Monchegorsk ecology of beautiful tundra
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ABSORPTION OF HEAVY METALS IN WILD BERRIES
AND EDIBLE MUSHROOMS IN AN AREA AFFECTED BY SMELTER EMISSIONS

V. SH. BARCAN, E. F. KOVNATSKY and M. S. SMETANNIKOVA
Lapland Biospheric Reserve, Zeleny, 8, 184280 Monchegorsk, Russia;
Institute of Experimental Meteorology, 249020, Obninsk, Russia
(Received 22 November, 1994; accepted in final form 12 November, 1996)


Abstract

The total concentrations of nickel, copper, chromium, strontium, arsenic, lead, cadmium and cobalt were measured in berries and mushrooms, as well as manganese and iron in mushrooms. The study area (about 3500 km2) is situated on the border of the northern taiga and tundra forests (68-690 N) and is affected by emissions from the extensive Ni-Cu smelter complex at Monchegorsk, Kola Peninsula, NW Russia. Part of the study area, extending along the railway line used for transporting apatite concentrate, contains elevated quantity of strontium. Berries of Vaccinium vitis-idaea (82 samples), Vaccinium myrtillus (28), Rubus chamaemorus (42) and Empetrum hermaphroditum (40) and mushrooms of Leccinum auantiacum (47 samples), Leccinum scabrum (32), Russula vesca (25), Lactarius torminosus (8), Lactarius trivialis (9), Suillus luteus (10) and Xerocomus subtomentosus (20 specimens) were collected from 98 locations during 1987-1992. The nickel and copper concentrations in the berries, and nickel in mushrooms, correlated satisfactorily with the corresponding metal concentrations in the soil. The berries and mushroons growing over an area of at least 3000 km2 around the smelter complex are unsuitable for human consumption due to the elevated nickel concentrations caused by the smelter dust emissions. The berries and mushrooms gathered in the studied polluted forests were found to be contaminated by nickel by a factor of 15-30 times (berries) and 15—40 times (mushrooms) more than the background level. Increased levels of strontium were found close to the railway line. The concentrations of all the other metals in the studied area did not exceed sanitary standards.

Keywords: absorption, edible mushrooms, fruit bodies, heavy metals, sanitary standards, wild berries

1. Introduction

Inhabitants of North provinces of Russia, Norway, Sweden and Finland consume a lot of wild berries and edible mushrooms. The scale of consumption is illustrated in our estimation as follows. Inhabitants of towns in the centre of Kola Peninsula gather approximately 20-30 kg of berries and 20^1-0 kg of mushrooms per family annually; and many gather hundreds of kilograms of these plants. The centralized purchasing of berries in the Murmansk province is for the resale in other Russian regions and abroad. For example, commercial organizations in Monchegorsk buy 40-50 tonnes of cowberry Vaccinium vitis-idaea per season, and some companies buy 1000-1200 tons of cowberry per season targeted specially for export. The demand for these attractive food items increases continually. It should mentioned that most of the berries, and specially the mushrooms, are gathered in the most densely populated parts of the Kola Peninsula, where the industry is concentrated, including the nonferrous smelter complexes and that these territories are affected by industry emissions. It has been shown earlier (Barcan et al., 1990,1993-a) that wild berries and edible mushrooms growing in an area of ca. 2000 km2around the Smelter complex contain nickel concentrations exceeding sanitary standards and hence are unsuitable for human food. The medical and sanitary approach to the problem seems to be important because of the consumption of foods polluted by the toxic heavy metals augments the risk of human diseases. The object of the study was to document the concentrations of toxic metals As, Cd, Cr, Ni, Pb, Sr and some essential metals (Cu, Fe, Mn) in wild berries and edible mushrooms growing in the zone affected by the emissions of the smelter complex, and to estimate the area where the concentrations of toxic metals exceed sanitary standards.



