Technical chlordane is a mixture of chlorinated hydrocarbons that has been used as an insecticide since its introduction in 1947. Chlordane was the first cyclodiene insecticide to be used in agriculture and was the second most important organochlorine insecticide in the United States in 1976-77, behind toxaphene, with an estimated annual production of 9 million kilograms (Nomeir and Hajjar 1987). Chlordane is now the leading insecticide in controlling termites, with about 1.2 million homes in the United States alone treated annually for this purpose (Nomeir and Hajjar 1987). Chlordane has been detected in human milk in Canada, Hawaii, Japan, Mexico, Mississippi, and Spain (World Health Organization [WHO] 1984; Ohno et al. 1986). Chlordane compounds have been detected in oysters from the South Atlantic Ocean and Gulf of Mexico, in fish from the Great Lakes and major river basins of the United States, in the blubber of cetaceans from the coastal waters of North America, and the Antarctic atmosphere (Kawano et al. 1988). In fact, all available evidence suggests that chlordane is ubiquitous in the environment. Air and water transport of technical chlordane has resulted in the detection of chlordane and its metabolites in rainwater, drinking water, air, surface waters, soils, sediments, plankton, earthworms, fish, shellfish, birds and their eggs, aquatic invertebrates, cats, dogs, livestock, and humans (Zitko 1978; Environmental Protection Agency 1980; Sudershan and Khan 1980; Kerkhoff and Boer 1982; Wickstrom et al. 1983; Johnson et al. 1986; Nomeir and Hajjar 1987; Suzaki et al. 1988). Despite its widespread use, persistence, and tendency to accumulate in fat, there was no firm evidence of direct lethal or sublethal effects on terrestrial vertebrate wildlife until Blus et al. (1983) recorded several chlordane-related mortalities. A North Dakota marsh treated with chlordane had decreased reproductive success and some deaths of young of several bird species but this was attributed to depletion of invertebrate prey and not to acute poisoning (Hanson 1952). More recently, chlordane was implicated as the principal toxicant in 30 pesticide poisoning cases of hawks, owls, herons, and other birds in New York between 1982 and 1986 (Stone and Okoniewski 1988). The U.S. Environmental Protection Agency (EPA) considers chlordane as a probable human carcinogen (defined as inadequate evidence from human studies and sufficient evidence from animal studies), as judged by chlordane-induced cancer of the liver in domestic mice (Arruda et al. 1987). In 1978, EPA restricted chlordane use to subterranean termite control, nonfood plants, and root dip. Limited agricultural use was permitted until 1980. In 1987, EPA registered chlordane again, limiting its sale and use to licensed applicators for subterranean termite control (Arruda et al. 1987). However, it seems that significant home and garden use exists, especially for control of termites and undesirable lawn insects (Wood et al. 1986). Reviews on ecological and toxicological aspects of chlordane in the environment are available; particularly useful are those by Ingle (1965), Menzie (1974), National Research Council of Canada [NRCC] (1975), International Agency for Research on Cancer [IARC] (1979), EPA (1980, 1988), WHO (1984), Klaassen et al. (1986), and Nomeir and Hajjar (1987). This report was prepared in response to requests for information on chlordane from regional environmental contaminant specialists of the U.S. Fish and Wildlife Service. It is part of a continuing series of brief reviews on chemicals in the environment, with emphasis on fishery and wildlife resources. Chemical and Biochemical Properties Technical chlordane (64 to 67 % chlorine) is produced by the condensation of cyclopentadiene and hexachlorocyclopentadiene to yield chlordene (Figure). Addition of chlorine across the 2-3 olefinic bond of chlordene forms cis-chlordane and trans-chlordane; substitution of chlorine into position 1 of chlordene forms heptachlor, and further addition of chlorine across the 2-3 olefinic bond forms cis-nonachlor and trans-nonachlor (Ribick and Zajicek 1983). Technical chlordane includes about 45 components. Its approximate composition is 19% cis-chlordane (C10H6Cl8), 24% trans-chlordane (C10H6Cl8), 21.5% chlordene isomers (C10H6Cl6), 10% heptachlor (C10H5Cl7), 7% cis- and trans-nonachlor (C10H5Cl9), 2% Diels-Alder adduct of cyclopentadiene and pentachlorocyclopentadiene, 1 % hexachlocycloropentadiene, 1 % octachlorocyclopentene, and 15.5% miscellaneous constituents (NRCC 1975; IARC 1979; EPA 1980; WHO 1984). Oxychlordane and heptachlor epoxide are toxicologically significant degradation products (Figure; Perttila et al. 1986). Chlordane produced before 1951 contained a significant quantity of hexachlorocyclopentadiene--a toxic irritant to warm-blooded animals; chlordane produced after 1951 contains little or none of this compound (Ingle 1965). A high-purity chlordane formulation containing about 74% cis-chlordane and 24% trans-chlordane is also available (Nomeir and Hajjar 1987).

