the United States. In fact, because DDT manufactured in the United States was superior to others, manufacture for use in international health programs was permitted after the ban on use in the United States took effect. For several years, unfortunately, the manufacturer was less adept at controlling wastes from the manufacturing process than at main- taining purity of the product, so considerable waste DDT and related products continued to be emptied into the Pacific Ocean, with detrimental effects on the brown pelican and other species. Study Strategy Because of the nature of the problem, there was no formal study strategy. Studies simply built on earlier studies. The earliest studies were carried out largely by government scientists, especially fish and wildlife biolo- gists. As results were disseminated, more people became interested in the problem, and more academic scientists began to participate. Extensive, informal cooperation developed among scientists in the United States, Canada, and Great Britain. Results of field and laboratory studies were exchanged, and these results were often used in shaping the work of other investigators. In addition, more formal cooperation was arranged through such international agencies as the North Atlantic Treaty Organization, the Organisation for Economic Co-operation and Development (OECD), and various bodies of the United Nations. Monitoring Measurements of eggshell thickness were made in many areas of North America and Europe by using eggs of predatory birds in museums and in nests. Thinning of 20% or more was found in many species (see Cooke, 1973, for a review of eggshell thinning). The thinning seems to be caused only by DDE, inasmuch as experiments with other chlorinated hydrocar- bons showed thinning only when the other compounds were at nearly toxic concentrations, and it disappeared as soon as signs of toxicity diminished (Haegele and Tucker, 19741. In the years after cancellation of DDT use in the United States and after elimination of industrial discharge by Mon- trose Chemical Company's DDT manufacturing plant, residues in many

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ENVIRONMENTAL EFFECTS OF DDT 367 aquatic species began to decrease, and field studies of predatory birds showed increasing shell thickness and improved reproductive success (U.S. EPA, 1975). Extensive programs for monitoring pesticide residues, including those of DDT and its metabolites, began in the United States during the 1960s under the sponsorship of the Federal Committee on Pest Control. Results of these programs in which sampling and analytical methods were stan- dardized and which covered human food and animal feeds, air, freshwater, estuarine areas, soils, and selected members of the biota were published in the Pesticide Monitoring Journal. Less extensive results were available through a cooperative program sponsored by OECD that provided com- parable data from Canada, the United States, and several European coun- tries. It was in the course of these monitoring studies involving marine species that substances interfering with DDT residue analyses were identified as polychlorinated biphenyls (PCBs). This discovery, by the Swedish chemist Jensen (1966), laid the groundwork for extensive studies of what has turned out to be the most severe nonpesticide chemical contamination problem in the world. Enactment of toxic-substance control legislation in the United States was probably a result of studies on PCBs. Effects of DDT and its metabolites undoubtedly are aggravated by other hydrocarbon residues. Hardly any wild species on which residue analyses have been completed contain only DDT residues, and laboratory studies have shown that many of the other compounds are at least as toxic as DDT. The interaction of these residues is poorly understood. SOURCES OF KNOWLEDGE AND UNDERSTANDING Generally Accepted Ecological Facts Studies of acute toxicity of DDT to birds and fish were undertaken with bioassay methods devised by pollution control biologists and toxicologists. Data on mammals, at least laboratory rats and mice, were available and, in the absence of specific tests on wild mammals, were used to predict effects on wild mammals. Feeding studies were conducted on pheasants and bobwhite quail, which were available because they were routinely raised for release to the wild. Later, to answer specific questions, studies were carried out on species not routinely kept in captivity. Such studies usually required prior development of appropriate husbandry. The captive birds studied eventually included bald eagles, kestrels, cowbirds, mallards, pigeons, and others. Similarly, trout and goldfish were exposed, and LCsoS for 24-48 hours were determined. The aquatic organisms studied included

