ENVIRONMENTAL CONTAMINATION by fluorides exposes many organisms to potentially toxic effects and may exert some stress on the ecological interrelationships among plant and animal populations in natural biological communities. Research to date has focused on human beings and species important to humans;
(1) relatively little is known of the potential ecological consequences of fluoride pollution. This article presents a literature review of what is known about the ecological effects.
In brief, the available data fall short of providing conclusive proof that any major, significant, or irreversible ecological changes have occurred, or are likeIy to occur, as a result of existing levels of fluoride pollution. (In this context, ecological effects means changes in the balance of natural ecosystems, not the very severe damage to commercial timber crops and livestock that has occurred because of fluoride pollution. See, for example, "Fluorides in the Air," Environment, April 1973.) Nevertheless, the available evidence does support the view that fluorides are pollutants with considerable potential for producing ecological damage. The compounds are potentially serious contaminants not only when present in highly localized, massive concentrations, but also when distributed in low-level amounts over a long period of time. As future research begins to bring potential ecological impacts of fluoride into better focus, it seems very likely that proof will develop that the ecosystem does suffer damage when fluoride levels of the magnitude discussed here are present.
The evidence which supports concern over potential ecological impacts of low-level fluoride pollution can be summarized as follows:
* Levels of fluoride air pollution capable of leading to significant accumulation in vegetation and consequent injury to some sensitive plants have occurred several miles or more from sources of fluoride emissions, despite air pollution controls.
* Significant fluoride accumulation has been demonstrated in insects and in birds and mammals that feed on plants in the vicinity of pollution sources. The accumulated levels have been high enough, in some cases, to be potentially toxic, and such buildup represents a major increase of fluoride in food chains.
* Water pollution from both industrial sources and municipal sewage seems capable of producing downstream concentrations of 0.5 to 3 parts per million (ppm). Concentrations are highest during summer months, when biological activity is also at its peak. Some reports of toxic effects in algae and freshwater vertebrates at 1 to 2 ppm fluoride have been published. Most invertebrate species studied can accumulate significant bodily burdens of fluoride at this level of pollution, and there are indications that aquatic vegetation may also concentrate the element. It seems very likely that fluoride is accumulating, and probably being magnified, along aquatic food chains.
* Substantial amounts of fluoride are transferred to the soil each year. The degree to which this fluoride is available for uptake by soil organisms, and the extent to which soil life may be affected by fluoride in the environment, remain unknown.
* Possible conversion of fluoride into fluoroacetate (more toxic than fluoride itself and related organic forms), and the likelihood that fluoride may enter into synergistic actions with other contaminants, greatly expand the potential for ecological damage by low-level fluoride contamination.
Fluoride Air Pollution
Estimates by the National Research Council and the Environmental Protection Agency
(3) suggest that between 120,000 and 155,000 tons of fluoride (calculated as hydrogen fluoride) are emitted into the atmosphere each year in the U.S. Fluoride is released from a variety of sources including aluminum smelting and phosphate processing operations; the combustion of coal; and the manufacture of steel, brick, tile, clay, and glass products. Reductions in fluoride emissions with increasing application of control regulations may be offset by the rapid growth of some fluoride sources, particularly phosphate fertilizer and aluminum production.
Most major fluoride sources use wet scrubbers to remove the pollutant from exhaust streams. Such controls are essential because concentrations as low as one part per billion (ppb) in ambient air are capable of causing serious damage to vegetation and may threaten livestock.(2) Concentrations of 10 ppb or higher have been measured in the immediate vicinity of a source, (4) and fluoride levels in the 1 ppb range may occur for several miles downwind of an emission point. In general, however, except downwind of a source, or in urban areas where many sources are present, the air rarely contains measurable fluorides.