Figure 1. Map of the area with high berry nickel concentrations

2. Site

The study site is situated near the town of Monchegorsk (68-690N, 330E), Kola Peninsula (Figure 1), on the border of the northern taiga and near-tundra forest zones. Lapland Biospheric Reserve 2800 km2 area is situated to west of Monchegorsk. The landscape is very diverse and includes coniferous and mixed forests, maintain tundras, peat bogs and many lakes.

3. Climate

The climate type is maritime subarctic, the number of days having the temperature more than 50C is 109-130, the thermal sum during the vegetation period is 13000C, the mean annual temperature is -20C, the mean temperature of January and July is -140 to -90C and 110C to 150C respectively, the mean temperature of the warm season (May - September) is 7.50C to 10.60C, the annual sum of precipitations is 329 to 445 mm, the mean relative humidity is 72 to 81 %, the mean wind velocity is 3.0 to 5.4 m/sec, the prevaling direction of winds is meridional (Yackovlev, 1961).

4. Vegetation

The vegetation in the region is of the North European taiga zone type. Scots pine forest accounts for 40% of the area, spruce forest 30%, and open bogs 30%. The main forest tree species are Pinus sylvestris and Picea abies var. obovata, and Betula pubescens and Populus tremula are found in all areas. The following forest vegetation types are predominant: Pinetum empetroso-cladinosum, Pine-tum empetroso-cladinoso-hylocomiosum, Piceeto-Pinetum empetroso-myrtilloso-hylocomiosum, Pineto-Piceetum empetroso-myrtilloso-hylocomiosum and Picee-tum empetroso-myrtilloso-hylocomiosum. The bog complexes are high dwarf-shrub Sphagnum-Rubus bogs and aapa (Payanskaya-Gvozdeva, 1990).

5. Soils

The predominant forest soil type is illuvial humus-ferriferous podzol, with a thick organic horizon (Ao), a rather shallow profile (30-60 cm), and very clear differentiation of the soil horizons. The peat soils consist mainly of Sphagnum peat (Below and Baranovskaya, 1969).

6. Emissions

The emission source is a large copper-nickel smelter complex, named 'Severon-ickel', using sulphide ores from the Kola Peninsula and from Norilsk in Siberia. The smelter is the only metallurgical factory in the region. During the study period 1987-1992 annual emissions (calculated on the basis of production losses) were about 220 to 240 thousand tons of sulphur dioxide, and nickel and copper 3000-4000 tons each. Emissions of other metals were considerably lower. The reference data of composition of dust collected from below the chimneys of different metallurgical processes are given in Table I. The dust corresponds approximately to that deposited on the surrounding landscape. The composition of the dust from emission sources varies and is dependent on the raw material composition and the quality of gas purification. Nickel and copper are prominent in dusts among the heavy non-ferous metals. In some kinds of dust lead and arsenic are markedly concentrated - to 0.6 and 0.9% respectively. The chromium and cadmium concentrations are small - 0.04 and 0.2% respectively. The source of strontium contamination is dust from the apatite concentrate during transportion by rail and from the nepheline tail depot, i.e. waste products resulting from apatite ore dressing! Air-borne pollutants are mainly spread to the north and south of the point source owing to the prevailing wind directions.

Table 1
Some metallurgical dusts of Severonickei smelter complex
Element Concentration, % nickeli-ferous Copper bearing Detection limit %
1 2 3 4
Ni8.43.12.11.811.00.0025
Cu3.23.21.41.771.70.0025
Co0.20.20.10.10.50.0125
Fe33.812.413.011.33.20.0125
Al1.71.01.3 1.3 < d.lim.0.0025
Zn-1.81.41.4-0.0020
Pb-0.60.020.3-0.0125
Cr-0.04 -0.07,-0.0125
Mn-0.050.060.07-0.0125
As0.10.90.10.150.10.0125
Se0.010.040.01-0.0125
V-0.010.01-0.0125
W-0.05-0.09-0.0125
Ti-0.10.010.1-0.0125
Mo-0.2-0.05-0.0125
Cd-0.040.030.02-0.0025
Ca2.10.351.11.6 < d.lim.0.0025
Mg3.40.302.33.0 < d.lim.0.0025
Stot3.2--3.215.70.0005
Si7.12.415.015.00.20.01


7. Metal Toxicity and Sanitary Standards


Metal absorption by berries and mushrooms never reaches acute levels, because the plant perishes before (Kabata-Pendias and Pendias, 1989), but the chronic poisoning of organism takes place when products containing elevated concentrations of toxic metals are continuously consumed. Therefore only the after-effects of chronic metal poisoning are considered below.

