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Effects of Industrial Fluoride on Black-Tailed Deer
 
Fluoride: Journal of the International Society for Fluoride Research
July 1979 (Volume 12, Issue 3, Pages 129-135)

EFFECTS OF INDUSTRIAL FLUORIDE ON BLACK-TAILED DEER
(PRELIMINARY REPORT)


by J.R. Newman* and J.J. Murphy**

* Terrestrial Ecology Group Leader, Environmental Science and Engineer Engineering, Inc., Gainesville, Florida 32604
** Biologist, 15425 N.E. 12th St., Apt. E-346, Bellevue, Washington 98007.

Presented at the 9th Conference of the International Society for Fluoride Research, Fribourg, Switzerland, July 23-25, 1978.

SUMMARY: Symptoms of fluorosis described for cattle and other domestic animals appear to be similar for those observed in fluoride-intoxicated deer. A study of fluorosis in black-tailed deer (Odocoileus hemionus columbianus) has revealed that deer exhibit dental and osseous lesions whose severity increases with increasing levels of fluoride in the tissues. The major pathway of fluoride intoxication of the population is through fluoride contaminated browse. Greatest exposure to fluoride occurs during the winter months when browsing is confined to a few plant species with high fluoride levels.


In the last ten years increasing attention has been given to studies on the effects of fluoride and other air pollutants on wildlife (1). Most of the recent investigations involving fluoride contamination have dealt with fluoride levels in various wildlife groups (2-4). Fluorosis has been thoroughly studied and characterized for domestic herbivores whereas in naturally occurring herbivores observations on the occurrence of fluorosis are sparse. Robinette et al. (5), Karstad (6), Kay et al. (3), and Newman and Yu (7) have identified the occurrence of fluorosis in North American deer; genus Odocoileus. These studies have been limited, however, in their description of deer fluorosis. This paper presents the preliminary findings of a study to describe, in greater detail, fluorosis in a population of Columbian blacktailed deer (Odocoileus hemionus columbianus) as well as the food chain contamination of this population.

Study Area

The study area, in the Pacific Northwest, of the U.S.A. near Ferndale, Washington, is a coastal lowlands, characterized by a mixture of coniferous and broadleaf woodlands, dairy farms and pastures, residential and industrial areas. The major industries of the area include several oil refineries as well as a large aluminum plant. The aluminum plant is the primary source of fluoride emissions for the area.

Black-tailed deer as well as other wildlife are common throughout this coastal region. The Columbian black-tailed deer is a native species of deer occurring in the coastal areas of North America from central British Columbia to cental California and eastward to the crest of the Cascade-Sierra Nevada mountain range (8). For most of the year these deer are browsers eating leaves, buds, and twigs of woody vegetation. During the late spring and summer they will graze on grassy vegetation (9).

Methods

Investigation into the problem of deer fluorosis was started in 1971 and continued through 1977. Black-tailed deer from the study area were collected with the aid of the Washington State Game Department. The animals examined were either road kills or confiscated illegal hunter kills. The deer were sexed and aged. Aging was done by the tooth replacement for animals less than 2 years of age (8). Because of the abnormal tooth wear associated with fluorosis, older animals are being aged by annual layers of growth method (10). Bones were cleaned and defatted. Fluoride analysis of the distal ends of the metatarsals and ribs were analyzed following the method of Singer and Armstrong (11). Pathological analysis of the bones and teeth of the deer was made using the criteria described by Shupe et al. (12) for cattle. Radiographic analysis was made of selected bones by the use of a standard X-ray machine.

To study the food chain contamination of the population, a two year browse study was conducted by means of a modified plot-transect method of Aldous (13) and Dasmann and Hines (14). Information was collected on the browse utilization patterns and browsing preference of the deer living within a 6 km radius of the aluminum plant. Fluoride analysis was made on unwashed winter browse vegetation following the method of Weinstein et al. (15). Vegetation samples were collected from locations where active browsing was occurring.

Results and Discussion

Deer Fluorosis: Fluoride concentrations in the metatarsals of deer ranged from 638 ppm fluoride in a nine month old fawn up to 5426 ppm fluoride in a male deer over two years of age (Table 1). Those deer which came from within 5 km of the aluminum plant had fluoride levels 7 to 40 times greater than controls. The fluoride levels in these deer are similar to the fluoride levels observed in mule deer (0. h. hemionus) (3) and white-tailed deer (0. virginianus) (6) living near other industrial fluoride sources.