Environmental Effects
According to a review by the US Department of Agriculture, fluorides have done more damage to livestock, worldwide, than any other air pollutant. (6) Some plants, including several important timber varieties of coniferous trees, are sensitive to fluoride damage. (2) Concentrations of 1.0 ppb or less can lead to long-term environmental damage because of biological magnification (the significant increases in pollutant concentrations which occur at each successively higher level in a food chain).(7) Some forage grasses can accumulate 200,000 times the level of fluoride present in the surrounding air. (2) Prolonged ingestion of contaminated forage by livestock can lead to excessive accumulation of fluoride in the bones which may, in turn, produce skeletal deformities and other damage to the animals' health. (6)
Several studies in the past five years have begun to explore potential effects of fluoride on natural vegetation and wildlife species not previously investigated. For example, when samples of lichens and mosses were exposed to pollution from an aluminum smelter in Quebec in four- or twelve-month studies at distances of from about one-half to nine miles downwind of the source, the lichens showed severe fluoride injury symptoms, especially near the source, and both lichens and mosses accumulated the pollutant. Lichens, exposed for four months about one-half mile from the source had 990 ppm, mosses, 570 ppm Even samples nine miles from the source showed 190 ppm (lichens, at four months) and 78 ppm (mosses, at twelve months). (8) Similar accounts of the effects of fluorides on lichens in Pennsylvania and Scotland have been published. (9)
Several scientific groups in Montana recently investigated the effects of fluoride on a wide range of plants and animals exposed to the contaminant. The polluted areas studied were near the Anaconda Aluminum Company smelter in Columbia Falls and the Rocky Mountain Phosphate Company plant in Garrison. Despite pollution control measures employed by both companies (reported to be 99 percent efficient in controlling fluoride emissions), fluoride contaminated the environment and accumulated in a large number of organisms.
Vegetation in a 400-square-mile area downwind of the Columbia Falls aluminum smelter accumulated significantly elevated levels of fluoride (more than 10 ppm); on more than one-quarter of that area, foliage levels exceeded 30 ppm (10) Several species of pines, firs, grasses, hay, and a large number of of shrubs and herbs were sampled, and many were found to contain significant amounts of fluoride, even at distances of more than twenty miles from the source. Insects of several dozen species were captured in the polluted area, and almost all samples had high levels of fluoride. Control samples, taken from a nonpolluted area, showed fluoride levels of 3.5 to 16.5 ppm in their tissues while insects from the study area had 6.1 to 585 ppm. Insects from the pollinator group (such as bees) generally had the highest fluoride levels. Some species that are predatory throughout their life cycles had an elevated fluoride content, suggesting the transfer of the pollutant through the food chain. (11)
University of Montana investigators analyzed the thigh bones of more than 300 animals taken from different parts of the study area. They found that skeletal fluoride accumulation was 10 to 40 times higher than that in animals taken from nonpolluted areas. Many of the chipmunks, ground squirrels, and other mammals and birds in the sample had bone fluoride levels in excess of 1,000 ppm, and several individual animals had concentrations of from 5,000 to 13,333 ppm (12)
The investigation of the area around the Garrison phosphate operation revealed a similar, although geographically more limited, pattern. The fluoride levels of many samples of vegetation exceeded the 35 ppm state standard, some samples contained more than 100 ppm. Animal specimens had above normal accumulations which correlated well with the concentrations in plants at the sites where the animals were trapped. (13)
A similar study showed significantly elevated fluoride levels in grass, and in bones of sparrows and frogs near an aluminum smelter in Czechoslovakia. (14) In general, however, few other data have been gathered on the potential impact of fluoride pollution on wildlife species.
Although the data available to date are few, they fit a pattern. The ability to accumulate fluoride from very low ambient air concentrations, and to build up levels of 10 to 100 ppm or more appears to be very widespread among different kinds of vegetation. A broad range of herbivorous (plant-eating) animals in polluted regions, sometimes many miles from the source of pollution, seem to be accumulating substantial fluoride, primarily through their diet. Levels in animals are generally higher relative to control sample levels than levels in plants, reflecting the magnified effects which occur as a pollutant moves up the food chain. Since very few samples of predatory animals have been analyzed, no solid conclusions can be drawn about the potential hazards to animals higher in food chains. However, experience with other food chain pollutants (for example, DDT) indicates that predators are often hardest hit by cumulative contaminants. It seems urgent, therefore, to obtain further data on fluoride accumulation in predatory species.
Fluoride Toxicity
The potential biological and ecological significance of fluoride accumulation, as reported in these studies, is not easy to evaluate. In general, there is little information available on the toxicity of fluoride to most wildlife species. Data on domestic plants and livestock indicate wide differences in the sensitivity, of various species to fluoride injury. (5) Some conifers are among the most sensitive plant varieties. Investigators in Montana reported that pines, especially the western white pine, were dying out over hundreds of acres near the aluminum plant in their study. They concluded that loss of the pine trees was altering the normal ecological succession of the forest community at those sites and could lead to major changes in the vegetation patterns of the area. (16) It is not known whether fluoride may be having injurious effects on other important members of the plant community in the polluted areas, but should such effects occur, they would alter not only the balance of vegetative types, but of animals as well.