7.1. MAJOR TOXIC METALS WITH MULTIPLE EFFECTS

7.1.1. Nickel

Nickel is a respiratory tract and dietary carcinogen in workmen in the nickel-refining industry and in inhabitants near smelters (Doll et al., 1977; Sunderman, 1981,b; Pedersen et al., 1978). Dietary nickel intake in absence of emission affects was estimated to be average 165 ± 11 /xg day-1 (Myron et al., 1978).

7.1.2. Lead

Lead, the most ubiquitous toxic metal, is detectable in practically all phases of the abiotic, inert environment and in all biologic systems. The major urban source of lead is alkyl lead compounds, used as gasoline additives. The major source of daily intake of lead is in food and beverages (NAS, 1972; Nriagu, 1978). Lead is toxic to most living organisms and there is no demonstrated biological need. Lead shows toxic neurologic, hemetologic, hametotoxic and renal effects (Singhal and Thomas, 1980; Rutter and Jones, 1983). It is clear that lead can induce cancer in kidneys, but the evidence that lead is carcinogenic to humans is very limited (IARC, 1980). The Provisional Tolerable Weekly Intake (PTWI) of lead is recommended by WHO for adults of 50 fig kg-1 of body weight, and 25 fxg kg-1 of body weight for infants and children (WHO, 1993), It should be emphasized that these PTWI-s apply to lead from all sources.

7.1.3. Cadmium

Cadmium is more readily taken up by plants than other heavy metals such as lead (WHO, 1977). Cadmium has an extremely long biological half-life in humans and is accumulated in body tissues, particularly in the liver and kidney. The principal long-term effects of low-level exposure to cadmium are chronic obstructive pulmonary disease and emphysema and chronic renal tubular disease. There may also be effects on the cardiovascular and skeletal systems (Nomiyama, 1980; Friberg and Kjellstrom, 1981). There have been numerous experimental studies supporting the potential carcinogenicity of cadmium (Piscator, 1981; Armstrong and Kazantzis, 1983). Joint FAO/WHO Expert Comittee on Food Additives allocated a PTWI of 400-500 ng of cadmium per person, or 7 /ig kg-1 of body weight (WHO. 1993).

7.1.4. Chromium

Chromium is abundant element in the earth's crust and occurs in oxidation states ranging from Cr(II) to Cr(VT), but only the trivalent and hexavalent forms are of biologic significance. Trivalent chromium is the most common form found in nature, and chromium in biological materials is probably always trivalent, because the hexavalent form is one of stongest oxidants of organic matter. There is no evidence that trivalent chromium is converted to hexavalent forms in biological systems (NAS, 1974; Fishbein, 1981). Exposure to chromium is associated with cancer of the respiratory tract (Norseth, 1981). The greatest risk to cancer is attributed to exposure to acid-soluble, water-insoluble or slightly soluble hexavalent chromium. Tnvalent chromium compounds are considerably less toxic than the hexavalent ones, but Norseth (1981) suggests that trivalent chromium should be considered as an equally potent carcinogen as are the hexavalent compounds. Chromium in food is low, and estimates of daily intake by humans is under 100 p,g, mostly from food, with trivial quantities from most water supplies and ambient air (Klaassen et al., 1986).