ingredients were still measurable; in another study, 15 % of the active ingredients remained in turf soils after 15 years (WHO 1984). Cis- and trans-chlordanes were less persistent in mineral soils than in organic mucky soils (WHO 1984). Chlordanes were usually detected in surface soils of basins receiving urban runoff water at a maximum concentration of 2.7 mg/kg; this decreased with soil depth to <0.03 mg/kg at depths below 24 cm (Nightingale 1987). Chlordane levels in soils near Air Force bases in the United States in 1975-76 were similar to those found in nonmilitary urban environments (Lang et al. 1979). Chlordanes in sediments usually were highest in those sediments with the highest organic content, especially downstream from the center of anthropogenic activities (Smith et al. 1987). Sediments from a lake in which the overlying water column initially was treated to contain 10 g technical chlordane per liter contained measurable residues 2.8 years after application: total chlordanes--consisting of cis-chlordane, trans-chlordane, and trans-nonachlor--averaged 20 g/kg and ranged up to 46 g/kg (Albright et al. 1980). The yearly flux of chlordanes from sediments to the overlying water column has been estimated at 0.02 g/m2, based on measurements made in the Sargasso Sea and deep North Atlantic Ocean between 1978 and 1980 (Knap et al. 1986). Terrestrial Crops Maximum total chlordane concentrations in corn (Zea mays) and sorghum (Sorghum halepense) samples collected nationwide in 1971, in /kg dry weight, were 480 in corn kernel, 1,260 in cornstalk, and 420 in sorghum (Carey et al. 1978); these values were somewhat lower in 1972: 150 in kernels, 410 in stalks, and 150 in sorghum (Carey et al. 1979). Concentrations in various crops grown in soils treated with 15 kg technical chlordane per hectare were always <260 g/kg dry weight when clay content was 12 %, and < 150 g/kg when clay content was 28% (WHO 1984). Table 1. Chlordane concentration in selected nonbiological samples. Sample, units of measurement, chlordane Isomer, and other variables Concentrationa Referenceb
_________________________________________________________________________________________ Air, in ng/m3 Between Bermuda and Rhode Island, February June 1973, total chlordanes United States, 16 States 2,477 of 2,479 samples 2 samples Southern Hemisphere, 198084, various locations, total chlordanes Northern Hemisphere, 197378, Atlantic Ocean, total chlordanes Pacific Ocean, 197981, total chlordanes Canadian Arctic, summer 1984 cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor Fresh water, in ug/L Nova Scotia cis-chlordane (ND to 31.3) 1 ~0.0015 (0.00050.002) (ND to 0.0004) ~0.4 (0.0090.084) 0.3 (0.0050.19) 3 ND 84,2 (<0.0050.9) 1

trans-chlordane cis-nonachlor trans-nonachor oxychlordane total chlordanes Zooplankton, North Pacific Ocean, 198082, whole cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor oxychlordane total chlordanes Fish Goby, Acanthogobius flavimanus, Tokyo Bay, Japan, 1978 whole cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor oxychlordane White shark, Carcharodon carcharius, liver, east coast of Canada, 1971 cis- and trans-chlordanes cis-nonachlor trans-nonachlor Baltic herring, Clupea harengus, Baltic Sea, 197882, whole Total chlordanes Atlantic herring, Clupea harengus harengus, oil, east coast of Canada, 1977 cis- and trans-chlordanes cis-nonachlor trans-nonachlor Lake whitefish, Coregonus clupeaformis Great Lakes, 1978, whole cis-chlordane trans-chlordane total chlordanes Lake Superior, Siskiwit Lake, Isle Royale, 1983, whole chlordanes nonachlors oxychlordane
5.7 FW 3.7 FW 4.4 FW 0.3 FW 21.0 FW 19 (1327) LW 13 (720) LW 5 (3.28.7) LW 14 (1215) LW 3 (2.33.8) LW 54 (4072) LW
6 FW; Max. 62 FW 9 FW; Max. 15 FW 8 FW; Max. 21 FW 18 FW; Max. 120 FW 3 FW; Max. 25 FW
11, 12 11, 12 11, 12 11, 12 11, 12
2,600 LW 1,700 LW 8,500 LW

(200600) LW (400800) LW

(40110) LW Max. 30 LW Max. 170 LW
(1694) FW (2187) FW 111 FW 260 LW; Max. 330 LW 450 LW; Max. 500 LW 16 LW; Max. 200 LW
Common carp, Cyprinus carpio Great Lakes, 1979, whole cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor San Joaquin River, California, 1981, whole Total chlordanes Shad, Dorosoma spp., Louisiana, 197879, whole body cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor Northern pike, Esox lucius, Baltic Sea, 197182 Total chlordanes Muscle 1982 Liver 1982 Fish, 2 species, muscle, Belmont Lake, Long Island, New York Total chlordanes Fish, 4 species, Chesapeake Bay, Maryland, 197680 Total chlordanes Muscle Gonad Fish, 4 species, eastern Finland, 197982 Liver cis-chlordane trans-chlordane (ND to 76) FW (ND to 277) FW 70120 FW; Max. 310700 FW (101,900) FW 3805,200 FW 18 (100400) LW (100300) LW 500 LW 600 LW 700 LW 700 LW (1,1002,100) LW 13 (1001,000) LW (1001,300) LW 100 LW 800 LW 1,900 LW (2,6003,100) LW (2,3006,300) LW 13 Max. 76 FW Max. 82 FW Max. 26 FW Max. 12 FW Max. 273 FW; Max. 3,578 LW 17 Max. 390 FW Max. 360 FW Max. 390 FW Max. 300 FW 16 16
trans-nonachlor total chlordanes Muscle cis-chlordane trans-chlordane trans-nonachlor total chlordanes Fish, 11 species, Lake Texoma, Texas and Oklahoma, 1979 Total chlordanes Whole fish Fish, Mississippi River, 198486 Total chlordanes Shovelnose sturgeon, Scaphirhynchus platyrynchus Muscle Eggs Common carp, muscle Channel catfish, Ictalurus punctatus, muscle Fish, Mississippi River, 1988, muscle Total chlordanes Channel catfish Common carp Freshwater drum, Aplodinotus grunniens Flathead catfish, Pylodictis olivaris River carpsucker, Carpiodes carpio Smallmouth buffalo, Ictiobus bubalus Sauger, Stizosteiden canadense Paddlefish, Polyodon spathula Blue catfish, Ictalurus furcatus Bigmouth buffalo, Ictiobus cyprinellus White bass, Morone chrysops Fish, Missouri River, 198486 Total chlordanes, 3 locations Shovelnose sturgeon Muscle Eggs Channel catfish, muscle Common carp, muscle Fish, Missouri River, 1988, muscle Near Rockport, 6 species total chlordanes heptachlor epoxide heptachlor

