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Selenium in Agriculture: Crisis or Opportunity1
The Professional Animal Scientist 8:1-4
Selenium in Agriculture: Crisis or Opportunity1 J. E. OLDFIELD2 Oregon State University Corvallis, OR 97330
service of humanity, and more specifically, to assess the long-term effects that their findings may have on ·the environment. Selenium is a case in point. I have referred to it as a "Jekyll-Hyde" element, which it is, and it has exhibited its two personalities alternatively at various times throughout its existence. I think it makes an excellent example of the new type of environmental problems facing animal agriculture, which is the topic of this Symposium, and I would like to detail some of its complex involvements for you. Selenium was discovered, in Sweden, by Berzelius in 1818, but I'd like to start my story years later, about 1937, when A. L. Moxon (3), then at the South Dakota Agricultural Experiment Station, published a bulletin that identified excessive selenium as the cause of "alkali disease," a continuing local problem among range livestock. It adversely affected cattle and sheep, causing emaciation, loss of hair or wool, hoof changes, and lameness [James et al. (2)]. So the first face that selenium turned toward agriculture was an unfriendly one and I remember in early textbooks on animal nutrition, finding selenium described simply as a "toxic element." The link to the environment at the time of this first disclosure was twofold: soils in certain regions, like the Dakotas, were seleniferous, and certain peculiar range plants growing in the areas had the ability to accumulate selenium to levels that were highly toxic to animals (Figure 1). Then, in the late 1950s, selenium made an about-face and became an essential nutrient. The credit for this finding belongs to Klaus Schwarz, who after some very carefully controlled studies, showed that it would protect against liver damage in rats whose dietary protein was supplied by torula yeast [Schwarz and Foltz (8)]. The following year, we discovered that a perplexing problem of range cattle and sheep called "white muscle disease," on
Abstract
Selenium has been identified for over 30 yr as an essential micronutrient. Areas of soil, and consequently of forage and other crop deficiencies of the element, have been charted worldwide, and livestock fed exclusively on such indigenous feeds exhibit characteristic signs of selenium deficiency, including white muscle disease in calves and lambs, liver necrosis in pigs, and exudative diathesis and pancreatic dysfunction in poultry. Protection against these metabolic diseases, plus demonstrated benefits to reproduction and growth, has made selenium supplementation an important livestock production practice in areas of deficiency, worldwide. But selenium is also known to be highly toxic in excess, and situations in which toxic levels of selenium have accumulated have been recognized in this country and elsewhere. Concerns have been raised that continued agricultural use of selenium in domestic animal production may add to environmental burdens of the selenium and hence contribute to selenotoxicity. This paper examines issues involved and concludes that the low levels of selenium involved, together with protective mechanisms operating in the environment, render agricultural usage effective and safe. The day of "Ivory Towers" for scientists involved in agricultural research, if indeed they ever really existed, is now past. Scientists are being increasingly called upon not merely to generate new knowledge, but to interpret that knowledge in the
1Presented as part of a Symposium on Agriculture and the Environment, sponsored by t'le American Registry of Professional Animal Scientists, at Columbus, OH, June 22, 1992. 2Professor Emeritus, Dept. Anim. Sci. Reviewed by K. S. Lusby and T. W. White.
1
2
OLDFIELD
Figure 2. An extreme case of "white muscle disease" in the heart of a calf in central Oregon's selenium-deficient range area. Such affected calves appear healthy but may die suddenly if involved in any unusual exertion.
Figure 1. One ofthe peculiar, selenium-accumulating plants, Stan/eya pinnata (Prince's Plume), which cause buildup of selenium toxicity in seleniferous range areas.
