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Concentrations of metals in mink and other mammals from Washington and Idaho
Environmental Pollution 44 (1987) 307-318
Concentrations of Metals in Mink and Other Mammals from Washington and Idaho Lawrence J. Blus, Charles J. Henny & Bernard M. Mulhern Patuxent Wildlife Research Center, US Fish and Wildlife Service, 480 SW Airport Road, Corvallis, OR 97333, USA (Received 5 August 1986; accepted 5 October 1986) A BSTRA CT From 1981 to 1983, concentrations of metals were determined in mink Mustela vison, muskrats Ondatra zibethica, and small mammals at one contaminated site in Idaho and at two less contaminated sites in Idaho and Washington. The highest concentrations o f Pb and Cd occurred in samples from the Coeur d'Alene River system near or downstream from an extensive mining-smelting complex in northern Idaho. Maximum concentrations of Pb in the liver o f a mink ( 22 ltgg -x ) and in pooled liver samples of both voles (Microtus spp., 5"811gg -1) and deer mice (Peromyscus maniculatus, 10.5 #g g - l ) were higher than those inducing serious problems. including mortality, in experimental mammals on Pb-contaminated diets. Concentrations o f Cd, Cu, Hg, and Zn were generally low. Declines in certain mammal populations have probably occurred in northern Idaho as a result of direct toxicity of metals and associated secondary effects on cover and food supply.
INTRODUCTION Several studies have reported concentrations of metals in wild mammals living in highly contaminated areas near smelters (Beyer et al., 1985), chloralkali plants (Dustman et al., 1972; Wren, 1985), verges of heavily-used highways (Clark, 1979) and mines or mine waste sites (Roberts et al., 1978; Andrews et al., 1984). Most of the Coeur d'Alene River system in northern Idaho has been severely impacted by metals contamination that originated from smelters 307
Lawrence J. B/us, Charles J. Henny, Bernard M. Mulhern
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and numerous mines along the South Fork in an area known as the Silver Valley (Fig. 1). Average monthly emissions of lead from the main smelter stack were estimated to be from 8.3 to 11"7 metric tons from 1955 to 1973 (Burrows et al., 1981). Even as late as 1973, daily discharges of metals into the South Fork involved 4400 kg of zinc, 245 kg of lead and 57 kg of arsenic (Rabe & Flaherty, 1974). Waterfowl mortality, associated with the mining and smelting activities, has occurred in that area since at least the early 1900s (Chupp & Dalke, 1955; Benson et aL, 1976) and continues to the present day (Robert Krieger, Washington State Univ., pers. comm.). Metal contaminant problems documented in mammals (other than humans) from this area occurred in domestic dogs Canis familaris and livestock (Rabe & Flaherty, 1974; Burrows et al., 1981). High concentrations of several metals were found in small mammals trapped near Kellogg--the centre of the mining and smelting activities in the Silver Valley (Herman, 1975); thus, it is likely that wild mammals were also adversely affected. From 1981 to 1983, we obtained specimens of mammals in the vicinity of Kellogg and other areas in Idaho and Washington; these were analysed for contaminants. In this paper, we present concentrations of metals in mink Mustela vison, other furbearers, and small mammals from heavily 124°
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contaminated and less contaminated sections of the Coeur d'Alene River system and from an apparently uncontaminated area in the State of Washington; and we discuss potential problems associated with these concentrations.
METHODS Personnel of the Washington Department of Game and Idaho Department of Fish and Game supplied skinned carcasses of furbearers obtained from trappers or found dead. Mink (26) were taken during the 1981-82 or 1982-83 trapping seasons in less contaminated sites in Okanogan County, Washington and the North Fork of the Coeur d'Alene River, as well as the contaminated main channel of the Coeur d'Alene River. Eight of the nine mink from the main channel were trapped near Thompson L a k e - - a b o u t 70 km downstream from the centre of the mining and smelting activities near Kellogg (Fig. 1). Six muskrats were taken from Thompson Lake in the 1982-83 season. Voles M i c r o t u s spp. and deer mice P e r o m y s c u s maniculatus were killed after they were live-trapped in July of 1982 (50 trap nights) and May 1983 (25 trap nights) in a small area near Interstate Highway 90 that abutted the east end of the main tailings pond at the Bunker Hill smelter complex in Kellogg, Idaho (Fig. 1). Specimens were frozen after they were trapped. They were later thawed and livers and kidneys were removed from the furbearers, weighed, placed in glass jars (cleaned with acetone, hexane, and dilute nitric acid) and stored in a freezer. Samples from mice were handled in the same manner as furbearers except that pooled samples of unskinned whole bodies, embryos, livers, and kidneys were analysed. For pools of whole bodies, concentrations were adjusted to include tissues that were analysed separately. Specimens were grossly examined for developmental or disease problems.
Chemical methodology All livers were analysed for concentrations of Cu, Hg, Pb, and Zn; kidneys were only analysed for Cd. Stomach contents of mink and muskrats and whole bodies and embryos of mice were analysed for Cd, Cu, Hg, Pb, and Zn. For Hg analysis, the samples were prepared and extracted using methods described by M o n k (1961). Determinations were made using the method of Hatch & O t t (1968). Analytical methodology for the other metals followed that described by Haseltine et al. (1981). Concentrations were determined by comparison with aqueous standards on a Perkin-Elmer
310
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Model 5000 atomic absorption spectrophotometer. The lower sensitivity limits were 0.1/zg g-1 for Cd, Cu, Pb, and Zn; and 0.02 #g g-1 for Hg. All concentrations of metals are reported on a wet weight basis. For ease of comparison, concentrations of metals expressed on a dry weight basis in a few other studies were converted to approximate wet weight using a fixed value of 70% moisture content; the original dry weight values are listed in parentheses. One-way analysis of variance (ANOVA) was used to compare concentrations of five metals in livers and kidneys of muskrats from Thompson Lake and mink from three areas. When significant differences (P < 0-05) were derived from ANOVA, means were separated using Tukey's Q-test (Neter & Wasserman, 1974).