Extensive studies on domestic animals indicate that 30 to 40 ppm fluoride in forage can be seriously toxic to cattle when ingested on a prolonged basis, and that sheep, swine, and other species seem to be able to tolerate higher amounts of fluoride in their feed.(6) Data on herbivorous wildlife species are not available, but it should be assumed, in the absence of contrary information, that fluoride levels of 30 ppm or more found in large areas in Montana may represent a hazard to animals which habitually feed on the contaminated vegetation.
In domestic cattle, skeletal concentrations ranging from 1,450 to over 8,000 ppm have been associated with fluorosis (fluoride poisoning), and bones from a horse injured by fluoride pollution had 1,060 to 1,500 ppm (6) Although no direct relationship was established between skeletal fluoride accumulation and health effects in the animals in Montana, it seems logical that at least those animals in which skeletal fluoride exceeded 5,000 ppm could have suffered some adverse health impact.
Some information on fluoride toxicity to insects is available. Mulberry leaves containing 10 to 15 ppm fluoride were lethal to silkworm larvae, while leaves containing lower fluoride levels led to reduced growth of the insects. (17) In other studies, (18) sodium fluoride added to flour affected the survival and reproduction of the flour beetle, Tribolium confusum; some concentrations appeared to inhibit, and others to enhance, egg production. Considerable evidence is available to indicate that honeybees are highly sensitive to fluoride. Bee colonies in the vicinity of fluoride sources have frequently been heavily damaged. Two of the Montana investigators commented that the highest accumulation of fluoride among insects in their study was in members of the pollinator group. (16) They speculated that if other pollinators should prove as susceptible to fluoride injury as the honeybee, patterns of pollination in a polluted region could be substantially altered; and, as a consequence, the abundance of many insect-pollinated plants could shift, with attendant major changes in the ecology of an entire community.
It must be emphasized that research to date has not probed for such ecological effects, and we cannot say that they are occurring in the vicinity of fluoride air pollution sources. Nevertheless, the potential for such effects seems real enough, making this an area in which more research would be desirable.
Water Pollution Sources
While fluoride air pollution primarily occurs in the vicinity industrial sources, fluoride is released into the aquatic environment by a far wider range of sources, and it seems very likely that most bodies of water are contaminated by fluoride to some extent. Some fluoride is present in waters from natural sources. Many minerals contain soluble fluoride, and when ground water passes through such fluoride-bearing rock formations, the water may become contaminated. A few sources, primarily deep wells, contain 1 ppm fluoride or more. Most surface waters contain less than 0.2 ppm fluoride, and the majority are below 0.1 ppm (19) The oceans, as the result of eons of leaching of mineral salts from the land, contain from 1.2 to 1.4 ppm fluoride, about half in the form of fluoride ion and half in the relatively insoluble, magnesium fluoride complex ion. (20) Although natural, or "background," fluoride levels in most fresh-water streams are in the 0 to 0.2 ppm range, available data indicate that concentrations above 0.5 ppm, and occasionally as high as 2 or 3 ppm, may be fairly common in watercourses contaminated by human activities.
Several human activities result in substantial fluoride input to the aquatic environment. Many of the industries which have fluoride air pollution problems are also sources of fluoride water pollution. Air pollution control equipment often produces a fluoride laden liquid waste which requires disposal. (Fluoride can be removed from wastewater by treatment with lime in settling ponds, a form of treatment which can reduce the fluoride content of an effluent stream from more than 5,000 ppm to about 5 to 50 ppm) (21) Aggregate figures for all fluoride sources are not available, but the phosphate industry may discharge from 6,000 to 30,000 tons of fluoride into waterways in the US annually.(22) The Environmental Protection Agency has proposed standards for the primary aluminum industry which, starting in 1977, would restrict fluoride in wastewater discharge to an average of two pounds per ton of aluminum produced. If all aluminum smelters were currently meeting that standard, fluoride discharges would be 4,000 to 5,000 tons per year from this industry. However, only about one-third of the plants now in operation are presently in compliance, so actual fluoride pollution from the aluminum industry is probably substantially larger. (23) Fluoride discharges from other industries are not negligible, but are probably smaller than from phosphate and aluminum operations.