cis-chlordane cis-nonachlor oxychlordane Carcass (less GI tract, skin, feet, beak) Chesapeake Bay, Maryland, winter cis-chlordane trans-nonachlor oxychlordane Birds, 4 species, eastern and southern United States, 197274, egg, total chlordanes Birds, New York State, 198286, found dead or debilitated, brain tissue, chlordane implicated as primary cause of distress Cooper's hawk, Accipiter cooperii oxychlordane heptachlor epoxide trans-nonachlor Sharp-shinned hawk, Accipiter striatus oxychlordane heptachlor epoxide trans-nonachlor Great blue heron oxychlordane heptachlor epoxide Great horned owl, Bubo virginianus oxychlordane heptachlor epoxide trans-nonachlor Blue jay, Cyanocitta cristata oxychlordane heptachlor epoxide trans-nonachlor Eastern screech owl, Otus asio oxychlordane heptachlor epoxide trans-nonachlor Common grackle, Quiscalus quiscula
<1,000 FW ND <1,000 FW
ND 9,000 FW ND 11,000 FW ND 5,000 FW <100 FW
Max. 5,800 FW Max. 4,300 FW Max. 1,300 FW Max. 4,300 FW Max. 3,500 FW Max. 1,000 FW Max. 2,400 FW Max. 600 FW Max. 8,700 FW Max. 7,700 FW Max. 2,300 FW Max. 5,000 FW Max. 3,700 FW Max. 2,000 FW Max. 2,600 FW Max. 1,800 FW Max. 1,800 FW
oxychlordane heptachlor epoxide Eastern bluebird, Sialia sialis oxychlordane heptachlor epoxide European starling, Sturnus vulgaris oxychlordane heptachlor epoxide trans-nonachlor American robin, Turdus migratorius oxychlordane heptachlor epoxide trans-nonachlor Cackling Canada goose, Branta canadensis minima, 197374, carcass, breeding areas, total chlordanes Uncontaminated Contaminated (Oregon, California) Immature male Adult male Adult female Common goldeneye, Bucephala clangula, fat, oxychlordane On arrival at wintering grounds, New York Juveniles Adults Just before to spring migration Adults Dunlin, Calidris alpina, Washington State, 1980, whole Total chlordanes Peregrine, Falco peregrinus, Alaska, 197984, egg trans-nonachlor oxychlordane Atlantic puffin, Fratercula arctica, Hornoy, Norway, 198283, oxychlordane plus trans-nonachlor Adults Uropygial gland Liver Chicks Brain Chicken, Gallus sp., contaminated through use of former chlordane container to hold cage disinfectants, Australia Egg Pullets, fat 30 weeks old
Max. 10,800 FW Max. 9,100 FW Max. 3,000 FW Max. 2,200 FW Max. 7,700 FW Max. 5,000 FW Max. 500 FW Max. 1,300 FW Max. 2,700 FW Max. 1,900 FW
<1 FW <0.2 FW 1.7 FW 2.0 FW
40 (10300) LW 220 (120370) LW 250 (190320) LW Max. 60 FW Max. 290 FW 130 FW; Max. 960 FW
1,429 (482,815) LW 93 (2621,531) LW 833 (4451,289) LW