central Oregon's volcanic plateau, was caused by a dietary deficiency of selenium [Muth et al. (4); Figure 2], and this started identification of other "selenium-responsive" diseases of livestock, virtually worldwide. A regular explosion of biological research with selenium followed. In areas of selenium-deficient soils (and there are many of them), careful supplementation of indigenous animals with selenium improved reproductive and productive (weight gain) performance. Livestock producers responded promptly, and selenium was given by mouth in some slow-release "bullets," by injection, and was added to fertilizers to improve the selenium status of forage plants. Selenium was inCidentally elevated from the status of an environmental prob-
lem to one of providing necessities that certain environments lacked. As one might expect, in view of selenium's known toxicity, regulatory problems occurred almost immediately. In this country, the basic concern was that selenium had been declared carcinogenic by research at the Food and Drug Administration laboratories, and therefore ran counter to the Delaney Amendment to the Food and Drug Act, which prohibited adding carcinogens at any level to diets of food-producing animals, if any residue remained in the meat. The situation was paradoxical, internationally, since selenium supplementation was permitted in New Zealand, which competed directly with our lamb producers on the U.S. market. Sheep producers in seleniumdeficient areas of the U.S. were disturbed that they could not apply results of selenium research, paid for with their tax dollars, while a major competitor could, and did. The situation was resolved when a consortium of American universities gathered data testifying to the safety of the U.S. selenium supplementation practices, which was accepted by the FDA, and when research at Oregon State University showed that selenium at physiological levels was not carCinogenic [Harr et al. (1)]. Finally, in 1974, FDA approval was given for the addition of
SELENIUM IN AGRICULTURE
selenium at levels up to 0.1 ppm in the dry matter of the diets of certain specified types of animals. As an essential nutrient, selenium is required in finite amounts in animal diets. When the diet feedstuffs do not supply these requirements, the animals suffer from deficiency disease and respond promptly and effectively to selenium supplementation. When the diet is adequate in selenium, there is no benefit and no incentive to adding selenium, and when the exposure of animals to selenium becomes too high, they may show signs of toxicity and perhaps die. The extent of selenium deficiency naturally varies from region to region, and experience in its use soon showed that in areas of extreme deficiency such as occur in my home state of Oregon and in parts of China, Finland, and New Zealand, animals could benefit from additions of more than the accepted supplementary level of 0.1 ppm in the diet. In 1979, the FDA raised the allowable level to 0.3 ppm and this level is still permissible, although hearings are currently scheduled by the FDA concerning it. Then, recently, selenium's character reverted again from Jekyll to Hyde, following the investigation of problems in the reproduction of wild birds in the Kesterson Wildlife Refuge at the north end of the San Joaquin Valley, in California [Ohlendorf (6)]. For background, one must appreCiate that the extremely productive agriculture of the San Joaquin Valley, fueled by heavy fertilizer applications and intensive irrigation, has caused concerns for some years now about eventual salinization of the topsoil. To counter these, a system of deep drains to collect irrigation runoff was built, with the effluent collected in what has been called the San Luis drain, which runs northward through the San Joaquin Valley. The original intent was for the San Luis drain to empty into the Sacramento River Delta or into San Francisco Bay, where it contents would be rapidly diluted. This plan did not materialize, for reasons of lack of financing and later on of political opposition, so the drain was terminated instead in a series of 12 evaporation ponds on the Kesterson Wildlife Refuge. During the decade of the 19805, deaths and embryonic malformations were observed among waterfowl nesting at the Refuge (Figure 3), and analyses of their tissues revealed high levels of
3
c-
Figure 3. Deformed waterfowl chick from the Kesterson Wildlife Refuge. Teratogenesis is known to result from selenium toxicity, and tissue analyses confirmed this. (Photo courtesy of H. A. Ohlendorf, University of California/Davis.)
selenium [Williams (10)]. A chain of events was charted that was apparently responsible. Near the southern end of the San Joaquin Valley, a rocky outcrop, thrust upward by earlier earthquake activity, proved to be highly seleniferous. Downward leaching of this selenium over a period of years had caused selenium to accumulate in the soils of the valley floor. From there, irrigation leaching had conveyed the selenium down into the deep drains that fed into the San Luis drain and ultimately into the evaporating ponds at Kesterson. There the selenium bioaccumulated in various types of water plants, insects, and small fish that were eventually eaten by the wild bird population, where they caused selenium poisoning. The embryonic deformities were the tip-off; teratogenesis was known to be related to selenium toxicity [Palmer et al. (7)]. There have apparently not been proven, documented problems of selenium toxicity in
4
OLDFIELD
domestic livestock in the vicinity of the Kesterson Refuge; paradoxically, selenium deficiency has been diagnosed and animals have responded positively to selenium supplementation in Tulare county, not far from the seleniferous outcrops [Nelson and Miller (5)]. Nevertheless, concerns have been raised whether selenium use as a dietary supplement in animal agriculture may contribute, over a long time period, to selenium toxicity. The continued successful supplementary use of selenium in animal agriculture for over 30 yr now argues against such concerns, as does careful monitoring of the selenium content of food crops in relevant areas of California [Tanji, Valoppi, and Woodring (9)]. The lesson to be learned, it seems to me, is one of the importance of well-controlled scientific research. The dual personality of selenium is well documented. We need to apply relevant research data carefully and appropriately. If properly used, where needed, in livestock operations, selenium can convey extensive benefits in a highly costeffective manner. And if knowledge of its toxicity at high levels is similarly carefully used, the inherent