Table 1
F- Concentration in Metatarsals of Contaminated and Control Black-Tailed Deer
No. of Deer Age Classes
F- Conc. in Metatarsals
Average
Range
Contaminated  
1 >1 yr
638
----
4 1 to 2 yrs
3411
2475-4760
4 >2 yrs
3161
1112-5426
Controls  
1 1 to 2 yrs
442
----
2 >2 yrs
81
73-89

Symptoms similar to fluorosis in cattle were observed in Columbian black-tailed deer. These symptoms included extensive dental disfigurement and excessive tooth wear. Dental fluorosis was most obvious in deer with metatarsal fluoride concentrations greater than 2400 ppm fluoride. Commonly, the incisors were pitted and discolored along with severely worn, pitted and chipped premolars and molars. In a male deer, at least three years of age, the first, second and third molars of the lower jaw and the second, third and fourth premolars of the upper jaw were worn down to the gum line. In a doe 1 1/2 years old, pitting was quite extensive on the erupting third molars. Using the tooth damage classification system developed for fluoride-intoxicated cattle (12) 50% of the adult animals examined exhibited "moderate to excessive" dental effects. These symptoms are similar to those described by Karstad for white-tailed deer (6) and by Robinette for mule deer (5) and support the initial observations of Newman and Yu for the Columbian black-tailed deer (7). The dental lesions of deer resulting from fluoride intoxication appear to be similar to those described for cattle, horses and other domestic animals. In the Columbian black-tailed deer, the abnormal tooth wear frequently occurs on the teeth which normally show the least tooth wear (16), namely the second molars.

Preliminary results of the gross morphological and radiological analysis of the leg bones of these fluoride-intoxicated deer revealed that deer with fluoride concentrations over 2000 ppm in the metatarsals exhibited chalky white and roughened periosteal surfaces as well as a thickening of these bones. A pronounced thickening of the shaft of the humeri was observed in a male deer over two years of age with metatarsal fluoride concentration of 2076 ppm. A bone spur approximately 0.6 cm long was found on one humerus. Radiographs of the bones of these deer showed a coarseness and thickening of the trabecular pattern of the metatarsals, metacarpals, humeri and femurs, and the mandibles.

Karstad reported a high incidence of hyperostosis in the mandibles of young white-tailed deer (6). This symptom included a thickening of the mandibular bone over the erupting molars. Mandibular thickening was also observed in our study in a doe, approximately fifteen months of age. Karstad reports jaw fracturing in several of the young white-tailed deer. No jaw fracturing was observed in the Columbian black-tailed deer. Kay (4) describes the fluoride distribution in mule deer bones but gives no description of any pathological changes in the bones. He does refer to lameness in the fluoride-contaminated mule deer herd, thus indicating possible pathological effects on the legs and joints of these deer.

Food Chain Contamination: Three pathways of fluoride contamination of this deer population are possible: inhalation of large amounts of airborne fluoride, drinking water with high fluoride concentrations, ingestion of vegetation with high fluoride levels.

The first pathway was not considered significant given the habits of deer and its minor contribution to contamination in cattle and other domestic animals. The fluoride content of the natural waters of the study area was not high (17). This fact along with the continual dilution of natural waters by the moderate rainfall of the region and the dispersed habits of the deer made this second pathway an unlikely major source of fluoride contamination. Based on these considerations and the results of other studies (12), the vegetative pathway was considered to be of prime importance and was consequently evaluated.

As mentioned earlier black-tailed deer are primarily browsers throughout most of the year, especially during the fall, winter and spring. The purpose of the browse study was to determine the specific browse habits of the deer and the fluoride levels in this browse. The browse study revealed that the deer living in this mixed agro-industrial area exhibited distinct browse preference. Of the 29 species of plants available to them during the autumn, winter and early spring over 97% of their browsing was confined to 5 species of plants: 3 types of blackberry plants, 1 type of fern and 1 type of coniferous tree (Table 2).

Table 2
Browse Species Utilization of Columbian Black-Tailed Deer,
F- Levels in Control and Contaminated Browse and F- Intake Estimate
 
Ave. Browse Utilization (% to Total Utilization)
(A)
F- Concentration
Potential F- Intake Index (AxB) (C)
% F- Intake for each Browse Species (% of Total C)
 
Controls (1) (mean)
Contaminated (2) (mean) (B)
Evergreen Blackberry (Rubus lacinatus)
9.7
4.6 + 1.5
45.4 + 16.9
(20.8 to 84.6)
440
5.3
Himalayan Blackberry (Rubus discolor)
33.4
3.6 + 1.1
46.5 + 18.7
(14.0 to 86.8)
1553
18.8
Trailing Blackberry (Rubus ursinus)
9.6
7.0 + 4.1
44.4 + 18.8
(11.8 to 83.8)
426
5.1
Red Cedar (Thuja plicata)
35.8
4.6 + 2.1
72.3 + 28.9
(21.8 to 130.0)
2588
31.3
Sword Fern (Polystichum munitum)
9.8
5.6 + 9.0
333.5 + 105.2
(63.8 to 901.4)
3268
43.1
Others
1.7
---      

1 = 5 samples for each species; 2 = 20 samples for each species; ( ) = range of mean

An evaluation of the preferred browse plants showed that red cedar, a coarse woody species was most preferred. Sword fern, a species of questionable nutritional value (9) was second most preferred and blackberry, the most common and nutritious (9) browse species was third in preference. Blackberry comprised most of the utilized browse from autumn until midwinter. Red cedar (11) was used primarily from midwinter to early spring. Throughout the non-summer months sword fern was utilized about 10% of the time.