River otter, Lutra canadensis, liver, Alberta, Canada, 198083 cis-chlordane oxychlordane Gray bat, Myotis grisescens, Missouri, 197677, found dead Brain cis-chlordane trans-nonachlor oxychlordane Carcass cis-chlordane trans-nonachlor oxychlordane Pacific walrus, Odobenus rosmarus divergens, oxychlordane, blubber Alaska, 198184 Soviet Union, 1984 Saimaa ringed seal, Phoca hispida saimensis, Finland, 197781 Total chlordanes Blubber Liver Muscle Harbor seal, Phoca vitulina, Netherlands, blubber trans-nonachlor oxychlordane Dall's porpoise, Phocoenoides dalli, North Pacific Ocean, 198082, blubber cis-chlordane trans-chlordane cis-nonachlor trans-nonachlor oxychlordane total chlordanes Raccoon, Procyon lotor, Louisiana, 197879, muscle cis-chlordane trans-chlordane Gray squirrel, Sciurus carolinensis, Jacksonville, Florida, 1974, fat nonachlors oxychlordane Max. 110 LW Max. 62 LW 17 FW 17 FW 440 (360550) LW 63 (5373) LW 270 (240310) LW 1,800 (1,6002,000) LW 250 (160340) LW 2,800 (2,7003,000) LW 2,700 LW 3,000 LW 590 (1101,700) LW 200 (10400) FW 20 (1030) FW FW 100 FW 6,300 (15,000108,000) LW 159,000 (91,000252,000) LW 68,000 (16,000167,000) LW 71 Max. 1,000 FW Max. 2,100 FW Max. 2,300 FW 71 Max. 6 FW Max. 13 FW 70 70
_________________________________________________________________________________________ aConcentrations are shown as mean, extremes in parentheses, maximum (Max.), and nondetectable (ND).
bRisebrough et al. 1983; 2, DouAbul et al. 1988; 3, Rosales et al. 1979; 4, Kawano et al. 1988; 5, Kawano et al. 1986; 6, Zitko 1978; 7, Evans et al. 1982; 8, Ray et al. 1983; 9, IARC 1979; 10, Dowd et al. 1985; 11, Yamagishi et al. 1981; 12, Miyazaki et al. 1980; 13, Moilanen et al. 1982; 14, Kaiser 1982; 15, Swackhamer and Hites 1988; 16, Kuehl et al. 1980; 17, Saiki and Schmitt 1986; 18, Kuehl et al. 1983; 19, Eisenberg and Topping 1985; 20, Pyysalo et al. 1981; 21, Pyysalo et al. 1983; 22, Hunter et al. 1980; 23, veith et al. 1981; 24, Schmitt et al. 1985; 25, Wickstrom et al. 1981; 26, Albright et al. 1980; 27, Zitko and Saunders 1979; 28, DeVault et al. 1986; 29, Hall et al. 1979; 30, Heinz et al. 1980; 31, White 1979; 32, Prouty and Bunck 1986; 33, Haseltine et al. 1980; 34, Stendell et al. 1977; 35, White et al. 1979; 36, Klaas et al. 1980; 37, Anderson et al. 1984; 38, Foley and Batcheller 1988; 39, Schick et al. 1987; 40, Ambrose et al. 1988; 41, Ingebrigtsen et al. 1984; 42, Reece et al. 1985; 43, Barbehenn and Reichel 1981; 44, Kaiser et al. 1980; 45, Reichel et al. 1984; 46, Szaro et al. 1979; 47, Peakall et al. 1986; 48, Ohlendorf et al. 1982; 49, Blus et al. 1985; 50, Wiemeyer et al. 1987; 51, Littrell 1986; 52, Wiemeyer et al. 1988; 53, De Weese et al. 1986; 54, White et al. 1980; 55, Nickerson and Barbehenn 1975; 56, Cain and Bunck 1983; 57, Bunck et al. 1987; 58, Elliott et al. 1988; 59, Shaw 1984; 60, King and Krynitsky 1986; 61, Clark and Prouty 1976; 62, EPA 1980; 63, Petterson et al. 1988; 64, Muir et al. 1988; 65, Perttila et al. 1986; 66, Wickstrom et al. 1983; 67, Tojo et al. 1986; 68, Wariishi et al. 1986; 69, WHO 1984; 70, Somers et al. 1987; 71, Clark et al. 1980; 72, Helle et al. 1983; 73, Kerkhoff and Boer 1982; 74, Nalley et al. 1978; 75, Bush and Grace 1989; 76, Schmitt et al. 1990; 77, Kubiak et al. 1989; 78, Fitzner et al. 1988; 79, Stone and Okoniewski 1988; 80, Blus and Stafford 1980; 81, Blus et al. 1979; 82, S. Wiemeyer, Patuxent Wildlife Research Center, personal communication; 83, Taylor et al. 1989; 84, Glynn et al. 1989; 85, Loganathan et al. 1989. Fishes Health advisories have been issued near Lawrence Kansas, based on chlordane levels in edible fish tissues. In fish from the Kansas River, Kansas, in 1986, chlordanes were detected more frequently and at higher levels than other contaminants measured (Arruda et al. 1987). More than 80% of the sites sampled in Kansas had detectable chlordanes in fish; at more than 50% of these sites, levels exceeded 0.1 mg/kg fresh weight--a guideline for the protection of predatory fish. At three urban sites in Kansas, concentrations of chlordanes in fish have approached or exceeded the Food and Drug Administration action level of 0.3 mg chlordane per kilogram of fresh weight for protection of human health. The most likely source of chlordane in fish from the Kansas River is urban and suburban use of chlordane as a termite control agent (Arruda et al. 1987). Other health advisories based on chlordane contamination have been issued. In 1985, people were warned not to eat shovelnose sturgeon (Scaphirhynchus platyrynchus) from the Missouri and Mississippi rivers. In 1987, advisories warned against the consumption of sturgeon from the Missouri River between Kansas City and St. Louis, and against bullhead catfishes, suckers, carps, sturgeons, and sturgeon eggs from the Mississippi River near St. Louis (Bush and Grace 1989). Chlordane residues were detected in 36% of all fish samples collected in major domestic watersheds in 1976 (Veith et al. 1979). In the Great Lakes region in 1979, chlordane residues in fish tissues exceeded 100 /kg on a fresh weight basis in about 40% of the samples measured; residues were highest in samples collected near Alton, Illinois, and Fairborn, Ohio (Kuehl et al. 1983). The two most abundant components of technical chlordane found in fish tissues from Tokyo Bay, Japan, were trans-nonachlor and cis-chlordane (Yamagishi et al. 1981 b; Table 2). However, this may vary between locales. For example, cis-chlordane and trans-chlordane were the most abundant components in fish samples collected throughout Japan during the past 20 years, followed, in order, by cis-nonachlor, trans-nonachlor, and oxychlordane (Loganathan et al. 1989). Of the total chlordanes measured in muscle of northern pike (Esox lucius) from the Baltic Sea, 37% was cis-chlordane, 34% trans-chlordane, and 15% each trans-nonachlor and oxychlordane ((Esox lucius) and Baltic herring (Moilanen et al. 1982). For liver tissue of northern pike, 35 % was oxychlordane, 28% trans-chlordane, 22% cis-chlordane, and 14% trans-nonachlor ((Esox lucius) and Baltic herring (Moilanen et al. 1982). In the United States, only chlordanes and nonachlors have been detected as significant residues in fish collected nationwide. The most abundant component was cis-chlordane, followed by trans-nonachlor, trans-chlordane, and cis-nonachlor (Ribick and Zajicek 1983). The two most abundant components were detected in about 93 % of all fish samples collected in 1978 and 1979; residues were usually highest in Hawaii, the Great Lakes, and the Corn Belt (Ribick and Zajicek 1983). Fish from Manoa Stream in Hawaii had high residues because of heavy use of technical chlordane in pineapple culture and termite control (Ribick and Zajicek 1983). Nationwide monitoring of freshwater fishes showed that chlordane concentrations in