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368 SELECTED CASE STUDIES other species of fish and a number of invertebrates. Relatively elaborate exposure systems for aquatic species were devised to overcome the prob- lems of DDT adsorption on surfaces and loss to the air through codistil- lation. On the basis of these laboratory-determined estimates of toxicity, nat- uralists observed field applications of DDT for control of forest insects. In addition to observations of deaths of birds and aquatic organisms, analytical chemistry was used to measure DDT residues in organisms from treated areas. General knowlege of food chains, coupled with residue analyses, led to predictions of effects on organisms at higher trophic levels, which were indeed observed. An iterative process of field observation, chemical analysis, laboratory bioassay, and field experimentation was followed, and a reasonable un- derstanding of the movement, concentration, and effects of DDT began to emerge. The ecological theory of food chains and cycling of nutrients (substituting "toxicants" for "nutrients") was used. In the case of de- creasing populations of predatory birds, a hypothesis of pesticide causation emerged. So, too, did a series of hypotheses on sublethal effects operating through behavioral changes e.g., increased stress-and selection of un- desirable temperatures. Some results of field studies of effects on bird populations were sur- prising. In some environments, few dead birds were found, although many should have been, because residue in or on prey insects exceeded the predicted LCso for birds. At the same time, populations of birds did not decrease noticeably. Two kinds of studies were carried out: one to deter- mine disappearance of bird carcasses, the other to determine repopulation. It was hypothesized that only a small fraction of bird carcasses present were found and that, at least in areas of a few to hundreds of acres in relatively homogeneous habitat during the early nesting season, repopu- lation would take place very rapidly. Studies carried out at Patuxent Wild- life Research Center in Laurel, Maryland, confirmed both hypotheses. Some 30-90% of the small-bird carcasses spread along a powerline through a wooded area were not found by trained observers 4 days later; some of the carcasses were simply not seen, but many were later deter- mined to have been buried by beetles or carried away by scavengers. Where 44% of the singing males of nine species of songbirds on a 100- acre tract of bottomland forest were removed by mist netting, the removal was estimated at only one-fourth of the actual removal. Banding data showed that an influx of new birds,which took place immediately after the 3-day removal period, made it impossible to measure accurately the number of birds removed (U.S. FWS, 19631.

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ENVIRONMENTAL EFFECTS OF DDT Theory and General Principles of Ecology 369 Knowledge of trophic interactions and food webs was an inherent part of the studies of accumulation of DDD at Clear Lake, California, and of the studies of robin mortality after DDT spraying for Dutch elm disease control. Mortality of bald eagles and other predators was shown to be caused by DDT (and other pesticides) accumulated through the food webs of which these predators were a part. Eggshell thinning also was caused by food-chain accumulations of DDE, which was formed from ODT by organisms lower in the food chain. The importance of the eggshell thinning and consequent reduced reproductive success was understandable only in terms of population dynamics. The observations of distribution of DDT in field studies and monitoring led Metcalf (1972) to devise microcosms in which radioactively labeled substances could be followed as they