RESULTS Contaminants in mink
Livers of mink from the main channel of the Coeur d'Alene River (eight trapped from the Thompson Lake area) contained significantly higher mean levels of Pb (4.1 #g g-1) than the other two collection sites (Table 1). Mean levels of Pb in livers were lowest in mink from north-central Washington (0-10/~g g-1) and only slightly higher in mink from the North Fork (0.27 #g g- 1). Four mink livers from the main channel contained high levels of Pb (7.6-22.0#g g-1), compared to a maximum concentration of 3.2 pg g-1 in the other two areas (Table 1). Levels of Pb in livers of mink from the main channel were not consistently high; one contained only 0"39 pgg-1. The mean Cd concentration in livers of mink from the main channel was significantly higher than that recorded in north-central Washington. Livers of mink from Washington (Table 1) contained the highest mean concentration of Hg (1.26 ~gg-1). Concentrations of metals tended to be lowest in mink from the North Fork of the Coeur d'Alene River. Samples of unidentified food (primarily mammalian) taken from stomachs of four mink were analysed individually for concentrations of metals. Concentrations of Pb, Cu, and Zn were detected in all four samples; the maximum concentration of Pb (3.8 #g g-1) was detected in the sample from the main channel. No concentrations of As, Mo and Co were detected in a food sample taken from a mink from the North Fork (Table 1). The small sample size precludes comparison of metals in food samples and mink tissues.
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Metals in muskrats Livers of muskrats from the T h o m p s o n Lake area contained significantly lower concentrations of Pb, Cu, and Hg than those of mink trapped in the same area (Tables 1 and 2). Compared to the amount of Pb found in the stomach contents of muskrats (1.6-14.0~gg-~), the levels found in their livers were relatively low (0-27-0-96 ktg g- ~). Metals in mice Whole bodies of deer mice and voles trapped in a heavily contaminated area in Kellogg had elevated Pb concentrations that varied from 23.5 to 173/1gg -1 and 52.7 to 58"0#gg -1, respectively (Table 2). In contrast, Pb concentrations in livers of both species and normal-appearing embryos of voles were much lower than whole body values. Concentrations of Pb exceeded 5 ~g g-1 in pooled liver samples of both the vole and the deer mouse with a maximum of 10-5 #g g- 1 in a deer mouse sample. The relationship of much higher concentrations in whole bodies compared to livers also held for Zn with maxima of 62"7 ~g g- 1 in livers and 362/~gg-' in whole bodies. Concentrations of Cu were similar in whole bodies and livers; whereas Cd concentrations in kidneys were 10 times those found in whole bodies. This difference is probably related to the primary storage of Cd in soft tissues (mainly kidney and liver) compared to storage of other metals in both soft tissues and bone (Andrews et al., 1984). The maximum concentration of Cd was 10/~gg -1 in a pooled sample of kidneys from the vole. Based on limited effort of 75 trap nights that resulted in trapping of 25 small mammals, population densities of voles and deer mice appeared high in the small roadside area in Kellogg. Suitable cover was sparse adjacent to the trapping site. The source of some metals such as Pb probably originated from automobiles (Clark, 1979) as well as from mining and smelting activities. We observed only two physical problems--both in adult female voles--including embryo resorbance (sample lost and not analysed for metals) and serious disease of the tail and feet.
DISCUSSION Concentrations of Pb in livers of mink and deer mice in this study exceeded 10/~g g-1, a level that is considered of diagnostic significance in livers of experimental mammals (Osweiler et al., 1978); however, mammals with
314
Lawrence J. Blus, Charles J. Henny, Bernard M. Mulhern
behavioural and physiological signs of Pb intoxication have died with < 5 pg g - 1 in their livers (Zook et al., 1972; Clarke, 1973). Thus, Pb levels in some mink and small mammals in northern Idaho were probably sufficiently elevated to induce adverse effects. In addition to Pb concentrations, behavioural and physiological correlates are frequently required to substantiate Pb-induced intoxication because some living mammals may carry large burdens of Pb and physiological indicators of Pb intoxication are sometimes detected at low concentrations. For example, deer mice trapped in Illinois near a battery lead reclamation plant had as much as 43/~g g-1 in their livers; and acid-fast eosinophilic intranuclear inclusions, a sensitive indicator of Pb toxicosis in rats (Goyer et al., 1970), occurred in kidneys of some deer mice that had < 1 #g g - ~ in their livers (Kisseberth et al., 1984). Deer mice and voles that we trapped in Kellogg, Idaho contained high Pb levels; Herman (1975) reported even higher concentrations, over 300 pg g-~, in whole bodies of some rodents trapped in the Kellogg area. These Pb concentrations in small mammals from the Silver Valley from both studies were much higher than in two species of voles (Microtus agrestis and M. pennsylvanicus) that were trapped in a variety of contaminated sites by a number of investigators in England and North America (Cloutier et al., 1985). Levels of Pb in livers of voles and deer mice in our study were similar to liver concentrations of 4.4 pg g-1 in laboratory mice given lead acetate in water; the experimental mice had increased urinary aminolevulinic acid excretion and Pb-induced anaemia (Mylroie et al., 1977) It is uncertain whether resorbtion of embryos and tail and foot problems noted with voles in our study are related to Pb and other metals. Experimental studies indicate that metals such as Cd and Pb are capable of inducing adverse effects on the immune (Hemphill et al., 1971) and reproductive (Mattison et al., 1983) systems of laboratory mice. One aspect that may ameliorate effects of metals on reproduction of mice in the Kellogg area is that the placenta is a general barrier preventing certain metals including Cd (Piscator, 1985) and Pb (McClain & Becker, 1972) in maternal blood from reaching the developing embryo. Muskrats in our study contained low concentrations of metals. Everett and Anthony (1976) also found that livers of muskrats trapped in four areas in Pennsylvania contained low mean levels of Pb ( < 0"15 pg g-~), Cu ( < 4.6 #g g- 1), Hg ( _<0-07 pg g - 1), and Cd ( < 0.32 pg g - 1) that were similar to those in our study, although Zn ( < 8 1 . 2 # g g -1) was higher. Metals in plants collected from the four areas in Pennsylvania were much higher than in livers of muskrats ' inhabiting those areas suggesting that biomagnification was low (Everett & Anthony, 1976). Captive mink have died from accidental exposure to Pb (Werner, 1932;