whole fish did not change from 1980 to 1994, following a period of decline; however, trans-nonachlor replaced cis-chlordane as the most abundant component, suggesting a lower influx of chlordane to the aquatic environment from terminated use of chlordane in agriculture in the mid- 1970's (Schmitt et al. 1990; Table 2). Residues of cis-chlordane and trans-nonachlor--the most abundant and persistent of the chlordane components measured --were present at 85 and 89% of the stations sampled in 1984 (Schmitt et al. 1990). Maximum chlordane levels in fish in 1984 occurred in the Great Lakes, Hawaii, watersheds of the Ohio, Missouri, and Mississippi rivers, and in the Delaware and Raritan rivers in the Northeast (Schmitt et al. 1990). Atmospheric transport may be the main source of chlordane in Finland --a country that prohibits chlordane use because chlordanes are distributed evenly in the Finnish environment (Pyysalo et al. 1983). No chlordane compounds were detected in rainbow trout (Oncorhynchus mykiss) taken from lakes in eastern Finland, although measurable residues were detected in other fish species. This phenomenon is attributed to the superior ability of rainbow trout to metabolize chlordanes to oxychlordane (Pyysalo et al. 1981). Amphibians and Reptiles Chlordane residue data for amphibians and reptiles are extremely limited. Maximum concentrations of chlordane isomers did not exceed 70 g/kg FW of oxychlordane in eggs of the American crocodile, Crocodylus acutus, or 250 g/kg FW in carcass of the common garter snake, Thamnophis sirtalis (Table 2). However, California newts, Taricha torosa, taken near a lake treated with 10 g/L technical chlordane had greatly elevated chlordane residues in liver and comparatively low concentrations in carcass, stomach, and stomach contents. After 14 days, livers contained about 34 mg/kg total chlordanes lipid weight--about 19% chlordanes, 9% nonachlors, and 6% chlordanes (Albright et al. 1980). After 2.8 years, 98% of the total chlordanes was lost. Trans-nonachlor was the most persistent component in newt liver, accounting for up to 55% of the total chlordanes in specimens collected 2.8 years after application (Albright et al. 1980; Table 2). Birds Technical chlordane components and their metabolites--especially oxychlordane--are comparatively elevated in tissues with high lipid content, in older birds, and in raptors (Table 2). Chlordane isomers occur frequently in birds collected nationwide. In 1976, for example, 41 % of European starlings (Cain and Bunck 1983). In 1982, oxychlordane was detected in 45 % of all starlings analyzed, transnonachlor in 40%, cis-nonachlor in 9%, and cis- and trans-chlordanes in fewer than 2% (Bunck et al. 1987). Chlordane isomers were detected at frequencies exceeding 50% in wings of American black ducks (Anas rubripes) and mallards (Anas platyrhynchos) from the Atlantic Flyway in 1976-77 (White 1979), in eggs of 19 species of Alaskan seabirds in 1973-76 (Ohlendorf et al. 1982), and in carcasses of ospreys (Pandion haliaetus) found dead in the eastern United States between 1975 and 1982 (Wiemeyer et al. 1987). Frequency of detection for chlordane isomers ranging between 14 and 40% has been reported in wings of American black ducks and mallards from flyways other than the Atlantic Flyway (White 1979), in 19 species of passeriformes from the western United States in 1980 (DeWeese et al. 1976), and in 7 species of Texas shorebirds in 197677--although residues in shorebirds were below levels known to adversely affect reproduction or survival (White et al. 1980). Carcasses of bald eagles (Haliaeetus leucocephalus) collected between 1978 and 1981 usually contained oxychlordane at 45 to 56% frequency, trans-nonachlor at 62 to 74%, cis-chlordane at 38 to 45%, and cisnonachlor at 38 to 47%. Frequency of occurrence in the brain was lower, ranging between 19 and 55% for individual isomers (Reichel et al. 1984). However, a positive correlation was established in bald eagles between concentration of chlordanes in brain on a fresh weight basis and in carcass on a lipid weight basis; this relation seems to extend to other birds as well (Barbehenn and Reichel 1981). Bald eagles also contained appreciable quantities of other organochlorine compounds, and a few--for example, dieldrin--were sometimes present at concentrations considered life-threatening (Reichel et al. 1984). A similar situation exists in other species of raptors (Ambrose et al. 1988). Some chlordane isomers tend to persist in avian tissues for lengthy periods. In northern gannets (Sula bassanus), the half-time persistence of cis-chlordane, cis-nonachlor, and oxychlordane was estimated at 11.2, 19.4, and 35.4 years (Elliott et al. 1988). Oxychlordane residues in the thick-billed murre (Uria lomvia) tend to be high because of rapid excretion through uropygial gland secretions of cis- and trans-chlordanes and

