DDT is the best-known organochlorine pesticide. It was synthesized in 1874, and discovery of its insecticidal activity by Paul Müller in 1939 subsequently led to his receiving the Nobel Prize.90 Early work with heavy applications of DDT resulted in mortality of nontarget organisms,91–93 but it was not until the program to control Dutch elm disease was initiated that the lethal risk caused widespread concern. More than 90 species of birds, particularly American robins (Turdus migra- torius), were found dead in neighborhoods where DDT was applied to trees.47,94–95 Subsequently, a large-scale mortality of insects and other invertebrates was discovered as well; earthworms accu- mulated high concentrations of DDT and metabolites that subsequently proved lethal to robins and other birds that ingested contaminated prey.25
Determination of lethal brain residues of DDT and its metabolites in experimental animals46–51 provided the scientific evidence whereby these die-offs were linked with the DDT group.
It took several additional years to document the major sublethal risk of DDT; that is, the effects of its metabolite DDE on embryotoxicity, eggshell thinning, and related effects that adversely influence avian reproductive success. In Great Britain, Ratcliffe96 initially documented eggshell thinning, depressed reproduction, and population declines of peregrine falcons (Falco peregrinus) and other birds. Experimental studies with birds verified that DDE was primarily responsible for thinning of eggshells and adverse affects on reproduction.97–99 Of the DDT group, DDE residues are usually highest and are found most frequently in environmental samples, particularly at higher trophic levels.100 After application of DDT, DDE residues increase because of breakdown of the parent compound.11,100 The mode of action of DDE in eggshell thinning has been the subject of studies that should be consulted for further information on physiological relationships and structural changes.66,100,101 The latest information indicates that thinning is related to inhibition of prostaglandin synthetase in the eggshell gland mucosa.102
Shortly after the initial work, many studies documented eggshell thinning in 18 families of wild birds in North America104–106 and throughout the world.101–107 In field studies, statistical analyses revealed that DDE was the contaminant primarily responsible for eggshell thinning108–110 and associated lowered productivity.111–112 Generally, thinning of 18 to 20% or more over several years is related to population decline.104 Eggshell thinning and a number of other factors are related to adverse effects of DDE on productivity.112 Despite the devastating effects of DDE on avian pro- ductivity and resultant population decreases described here, this metabolite has caused few docu- mented mortalities in wild adult birds.113–114 Additionally, some segments of the avian fauna, including a raptorial species like the great horned owl (Bubo virginianus), a fish-eating species like the great blue heron (Ardea herodias), and the gray heron (A. cinera), showed minimal effects and no population declines even at the peak of usage of OCs.115–116
The brown pelican is the most sensitive avian species to effects of DDE on reproduction; 3 àg/g in the egg is associated with near total reproductive failure.112 Based on individual eggs,
residues are a more accurate indicator of nest success than eggshell thickness.117 The most extreme incidence of avian eggshell thinning was noted in 1969 on Anacapa Island in southern California;
nearly all eggs of brown pelicans in the colony collapsed under incubating birds.118–120 Eggshell thinning of collapsed eggs was 53% compared with 34% in intact eggs. Only five young pelicans hatched from nearly 1300 nesting attempts in 1969.119 Eggshell thickness and reproductive success were only slightly higher at three colonies of brown pelican in northwestern Mexico in 1969.121 In comparison with other colonies, reproductive success and eggshell thickness were highest at three pelican colonies in the Gulf of California, but productivity was less than normal.118 Residues (lipid basis) in 1969 were extremely high and means ranged from 58 àg/g at Isla Piojo in the Gulf of California, 1310 àg/g at Coronados (northwestern Mexico) to 1818 àg/g at Anacapa Island.118,121 Residues largely originated from a DDT manufacturing plant near Los Angeles; residues remained high and pelicans experienced serious reproductive problems for many years.122 Except in Louisiana (see the endrin section), DDE was primarily responsible for declines of brown pelican populations in the United States and part of Mexico.112,121–123
The peregrine falcon is considered sensitive to reproductive effects from DDE (but also see the section on dieldrin) because there were population declines associated with eggshell thinning and decreased productivity throughout much of its range.107,124–127 The sensitivity of the peregrine falcon to DDE depend not so much on the levels that adversely affect reproductive success as on its very high potential for bioaccumulation. The lowest level of DDE in peregrine eggs that adversely affects reproductive success was estimated at 15 to 20 àg/g.126 However, a recent study more clearly defined this level at near 30 àg/g.128 The peregrine is at the top of a complex food chain and has a far greater capacity to bioaccumulate residues of DDE and other OCs than a more sensitive species such as the brown pelican that is situated at a lower trophic level atop a less complicated food chain. Therefore, quantifying differences in species is complex; the above example with falcons and pelicans demonstrates that many factors affect toxicity of OCs to various segments of the biota.
