Nickel Hazards to Fish, Wildlife, and Invertebrates: a Synoptic Review
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Biological Science Report USGS/BRD/BSR-1998-0001 Contaminant Hazard Reviews April 1998 Report No. 34 NICKEL HAZARDS TO FISH, WILDLIFE, AND INVERTEBRATES: A SYNOPTIC REVIEW by Ronald Eisler Patuxent Wildlife Research Center U.S. Geological Survey Laurel, MD 20708 TABLE OF CONTENTS Abstract Introduction Sources and Uses General Sources Uses Chemical and Biological Properties General Physical and Chemical Properties Metabolism Interactions Carcinogenicity, Mutagenicity, Teratogenicity General Carcinogenicity Mutagenicity Teratogenicity Concentrations in Field Collections General Abiotic Materials Terrestrial Plants and Invertebrates Aquatic Organisms Amphibians Birds Mammals Integrated Studies Nickel Deficiency Effects General Bacteria and Plants Birds Mammals Lethal and Sublethal Effects General Terrestrial Plants and Invertebrates Aquatic Organisms Birds Mammals Proposed Criteria and Recommendations Conclusions Acknowledgments Cited Literature TABLES Number 1 Nickel chronology 2 World mine production of nickel 3 Nickel consumption in the United States by intermediate product and end-use industry in 1985 4 Inventory of nickel in various global environmental compartments 5 Nickel concentrations in selected abiotic materials 6 Nickel concentrations (milligrams of nickel per kilogram fresh weight [FW] or dry weight [DW]) in field collections of representative plants and animals 7 Nickel effects on selected aquatic plants and animals 8 Nickel effects on birds 9 Nickel effects on selected mammals 10 Proposed nickel criteria for protection of natural resources and human health 2 NICKEL HAZARDS TO FISH, WILDLIFE, AND INVERTEBRATES: A SYNOPTIC REVIEW by Ronald Eisler Patuxent Wildlife Research Center U.S. Geological Survey Laurel, MD 20708-4017 Abstract Abstract. This account is a selective review and synthesis of the technical literature on nickel and nickel salts in the environment and their effects on terrestrial plants and invertebrates, aquatic plants and animals, avian and mammalian wildlife, and other natural resources. The subtopics include nickel sources and uses; physical, chemical, and metabolic properties of nickel; nickel concentrations in field collections of abiotic materials and living organisms; nickel deficiency effects; lethal and sublethal effects, including effects on survival, growth, reproduction, metabolism, mutagenicity, teratogenicity, and carcinogenicity; currently proposed nickel criteria for the protection of human health and sensitive natural resources; and recommendations for additional research. Key words: Nickel, nickel compounds, toxicity, deficiency, cancer, residues, criteria, fishes, invertebrates, amphibians, birds, wildlife, livestock. Introduction In Europe, nickel (Ni) is listed on European Commission List II (Dangerous Substances Directive) and regulated through the Council of European Communities because of its toxicity, persistence, and affinity for bioaccumulation (Bubb and Lester 1996). In Canada, nickel and its compounds are included in the Priority Substances List under the Canadian Environmental Protection Act (Hughes et al. 1994). The World Health Organization (WHO) classifies nickel compounds in Group 1 (human carcinogens) and metallic nickel in group 2B (possible human carcinogen; U. S. Public Health Service [USPHS] 1993). The U.S. Environmental Protection Agency (USEPA) classifies nickel refinery dust and nickel subsulfide as Group A human carcinogens (USPHS 1993) and nickel oxides and nickel halides as Class W compounds, that is, compounds having moderate retention in the lungs and a clearance rate from the lungs of several weeks (USEPA 1980). Nickel and its compounds are regulated by USEPA’s Clean Water Effluent Guideline for many industrial point sources, including the processing of iron, steel, nonferrous metals, and batteries; timber products processing; electroplating; metal finishing; ore and mineral mining; paving and roofing; paint and ink formulating; porcelain enameling; and industries that use, process, or manufacture chemicals, gum and wood, or carbon black (USPHS 1993). Nickel is ubiquitous in the biosphere. Nickel introduced into the environment from natural or human sources is circulated through the system by chemical and physical processes and through biological transport mechanisms of living organisms (National Academy of Sciences [NAS] 1975; Sevin 1980; WHO 1991). Nickel is essential for the normal growth of many species of microorganisms and plants and several species of vertebrates, including chickens, cows, goats, pigs, rats, and sheep (NAS 1975; USEPA 1980; WHO 1991; USPHS 1993). Human activities that contribute to nickel loadings in aquatic and terrestrial ecosystems include