nonachlors, and to biotransformation of these and other chlordane components to oxychlordane (Kawano et al. 1988). This observation is alarming because the metabolite oxychlordane has proven much more toxic and persistent than the parent chemicals (Kawano et al. 1988). Secondary poisonings of raptors after consumption of poisoned bait or prey that had accumulated a large quantity of chlordane were documented for the redshouldered hawk (Buteo lineatus) and the great horned owl (Bubo virginianus); concentrations of oxychlordane and heptachlor epoxide found in brain and carcass of both species (Blus et al. 1983) were within the lethal range reported in experimental studies (Stickel et al. 1979). Chlordane-induced mortality of the long-billed curlew (Numenius americanus) has been documented at least four times since 1978, despite restriction of technical chlordane use since 1980 to subterranean applications for termite control (Blus et al. 1985). Death of these curlews was probably due to over-winter accumulations of oxychlordane of 1.5 to 5.0 mg/kg brain FW and of heptachlor epoxide at 3.4 to 8.3 mg/kg--joint lethal ranges for oxychlordane and heptachlor epoxide in experimental birds compared with 6 mg/kg brain for oxychlordane alone, and 9 mg/kg for heptachlor epoxide alone (Blus et al. 1985). Additional research is needed on toxic interactions of chlordane components with each other and with other chemicals in the same environment. Mammals Chlordane levels in mammals were usually highest in lipids, in animals collected near areas of high chlordane use, and in aquatic mammals, especially marine species (Table 2). Biomagnification of total chlordane through the food chain was strongly evident in marine mammals; chlordanes were concentrated gradually from zooplankton, through squid and fish, to porpoises and dolphins (Kawano et al. 1986; Muir et al. 1988; Table 2). Chlordane residues in marine mammals were positively related to lipid content and not to the age of the animal (Perttila et al. 1986). A high death rate over a 2-year period was evident in the little brown bat (Myotis lucifugus) following application of chlordane; young bats were most affected in the first year after application and adults in the second year (Kunz et al. 1977). Residues were greatly elevated in the brain and carcass of another bat, the gray bat (Myotis grisescens)-an endangered species--found dead near areas of high chlordane use (Table 2). Chlordane levels in human blood were comparatively elevated among individuals living in residences treated with chlordane during the past 5 years, and in termite control operators; oxychlordane levels were usually significantly higher than trans-nonachlor except among those who consumed large quantities of fish (Wariishi et al. 1986; Wariishi and Nishiyama 1989). Lethal and Sublethal Effects General Chlordane has been applied extensively to control pestiferous soil invertebrates, usually at rates between 0.6 and 2.24 kg/ha; within this range sensitive nontarget species, especially earthworms, were adversely affected. Nominal water concentrations between 0.2 and 3.0 g/L were harmful to various species of fish and aquatic invertebrates. Effects included a reduction in survival, immobilization, impaired reproduction, histopathology, and elevated chlordane accumulations. Cis-chlordane, when compared with trans-chlordane, was more toxic, preferentially stored, and concentrated to a greater degree. In aquatic organisms, cis-chlordane photoisomers were frequently more toxic than the parent form. Oxychlordane was not a major metabolite in aquatic fauna. Sensitive bird species had reduced survival after consumption of diets as low as 1.5 mg chlordane per kilogram of ration, or after a single oral dose as low as 14.1 mg/kg BW; accumulations were documented in tissues following consumption of diets containing 0. 1 to 0.3 mg chlordane per kilogram of feed. Oxychlordane was the most persistent metabolite in avian brain tissue. Concern for the continued widespread use of chlordane centers on its ability to cause liver cancer in domestic mice. Other adverse effects in mammals, such as elevated tissue residues and growth inhibition, were frequently associated with diets containing between 0.76 and 5.0 mg chlordane per kilogram of feed. Metabolism of technical chlordane by mammals results primarily in oxychlordane, a metabolite that is about 20 times more toxic than the parent compound and the most persistent metabolite stored in adipose tissues.

Red-winged blackbird, Agelaius phoeniceus, fed diets containing 10 mg/kg for 84 days 50 mg/kg for 42 days 100 mg/kg for 21 days Plus 3 or 7 days off dosage 200 mg/kg diet Mallard, Anas platyrhynchos Single oral dose, age 45 months, 1,200 mg/kg BW LD50 Hudson et al. 1984 Residue of 1.8 mg cis-chlordane per kilogram body weight (BW), fresh weight (FW) Whole body cis-chlordane content of 9.2 mg/kg FW Whole body cis-chlordane content of 14.8 mg/kg FW Whole body cis-chlordane content of 5.4 and 2.6 mg/kg FW, respectively LD50 within 9 days Stickel et al. 1983 Stickel et al. 1983 Stickel et al. 1983 Stickel et al. 1983 Stickel et al. 1983

Effect

Reference
858 mg/kg diet for 5 days followed by 3 days of clean diet, ducklings age 10 days 709 mg/kg diet Birds, 4 species, from marsh treated with 1.12 kg chlordane per hectare
LD50 LD50 No reproduction in blue-winged teal (Anas discors) and northern shovelers (Anas clypeata); reproduction inhibited by 60% in coots (Fulica americana) and red-winged blackbirds (Agelaius phoeniceus); disruption of food cycles in marsh was probable cause
Hill et al. 1975 NRCC 1975 NRCC 1975
Birds, 4 species, fed diets containing 71% cis-chlordane and 23% trans-chlordane at 50500 mg/kg diet
Oxychlordane concentrations in brain of dead birds ranged from 9.422.1 mg/kg FW in brown-headed cowbirds (Molothrus ater), common grackles (Quiscalus quiscula), and red-winged blackbirds. In European starlings (Sturnus vulgaris), oxychlordane ranged from 5.0 to 19.1 mg/kg FW in birds that died, and from 1.4 to 10.5 mg/kg FW in sacrificed birds

Stickel et al. 1983

Birds, 3 species, fed diets containing 150 mg technical chlordane per kilogram California quail, Callipepla californica Single oral dose of 14.1 mg/kg BW Northern bobwhite, Colinus virginianus 10120 mg/kg diet for 14 weeks 250 mg/kg diet for 10 days, juveniles 250 mg/kg diet for 100 days, adults Japanese quail, Coturnix japonica 25 mg/kg diet, 4 weeks 200 mg/kg diet, 7 days 14-day-old chicks fed treated diets for 5 days, then untreated diets for 3 days 203 mg/kg diet 308 mg/kg diet 370 mg/kg diet 500 mg/kg diet Chicken, Gallus sp. Fed diet containing 0.1 mg/kg for 6 weeks Adults fed diet containing 0.3 mg/kg for 4 weeks Fed diet containing 10 mg/kg for 5 days 220230 mg/kg BW Ring-necked pheasant, Phasianus colchicus Single oral dose of 2472 mg/kg BW 50 mg/kg diet for 100 days, juveniles 318 mg/kg diet 430 mg/kg diet for 5 days, then clean diet
LD50 reached in 67 days for starlings, cowbirds, and red-winged blackbirds LD50 LD50 LD50 LD50 No effect on survival, weight gain, or activity LD100