dangers can be avoided and human and environmental safety preserved. Literature Cited 1. Harr, J. R., J. F. Bone, I. J. Tinsley, P. H. Weswig, and R. S. Yamamoto. 1967. Selenium toxicity in rats. II. Histopathology. In: Selenium in Biomedicine. O. H. Muth, J. E. Oldfield, and P. H. Weswig (Eds.) AVI Publ. Co., Westport, CT. pp. 158-178. 2. James, L. F., K. E. Panter, H. F. Mayland, M. R. Miller, and D. C. Baker. 1989. Selenium poisoning in livestock: a review and progress. In: Selenium in Agriculture and the Environment. L. W. Jacobs (Ed.) Soil Sci. Soc. Am., Madison, WI. pp. 123-131. 3. Moxon, A. L. 1937. Alkali disease or selenium pOisoning. South Dakota Agric. Exp. Sta. Bull. 311. 4. Muth, O. H., J. E. Oldfield, L. F. Remmert, and J. R. Schubert. 1958. Effects of selenium and vitamin E on white muscle disease. Science 128:1090. 5. Nelson, A. O. and R. F. Miller. 1987. Responses to selenium in a range beef herd. Calif. Agric. 41 :4-5. 6. Ohlendorf, H. M. 1989. Bioaccumulation and effects of selenium in wildlife. In: Selenium in Agriculture and the Environment. L. W. Jacobs (Ed.) Soli ScI. Soc. Am., Madison, WI. pp. 133-1n. 7. Palmer, I. S., R. L. Amold, and C. W. Carlson. 1973. Toxicity of various selenium derivatives to chick embryos. Poult. Sci. 52: 1841-1846. 8. Schwarz, K. and C. M. Foltz. 1958. Selenium as an integral part of factor 3 against dietary, necrotic liver degeneration. J. Am. Chem. Soc. 79:3292--3293. 9. Tanji, K. K., L. Valoppi, and R. C. Woodring (Eds.). 1989. Selenium contents in animal and human food crops grown in California. Publ. No. 3330. Coop. Ext. Univ. Califomia, Oakland. 102 pp. 10. Williams, M. L. 1986. Reproduction of American avocets and blacknecked stilts nesting at Kesterson Reservoir, Califomia. M. A. Thesis, San Francisco State Univ., San Francisco, CA.
Selenium in Agriculture: Crisis or Opportunity1 J. E. OLDFIELD2 Oregon State University Corvallis, OR 97330
service of humanity, and more specifically, to assess the long-term effects that their findings may have on ·the environment. Selenium is a case in point. I have referred to it as a "Jekyll-Hyde" element, which it is, and it has exhibited its two personalities alternatively at various times throughout its existence. I think it makes an excellent example of the new type of environmental problems facing animal agriculture, which is the topic of this Symposium, and I would like to detail some of its complex involvements for you. Selenium was discovered, in Sweden, by Berzelius in 1818, but I'd like to start my story years later, about 1937, when A. L. Moxon (3), then at the South Dakota Agricultural Experiment Station, published a bulletin that identified excessive selenium as the cause of "alkali disease," a continuing local problem among range livestock. It adversely affected cattle and sheep, causing emaciation, loss of hair or wool, hoof changes, and lameness [James et al. (2)]. So the first face that selenium turned toward agriculture was an unfriendly one and I remember in early textbooks on animal nutrition, finding selenium described simply as a "toxic element." The link to the environment at the time of this first disclosure was twofold: soils in certain regions, like the Dakotas, were seleniferous, and certain peculiar range plants growing in the areas had the ability to accumulate selenium to levels that were highly toxic to animals (Figure 1). Then, in the late 1950s, selenium made an about-face and became an essential nutrient. The credit for this finding belongs to Klaus Schwarz, who after some very carefully controlled studies, showed that it would protect against liver damage in rats whose dietary protein was supplied by torula yeast [Schwarz and Foltz (8)]. The following year, we discovered that a perplexing problem of range cattle and sheep called "white muscle disease," on
Abstract
Selenium has been identified for over 30 yr as an essential micronutrient. Areas of soil, and consequently of forage and other crop deficiencies of the element, have been charted worldwide, and livestock fed exclusively on such indigenous feeds exhibit characteristic signs of selenium deficiency, including white muscle disease in calves and lambs, liver necrosis in pigs, and exudative diathesis and pancreatic dysfunction in poultry. Protection against these metabolic diseases, plus demonstrated benefits to reproduction and growth, has made selenium supplementation an important livestock production practice in areas of deficiency, worldwide. But selenium is also known to be highly toxic in excess, and situations in which toxic levels of selenium have accumulated have been recognized in this country and elsewhere. Concerns have been raised that continued agricultural use of selenium in domestic animal production may add to environmental burdens of the selenium and hence contribute to selenotoxicity. This paper examines issues involved and concludes that the low levels of selenium involved, together with protective mechanisms operating in the environment, render agricultural usage effective and safe. The day of "Ivory Towers" for scientists involved in agricultural research, if indeed they ever really existed, is now past. Scientists are being increasingly called upon not merely to generate new knowledge, but to interpret that knowledge in the
1Presented as part of a Symposium on Agriculture and the Environment, sponsored by t'le American Registry of Professional Animal Scientists, at Columbus, OH, June 22, 1992. 2Professor Emeritus, Dept. Anim. Sci. Reviewed by K. S. Lusby and T. W. White.