Another significant source of fluoride water pollution is domestic sewage. Approximately one-half of the communities in the US which have centralized water distribution systems now add fluoride to their water supplies for the partial control of tooth decay. (24) Provision of fluoridated water for 100 million people requires the addition of approximately 20,000 tons of fluoride to domestic water supplies each year. Most of the water used in urban areas, and thus most of the fluoride added to water supplies, is returned through sewage systems to the aquatic environment.
A study of fluoride levels in sewage in 56 California cities demonstrated that domestic sewage already contains fluoride, over and above that naturally present in water or added for dental health. (26) Fluoride in human wastes, originating with fluoride in foods, was tentatively identified as the source of the excess. The investigator concluded that fluoride from toothpastes and other sources would make a negligible contribution, and that no industrial sources were contributing fluoride to the sewage samples studied. The findings suggest that the total input of fluoride into the environment from domestic sewage is probably more than the 20,000 tons estimated to be added to water supplies in communities where fluoridation of drinking water takes place. Thus, even communities not fluoridating water may release significant fluoride into receiving streams in their sewage.
The same study showed that secondary sewage treatment (biological digestion of wastes) reduced fluoride in the final effluent by an average of 57 percent, while primary treatment had no appreciable effect on fluoride levels. Even with secondary sewage treatment, however, it was concluded that significant amounts of fluoride persisted in effluents.
Fluoride is present in phosphate fertilizers, and some fluoride may be carried into surface waters in runoff from agricultural lands. It is also likey that some portion of fluorides emitted into the air is eventually carried by precipitation into surface waters. (27) While these sources may be significant, good quantitative estimates of the magnitude of fluoride input to the aquatic environment by these routes are not available.
Environmental Concentrations
Although fluoride air pollution leads to significant environmental concentrations only in the vicinity of sources, low-level fluoride water pollution appears to be more widespread.
The US Geological Survey monitors water quality at several thousand sites around the country, but fluoride data are not routinely included in chemical analyses. Fluoride readings for some streams are available, however. Many rivers have fluoride contents ranging from 0 to 0.2 ppm, but some have much higher levels. For example, 1967 data for the Santa Ana River in California showed fluoride levels of 0.9 to 3.6 ppm (average, 1.1 ppm), and single readings in the Pit River (also in California) reached 1.8 and 2.1 ppm (28) (Earlier monitoring at the same sites on the Pit River recorded levels of 0.1 to 0.2 ppm) (29)
A number of published studies relate environmental fluoride concentrations to specific sources of the contaminant. Tributaries of the East Gallatin River above the town of Bozeman, Montana, contain 0.1 ppm fluoride or less, while the river below the city's sewage outfall (the only fluoride source in the area) has been found to have concentrations of 0.3 to 0.8 ppm (30)
Fluoride concentrations of from 0.17 to 2.06 ppm were measured in a study of the Illinois River. (31) The highest concentrations occurred during the summer months, when stream volume was lowest. Fluoride sources upstream from the monitoring site included several communities with fluoridated water supplies and several major fertilizer manufacturing plants. A study of fluoride input to Narragansett Bay, in Rhode Island, showed that 36 percent of the fluoride entering the bay was due to fluoridation of water supplies in five communities on rivers feeding into the estuary. (32) In midsummer, pollution from these sources was enough to double the fluoride content of the rivers. A similar study in Japan showed fluoride concentrations of 0.15 to 1.07 ppm in rivers feeding into Tokyo Bay. (33)
Pollution near industrial sources, especially where only limited wastewater treatment to remove fluoride is employed, can be much more serious. Concentrations of 20 ppm or more were reported for the Pamlico River (in North Carolina) near a phosphate plant. (34) In most states where industrial fluoride discharge is a problem, relevant water quality standards have been adopted. Standards for drinking water sources generally are based on the US Public Health Service Drinking Water Standards and prohibit concentrations in excess of 1.5 to 2.0 ppm Some states permit levels of 5 to 10 ppm for bodies of water which are not sources of public water supplies in order to prevent toxic effects to wildlife. (35)
Ecological Effects
The critical question for biologists is whether chronic exposure to these fluoride concentrations, which may be from two to ten or more times higher than the background level, poses any significant physiological or ecological hazard to aquatic life. It seems reasonable to conclude that fluoride at these levels poses no major risk to marine organisms. (32) Both the dilution factor, and the fact that most oceanic forms evolved in an environment that contains from 0.6 to 0.7 ppm fluoride ion, suggest that potential effects on marine life should be minimal if fluoride in rivers rarely exceeds 2 ppm However, freshwater organisms evolved in an environment that was almost fluoride-free, and thus might be expected to be less well-equipped to tolerate fluoride concentrations encountered in polluted streams.