Other examples of species that experienced widespread declines, primarily related to DDE, included the double-crested cormorant (Phalacrocorax auritus),129,130 osprey (Pandion haliae- tus),132–133 bald eagles (Haliaeetus leucocephalus),134–135 merlins (Falco columbarius),136 great cor- morants (Phalacrocorax carbo),137 Mexican free-tailed bats (Tadarida brasiliensis),138 and other species.
The bald eagle seemed moderately sensitive to DDE with normal reproductive success when sample eggs contained ð 3 àg/g and nearly complete failure when eggs contained Š 16 àg/g.135 The critical level of DDE in eggs of osprey that resulted in reproductive impairment was about 10 àg/g.139 Although the evidence indicated that DDE was primarily related to these declines, some interaction with other contaminants is possible (see the section on dieldrin).
American kestrels (Falco sparverius) seemed tolerant of DDE in eggs; success was apparently unaffected when residues ranged from 5 to 100 àg/g.140 Great blue herons produced fledglings from nests with sample eggs that contained up to 16 àg/g of DDE.141 Pipped great blue heron eggs with viable embryos contained as much as 78 àg/g.142 Viable herring gull eggs collected from an island in the Great Lakes in 1964 contained very high mean residues of DDT (19 àg/g), DDD (6 àg/g), and DDE (202 àg/g); however, productivity was reduced to only about 50% of the normal (pre-DDT) levels143 and returned to normal in 1965, despite persistence of high residues.144 Domestic chickens experienced few effects on eggshell thickness or reproductive success even at high dietary levels of DDT or DDE.145–146 Lundholm66 characterized birds as very sensitive, moderately sensitive, or insensitive to effects of DDE on eggshell thinning that may persist for up to 1 year after dosage ceases.147–148
Although ecotoxicological effects of DDT were demonstrated most often in birds, and to a lesser extent in mammals,149 particularly bats,30,138 other segments of the biota have been affected.
Lake trout (Salvelinus namaycush) fry that absorbed the yolk sac and died contained Š 2.9 àg/g of DDT;150 this apparently had some adverse effect on the population.
Usage of DDT in the United States peaked in 1959 when 78 × 106 pounds were applied, but only one third that amount was used in 1970.1 The primary reason for decline in use, before the ban of nearly all uses of DDT in the United States in 1972,151 was the development of resistance in major invertebrate pests. With the ban in the United States and many other countries, adverse effects of DDT on wildlife decreased, and depressed populations of brown pelicans,112,122 bald eagles,152,153 osprey,154,155 merlins (Falco columbarius),136 double-crested cormorants,156 great cor- morants,137 Mexican free-tailed bats,138 and other species experienced full or partial recovery in much of North America, Europe, and certain other areas. Recent changes in peregrine falcon populations have ranged from small increases to essentially full recovery.157
DDT proved more persistent than first estimated, particularly around sites of heavy contami- nation such as fruit orchards158 other agricultural lands159,160 and manufacturing and formulating plants.122,161–163 DDT use continues in Brazil, Mexico, South Africa, and other countries,164 where it is used primarily for mosquito control3 and in Zimbabwe and possibly other African countries, where it was used for tsetse fly (Glossina spp.) control.165 Residues sufficient to induce eggshell thinning, reproductive effects, and mortality were documented recently in some avian populations including the white-headed black chat (Thamnolaea arnoti) in Zimbabwe.165
Bald eagles were extirpated on Santa Catalina Island in California about 50 years ago. The current breeding population originated from a transplanting program initiated in the 1980s (first egg laid in 1987) and extending into the 1990s. Eggs of eagles on Santa Catalina contained high residues of DDE (25 to 67 àg/g) in 1990; all nests on the island failed.166 The bald eagle transplanting program was initiated because brown pelicans in the Channel Islands were recovering from effects of DDT. In retrospect, it seems unreasonable to continue the transplanting program as long as the serious problems from DDE persist in bald eagles. This tale of response of two species to a pollutant in a common area further emphasizes the complexity of ecotoxicological research.
In Nevada in 1996 mean residues of 2.7 àg/g of DDE in eggs of white-faced ibis (Plegadis chihi) were associated with decreases of 20% in productivity and 18% in eggshell thickness.167 Residues in eggs of ibis were similar to those reported 10 years earlier; residues were apparently accumulated on the wintering ground. In 2000 another study of the white-faced ibis along the Colorado River in Arizona also revealed continuing problems from DDE. Average eggshell thinning of 15% were associated with DDE a mean residue of 2.2 àg/g in eggs apparently was related to poor reproductive success.168
In Canada from 1993 to 1995 American robins occupying fruit orchards were accumulating very high levels (x = 85 àg/g) of DDE several decades after the last use of DDT in the orchards.26 Although these high DDE levels had no demonstrable effect on reproductive success of the robins, predators consuming robins were probably at risk.169 Another study (1988–1994) of DDE persis- tence in Canadian apple orchards revealed that eastern bluebirds (Sialia sialis) in Ontario were accumulating residues as high as 105 àg/g in pooled egg samples.170 There was some indication that organochlorine pesticides were associated with a reduction in reproduction of ð 14% in 4 of 6 years; however, pooling of eggs for analysis probably confounded the conclusions.