Chlordane interactions with other agricultural chemicals are significant and merit additional research. In one study, male Japanese quail (Coturnix japonica) pretreated for 8 weeks with 10 mg chlordane per kilogram of diet had increased resistance to parathion, but not to paraoxon, as judged by cholinesterase activity (Ludke 1977). In another study, northern bobwhites (Colinus virginianus) treated with 10 mg chlordane per kilogram of diet for 10 weeks, followed by endrin stress, had greater accumulations of chlordane in the brain than did birds treated only with chlordane (Ludke 1976). Mammals Concern for the continued widespread use of chlordane is centered around its carcinogenicity in mice, Mus sp. (Ewing et al. 1985). Chlordane produced liver cancer in both sexes of two different strains of domestic mice (EPA 1980; WHO 1984; Tojo et al. 1986; Table 5). A dose-dependent incidence of hepatocellular carcinoma was evident in mice fed chlordane in their diets; frequency of liver carcinomas was not significantly different from controls at dietary levels of 5 mg/kg and lower but were greatly elevated (i.e., 70% frequency) at dietary levels of 50 mg/kg and higher (EPA 1980). In contrast to mice, chlordane was not a hepatic carcinogen in rats at dietary levels up to 64 mg/kg ration (WHO 1984; EPA 1988); however, a dose-related increase in follicular cell thyroid neoplasms and malignant fibrous histocytomas was recorded in chlordane-exposed rats Ohno et al. 1986). In humans, no increased evidence of cancer was proven among employees in chlordane manufacturing facilities, although there was a statistically significant increase in death rate from cerebrovascular disease in that group (Klaassen et al. 1986). Human toxicity data for chlordane usually are obtained after accidental exposure through spillage onto clothing or ingestion (Ingle 1965; NRCC 1975; EPA 1980). In one case, a 15-month-old girl accidentally swallowed a mouthful of chlordane suspension and within 3 h displayed tremors and incoordination. Repeated seizures developed and she was treated with ethyl chloride, amobarbitol, and gastric lavage with magnesium sulfate; ataxia and excitability disappeared in about 3 weeks. At age 26, she was in excellent health and seemed not to have experienced latent effects from the childhood incident (WHO 1984). Other cases of accidental chlordane poisoning in children are documented, and all seem to have recovered completely after treatment (WHO 1984). Symptoms of acute chlordane poisoning in humans include irritability, salivation, labored respiration, muscle tremors, brain wave abnormalities, incoordination, convulsions, deep depression, and sometimes death (IARC 1979; EPA 1980, 1988). Signs of acute chlordane intoxication in other mammal species are similar to those in humans and may also include aplastic anemia and acute leukemia; cyanosis; pathology of gastrointestinal tract, liver, kidney, lung, and heart; pulmonary congestion; degenerative changes in the central nervous system; impaired uptake and utilization of glucose; interference with immunocompetence response; diarrhea; avoidance of food and water; enhanced estrone metabolism; increased production of hepatic mixed function oxidase enzymes; altered enzyme activity in brain and in kidney cortex; enlarged liver; hair loss; abdominal distention; hunched appearance; inhibited oxidative phosphorylation in liver mitochondria; and thyroid carcinoma (Saxena and Karel 1976; IARC 1979; Reuber and Ward 1979; WHO 1984; Barnett et al. 1985; Johnson et al. 1986, 1987; Klaassen et al. 1986; EPA 1988; Suzaki et al. 1988). Acute oral LD50 values for technical chlordane and sensitive mammals usually ranged between 25 and 50 mg/kg BW (Table 5). Chlordane-related compounds (i.e., cis-chlordane, trans-chlordane, heptachlor, heptachlor epoxide) stimulate superoxide (O2-) generation in guinea pig leucocytes, alter membrane potential, and increase intracellular calcium concentration; toxicity of individual compounds seems to be related to superoxide generation (Suzaki et al. 1988). Metabolism of chlordane isomers results in oxychlordane, a metabolite that is about 20 times more toxic to rats than is the parent compound and is the most persistent metabolite stored in rat adipose tissue (Menzie 1978; EPA 1980). Oxychlordane accounted for 53% in females and 63% in males of all chlordane isomers in fat of rats killed 24 h after a single oral dose of 1.0 mg/kg BW technical chlordane (Nomeir and Hajjar 1987). Acute oral LD50 values in the rat, in mg/kg BW, were 19.1 for oxychlordane; 89 to 392 for cis-chlordane; 200 to 590 for technical chlordane; 327 for trans-chlordane; >4,600 for chlordane, 3-chlordene, 1-hydroxychlordene, chlordene epoxide, 1-hydroxy, and 2,3-epoxy chlordane; and >10,000 for 2-chlorochlordene (Table 5). Chlordane adversely affects growth and fertility of laboratory animals (Talamantes and Jang 1977; IARC 1979; Klaassen et al. 1986; EPA 1988; Table 5). Neonatal exposure of mice to chlordane retards growth, as judged by lowered body weights during the first 12 weeks (Talamantes and Jang 1977). No fetotoxic or teratogenic effects were observed in rats born to dams fed chlordane in their diets for 2 years at levels up to 300

Fed diets containing 5, 25, or 50 mg technical chlordane per kilogram ration for 18 months
Dose-related incidence of hepatic nodular hyperplasias in the 25 and 50 mg/kg diets and an increased incidence of hepatomas in the male 5 and 25 mg/kg groups. Controls experienced a high incidence of premature deaths

Epstein 1976

Females injected intraperitoneally with 25 mg/kg BW once weekly for 3 weeks
Fertility reduced by about 50%