7.1.5. Arsenic

Arsenic is mainly transported in the environment by water, and airborne arsenic is generally due to contributions from industrial contamination. Non-worker polula-tions living near point emission souces of arsenic to air may have increases in lung cancer. The relationship of ingestion of arsenic with skin cancer and angiosarcoma and inhalation of containing particles arsenic and lung cancer establishes arsenic as a human carcinogen (Pershagon, 1981; Leonard and Lauwerys, 1980). This specific effect seems to be related to the cumulative dose of arsenic (WHO, 1981). Most, foods contain some level of arsenic. The total daily intake of arsenic by humans , without industrial exposure is usually less than 0.3 mg day-1 (WHO, 1981).

7.1.6. Strontium

Strontium isomorphously replaces calcium in bones and, being more mobile than calcium, it causes the Urov desease (Osteoarthritis Deformans Endemica) (Sergievsky, 1948).

7.2. ESSENTIAL METALS WITH POTENTIAL FOR TOXICITY

This group includes four metals generally accepted as essential: cobalt, copper, iron manganese. Each of the four essential metals has three levels of biological activity, trace levels required for optimum growth and development, homeostatic levels (storage levels) and toxic levels. For these metals, environmental accumulations are generally less important routes of excess exposure than accidents or occupation (Klaasen et al., 1986).

8. Material and Methods

8.1. BERRY AND MUSHROOM SAMPLES

The berry and mushroom samples were collected during 1987-1992. The following species of berries were collected and analysed: Vaccinium vitis-idaea (82 samples), Vaccinium myrtillus (27), Rubus chamaemorus (31) and Empetrum hermaphrodi-tum (39). The mushroom species were Leccinum aurantiacum (46 samples), Lec-cinum scabrum (32), Russula vesca (25), Xerocomus subtomentosus (25), Suillus luteus (10), Lactarius trivialis (8) and Lactarius torminosus (8). The samples were taken primarily from sites which were the most heavily polluted and those most frequently visited by people. As a rule these sites were the same. The total number of sampling points was 98. Each sample consisted of 200-1000 g fresh berries or fresh mushrooms (fruit bodies). The berries and mushrooms were not washed before drying in order to avoid leaching of mineral components and alteration of moisture content. The soil admixture was removed from the mushrooms, which were then cleaned using a wet cloth, changing after each sample. Large mushrooms were cut up. The samples were dried at 40-500Ñ in a warm air flow. The samples were weighed before and after drying in order to determine water content. The dry mushrooms were crumbled up.

8.2. SOIL SAMPLES

The soil study of the investigated area is the subject of a separate research therefore only summary soil characteristics are considered here. The soil samples were collected from the same places where plants samples were taken, but not necessarily from the same plots. The disposition of soil sampling plots was at random as well as that of plant sampling plots. The soil samples (triplicates) were cut by a spade and knife from the whole depth of the organic layer Ao of forest podzol, and from the upper 5 cm layer of peat bog. The samples were sorted out manually, the roots, stones, gravel and other external materials were removed, and after drying at room temperature, were kneaded and averaged by shoveling. A 2-mm mesh-size limit was used.

9. Chemical Analysis


The chemical analyses of dust were made after extraction with a mixture of concentrated HC1 and HNO3 (3:1 aqua regia), analyses of soils, berries and mushrooms -after ashing at 4500Ñ - by the same extraction with aqua regia. The total metal concentrations in solution were determined by the following methods: Ni, Cu, Co, Fe, Zn, Pb by atomic absorption spectrometry with a Perkin-Elmer 3030B spectrometer in a flame, Al, Cr, Mn, Se, V, W, Ti, Sr, Mo, Ca, Mg with an AtomSc^n 25 emission ISP spectrometer, trade name Thermo Jarrell Ash. Cd and As was determined by AAS with a Perkin-Elmer 3030B spectrometer in a furnace cuvette. The Ni and Cu total concentrations in mushrooms and berries for control were determined also by colorimetric methods, namely Ni after complexation with dimethylglyoxime, and Cu by reaction with lead diethyl carbamate after extraction with chloroform (Hillebrand and Lundell, 1953; Sandell, 1959). Total sulphur concentration in a dust was determined with the LECO SC-444 instrument by burning in a current of oxygen and then by infrared detection of sulphur dioxide in the obtained gas (Instruction Manual LECO SC-444, 1991). Total silicon concentration in a dust was determined by standard operation with alkaline melting (Ponomaryov, 1955). Detection limits of elements are shown in the relevant chapters of that paper.