From 1994 to 1995 some eggs of double-crested cormorants in Green Bay, Wisconsin contained DDE residues sufficient to reduce hatching success of some eggs; however, there was no apparent effect on cormorant population trends.171
A study of burrowing owls (Athene cunicularia) in 1996 in four areas in southern California revealed no effects of contaminants in eggs on reproductive success or the owls, even though DDE residues in one area averaged 7.5 àg/g and eggshell thinning averaged 42%.172 The extreme thinning of burrowing owl eggshells appears anomalous and was apparently too high. Use of the pre-1947 mean thickness listed by Henny et al.,173 compared to the data from California, indicated 12%
thinning in the most contaminated area and 4% in the least contaminated areas.
The only major problem with DDD occurred in California when it was applied three times from 1949 to 1957 to Clear Lake to control gnats (Haoporus astictopus).174,175 Residues of DDD reached high levels in the biota, especially in western grebes (Aeschmorphorus occidentalis), where
levels (lipid basis) were as high as 1200 àg/g in body fat and 1007 àg/g in eggs. The Clear Lake study was probably the first to document trophic level accumulation that proved so important in explaining the persistence of residues and residual effects of the OCs.177 After the first application of DDD, the number of breeding pairs of western grebes decreased from 1000 in 1949 to none the following year. The western grebe breeding population had increased to only 165 pairs in 1967, and their reproductive success was still poor. The only other known environmental problem from DDD was mortality of a common loon (Gavia immer).178
13.3.2 Aldrin/Dieldrin
These two closely related OCs are very toxic and were involved in numerous incidents of wildlife mortality. When aldrin is applied in the field, it is rapidly broken down to dieldrin; aldrin is found in biological samples only near application sites.179
In 1960 and 1961 aldrin was applied in April to agricultural land in Illinois to control an infestation of Japanese beetles (Popillia japonica). The solid-block application of 2.2 kg/ha resulted in an estimated mortality of 25 to 50% of the adult ring-necked pheasants (Phasianus colchicus) within 1 month.180 Reproduction of pheasants the year of application was severely depressed, as evidenced by the low numbers of chicks and the abnormally high proportion (52 to 56%) of broodless hens, the low ratio of young per adult in autumn, and reduced numbers of cock-calls the following spring. Reproduction on the treated area returned to normal the following year. Dieldrin residues ranged from 2.9 to 15 àg/g in breast muscle of pheasants found dead and from 4.6 to 7.9 àg/g in eggs.180
In experimental studies as little as 1 àg/g of aldrin in the diet caused mortality of 20% of adult ring-necked pheasants.181 Egg production ceased by 10 weeks in hens receiving only 1 or 2 àg/g of aldrin in their diet.184 Fulvous whistling-ducks (Dendrocygna bicolor), snow geese (Chen cae- rulescens), and a number of other birds and invertebrates died after ingesting aldrin-treated rice seed in Texas from the late 1960s until 1974, when this use of aldrin was banned.183,184 Brains of most waterfowl and other birds found dead contained lethal levels of dieldrin as determined by the lower diagnostic lethal level of 5 àg/g in brains of experimental birds receiving dieldrin-contami- nated diets.52 The fulvous whistling-duck population decrease was apparently related to aldrin use.183 The whistling-duck population started to increase after the 1974 ban,185 but the population estimates in the mid-1980s were still less than those of the early 1950s.186
In one of the most vivid examples of the toxicity of dieldrin, Scott et al.187 found virtual elimination or extreme mortality of most species of terrestrial mammals when dieldrin was applied in Illinois to control the Japanese beetle. Dieldrin was also used for a short time in the attempted eradication of the imported fire ant (Solenopsis saevissima) in the southeastern United States.188
Dieldrin induced adverse effects on reproduction of birds in experimental studies,189,190 but there are few data from the field. Shags had low productivity when dieldrin residues reached 2 to 3 àg/g in their eggs.191 Golden eagles (Aquila chrysaetos) in Scotland and brown pelicans in the south- eastern United States seemed to have lowered productivity when dieldrin residues in sample eggs were Š1 àg/g.111,192 However, further investigation seemed to indicate that at least the pelican relationship was spurious because brown pelicans in Louisiana had good productivity when dieldrin residues averaged nearly 1 àg/g in their eggs.112,193,194 Such interpretive problems arise because many of the OC residues are positively intercorrelated; this may confound identification of effect levels of individual compounds because effects of multiple contaminants may or may not be additive. Dieldrin only induced up to 6% shell thinning in eggs of experimental birds;195,196 evidence from field studies also indicated that this OC is unimportant in eggshell thinning.109,132
In the United States dieldrin killed 28 of 444 bald eagles analyzed from 1964 to 1977; however, it was concluded that DDE was the primary factor in the widespread population declines.135 In contrast, several investigators have postulated that dieldrin, in concert with DDT, was responsible for population declines of certain birds including the Eurasian sparrowhawk (Accipiter nisus), the
merlin, and the peregrine falcon in Great Britain,17,197–199 and the peregrine falcon in the eastern United States.200 It was postulated that DDE adversely affected eggshell thickness and reproduction and that dieldrin and related cyclodienes (heptachlor and aldrin) induced mortality of adults in these populations. In the Eurasian sparrowhawk studies the role of dieldrin was emphasized because the population apparently crashed more quickly than could be accounted for by reproductive failure alone.201 Secondary exposure of Eurasian sparrowhawks to dieldrin was mostly through ingestion of birds that had consumed treated seed.