Relatively little is known about the potential impact of fluoride on either freshwater or marine organisms. A number of investigators have measured the short-term toxicity of various fluoride compounds for a good number of species, but systematic inquiries on the more general effects of long-term, low-level pollution, analagous to the Montana air pollution studies discussed above, have rarely been published. Thus, we may know the lethal concentrations for many organisms, but we have very little knowledge of the sublethal effects of fluoride on behavior or reproductive processes, or of potential accumulation of the pollutant in aquatic food chains. Yet such effects, should they occur, would probably be more important ecologically than the mortality which might result from very high, but short-lived, pollution episodes. (36)
Several investigators have exposed a variety of bacteria and microscopic animal species that live in freshwater to a range of fluoride concentrations extending well above those likely to be encountered in streams, without any demonstrable toxic effects. (37) Not many species have yet been tested, however, and the criteria for evaluating toxicity were not sophisticated. The finding that bacterial digestion of sewage removes much of the fluoride content of the effluent (26) suggests that some bacteria may accumulate fluoride from water. The importance of bacteria as a basic element in food chains makes it important to learn more about the capacity of microorganisms to bioconcentrate this contaminant.
The single-celled green alga Chlorella showed a 37 percent reduction in growth over 48 hours when exposed to a 2 ppm fluoride solution; (38) 43 ppm was reported lethal to another alga, Scenedesmus. (39) Few other data on toxicity of fluoride to aquatic plants are available, but several studies suggest that water plants can accumulate the element. Five-day exposures to 100 ppm led to a 50-told concentration of fluoride by aquatic plants, and fourteen days at 20 ppm produced a 38 fold increase. (27) Water hyacinths absorb fluoride efficiently at concentrations above 10 ppm, and to a much lesser extent at lower Ievels. (40) Several species of marine algae (exposed to 0.5 to 0.7 ppm) contained 2 to 22 ppm fluoride. Eel grass and the alga Cladophora, however, showed no significant fluoride buildup after seventy-two days in sea water with 52 ppm fluoride. (42) One Russian study found an average fluoride content of 40.5 ppm in samples of several freshwater plants, (43) and other studies strongly suggest that aquatic vegetation accumulates fluoride. (44) However, the evidence as a whole is still too fragmentary to provide a clear or systematic picture of the capacity for fluoride buildup in aquatic plants.
Effects on Aquatic Animals
Short-term fluoride toxicity data are available for a number of invertebrate species, the majority of them marine varieties. Water fleas are killed or immobilized by concentrations of various fluoride compounds ranging from 5 to 500 ppm (45) Lobsters are not harmed by 5 ppm fluoride. (46) Mussels may be killed by 1.4 to 7.2 ppm, (42) and concentrations of 20 ppm or higher for extended periods have been shown to be toxic or lethal to oysters, two species of crabs, and a sand shrimp, but not to two types of prawns. (47) More significant than the lethal effects of high concentrations, however, is the marked ability demonstrated by almost all species studied in these investigations to accumulate substantial bodily burdens of fluoride. Even animals kept in sea water containing only 1 ppm fluoride had bodily concentrations of from 100 to 300 ppm (48) The entry of fluoride into food chains through bioconcentration in aquatic invertebrates is a subject in need of much more careful research.
Studies of the effects of fluoride on fish are far more numerous than for any other form of aquatic life . (49)
Short-term lethal effects may occur at concentrations as low as 3 ppm in sensitive species (for example, rainbow trout), while other fish are not damaged until fluoride levels reach 100 ppm Water temperature, hardness, chlorinity, and other environmental factors, as well as the age and physiological state of the fish, can influence the toxicity of a given concentration of fluoride. (50)
Sublethal concentrations may have adverse effects on fish behavior or reproduction, which could be ecologically significant. Research findings are few and not confirmed, but trout eggs seem to be delayed in development and hatching by 1.5 ppm fluoride. (51)
Fish are important food-chain organisms, and the ability of many fish, like many other vertebrates, to accumulate elevated fluoride levels in their skeletons (52) can introduce the contaminant into the diet of fish-eating predators. Levels of 550 to 6,800 ppm have been reported in bones of ocean fish, and 400 to 1,600 ppm in trout from a naturally high-fluoride stream in Yellowstone National Park. Such accumulation might pose a hazard to animals that eat whole fish.