were partitioned into different environmental compartments. The Value of Experiments Studies in the 1940s involved treatment of experimental areas with amounts of DDT similar to those used in actual forest insect control programs. It was hoped that the use of control and experimental areas and the study of the areas before and at various periods after treatment would make it possible to detect changes in the nontarget biota, including re- population if depopulation occurred. These studies were helpful in plan- ning large-scale studies. When first introduced in the United States, DDT was believed to be harmless to people and all other valued organisms. Therefore, the regis- tration permitted use in concentrations high enough to be effective. Tol- erances in food were based on the amount that would be present as a result of the approved uses. In the 1950s, DDT residues were discovered in cows' milk, so applications to animal feed crops were reduced to the point where the residues were not detectable in milk (i.e., to below about 1 ppm at that time). Expert Judgment Probably the most outstanding example of the role of expert judgment was that played by trained ornithologists (especially Hickey), who first noted the thinning of eggshells and hypothesized that it was caused by pesticides. In 1965, Hickey had convened an international conference to

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370 SELECTED CASE STUDIES bring together what was known about decreasing peregrine falcon popu- lations (Hickey, 1969). Hickey suggested that pesticide residues were probably responsible for reduced reproduction, primarily through egg de- struction and egg-eating, but there was no mention of shell thinning. In the next several years, the hypothesis of eggshell thinning was formulated. Another pertinent example of expert judgment was provided by Rachel Carson, a marine biologist, who saw and forcefully exposed the effects of widespread pesticide use on the functioning of the natural environment (Carson, 1962~. REFERENCES Adams, L., M. G. Hanavan, N. W. Hosley, and D. W. Johnston. 1949. The effects on fish, birds, and mammals of DDT used in the control of forest insects in Idaho and Wyoming. J. Wildl. Manage. 13:245-254. Anas, R. E., and A. J Wilson. 1970. Residues in fish, wildlife, and estuaries. Organo- chlorine pesticides in fur seals. Pestic. Monit. J. 3:198-200. Anderson, D. W., and J. J. Hickey. 1972. Eggshell changes in certain North American birds. Pp. 514-540 in Proceedings of the 15th International Ornithological Congress, Symposium on Chemical Pollutants. E. J. Brill, Leyden, Neth. Barker, R. J. 1958. Notes on some ecological effects of DDT sprayed on elms. J. Wildl. Manage. 22:269-274. Boyd, C. E., B. Vinson, and D. E. Ferguson. 1963. Possible DDT resistance in two species of frogs. Copeia 1963:426-429. Brown, A. W. A., and R. Pal. 1971. Insecticide Resistance in Arthropods. World Health Organization, Geneva. Buckley, J. L. 1979. Nontarget effects of pesticides in the environment. Pp. 73-81 in Pesticides: Their Contemporary Roles in Agriculture, Health and the Environment. Hu- mana, Clifton, N.J. Burdick, G. E., E. J. Harris, H. J. Dean, T. M. Walker, J. Skea, and D. Colby. 1964. The accumulation of DDT in lake trout and the effect on reproduction. Trans. Am. Fish. Soc. 93:127-136. Carson, R. 1962. Silent Spring. Houghton Mifflin, Boston. Cooke, A. S. 1973. Shell thinning in avian eggs by environmental pollutants. Environ. Pollut. 4:85-152. Cope, O. B. 1961. Effects of DDT spraying for spruce budworm on fish in the Yellowstone River System. Trans. Am. Fish. Soc. 90:239-251. Davison, K. L., and J. L. Sell. 1974. DDT thins shells of eggs from mallard ducks maintained on ad libitum or control-feeding regimens. Arch. Environ. Contam. Toxicol. 2:222-232. Haegele, M. A., and R. H. Hudson. 1973. DDE effects on reproduction of ring doves. Environ. Pollut. 4:53-57. Haegele, M. A., and R. K. Tucker. 1974. Effects of 15 common environmental pollutants on eggshell thickness in mallards and coturnix. Bull. Environ. Contam. Toxicol. 11:98- 102. Helle, W. 1965. Resistance in the Acarina: Mites. Advan. Acarol. 2:71-93. lIickey, J. J., ed. 1969. Peregrine Falcon Populations: Their Biology and Decline. Uni- versity of Wisconsin Press, Madison.