1
2
OLDFIELD
Figure 2. An extreme case of "white muscle disease" in the heart of a calf in central Oregon's selenium-deficient range area. Such affected calves appear healthy but may die suddenly if involved in any unusual exertion.
Figure 1. One ofthe peculiar, selenium-accumulating plants, Stan/eya pinnata (Prince's Plume), which cause buildup of selenium toxicity in seleniferous range areas.
central Oregon's volcanic plateau, was caused by a dietary deficiency of selenium [Muth et al. (4); Figure 2], and this started identification of other "selenium-responsive" diseases of livestock, virtually worldwide. A regular explosion of biological research with selenium followed. In areas of selenium-deficient soils (and there are many of them), careful supplementation of indigenous animals with selenium improved reproductive and productive (weight gain) performance. Livestock producers responded promptly, and selenium was given by mouth in some slow-release "bullets," by injection, and was added to fertilizers to improve the selenium status of forage plants. Selenium was inCidentally elevated from the status of an environmental prob-
lem to one of providing necessities that certain environments lacked. As one might expect, in view of selenium's known toxicity, regulatory problems occurred almost immediately. In this country, the basic concern was that selenium had been declared carcinogenic by research at the Food and Drug Administration laboratories, and therefore ran counter to the Delaney Amendment to the Food and Drug Act, which prohibited adding carcinogens at any level to diets of food-producing animals, if any residue remained in the meat. The situation was paradoxical, internationally, since selenium supplementation was permitted in New Zealand, which competed directly with our lamb producers on the U.S. market. Sheep producers in seleniumdeficient areas of the U.S. were disturbed that they could not apply results of selenium research, paid for with their tax dollars, while a major competitor could, and did. The situation was resolved when a consortium of American universities gathered data testifying to the safety of the U.S. selenium supplementation practices, which was accepted by the FDA, and when research at Oregon State University showed that selenium at physiological levels was not carCinogenic [Harr et al. (1)]. Finally, in 1974, FDA approval was given for the addition of
SELENIUM IN AGRICULTURE
selenium at levels up to 0.1 ppm in the dry matter of the diets of certain specified types of animals. As an essential nutrient, selenium is required in finite amounts in animal diets. When the diet feedstuffs do not supply these requirements, the animals suffer from deficiency disease and respond promptly and effectively to selenium supplementation. When the diet is adequate in selenium, there is no benefit and no incentive to adding selenium, and when the exposure of animals to selenium becomes too high, they may show signs of toxicity and perhaps die. The extent of selenium deficiency naturally varies from region to region, and experience in its use soon showed that in areas of extreme deficiency such as occur in my home state of Oregon and in parts of China, Finland, and New Zealand, animals could benefit from additions of more than the accepted supplementary level of 0.1 ppm in the diet. In 1979, the FDA raised the allowable level to 0.3 ppm and this level is still permissible, although hearings are currently scheduled by the FDA concerning it. Then, recently, selenium's character reverted again from Jekyll to Hyde, following the investigation of problems in the reproduction of wild birds in the Kesterson Wildlife Refuge at the north end of the San Joaquin Valley, in California [Ohlendorf (6)]. For background, one must appreCiate that the extremely productive agriculture of the San Joaquin Valley, fueled by heavy fertilizer applications and intensive irrigation, has caused concerns for some years now about eventual salinization of the topsoil. To counter these, a system of deep drains to collect irrigation runoff was built, with the effluent collected in what has been called the San Luis drain, which runs northward through the San Joaquin Valley. The original intent was for the San Luis drain to empty into the Sacramento River Delta or into San Francisco Bay, where it contents would be rapidly diluted. This plan did not materialize, for reasons of lack of financing and later on of political opposition, so the drain was terminated instead in a series of 12 evaporation ponds on the Kesterson Wildlife Refuge. During the decade of the 19805, deaths and embryonic malformations were observed among waterfowl nesting at the Refuge (Figure 3), and analyses of their tissues revealed high levels of
3
c-
Figure 3. Deformed waterfowl chick from the Kesterson Wildlife Refuge. Teratogenesis is known to result from selenium toxicity, and tissue analyses confirmed this. (Photo courtesy of H. A. Ohlendorf, University of California/Davis.)