Table II
Maximum tolerable concentrations of some metals in wild berries and edible mushrooms (ppm w.w.)
Ni Cu Pb Cd Cr As
Berries0.55.00.40.030.10,2
Mushrooms0.510.0 0.5 0.1 0.5


Table III
Range of concentrations of heavy nonferrous metals in forest podsols
Concentration in hor. Ao, pp, d.w.
PbAsSrCr CdCo -
Polluted areas 12-723-4033-1974-31 0.3-1.415-120
Background areas 10-462-9 29-21310-1000.3-0.82-15


10. Calculations and Statistics


Soil and plant samples were gathered randomly, and the maps were made. After that the transects including most number plots were chosen, and the dry weight metal concentrations in berry and mushroom samples were compared with the distance and direction from the pollution source, and with the corresponding total concentrations in the soil. When selecting the plots to include in the tables obtained results of metal concentrations in berries and mushrooms were broken up into three groups by nickel contents. The first and third groups include lowest and highest concentrations of nickel, obtained in the present work, and the second group include the intermediate ones between the first and second. Wet weight metal concentrations were compared with the maximum values tolerable for human consumption. The plot was attributed to polluted type in the case when even one plant species was polluted to more than tolerable level, i.e., if, for example, the nickel concentration in the samples of five species gathered on the given plot is tolerable, but at the same time nickel in the single species is above the sanitary standard, the plot is accepted as polluted one. The system of Food Quality Control accepted in Russia and based on the conception of Maximum Tolerable Concentrations (MTC) was used - (Sanitary norms, 1982, 1986, 1989) - see Table Ï. Having no acess to licensed software, we use the original program, elaborated by A. Koshurnikov, for calculation of linear regression by the method of least squares. Non-orthogonal regression with minimization of sum square roots of standard deviation on ordinate (function) was used. The type of regression function was accepted depending on the calculated correlation coefficient, i.e. after the calculation of sixteen functions we chose the one which had the maximum correlation coefficient and the minimum dispersion.



Table IV
Concentrations of heavy nonferrous metals in hor Ao of forest podzol close the railway line
The distance Concentration, ppm d.w.
of the plot from the railway, mNiCuCrPbAsSrCdCo
10202207-15534571.112
35404277193912030-2.128
60113743253846080.5-
8516310826760155680.612
110108801201233550.5-


11. Results


11.1. HEAVY METALS IN SOILS

Nickel and copper concentrations in the upper organic layers of the soils decreased hyperbolically with the increasing distance from the point source (Figure 2). The Ni and Cu concentrations in the affected podzolic and peat soils were very high -10 to 12 km from the smelter the Ni and Cu contents in the Ao horizon were 2000-2700 ppm and 1200-1600 ppm, respectively, i.e. 40-55-fold higher compared to the background levels. 30 km to the South of the smelter the concentration exceeded the background 20-fold, and 40 to 50 km to the NE 2- to 3-fold. The range of other heavy nonferrous metal concentrations in forest podzols is shown in Table Ø. As distinct from nickel and copper the regular relations of concentrations of these elements and distance and direction was not observed. In comparison with the background, the tendency of increasing of arsenic, cobalt an4 lead was observed in the affected area, but the content of cadmium increased insignificantly. The concentration of chromium in the background areas was found to be greater even than that around the town of Monchegorsk, but the strontium concentration did not differ. At the same time the content of strontium and some other metals in the soil of plots close to the railway line Murmansk-Petersbourg was found to be strikingly different from the afore-cited values - see Table IV. This railway is a haulage route for apatite concentrate which contains strontium. The concentration of the latter in upper soil organic layer was found to be increased from 350 ppm to 3500 ppm at a distance from 110m to 10m from the railway, and the concentration of chromium increased from 120 ppm ro 1940 ppm. The soil concentrations of lead, arsenic and cadmium were found to be also markedly elevated close to this railway.