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ENVIRONMENTAL EFFECTS OF DDT 371 Hill, F. F., R. G. Health, J. W. Spann, and D. Williams. 1975. Lethal Dietary Toxicities of Environmental Pollutants to Birds. U.S. FWS Special Scientific Report Wildlife No. 191. U.S. Fish and Wildlife Service, Washington, D.C. Hunt, E. C., and A. I. Bischoff. 1960. Inimical effects on wildlife of periodic DDD applications to Clear Lake, Calif. Calif. Fish Game Bull. 46:91-106. Ide, F. P. 1967. Effects of forest spraying with DDT on aquatic insects in salmon streams in New Brunswick. J. Can. Fish. Res. Bd. 24:769-805. Javaid, M. Y. 1972a. Effect of DDT on the locomotor activity of Atlantic salmon, Salmo salar, in a horizontal temperature gradient. Pak. J. Zool. 4:17-26. Javaid, M. Y. 1972b. Effect of DDT on temperature selection of some salmonids. Pak. J. Sci. Ind. Res. 15:171-176. Jensen, S. 1966. A new chemical hazard. New Sci. 32:612. Metcalf, R. L. 1972. A model ecosystem for the evaluation of pesticide biodegradability and ecological magnification. Outlook Agr~c. 7:55-59. Peakall, D. B., J. L. Lincer, R. W. Risebrough, J. B. Pritchard, and W. B. Kinter. 1973. DDE-induced eggshell thinning: Structural and physiological effects in three species. Comp. Gen. Pharmacol. 4:305-313. Risebrough, R. W., F. C. Sibley, and M. N. Kirven. 1971. Reproduction failure of the brown pelican on Anacapa in 1969. Am. Birds 25:8-9. Robbins, C. S., P. F. Spnnger, and C. G. Webster. 1951. Effects of five-year DDT application on breeding bird population. J. Wildl. Manage. 15:213-216. Sladen, W. J. L., C. M. Menzie, and W. L. Reichel. 1966. DDT residues in Adelie penguins and a crab-eater seal from Antarctica: Ecological implications. Nature 210:670- 671. U.S. EPA (U.S. Environmental Protection Agency). 1975. DDT: A Review of Scientific and Economic Aspects of the Decision to Ban Its Use as a Pesticide. EPA-540/1-75-022. U.S. Environmental Protection Agency, Washington, D.C. U.S. FWS (U.S. Fish and Wildlife Service). 1963. Pesticide-Wildlife Studies: 1963. A Review of Fish and Wildlife Service Investigations During the Calendar Year 1963. FWS Circular 199. U.S. Fish and Wildlife Service, Washington, D.C. Van Velzen, A. C., W. B. Stiles, and L. F. Stickel. 1972. Lethal mobilization of DDT by cowbirds. J. Wildl. Manage. 36:733-739. Woodwell, G. M. 1961. The persistence of DDT in a forest soil. For. Sci. 7:194-196. Committee Comment; The wide use of DDT after World War II for the control of insects that caused public health problems or were agricultural and forest pests created a global environmental problem. Scientists and regulators were unprepared to deal with this problem. Before 1947, the sole concern of regulatory processes for pesticides was protection of purchasers from fraud. The passage of the Federal Insecticide, Fungicide, and Rodenticide Act in 1947 permitted attention to the possible effects of a pesticide on nontarget organisms other than people and domestic animals; but in practice, if the proponent of a use certified that the product was both effective and safe, registration was granted. The regulatory agencies the Food and Drug

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372 SELECTED CASE STUDIES Administration (FDA) and the U. S. Department of Agriculture (USDA)- required additional information from the proponent; until they were sat- isfied, they could withhold registration (USDA) or a tolerance (FDA). However, a proponent could obtain a "protest registration," shifting the burden of proof from the proponent to the government, which had to disprove the proponent's claim. Furthermore, during this period, few on the staff of the pesticide registration office were knowledgeable about fish and wildlife. Little concern for ecological problems of any kind was evident in the regulatory agencies. Scientists were little better prepared to deal with the problems posed by DDT. Toxicologists believed that acute toxic effects of the chemicals were the central issues of concern and that the metabolism of toxic sub- stances invariably resulted in decreased toxicity. The possibility that me- tabolites of DDT might be as toxic as or even more toxic than DDT itself was not considered initially. Ecological investigations were similarly narrow. At first, ecologists concentrated their attention on field observations of areas that had been directly treated with DDT. These studies revealed much about acute tox- icity of DDT to different organisms and rates of recolonization of treated areas. But ecologists were not prepared for the striking phenomena of movement of DDT far from the sites of its application or for the remarkable bioconcentration of DDT that resulted in reproductive failure of top car- nivores. These ideas are now generally accepted, but in the late 1940s and l950s were not. As a result, the first data indicating that DDT was globally