Fluoride levels in the five major browse species were quite high (Table 2) and above the standards (approx. 40 ppm) recommended for forage consumed by domestic animals (12). Fluoride levels in the preferred browse of deer varied with distance from the aluminum plant and also varied considerably within each species. Sword fern showed the highest fluoride levels (up to 901 ppm) and blackberries the lowest levels (up to 85 ppm).

To determine the relative fluoride contribution of each browse species to the diet of black-tailed deer, a potential fluoride intake index was calculated. This index was determined by multiplying the average browse utilization by deer during the non-summer months times the average fluoride concentration in each contaminated browse species within the study area (Table 2). Red cedar and sword fern, found to be the major sources of fluoride, accounted for nearly 75% of the total fluoride exposure. Exposure of these black-tailed deer to fluoride is highest during the winter months. For example, in deer living within 2 km of the aluminum plant from mid-winter to early spring the bulk of their diet consists of red cedar with more than 100 ppm fluoride, sword fern (over 450 ppm) and Himalayan blackberry (over 60 ppm). This period of high fluoride exposure coincides with the period of the year of greatest natural physical and nutritional stress for the deer.

For this deer population the level of fluoride in their diet fluctuates throughout the year. Lowest exposure occurs for a short time in late spring and early summer when they feed on newly sprouted browse and grasses. Fluoride concentrations in the grasses of the study area are reported to have ranged from 10 ppm in early summer to 146 ppm in late summer (17). During the remaining two thirds of the year the levels of fluoride increase in the diet of browsers and reach a maximum in late winter.

Acknowledgements

The authors would like to thank the Washington State Game Department, especially Jack Adkins for help in collecting the deer; Environmental Science and Engineering, Inc., in particular Dr. J.D. Bonds for fluoride analysis of the bone samples; Terri Warrington for typing of the manuscript; Intalco Environmental Laboratory and Seattle Food Chemical Research for fluoride analysis of the vegetation samples.


Bibliography

1. Newman, J.R.: Effect of Industrial Air Pollution on Wildlife. Biological Conservation, In Press, 1979.

2. Kay, C.E., Tourangeau, P.C. and Gordon, Indigenous Animals and Plants Collected systems. Fluoride, 8:125-133, 1975.

3. Kay, C.E., Tourangeau, P.C. and Gordon, C.C.: Industrial Fluorosis in Wild Mule and White-Tailed Deer from Western Montana. Fluoride, 8:182-191, 1975.

4. Kay, C.E.: Fluoride Distribution in Different Segments of the Femur, Metacarpus and Mandible of Mule Deer. Fluoride, 8:92-97,

5. Robinette, W.L., Jones, D.A., Rogers, G. and Gashwiler, J.S.: Notes on Tooth Development and Wear for Rocky Mountain Mule Deer. J. Wildl. Mgmt., 21:134-153, 1957.

6. Karstad, L.: Fluorosis in Deer (Odocoileus virginianus). Bull. Wildl. Disease Assoc., 3:42-46, 1967.

7. Newman, J.R. and Yu, M.: Fluorosis in Black-Tailed Deer. J. Wildl. Diseases, 12:39-41, 1976.

8. Cowan, I. McT.: Distribution and Variation in Deer (genus Odocoileus) of the Pacific Coastal Region of North America. Calif. Fish and Game, 22:155-246, 1936.

9. Brown, E.R.: The Black-Tailed Deer of Western Washington. State Game Dept. Bull., 13:1-124, 1961.

10. Singer, L. and Armstrong, W.D.: Determination of Fluoride in Bone with the Fluoride Electrode. Anal. Chem., 40:613-614, 1968.

11. Low, W.A. and Cowan, 1. McT.: Age Determination of Deer by Annular Structure of Dental Cementum. J. Wildl. Mgmt., 27:466-471, 1963.

12. Shupe, J.L.: Clinical and Pathological Effects of Fluoride Toxicity in Animals. In Carbon-Fluorine Compounds: Chemistry, Biochemistry and Biological Activities pp. 357-388. CIBA Foundations Symposium (Sept. 13-15, 1971). ASP, Amsterdam, 1971.

13. Aldous, S.E.: A Deer Browse Survey Method. J. Mammal., 25:130-136, 1944.

14. Dasmann, R.F. and Hines, W.H.: Logging, Plant Succession and Black-Tailed Deer in the Redwood Region. Humbolt State College, Arcata, California, 12 pp. (mimeo), 1959.

15. Weinstein, L.H., Mandl, R.H., McCune, D.C., Jacabson, J.S. and Hitchock, A.E.: The Semi-Automated Method for the Determination of Fluorine in Air and Plant Tissues. Contrib. Boyce Thompson Institute, 22:207-220, 1963.

16. Lindsdale, J.M. and Tomich, P.Q.: A Herd of Mule Deer. Univ. of Calif. Press, Berkeley, 567 pp., 1953.

17. Barci vs. Intalco Aluminum Corp.; Whatcom County Superior Court, Bellingham, Washington, 1976.


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