5
Table V
Metal concentration in berries
Plot
¹/¹		 Plot position
in relation to Smelter		 Concentration,
ppm d.w.
Distance
km		 Azimuth
degrees		 Ni Cu As Cd Co Cr Pb Sr
Vaccinium vitis - idaea
4142269753------
46280.370.040.110.52.32.1
42918030230.200.030.050.30.52.2
7291551524------
501220615190.060.030.030.21.76.1
1414229110.090.060.080.31.21.6
1010202615------
1112222111------
6714229110.090.060.080.31.21.6
281190450.030.060.120.10.51.8
51620690.070.040.070.20.82.3
8539198560.060.040.040.90.41.8
9071310360.050.030.080.21.12.1
8983305260.110.040.071.51.12.1
Vaccinium myrtillus
49122059140.080.050.090.41.50.9
35181101110------
947243450.040.050.070.61.02.1
5232188680.250.030.050.51.61.3
5633213460.050.020.040.41.14.5
95562655110.040.040.050.50.83.1
8883295790.050.030.090.31.31.6
5532223550.020.030.050.60.71.9
Empetrum hermaphroditu
42918083115------
943119345720.090.030.080.51.51.0
491220525310.020.010.090.30.70.7
563321310130.020.040.050.20.82.1
543119412170.030.020.060.30.61.4
5332190580.040.050.040.20.50.5
516205110.070.020.090.10.40.4
8647199460.020.020.030.20.30.8
8750203470.020.020.080.30.70.4
517240370.050.040.07040.705
Rubus chamaemorus
2103305719------
3173504817------
416154319------
501220324240.050.060.200.21.90.3
621080.130.070.081.63.33.9b
51261973024------
83271979110.050.070.140.30.31.0
33420.170.020.081.52.811.0b
533219514170.030.070.180.51.93.1
14220.040.080.400.94.720.2b
7920959130.070.060.170.62.112.7a
221007535------
821024314130.100.090.120.71.31.3
32480.070.090.40_2.68.9b


a - Close to the railway.
b - Sepals.
- Not determined.


11.2. HEAVY METALS IN THE BERRIES

The dry residue after drying was, in V. vitis-idaea 14.3 ± 1.4% (n = 79), in V. myrtillus - 12.2 ± 1.6% (n = 25), in E. hermaphroditum- 11.2 ± 1.4% (n = 34) and in R. chamaemorus it was 14.7 ± 1.5% (n = 24). The examples of highest, mean and lowest metal concentrations found in the berries are shown in Table V. The nickel and copper concentrations in the berries V. vitis-idaea, E. hermaphroditum and R. chamaemorus depended on the distance and direction from the emission source: in general they decreased hyperbolically (Figure 3). The maximum Ni and Cu concentrations in these berries from the most polluted areas exceeded the lowest found levels as follows: V. vitis-idaea - 48- and 11-fold, E. hermaphroditum - 28- and 19-fold, and R. chamaemorus - 21- and 22-fold, respectively. The level of nickel and copper absorption by berries V. myrtillus was found to be 4-11 ppm, and 5-14 ppm, respectively, i.e. less than by three above-cited species, and no dependence on the distance was observed. Judging by relationship 'distance-concentration', the lowest concentrations are reached at the following distances from the source of emissions: in V. vitis-idaea - nickel 2-3 ppm at 80 km, copper 6 ppm at 40 km; in R. chamaemorus - nickel 3 ppm at 80 km, copper 5-6 ppm at 80 km, and in E. hermaphroditum - nickel 3-4 ppm at 50 km, copper 6-7 ppm at 50 km.