Metals in mink and other mammals
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Purdy, 1962), but there is no apparent documentation of Pb-induced mortality, or any other Pb-related problem for that matter, in wild mink. Over 300 mink trapped in Virginia from 1981 to 1983 (Ogle et al., 1985) contained levels of Cd, Cu, Pb, and Zn in their livers that were similar to those in most mink from our study. The mean, about 0.04pgg-1 (0-12pgg -1 dry wt), and maximum concentrations, about 3.8#gg -1 (12.7/ag g- 1 dry wt), of Pb in livers of mink from Virginia were much lower than those detected in livers of mink from the main channel of the Coeur d'Alene River. It is doubtful if mink could survive in certain sections of the Coeur d'Alene River not only because of the high concentrations of metals but also because of the apparent absence of both suitable cover and an adequate prey base. Although captive mink are sensitive to certain environmental contaminants such as polychlorinated biphenyls (Hornshaw et al., 1983) and methyl mercury (Aulerich et al., 1974), there is uncertainty regarding the relationship of metals and other contaminants to reported declines of populations of wild mink, such as that reported in Virginia (Ogle et al., 1985). Environmental contaminants are suspected of being a factor in declines of river otter L u t r a canadensis in several areas (O'Connor & Nielsen, 1980). Fimreite and Reynolds (1973) reported second-hand information from fur trappers that mink and river otter had recently disappeared from Clay Lake near Dryden, Ontario, Canada. Clay Lake was heavily contaminated with Hg, and probable Hg-induced poisoning of one river otter was later reported (Wren, 1985). Wobeser and Swift (1976) reported that the liver of a wild mink found sick near Saskatoon, Saskatchewan, Canada in 1975 contained 58.2 pg g- 1 Hg compared to a mean of 24.3/~g g- 1 in livers of experimental mink that died on Hg-contamiriated diets (Wobeser et al., 1976). Kucera (1983) summarised Hg concentrations in mink and otter from North America; levels were relatively low in most populations. Aulerich et al. (1974) determined that adult mink given 5 pg g-1 dietary methyl mercury died in about 1 month; their livers contained a mean of 55"6#gg-~ Hg. As little as 1.8pgg-1 dietary Hg has induced serious problems in mink including mortality (Wobeser et al., 1976). Intoxicated mink receiving methyl mercury-contaminated diets contained as little as 25 pg g-1 in their livers when they were sacrificed (O'Connor & Nielsen, 1980). Concentrations of Hg in livers of mink included in this study were well below known deleterious levels; only one of four samples of stomach contents of mink from Idaho contained detectable concentrations (0-05/~g g- 1). Mean concentrations of Hg were also low in tissues of other mammals from our study areas. The effects of metals, particularly Pb, on populations of wild mammals in
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Lawrence J. Blus, Charles J. Henny, Bernard M. Mulhern
the Silver Valley are unknown. Numbers have probably been seriously reduced in the heavily contaminated sites such as the nearly denuded area around the smelters and in the riparian and aquatic zones downstream to Lake Coeur d'Alene (Rabe & Flaherty, 1974). In addition to direct toxic effects of Pb and other metals, secondary effects associated with absence of cover and food are also probably important. The continued closure of the smelters and some of the mines in the Kellogg area since 1981 reduced airborne contaminants. Further research and monitoring are recommended because adverse effects on the biota are expected to continue indefinitely because of the high burden of metal contaminants in the area, particularly in the aquatic and riparian habitats (Rabe & Flaherty, 1974).
ACKNOWLEDGEMENTS We thank the Idaho Department of Fish and Game (J. Nigh and D. Reynolds) and Washington Department of Game (G. Brady) for supplying specimens, R. Grove for assistance with field work, and W. Beyer and G. Smith for manuscript review. Use of trade names or commercial products does not constitute endorsement by the US Government.
REFERENCES Andrews, S. H., Johnson, M. S. & Cooke, J. A. (1984). Cadmium in small mammals from grassland established on metalliferous mine waste. Environ. Pollut., Ser. A, 33, 153-62. Aulerich, R. J., Ringer, R. K. & Iwamoto, S. (1974). Effects of dietary mercury on mink. Arch. environ. Contain. Toxicol., 2, 43-51. Benson, W. W., Brock, D. W., Gabica, J. & Loomis, M. (1976). Swan mortality due to certain heavy metals in the Mission Lake area, Idaho. Bull. environ. Contain. Toxicol., 15, ~171-4. Beyer, W. N., Pattee, O. H., Sileo, L., Hoffman, D. J. & Mulhern, B. M. (1985). Metal contamination in wildlife living near two zinc smelters. Environ. Pollut., Set. A, 33, 63 86. Burrows, G. E., Sharp, J. W. & Root, R. G. (1981). A survey of blood lead concentrations in horses in the north Idaho lead/silver belt area. Vet. Human ToxicoL, 23, 328 30. Chupp, N. R. & Dalke, P. D. (1964). Waterfowl mortality in the Coeur d'Alene River Valley, Idaho. J. Wildl. Mgmt, 28, 692-702. Clark, D. R. (1979). Lead concentrations: bats vs. terrestrial mammals collected near a major highway. Environ. Sci. TechnoL, 3, 33841.