A recent study202 analyzed population trends of Eurasian sparrowhawks from 1963 to 1986;
dieldrin accounted for 29% of sparrowhawks found dead. In conjunction with adverse reproductive problems related to DDE, it was postulated to cause a population decline of 20% per year. The population recovery of Eurasian sparrowhawks and merlins in Great Britain proceeded as residues of dieldrin and DDE declined.203,204
Ratcliffe198 concluded that the dramatic decline of the peregrine falcon population in Great Britain was related to the combined effects of dieldrin, aldrin, and heptachlor (cyclodienes) that were used as seed treatments, soil treatments, sheep dips, and other purposes. DDT was apparently of secondary importance because it was used years before onset of the decline that coincided more closely with initial use of the other three insecticides. Peregrines in the Scottish Highlands during 1962 to 1966 were reproducing well despite a high mean level (1.2 àg/g) of dieldrin in their eggs.205 This seems to reinforce the conclusion that if population declines were attributable to dieldrin, the critical aspect was mortality of adults. In addition, the population in Great Britain increased shortly after restrictions on the cyclodienes were imposed in 1962 and apparently reached the pre-1940 level by 1985.198
Declines of peregrine populations occurred throughout Europe; lowest levels were found in the 1960s and early 1970s.206 Populations increased dramatically in most countries by 1985, but few populations were near pre-1940 levels. The pre-1940 population of 2000 to 3500 pairs in Fenno- scandia decreased to a low of 65 pairs in 1975 and had increased to just 120 to 150 pairs by 1985.207 Newton206 concluded that the cyclodienes were primarily responsible for declines of peregrine populations throughout Europe; DDT played a secondary role in spite of adverse effects on eggshell thickness and reproductive success. In Fennoscandia, however, Lindberg et at.207,208 stressed the role of DDE and polychlorinated biphenyls (OC contaminants of industrial origin) in peregrine declines in that region.
Nisbet200 concluded that declines in peregrine falcon populations in some regions of North America were too rapid to have been caused by reproductive failure alone. Actual and potential exposure of peregrines to dieldrin was considered sufficiently high and widespread by the mid- 1950s to have caused excessive adult mortality. Nevertheless, Nisbet200 concluded that the role of dieldrin in declines of the North American and British populations was based largely on circum- stantial evidence and that other OCs may have been involved. Peakall and Kiff127 concluded that DDE has been and continues to be the pollutant of primary importance adversely affecting peregrine falcon populations.
The gray bat (Myotis grisescens) population occupying a cave in Central Missouri experienced mortality from dieldrin (originating from agricultural applications of aldrin). Lethal levels of dieldrin in brains of gray bats were first noted in 1976, when the population contained 1800 individuals;209 the population was extirpated by 1979. Residues of dieldrin reached 89 àg/g in milk of lactating bats. Beginning in 1977 residues of heptachlor epoxide (heptachlor was intended as a substitute for aldrin) increased and also reached lethal levels in brains of some gray bats. After use of dieldrin and heptachlor was suspended, residues in the bats and their food decreased. Bats then returned to the colony, and the population increased from 8000 to 38,000 by 1994.138 Gray bats at several other caves in central Missouri also died with lethal levels of dieldrin and heptachlor epoxide in their brains.
Except for limited use, aldrin and dieldrin were canceled in the United States in 1974;151 several other countries also banned these pesticides in the 1970s. As a result, problems from these pesticides largely dissipated in these areas. Nevertheless, wildlife mortalities from dieldrin persisted long after