mining, smelting, refining, alloy processing, scrap metal reprocessing, fossil fuel combustion, and waste incineration (NAS 1975; WHO 1991; Chau and Kulikovsky-Cordeiro 1995). Nickel mining and smelting in the Sudbury, Ontario, region of Canada is associated with denudation of terrestrial vegetation and subsequent soil erosion (Adamo et al. 1996) and gradual ecological changes, including a decrease in the number and diversity of species and a reduction in community biomass of crustacean zooplankton (WHO 1991). At nickel-contaminated sites, plants accumulate nickel and growth is retarded in some species at high nickel concentrations (WHO 1991). But nickel accumulation rates in terrestrial and avian wildlife near nickel refineries are highly variable; Chau and Kulikovsky-Cordeiro (1995) claim similar variability for plants, soils, and interstitial sediment waters. The chemical and physical forms of nickel and its salts strongly influence bioavailability and toxicity (WHO 1991). In general, nickel compounds have low hazard when administered orally (NAS 1975; USEPA 1980). In humans and other mammals, however, nickel-inhalable dust, nickel subsulfide, nickel oxide, and especially nickel carbonyl induce acute pneumonitis, central nervous system disorders, skin disorders such as dermatitis, and cancer of the lungs and nasal cavity (Graham et al. 1975; NAS 1975; USPHS 1977; Sevin 1980; Smialowicz et al. 1984; WHO 1991; Benson et al. 1995; Table 1). Nickel carbonyl is acutely lethal to humans and animals within 3-13 days of exposure; recovery is prolonged in survivors (Sevin 1980). An excess number of deaths from lung cancer and nasal cancer occurs in nickel refinery workers, usually from exposure to airborne nickel compounds (USPHS 1977). At one nickel refinery, workers had a fivefold increase in lung cancer and a 150-fold increase in nasal sinus cancer when compared to the general population (Lin and Chou 1990). Pregnant female workers at a Russian nickel hydrometallurgy refining plant, when compared to a reference group, showed a marked increase in frequency of spontaneous and threatening abortions and in structural malformations of the heart and musculoskeletal system in live-born infants with nickel-exposed mothers (Chashschin et al. 1994). Nickel is also a common cause of chronic dermatitis in humans as a result of industrial and other exposures, including the use of nickel-containing jewelry, coins, utensils, and various prostheses (NAS 1975; Chashschin et al. 1994). Additional information on ecological and toxicological aspects of nickel in the environment is presented in reviews and annotated bibliographies by Sunderman (1970), Eisler (1973), Eisler and Wapner (1975), NAS (1975), USEPA (1975, 1980, 1985, 1986), International Agency for Research on Cancer (IARC; 1976), Nielsen (1977), USPHS (1977, 1993), Eisler et al. (1978b, 1979), Norseth and Piscator (1979), Brown and Sunderman (1980), Nriagu (1980a), Sevin (1980), National Research Council of Canada (NRCC; 1981), Norseth (1986), Kasprzak (1987), Sigel and Sigel (1988), WHO (1991), Hausinger (1993), Outridge and Scheuhammer (1993), and Chau and Kulikovsky-Cordeiro (1995). Table 1. Nickel chronology. Table 1. Date Event Referencea 220 BCE Nickel alloys made by the Chinese 1 1500’s Toxicity observed in miners of nickel 2 1751 Nickel isolated and identified. The name nickel 3 was derived from “Old Nick,” a gremlin to whom miners ascribed their problems early Purified nickel obtained 1 1800’s 1826 Nickel toxicity in rabbits and dogs demonstrated 1, 2, 4 experimentally. High doses of nickel sulfate given by stomach gavage caused gastritis, convulsions, and death; sublethal doses produced emaciation and conjunctivitis 1840’s Commercial nickel electroplating initiated 1 1850’s Commercial exploitation of nickel begins after 3 development of technology to remove copper and other impurities 1850- Nickel used therapeutically in human medicine to 2, 5 1900 relieve rheumatism (nickel sulfate) and epilepsy (nickel bromide) 1880’s Excess nickel found lethal to animals under 2 controlled conditions 1889 Skin dermatitis in humans caused by chemicals 5 used in nickel plating 1890 Extraordinary toxicity of nickel carbonyl 1 (Ni(CO)4) established 1893 Excess nickel found lethal to plants 2 1912 Nickel dermatitis documented 1 1915- Nickel applied as fungicide found to enhance plant 2 1960 growth and increase yield 4 Table 1. Date Event Referencea 1926 Nickel dust caused skin dermatitis, especially in 5 hot, industrial environments 1932 Increased frequency of lung and nasal cancers 1, 5, 6 reported among English nickel refinery workers exposed to high concentrations of nickel carbonyl 1939-1958 Certain forms of nickel found to be carcinogenic to humans 2 1943 Certain forms of nickel found to be carcinogenic to 2 animals 1965- Nickel found beneficial to