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Clarke, E. G. C. (1973). Lead poisoning in small animals. Small Anim. Pract., 14, 183-93. Cloutier, N. R., Clulow, F. V., Lim, T, P. & Dave, N. K. (1985). Metal (Cu, Ni, Fe, Co, Zn, Pb) and Ra-226 levels in meadow voles Microtus pennsylvanicus living on nickel and uranium mine tailings in Ontario, Canada: Environmental and tissue levels. Environ. Pollut., Ser. B, 10, 19-46. Dustman, E. H., Stickel, L. F. & Elder, J. B. (1972). Mercury in wild animals from Lake St. Clair. In Environmental mercury contamination, ed. by R. Hartung and B. D. Dinman, 46-52. Ann Arbor, Mich., Ann Arbor Science Publishers. Everett, J. J. & Anthony, R. G. (1976). Heavy metal accumulation in muskrats in relation to water quality. Trans. NE Sect. Wildl. Soc., 33, 105-18. Fimreite, N. & Reynolds, L. M. (1973). Mercury contamination of fish in northwestern Ontario. J. Wildl. Mgmt, 37, 62-8. Goyer, R. A., Leonard, D. L., Moore, J. P., Rhyne, B. & Krigman, M. R. (1970). Lead dosage and the role of the intranuclear inclusion body. Arch. environ. Hlth, 20, 705-11. Haseitine, S. D., Heinz, G. H., Reichel, W. L. & Moore, J. F. (1981). Organochlorine and metal residues in eggs of waterfowl nesting on islands in Lake Michigan off Door County, Wisconsin, 1977-78. Pestic. Monit. J., 15, 90-7. Hatch, W. R. & Ott, W. L. (1968). Determination of sub-microgram quantities of mercury by atomic absorption spectrophotometry. Anal. Chem., 40, 2085 7. Hemphill, F. E., Kaeberle, M. & Buck, W. B. (1971). Lead suppression of mouse resistance to Salmonella typhimurium. Science, N.Y., 172, 1031-2. Herman, S. G. (Faculty advisor) (1975). Lead and cadmium in soils, vegetation, and small mammals near Kellogg, Idaho. Student Originated Study, Evergreen State College, Olympia, Washington. Hornshaw, T. C., Aulerich, R. J. & Johnson, H. E. (1983). Feeding Great Lakes fish to mink; effects on mink and accumulation and elimination of PCBs by mink. J. Toxicol. environ. Hlth, 11, 933-46. Kisseberth, W. C., Sundberg, J. P., Nyboer, R. W., Reynolds, J. D., Kasten, S. C. & Beasley, V. R. (1984). Industrial lead contamination of an Illinois wildlife refuge and indigenous small mammals. JA VMA, 185, 1309 13. Kucera, E. (1983). Mink and otter as indicators of mercury in Manitoba waters. Can. J. ZooL, 61, 2250-6. Mattison, D. R., Gates, A. H., Leonard, A., Wide, M., Hemminki, K. & PeereboomStegeman, J. H. J. C. (1983). Reproductive and developmental toxicity of metals: female reproductive system. In Reproductive and developmental toxicity of metals, ed. by T. W. Clarkson, G. F. Nordberg and P. R. Sager, 43-91. New York, Plenum Press. McClain, R. M. & Becker, B. A. (1972). Effects of organolead compounds on rat embryonic and fetal development. Toxicol. appl. Pharmacol., 21,265 74. Monk, H. E. (1961). Recommended methods of analysis of pesticide residues in food stuffs. Report by the Joint Mercury Residues Panel. Analyst, 86, 608-14. Mylroie, A. A., Moore, L. & Erogbogbo, U. (1977). Influence of dietary factors on blood and tissue lead concentrations and lead toxicity. Toxicol. appl. Pharmacol., 41, 361-7. Neter, J. & Wasserman, W. (1974). Applied linear statistical models. Homewood, Ill., Richard D. Irwin Inc. O'Connor, D. J. & Nielsen, S. W. (1980). Environmental survey of methylmercury levels in wild mink (Mustela vison) and otter (Lutra canadensis) from the
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Northeastern United States and experimental pathology of methymercurialism in the otter. In Worldwide Furbearer Conference Proc., Vol. 3, ed. by J. A. Chapman and D. Pursley, 1728-45. Frostburg, Maryland. Ogle, M. C., Scanlon, P. F., Kirkpatrick, R. L. & Gwynn, J. V. (1985). Heavy metal concentrations in tissues of mink in Virginia. Bull. environ. Contam. Toxicol., 35, 29-37. Osweiler, G. D., Van Gelder, G. A. & Buck, W. B. (1978). Epidemiology of lead poisoning in animals. In Toxicity of heavy metals in the environment, Part l, ed. by F. W. Oehme, 1143-71. New York, Marcel Dekker Inc. Piscator, M. (1985). Dietary exposure to cadmium and health effects: Impacts of environmental changes. Environ. Health Perspect., 63, 127-32. Purdy, J. G. (1962). Lead poisoning in mink. Can. Vet. J., 3, 96. Rabe, F. W. & Flaherty, D. C. (1974). The river of green andgold. Idaho Research Foundation Inc., Natural Resources Series No. 4. Roberts, R. D. & Johnson, M. S. (1978). Dispersal of heavy metals from abandoned mine workings and their transference through terrestrial food chains. Environ. Pollut., 16, 293-310. Werner, F. (1932). Ueber Mennigevergiftungen bei Nerzruden. Deutsche Tierarztliche Wochenschrift, 18, 273-4. Wobeser, G. & Swift, M. (1976). Mercury poisoning in a wild mink. J. Wildl. Dis., 12, 335-40. Wobeser, G., Nielsen, N. O. & Schiefer, B. (1976). Mercury and mink. II. Experimental methylmercury intoxication. Can. J. comp. Med., 40, 34-45. Wren, C. D. (1985). Probable case of mercury poisoning in a wild otter, Lutra canadensis, in northwestern Ontario. Can. Field-Nat., 99, 112-14. Wren, C. D., MacCrimmon, H., Frank, R. & Suda, P. (1980). Total and methyl mercury levels in ~wild mammals from the PreCambrian JShield area of south Central Ontario, Canada. Bull. environ. Contam. Toxicol., 25, 100-5. Zook, B. C., Sauer, R. M. & Garner, F. M. (1972). Lead poisoning in captive wild animals. J. Wildl. Dis., 8, 264-72.