distributed and that concentrations were extremely high in the tissues of organisms high on food chains were not believed. The history of research to determine the results of the massive use of DDT and of how those results were achieved reveals strikingly how the state of science at any time constrains the questions that are likely to be asked and the range of answers that are considered reasonable. Had con- cepts of the trophic-dynamic organization of ecological communities been developed before 1950, progress in understanding the roots of the problems caused by DDT might have been much more rapid. Lindemann (1942) had published his pioneering paper on trophic-dynamic ecology, but this perspective had yet to become a part of the thinking patterns of ecologists at the end of World War II. Indeed, as this case study demonstrates, efforts to determine the causes of the effects of DDT were a major stimulus to the development of this field of ecology. Persistence of organic chemicals in their original form, or as toxic metabolites, is now routinely measured as an indicator of likelihood of ecological effects. Bioaccumulation of lipid-soluble chemicals to 104 or 1Os times the concentrations present in the physical environment is now expected as a normal part of food-chain

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ENVIRONMENTAL EFFECTS OF DDT 373 dynamics. Spread of materials far beyond the sites of their application is now considered characteristic of many chemicals in ecological systems. Toxicology has likewise been influenced by research on the effects of DDT. That metabolites of toxins can be toxic is now commonly accepted. Efforts are no longer directed exclusively or even primarily to determining lethal doses of toxins. Much more attention is now paid to sublethal effects that might affect behavior, survival, and population dynamics, because investigators recognize that severe decreases in animal populations can occur in nature without massive direct mortality of adults. As a result, although it can be argued that one "DDT" was inevitable, it is equally clear that another "DDT" would be inexcusable. Striking though these advances are, it is clear that the basic problems encountered in dealing with DDT can express themselves in the future. Metabolites, transport, and bioaccumulation are now routinely investi- gated, but we still know almost nothing about the effects of toxicants in mixtures. Nearly all toxicity studies still deal with chemicals one at a time. In nature, however, organisms encounter potentially toxic chemicals in complex mixtures. How these chemicals interact in the environment and in the bodies of animals to produce different and unexpected effects is still generally unknown. As long as this is true, effects that are unex- pected and difficult to believe or explain are likely. The general recognition that complex mixtures of toxicants require concerted efforts means that the speed with which scientists and regulators can respond to the surprises of the future should be greater than was the case with DDT. Nonetheless, the major lesson of the DDT story would be lost if it did not heighten our awareness of the current state of ignorance about important processes that affect the responses of individual organisms, populations, and ecological communities to toxic materials introduced into the environment. The real basis for banning of DDT was its ecological effects, rather than its effects on human health. Even today, the evidence on human health effects of DDT is inconclusive, whereas the data on adverse eco- logical effects are vast and convincing. Also, the decision to ban DDT, rather than to restrict its use, was based on the conclusion that there was no way to control its movement once it was released into the environment. The decision was made more palatable politically by the rapid evolution of resistance to DDT among crop pests. It is doubtful that the ban would have been proposed or sustained if DDT had not decreased substantially in its effectiveness as a result of evolved resistance. The agreement to allow continued manufacture of high-grade DDT for export for use in public health vector control programs also made the ban politically more acceptable. The assessment of the environmental effects of DDT is a good example

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374 of the interplay between laboratory analyses, field tests, and conceptual developments in both ecology and toxicology. The constraints imposed by the state of both sciences are clear in retrospect. We hope that our awareness of those limits and of the deficiencies in knowledge will make scientists and regulators more alert to evidence that does not fit into our current picture of how the world works. Reference Lindemann, R. L. 1942. The trophic-dynamic concept of ecology. Ecology 23:399-418. SELECTED CASE STUDIES