EPA 1988 WHO 1984

Fed diets containing 25 to 100 mg chlordane At 100 mg/kg, decreased viability in first and per kilogram food for six generations second generations and no offspring in third generation. At 50 mg/kg, viability was reduced in fourth and fifth generations. No significant effects in the 25 mg/kg group, even after six generations Males fed diets containing 29.9 or 56.2 mg technical chlordane per kilogram for 80 weeks Females fed diets containing 30 or 64 mg technical chlordane per kilogram for 80 weeks Males given single dose of 50 or 100 mg/kg BW, then mated with untreated females 390430 mg/kg BW Rabbit, Oryctolagus sp. Oral doses of 1, 5, or 15 mg/kg BW daily on days 618 of gestation Dosed orally with 14.3 mg of radiolabeled trans-chlordane daily for 10 weeks and killed 2 weeks after the last dose 20 mg/kg BW, single intravenous injection Dermal exposure for 90 days, equivalent to 2040 mg/kg BW Dosed orally with cis-chlordane at 67 mg/kg BW, or trans-chlordane at 30 mg/kg BW every 4 days for a total of 4 doses, then killed 5 days after the last dose Residues in the trans-chlordane group were higher (1777 mg/kg) than in the cis-chlordane group (867 mg/kg) although trans-chlordane was administered at a much lower dose. Fat and kidney usually contained the highest concentrations, and brain the lowest. Oxychlordane was measured in all tissues at 0.1 mg/kg in brains, 11 mg/kg in fat, and 0.5 to 2 mg/kg in liver, muscle, and kidney 100500 mg/kg BW 7801,200 mg/kg BW Acute oral LD50 Acute dermal LD50; death preceded by skin Some miscarriages in 1 and 15 mg/kg groups; no changes in behavior, appearance, or body weight; no teratogenic effects observed Residues were highest in abdominal and subcutaneous fat (235 mg/kg FW), followed by heart and spleen (7591 mg/kg), then liver, brain, and blood (2544 mg/kg) LD74 LD50 Acute oral LD50 Frequency of liver tumors was 88% in high-dose group, 33% in low-dose group, and 19% in controls Frequency of liver tumors was 70% in high-dose group, 6% in low-dose group, and 4% in controls No dominant lethal changes produced

Chlordane tends to accumulate in adipose tissues and, to a lesser extent, in liver (Table 5). In general, animals given a single oral dose of chlordane eliminated 80 to 90% of the dose within 7 days, usually by way of the feces; the cis isomer is eliminated more rapidly than the trans isomer and results in preferential accumulations of trans-chlordane (Nomeir and Hajjar 1987). In rats, trans-chlordane is rapidly absorbed and distributed to liver and kidney at single oral dosages as low as 0.05 mg/kg BW Ohno et al. 1986). Rabbits fed trans-chlordane for 10 weeks excreted 70% of accumulated chlordane during the following 2 weeks on a chlordane-free diet (Menzie 1974). Treatment with trans-chlordane resulted in a greater percentage of oxychlordane in fat than did treatment with cis-chlordane. When chlordane was removed from the diet of treated animals, levels in fat declined 60% at a relatively steady rate over 4 weeks, but then only slightly thereafter; accumulations in liver, kidney, brain, and muscle were much lower than in fat, but excretion kinetics were similar (Nomeir and Hajjar 1987). Results of chronic feeding studies show that dietary concentrations of chlordane between 0.76 and 5 mg/kg ration did not affect survival but did produce adverse effects on various species of laboratory animals and livestock (Table 5). Dietary concentrations of 0.76 mg/kg (equivalent to 0.09 mg/kg BW daily) were associated with enlarged livers in mice, 1.0 mg/kg produced elevated residues in cow's milk, 2.5 mg/kg resulted in liver pathology in rats, 3 mg/kg (equivalent to 0.075 mg/kg BW daily) produced high residues in fat of dogs, and 5 mg/kg caused liver pathology in mice (Table 5). Negative results for mutagenicity of cis-chlordane and trans-chlordane were reported in various strains of bacteria and in hepatocyte cultures of small mammals. But technical chlordane proved mutagenic to selected strains of Salmonella typhimurium and induced gene conversions in certain strains of the yeast Saccharomyces cervisiae (IARC 1979; EPA 1980, 1988; WHO 1984). Chlordane interacts with other chemicals to produce additive or more than additive toxicity. For example, chlordane increased hepatotoxic effects of carbon tetrachloride in the rat (EPA 1980; WHO 1984), and in combination with dimethylnitrosamine acts more than additively in producing liver neoplasms in mice (Williams and Numoto 1984). Chlordane in combination with endrin, methoxychlor, or aldrin is additive or more-thanadditive in toxicity to mice (Klaassen et al. 1986). Protein deficiency doubles the acute toxicity of chlordane to rats (WHO 1984). In contrast, chlordane exerts a protective effect against several organophosphorus and carbamate insecticides (WHO 1984) protects mouse embryos against influenza virus infection and mouse newborns against oxazolone delayed hypersensitivity response (Barnett et al. 1985). More research seems warranted on interactions of chlordane with other agricultural chemicals. Recommendations All use of chlordane was banned in Norway in 1967 (Ingebrigtsen et al. 1984). In August 1975, EPA issued its intent to suspend registrations and prohibit production of all pesticides containing heptachlor or chlordane, based on evidence of carcinogenicity (Glooschenko and Lott 1977). On 1 July 1983, chlordane use was prohibited in the United States for any purpose except to control underground termites; a similar situation exists in Japan (Ohno et al. 1986; Tojo et al. 1986). The continued use of chlordane, coupled with its general persistence in the environment, suggests that extreme caution be taken in all stages of its manufacture, transport, storage, and application (Greenhalgh 1986).

Acknowledgments I thank N. Bushby, J. Corley, and L. Garrett for literature search and retrieval; B. A. Roberts for secretarial assistance; L. J. Blus, R. Crunkilton, N. C. Coon, J. B. Hunn A. J. Krynitsky, D. H. White, and J. L. Zajicek for technical and scientific review; and C. M. Lemos, C. E. Puckett, and J. R. Zuboy for editorial services.
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