Concentrations of Metals in Mink and Other Mammals from Washington and Idaho Lawrence J. Blus, Charles J. Henny & Bernard M. Mulhern Patuxent Wildlife Research Center, US Fish and Wildlife Service, 480 SW Airport Road, Corvallis, OR 97333, USA (Received 5 August 1986; accepted 5 October 1986) A BSTRA CT From 1981 to 1983, concentrations of metals were determined in mink Mustela vison, muskrats Ondatra zibethica, and small mammals at one contaminated site in Idaho and at two less contaminated sites in Idaho and Washington. The highest concentrations o f Pb and Cd occurred in samples from the Coeur d'Alene River system near or downstream from an extensive mining-smelting complex in northern Idaho. Maximum concentrations of Pb in the liver o f a mink ( 22 ltgg -x ) and in pooled liver samples of both voles (Microtus spp., 5"811gg -1) and deer mice (Peromyscus maniculatus, 10.5 #g g - l ) were higher than those inducing serious problems. including mortality, in experimental mammals on Pb-contaminated diets. Concentrations o f Cd, Cu, Hg, and Zn were generally low. Declines in certain mammal populations have probably occurred in northern Idaho as a result of direct toxicity of metals and associated secondary effects on cover and food supply.
INTRODUCTION Several studies have reported concentrations of metals in wild mammals living in highly contaminated areas near smelters (Beyer et al., 1985), chloralkali plants (Dustman et al., 1972; Wren, 1985), verges of heavily-used highways (Clark, 1979) and mines or mine waste sites (Roberts et al., 1978; Andrews et al., 1984). Most of the Coeur d'Alene River system in northern Idaho has been severely impacted by metals contamination that originated from smelters 307
Lawrence J. B/us, Charles J. Henny, Bernard M. Mulhern
308
and numerous mines along the South Fork in an area known as the Silver Valley (Fig. 1). Average monthly emissions of lead from the main smelter stack were estimated to be from 8.3 to 11"7 metric tons from 1955 to 1973 (Burrows et al., 1981). Even as late as 1973, daily discharges of metals into the South Fork involved 4400 kg of zinc, 245 kg of lead and 57 kg of arsenic (Rabe & Flaherty, 1974). Waterfowl mortality, associated with the mining and smelting activities, has occurred in that area since at least the early 1900s (Chupp & Dalke, 1955; Benson et aL, 1976) and continues to the present day (Robert Krieger, Washington State Univ., pers. comm.). Metal contaminant problems documented in mammals (other than humans) from this area occurred in domestic dogs Canis familaris and livestock (Rabe & Flaherty, 1974; Burrows et al., 1981). High concentrations of several metals were found in small mammals trapped near Kellogg--the centre of the mining and smelting activities in the Silver Valley (Herman, 1975); thus, it is likely that wild mammals were also adversely affected. From 1981 to 1983, we obtained specimens of mammals in the vicinity of Kellogg and other areas in Idaho and Washington; these were analysed for contaminants. In this paper, we present concentrations of metals in mink Mustela vison, other furbearers, and small mammals from heavily 124°
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o
120"
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Localities of collection sites of mammals in Washington and Idaho.
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309
contaminated and less contaminated sections of the Coeur d'Alene River system and from an apparently uncontaminated area in the State of Washington; and we discuss potential problems associated with these concentrations.
METHODS Personnel of the Washington Department of Game and Idaho Department of Fish and Game supplied skinned carcasses of furbearers obtained from trappers or found dead. Mink (26) were taken during the 1981-82 or 1982-83 trapping seasons in less contaminated sites in Okanogan County, Washington and the North Fork of the Coeur d'Alene River, as well as the contaminated main channel of the Coeur d'Alene River. Eight of the nine mink from the main channel were trapped near Thompson L a k e - - a b o u t 70 km downstream from the centre of the mining and smelting activities near Kellogg (Fig. 1). Six muskrats were taken from Thompson Lake in the 1982-83 season. Voles M i c r o t u s spp. and deer mice P e r o m y s c u s maniculatus were killed after they were live-trapped in July of 1982 (50 trap nights) and May 1983 (25 trap nights) in a small area near Interstate Highway 90 that abutted the east end of the main tailings pond at the Bunker Hill smelter complex in Kellogg, Idaho (Fig. 1). Specimens were frozen after they were trapped. They were later thawed and livers and kidneys were removed from the furbearers, weighed, placed in glass jars (cleaned with acetone, hexane, and dilute nitric acid) and stored in a freezer. Samples from mice were handled in the same manner as furbearers except that pooled samples of unskinned whole bodies, embryos, livers, and kidneys were analysed. For pools of whole bodies, concentrations were adjusted to include tissues that were analysed separately. Specimens were grossly examined for developmental or disease problems.
Chemical methodology All livers were analysed for concentrations of Cu, Hg, Pb, and Zn; kidneys were only analysed for Cd. Stomach contents of mink and muskrats and whole bodies and embryos of mice were analysed for Cd, Cu, Hg, Pb, and Zn. For Hg analysis, the samples were prepared and extracted using methods described by M o n k (1961). Determinations were made using the method of Hatch & O t t (1968). Analytical methodology for the other metals followed that described by Haseltine et al. (1981). Concentrations were determined by comparison with aqueous standards on a Perkin-Elmer
310
Lawrence J. Blus, Charles J. Henny, Bernard M. Mulhern
Model 5000 atomic absorption spectrophotometer. The lower sensitivity limits were 0.1/zg g-1 for Cd, Cu, Pb, and Zn; and 0.02 #g g-1 for Hg. All concentrations of metals are reported on a wet weight basis. For ease of comparison, concentrations of metals expressed on a dry weight basis in a few other studies were converted to approximate wet weight using a fixed value of 70% moisture content; the original dry weight values are listed in parentheses. One-way analysis of variance (ANOVA) was used to compare concentrations of five metals in livers and kidneys of muskrats from Thompson Lake and mink from three areas. When significant differences (P < 0-05) were derived from ANOVA, means were separated using Tukey's Q-test (Neter & Wasserman, 1974).