selenium [Williams (10)]. A chain of events was charted that was apparently responsible. Near the southern end of the San Joaquin Valley, a rocky outcrop, thrust upward by earlier earthquake activity, proved to be highly seleniferous. Downward leaching of this selenium over a period of years had caused selenium to accumulate in the soils of the valley floor. From there, irrigation leaching had conveyed the selenium down into the deep drains that fed into the San Luis drain and ultimately into the evaporating ponds at Kesterson. There the selenium bioaccumulated in various types of water plants, insects, and small fish that were eventually eaten by the wild bird population, where they caused selenium poisoning. The embryonic deformities were the tip-off; teratogenesis was known to be related to selenium toxicity [Palmer et al. (7)]. There have apparently not been proven, documented problems of selenium toxicity in
4
OLDFIELD
domestic livestock in the vicinity of the Kesterson Refuge; paradoxically, selenium deficiency has been diagnosed and animals have responded positively to selenium supplementation in Tulare county, not far from the seleniferous outcrops [Nelson and Miller (5)]. Nevertheless, concerns have been raised whether selenium use as a dietary supplement in animal agriculture may contribute, over a long time period, to selenium toxicity. The continued successful supplementary use of selenium in animal agriculture for over 30 yr now argues against such concerns, as does careful monitoring of the selenium content of food crops in relevant areas of California [Tanji, Valoppi, and Woodring (9)]. The lesson to be learned, it seems to me, is one of the importance of well-controlled scientific research. The dual personality of selenium is well documented. We need to apply relevant research data carefully and appropriately. If properly used, where needed, in livestock operations, selenium can convey extensive benefits in a highly costeffective manner. And if knowledge of its toxicity at high levels is similarly carefully used, the inherent
dangers can be avoided and human and environmental safety preserved. Literature Cited 1. Harr, J. R., J. F. Bone, I. J. Tinsley, P. H. Weswig, and R. S. Yamamoto. 1967. Selenium toxicity in rats. II. Histopathology. In: Selenium in Biomedicine. O. H. Muth, J. E. Oldfield, and P. H. Weswig (Eds.) AVI Publ. Co., Westport, CT. pp. 158-178. 2. James, L. F., K. E. Panter, H. F. Mayland, M. R. Miller, and D. C. Baker. 1989. Selenium poisoning in livestock: a review and progress. In: Selenium in Agriculture and the Environment. L. W. Jacobs (Ed.) Soil Sci. Soc. Am., Madison, WI. pp. 123-131. 3. Moxon, A. L. 1937. Alkali disease or selenium pOisoning. South Dakota Agric. Exp. Sta. Bull. 311. 4. Muth, O. H., J. E. Oldfield, L. F. Remmert, and J. R. Schubert. 1958. Effects of selenium and vitamin E on white muscle disease. Science 128:1090. 5. Nelson, A. O. and R. F. Miller. 1987. Responses to selenium in a range beef herd. Calif. Agric. 41 :4-5. 6. Ohlendorf, H. M. 1989. Bioaccumulation and effects of selenium in wildlife. In: Selenium in Agriculture and the Environment. L. W. Jacobs (Ed.) Soli ScI. Soc. Am., Madison, WI. pp. 133-1n. 7. Palmer, I. S., R. L. Amold, and C. W. Carlson. 1973. Toxicity of various selenium derivatives to chick embryos. Poult. Sci. 52: 1841-1846. 8. Schwarz, K. and C. M. Foltz. 1958. Selenium as an integral part of factor 3 against dietary, necrotic liver degeneration. J. Am. Chem. Soc. 79:3292--3293. 9. Tanji, K. K., L. Valoppi, and R. C. Woodring (Eds.). 1989. Selenium contents in animal and human food crops grown in California. Publ. No. 3330. Coop. Ext. Univ. Califomia, Oakland. 102 pp. 10. Williams, M. L. 1986. Reproduction of American avocets and blacknecked stilts nesting at Kesterson Reservoir, Califomia. M. A. Thesis, San Francisco State Univ., San Francisco, CA.