Data on other aquatic vertebrates which may be exposed to fluoride are sparse. Frogs were killed in one week by 900 ppm fluoride, (53) and decreased red and white blood cell counts were observed in frogs kept in fluoride concentrations of 5 to 300 ppm (54) There have also been indications that sublethal fluoride concentrations may adversely affect amphibian reproductive cycles. (55) Frog eggs were retarded in development but hatched prematurely in 1 ppm fluoride in well water, higher concentrations (13 to 450 ppm) had the same effects on toad eggs, and metamorphosis in tadpoles was significantly delayed by fluoride at 0 5 and 4.5ppm. (56)
Most research on the effects of fluoride on aquatic organisms dates back to the early 1960s or before, and more definitive studies are required on the potential hazards suggested here. There is also a pressing need to examine the potential impact of chronic, low-level bioaccumulation of fluoride on predatory animals higher in aquatic-based food chains. As is the case with fluoride air pollution, the logic of ecosystem energy and nutrient flow patterns suggests that species at the highest levels of a food chain are likely to bear the greatest risk of harm, but virtually no effort has been made to look for such damage. If fluoride has had such adverse effects on aquatic wildlife, they have thus far been too subtle to attract attention. In the absence of any substantive research data, it would be unwise to assume that no risks exist.
Soil Pollution Sources
Because fluoride is a common constituent of several relatively abundant minerals, most soils contain this element. The range for most normal soils is 100 to 300 ppm, but levels of up to 8,300 ppm have been found in heavy clay soil. (2) Additional sources of fluoride input to the soil may be present in many localities. Air pollution can lead to a substantial increase in soil fluoride content, both through fallout of particulate fluorides and through the absorption of gaseous fluorides in rain and snow. (57) Phosphate fertilizers may contain 0.5 to 4.0 percent fluoride by weight as an impurity. One investigator calculated that fertilizer applications in Germany were adding from 7.0 to 17.6 pounds of fluoride each year per acre of land fertilized. (58) This compared to 1.8 pounds per acre of fluoride added to the soils in his study area by air pollution, and to values of 6.1 to 19.2 pounds for each acre input from air pollution in similar studies. In the US, 5 million tons of phosphate fertilizers were applied to soils in 1973. (59) If it is assumed that the average fluoride content of that fertilizer was 2 percent by weight, this represents an input of 100,000 tons of fluoride to US soils.
Additional fluoride input to soils may occur when fluoride-containing waters are used in irrigation. No quantitative estimates are available for the magnitude of such contributions to fluoride contamination of the soil, however.
Fate of Fluoride in Soils
More than 90 percent of the natural fluoride content of soils is insoluble, or tightly bound to soil particles. (27) Most soil samples show lower fluoride content near the surface than at depths of a few feet, indicating that the soluble fraction of fluoride may be removed from the surface by water seeping into the ground. It appears, therefore, that under normal conditions very little fluoride is available for uptake by plants, even in soils that may be relatively rich in fluoride.
Research findings differ on the degree to which fluoride added by pollution or fertilization is available for uptake in the plant roots. When soluble fluoride compounds (for example, sodium fluoride) were added to soils in concentrations of 150 ppm or more during one experiment, significant uptake by plants occurred. (60) Other experiments showed that a substantial amount of fluoride was removed from polluted soils by water. (61) On the other hand, it has been found that as much as 90 percent of fluoride from fertilizers and air pollution may remain in the soil; (58) another report showed that some soils, especially those with relatively high calcium
content, were very effective in fixing fluoride, with the result that little was available for plants to incorporate. (62)
It seems very likely that a number of soil characteristics, as well as other environmental factors, can have a marked influence on the availability of fluoride to plants. For example, fluoride is more readily available in sand or acid soils than in high-clay soils. (63) Also, a relationship exists between the type of nitrogen fertilizer applied and the toxicity of fluoride to crops. (64) The use of certain boron-containing fertilizers leads to a dramatic increase in the accumulation of fluoride in the leaves of fruit trees. (65)