RESULTS Contaminants in mink
Livers of mink from the main channel of the Coeur d'Alene River (eight trapped from the Thompson Lake area) contained significantly higher mean levels of Pb (4.1 #g g-1) than the other two collection sites (Table 1). Mean levels of Pb in livers were lowest in mink from north-central Washington (0-10/~g g-1) and only slightly higher in mink from the North Fork (0.27 #g g- 1). Four mink livers from the main channel contained high levels of Pb (7.6-22.0#g g-1), compared to a maximum concentration of 3.2 pg g-1 in the other two areas (Table 1). Levels of Pb in livers of mink from the main channel were not consistently high; one contained only 0"39 pgg-1. The mean Cd concentration in livers of mink from the main channel was significantly higher than that recorded in north-central Washington. Livers of mink from Washington (Table 1) contained the highest mean concentration of Hg (1.26 ~gg-1). Concentrations of metals tended to be lowest in mink from the North Fork of the Coeur d'Alene River. Samples of unidentified food (primarily mammalian) taken from stomachs of four mink were analysed individually for concentrations of metals. Concentrations of Pb, Cu, and Zn were detected in all four samples; the maximum concentration of Pb (3.8 #g g-1) was detected in the sample from the main channel. No concentrations of As, Mo and Co were detected in a food sample taken from a mink from the North Fork (Table 1). The small sample size precludes comparison of metals in food samples and mink tissues.
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Metals in muskrats Livers of muskrats from the T h o m p s o n Lake area contained significantly lower concentrations of Pb, Cu, and Hg than those of mink trapped in the same area (Tables 1 and 2). Compared to the amount of Pb found in the stomach contents of muskrats (1.6-14.0~gg-~), the levels found in their livers were relatively low (0-27-0-96 ktg g- ~). Metals in mice Whole bodies of deer mice and voles trapped in a heavily contaminated area in Kellogg had elevated Pb concentrations that varied from 23.5 to 173/1gg -1 and 52.7 to 58"0#gg -1, respectively (Table 2). In contrast, Pb concentrations in livers of both species and normal-appearing embryos of voles were much lower than whole body values. Concentrations of Pb exceeded 5 ~g g-1 in pooled liver samples of both the vole and the deer mouse with a maximum of 10-5 #g g- 1 in a deer mouse sample. The relationship of much higher concentrations in whole bodies compared to livers also held for Zn with maxima of 62"7 ~g g- 1 in livers and 362/~gg-' in whole bodies. Concentrations of Cu were similar in whole bodies and livers; whereas Cd concentrations in kidneys were 10 times those found in whole bodies. This difference is probably related to the primary storage of Cd in soft tissues (mainly kidney and liver) compared to storage of other metals in both soft tissues and bone (Andrews et al., 1984). The maximum concentration of Cd was 10/~gg -1 in a pooled sample of kidneys from the vole. Based on limited effort of 75 trap nights that resulted in trapping of 25 small mammals, population densities of voles and deer mice appeared high in the small roadside area in Kellogg. Suitable cover was sparse adjacent to the trapping site. The source of some metals such as Pb probably originated from automobiles (Clark, 1979) as well as from mining and smelting activities. We observed only two physical problems--both in adult female voles--including embryo resorbance (sample lost and not analysed for metals) and serious disease of the tail and feet.
DISCUSSION Concentrations of Pb in livers of mink and deer mice in this study exceeded 10/~g g-1, a level that is considered of diagnostic significance in livers of experimental mammals (Osweiler et al., 1978); however, mammals with
314
Lawrence J. Blus, Charles J. Henny, Bernard M. Mulhern
behavioural and physiological signs of Pb intoxication have died with < 5 pg g - 1 in their livers (Zook et al., 1972; Clarke, 1973). Thus, Pb levels in some mink and small mammals in northern Idaho were probably sufficiently elevated to induce adverse effects. In addition to Pb concentrations, behavioural and physiological correlates are frequently required to substantiate Pb-induced intoxication because some living mammals may carry large burdens of Pb and physiological indicators of Pb intoxication are sometimes detected at low concentrations. For example, deer mice trapped in Illinois near a battery lead reclamation plant had as much as 43/~g g-1 in their livers; and acid-fast eosinophilic intranuclear inclusions, a sensitive indicator of Pb toxicosis in rats (Goyer et al., 1970), occurred in kidneys of some deer mice that had < 1 #g g - ~ in their livers (Kisseberth et al., 1984). Deer mice and voles that we trapped in Kellogg, Idaho contained high Pb levels; Herman (1975) reported even higher concentrations, over 300 pg g-~, in whole bodies of some rodents trapped in the Kellogg area. These Pb concentrations in small mammals from the Silver Valley from both studies were much higher than in two species of voles (Microtus agrestis and M. pennsylvanicus) that were trapped in a variety of contaminated sites by a number of investigators in England and North America (Cloutier et al., 1985). Levels of Pb in livers of voles and deer mice in our study were similar to liver concentrations of 4.4 pg g-1 in laboratory mice given lead acetate in water; the experimental mice had increased urinary aminolevulinic acid excretion and Pb-induced anaemia (Mylroie et al., 1977) It is uncertain whether resorbtion of embryos and tail and foot problems noted with voles in our study are related to Pb and other metals. Experimental studies indicate that metals such as Cd and Pb are capable of inducing adverse effects on the immune (Hemphill et al., 1971) and reproductive (Mattison et al., 1983) systems of laboratory mice. One aspect that may ameliorate effects of metals on reproduction of mice in the Kellogg area is that the placenta is a general barrier preventing certain metals including Cd (Piscator, 1985) and Pb (McClain & Becker, 1972) in maternal blood from reaching the developing embryo. Muskrats in our study contained low concentrations of metals. Everett and Anthony (1976) also found that livers of muskrats trapped in four areas in Pennsylvania contained low mean levels of Pb ( < 0"15 pg g-~), Cu ( < 4.6 #g g- 1), Hg ( _<0-07 pg g - 1), and Cd ( < 0.32 pg g - 1) that were similar to those in our study, although Zn ( < 8 1 . 2 # g g -1) was higher. Metals in plants collected from the four areas in Pennsylvania were much higher than in livers of muskrats ' inhabiting those areas suggesting that biomagnification was low (Everett & Anthony, 1976). Captive mink have died from accidental exposure to Pb (Werner, 1932;
Metals in mink and other mammals
315
Purdy, 1962), but there is no apparent documentation of Pb-induced mortality, or any other Pb-related problem for that matter, in wild mink. Over 300 mink trapped in Virginia from 1981 to 1983 (Ogle et al., 1985) contained levels of Cd, Cu, Pb, and Zn in their livers that were similar to those in most mink from our study. The mean, about 0.04pgg-1 (0-12pgg -1 dry wt), and maximum concentrations, about 3.8#gg -1 (12.7/ag g- 1 dry wt), of Pb in livers of mink from Virginia were much lower than those detected in livers of mink from the main channel of the Coeur d'Alene River. It is doubtful if mink could survive in certain sections of the Coeur d'Alene River not only because of the high concentrations of metals but also because of the apparent absence of both suitable cover and an adequate prey base. Although captive mink are sensitive to certain environmental contaminants such as polychlorinated biphenyls (Hornshaw et al., 1983) and methyl mercury (Aulerich et al., 1974), there is uncertainty regarding the relationship of metals and other contaminants to reported declines of populations of wild mink, such as that reported in Virginia (Ogle et al., 1985). Environmental contaminants are suspected of being a factor in declines of river otter L u t r a canadensis in several areas (O'Connor & Nielsen, 1980). Fimreite and Reynolds (1973) reported second-hand information from fur trappers that mink and river otter had recently disappeared from Clay Lake near Dryden, Ontario, Canada. Clay Lake was heavily contaminated with Hg, and probable Hg-induced poisoning of one river otter was later reported (Wren, 1985). Wobeser and Swift (1976) reported that the liver of a wild mink found sick near Saskatoon, Saskatchewan, Canada in 1975 contained 58.2 pg g- 1 Hg compared to a mean of 24.3/~g g- 1 in livers of experimental mink that died on Hg-contamiriated diets (Wobeser et al., 1976). Kucera (1983) summarised Hg concentrations in mink and otter from North America; levels were relatively low in most populations. Aulerich et al. (1974) determined that adult mink given 5 pg g-1 dietary methyl mercury died in about 1 month; their livers contained a mean of 55"6#gg-~ Hg. As little as 1.8pgg-1 dietary Hg has induced serious problems in mink including mortality (Wobeser et al., 1976). Intoxicated mink receiving methyl mercury-contaminated diets contained as little as 25 pg g-1 in their livers when they were sacrificed (O'Connor & Nielsen, 1980). Concentrations of Hg in livers of mink included in this study were well below known deleterious levels; only one of four samples of stomach contents of mink from Idaho contained detectable concentrations (0-05/~g g- 1). Mean concentrations of Hg were also low in tissues of other mammals from our study areas. The effects of metals, particularly Pb, on populations of wild mammals in
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Lawrence J. Blus, Charles J. Henny, Bernard M. Mulhern
the Silver Valley are unknown. Numbers have probably been seriously reduced in the heavily contaminated sites such as the nearly denuded area around the smelters and in the riparian and aquatic zones downstream to Lake Coeur d'Alene (Rabe & Flaherty, 1974). In addition to direct toxic effects of Pb and other metals, secondary effects associated with absence of cover and food are also probably important. The continued closure of the smelters and some of the mines in the Kellogg area since 1981 reduced airborne contaminants. Further research and monitoring are recommended because adverse effects on the biota are expected to continue indefinitely because of the high burden of metal contaminants in the area, particularly in the aquatic and riparian habitats (Rabe & Flaherty, 1974).
ACKNOWLEDGEMENTS We thank the Idaho Department of Fish and Game (J. Nigh and D. Reynolds) and Washington Department of Game (G. Brady) for supplying specimens, R. Grove for assistance with field work, and W. Beyer and G. Smith for manuscript review. Use of trade names or commercial products does not constitute endorsement by the US Government.
REFERENCES Andrews, S. H., Johnson, M. S. & Cooke, J. A. (1984). Cadmium in small mammals from grassland established on metalliferous mine waste. Environ. Pollut., Ser. A, 33, 153-62. Aulerich, R. J., Ringer, R. K. & Iwamoto, S. (1974). Effects of dietary mercury on mink. Arch. environ. Contain. Toxicol., 2, 43-51. Benson, W. W., Brock, D. W., Gabica, J. & Loomis, M. (1976). Swan mortality due to certain heavy metals in the Mission Lake area, Idaho. Bull. environ. Contain. Toxicol., 15, ~171-4. Beyer, W. N., Pattee, O. H., Sileo, L., Hoffman, D. J. & Mulhern, B. M. (1985). Metal contamination in wildlife living near two zinc smelters. Environ. Pollut., Set. A, 33, 63 86. Burrows, G. E., Sharp, J. W. & Root, R. G. (1981). A survey of blood lead concentrations in horses in the north Idaho lead/silver belt area. Vet. Human ToxicoL, 23, 328 30. Chupp, N. R. & Dalke, P. D. (1964). Waterfowl mortality in the Coeur d'Alene River Valley, Idaho. J. Wildl. Mgmt, 28, 692-702. Clark, D. R. (1979). Lead concentrations: bats vs. terrestrial mammals collected near a major highway. Environ. Sci. TechnoL, 3, 33841.
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Clarke, E. G. C. (1973). Lead poisoning in small animals. Small Anim. Pract., 14, 183-93. Cloutier, N. R., Clulow, F. V., Lim, T, P. & Dave, N. K. (1985). Metal (Cu, Ni, Fe, Co, Zn, Pb) and Ra-226 levels in meadow voles Microtus pennsylvanicus living on nickel and uranium mine tailings in Ontario, Canada: Environmental and tissue levels. Environ. Pollut., Ser. B, 10, 19-46. Dustman, E. H., Stickel, L. F. & Elder, J. B. (1972). Mercury in wild animals from Lake St. Clair. In Environmental mercury contamination, ed. by R. Hartung and B. D. Dinman, 46-52. Ann Arbor, Mich., Ann Arbor Science Publishers. Everett, J. J. & Anthony, R. G. (1976). Heavy metal accumulation in muskrats in relation to water quality. Trans. NE Sect. Wildl. Soc., 33, 105-18. Fimreite, N. & Reynolds, L. M. (1973). Mercury contamination of fish in northwestern Ontario. J. Wildl. Mgmt, 37, 62-8. Goyer, R. A., Leonard, D. L., Moore, J. P., Rhyne, B. & Krigman, M. R. (1970). Lead dosage and the role of the intranuclear inclusion body. Arch. environ. Hlth, 20, 705-11. Haseitine, S. D., Heinz, G. H., Reichel, W. L. & Moore, J. F. (1981). Organochlorine and metal residues in eggs of waterfowl nesting on islands in Lake Michigan off Door County, Wisconsin, 1977-78. Pestic. Monit. J., 15, 90-7. Hatch, W. R. & Ott, W. L. (1968). Determination of sub-microgram quantities of mercury by atomic absorption spectrophotometry. Anal. Chem., 40, 2085 7. Hemphill, F. E., Kaeberle, M. & Buck, W. B. (1971). Lead suppression of mouse resistance to Salmonella typhimurium. Science, N.Y., 172, 1031-2. Herman, S. G. (Faculty advisor) (1975). Lead and cadmium in soils, vegetation, and small mammals near Kellogg, Idaho. Student Originated Study, Evergreen State College, Olympia, Washington. Hornshaw, T. C., Aulerich, R. J. & Johnson, H. E. (1983). Feeding Great Lakes fish to mink; effects on mink and accumulation and elimination of PCBs by mink. J. Toxicol. environ. Hlth, 11, 933-46. Kisseberth, W. C., Sundberg, J. P., Nyboer, R. W., Reynolds, J. D., Kasten, S. C. & Beasley, V. R. (1984). Industrial lead contamination of an Illinois wildlife refuge and indigenous small mammals. JA VMA, 185, 1309 13. Kucera, E. (1983). Mink and otter as indicators of mercury in Manitoba waters. Can. J. ZooL, 61, 2250-6. Mattison, D. R., Gates, A. H., Leonard, A., Wide, M., Hemminki, K. & PeereboomStegeman, J. H. J. C. (1983). Reproductive and developmental toxicity of metals: female reproductive system. In Reproductive and developmental toxicity of metals, ed. by T. W. Clarkson, G. F. Nordberg and P. R. Sager, 43-91. New York, Plenum Press. McClain, R. M. & Becker, B. A. (1972). Effects of organolead compounds on rat embryonic and fetal development. Toxicol. appl. Pharmacol., 21,265 74. Monk, H. E. (1961). Recommended methods of analysis of pesticide residues in food stuffs. Report by the Joint Mercury Residues Panel. Analyst, 86, 608-14. Mylroie, A. A., Moore, L. & Erogbogbo, U. (1977). Influence of dietary factors on blood and tissue lead concentrations and lead toxicity. Toxicol. appl. Pharmacol., 41, 361-7. Neter, J. & Wasserman, W. (1974). Applied linear statistical models. Homewood, Ill., Richard D. Irwin Inc. O'Connor, D. J. & Nielsen, S. W. (1980). Environmental survey of methylmercury levels in wild mink (Mustela vison) and otter (Lutra canadensis) from the
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Northeastern United States and experimental pathology of methymercurialism in the otter. In Worldwide Furbearer Conference Proc., Vol. 3, ed. by J. A. Chapman and D. Pursley, 1728-45. Frostburg, Maryland. Ogle, M. C., Scanlon, P. F., Kirkpatrick, R. L. & Gwynn, J. V. (1985). Heavy metal concentrations in tissues of mink in Virginia. Bull. environ. Contam. Toxicol., 35, 29-37. Osweiler, G. D., Van Gelder, G. A. & Buck, W. B. (1978). Epidemiology of lead poisoning in animals. In Toxicity of heavy metals in the environment, Part l, ed. by F. W. Oehme, 1143-71. New York, Marcel Dekker Inc. Piscator, M. (1985). Dietary exposure to cadmium and health effects: Impacts of environmental changes. Environ. Health Perspect., 63, 127-32. Purdy, J. G. (1962). Lead poisoning in mink. Can. Vet. J., 3, 96. Rabe, F. W. & Flaherty, D. C. (1974). The river of green andgold. Idaho Research Foundation Inc., Natural Resources Series No. 4. Roberts, R. D. & Johnson, M. S. (1978). Dispersal of heavy metals from abandoned mine workings and their transference through terrestrial food chains. Environ. Pollut., 16, 293-310. Werner, F. (1932). Ueber Mennigevergiftungen bei Nerzruden. Deutsche Tierarztliche Wochenschrift, 18, 273-4. Wobeser, G. & Swift, M. (1976). Mercury poisoning in a wild mink. J. Wildl. Dis., 12, 335-40. Wobeser, G., Nielsen, N. O. & Schiefer, B. (1976). Mercury and mink. II. Experimental methylmercury intoxication. Can. J. comp. Med., 40, 34-45. Wren, C. D. (1985). Probable case of mercury poisoning in a wild otter, Lutra canadensis, in northwestern Ontario. Can. Field-Nat., 99, 112-14. Wren, C. D., MacCrimmon, H., Frank, R. & Suda, P. (1980). Total and methyl mercury levels in ~wild mammals from the PreCambrian JShield area of south Central Ontario, Canada. Bull. environ. Contam. Toxicol., 25, 100-5. Zook, B. C., Sauer, R. M. & Garner, F. M. (1972). Lead poisoning in captive wild animals. J. Wildl. Dis., 8, 264-72.