A map of the area where berry nickel concentrations exceeded sanitary standard is shown in Figure 1. As mentioned above, when making this map the plot was attributed to polluted type even in the case when only plant species was polluted more than tolerable level. Nickel concentrations in all the berry species were higher than the tolerable level at almost all the sampling points in the area (more than 3000 km2). Only at distances of 53-80 km from the smelter the nickel concentration was less or equal to the tolerable level. The points where the berry nickel and copper concentrations were higher than the background values coincided with each other. However, although the absolute values of copper accumulation were close to those for nickel, the sanitary standard for copper is ten times higher than that for nickel. The copper concentrations in the berry samples therefore did not exceed the tolerable levels. None of the other metals determined (chromium, lead, arsenic, strontium, cadmium and cobalt) displayed any correlation between the berry accumulation level and the location of the sampling plots relative to the smelter, because the smelter complex is not an essential emission source of these metals - Table V.

The absorption of all analysed metals by sepals of R. chamaemorus was found to be significantly more than the absorption by berries - see Table V. The cadmium, chromium, lead and arsenic concentrations were less tolerable levels in practically all the berry samples. No tolerable cobalt and strontium levels are normatively accepted, but elevated strontium concentrations (6-13 mg kg-1 d.w.) were found near the Murmansk - St. Petersburg railway line - Table V.

11.3. HEAVY METALS IN THE MUSHROOMS

The dry residue after drying mushrooms is variable and depends on weather, i.e. the more rains, the more moisture. The dry residue after drying of species L. aurantiacum and L. scabrum was found to be 9 ± 1.7% (n = 75 in sum), of species X. subtomentosus and 5. luteus - 13.3 ± 3.3% (n = 26 in sum), and of species R. vesca, L. torminosus and L. trivialis - 12.9 ± 2.6% (n = 40 in sum). The examples of the highest, mean and lowest metal concentrations found in the mushrooms are shown in the Tables VI-VIII. The nickel concentrations in the mushroom species L. aurantiacum, L. scabrum, X. subtomentosus, S. luteus and/?, vesca showed a similar dependence on the distance and direction from the smelter as the berries (Figure 4).

The maximum nickel concentrations in the samples from polluted areas exceeded the lowest found levels as follows: L. aurantiacum 19-fold, L. scabrum - 9-fold, S. luteus - 4-fold, X. subtomentosus - 6-fold and R. vesca - 42-fold. Concerning species L. torminosus and L. trivialis, one observes the general tendency of nickel concentration decrease with distance from the emission source - Table VIII.

A map of the sampling points with high mushroom nickel concentrations is shown in Figure 5. The overwhelming majority of the samples contained nickel concentrations above the tolerable level. The tolerable copper concentration in mushrooms is 20 times higher than that of nickel, and was therefore not exceeded in all the samples. The concentration level of copper in mushrooms is higher, than in berries. The difference between the copper concentration in mushrooms from the polluted and background areas was considerably less than that for nickel. Perhaps mushrooms absorb certain quantities of copper as a vitally necessary element independently on its content in the soil. None of the other metals determined (chromium, lead, arsenic, strontium, cadmium, cobalt, manganese and iron) displayed any correlation between the mushroom accumulation level and location of the sampling points relative to the smelter-Tables VI-VIII.

The concentrations of chromium, cadmium, lead and arsenic were below the tolerable levels in practically all the mushroom samples. No tolerable cobalt and strontium levels are available. Manganese and iron are common metals in podzolic soils, and their concentrations in the mushrooms were rather high; the levels were approximately the same in the different species. However, the iron concentration (1500-2500 ppm d.w) in X. subtomentosus was 25^10 times greater than that in the other species. This mushroom species can be used as a source of physiologically assimilatable iron.







Table VI
Metal concentration in mushrooms
Plot
¹/¹		 Plot position
in relation to Smelter		 Concentration,
ppm d.w.
Distance
km		 Azimuth
degrees		 Ni Cu As Cd Co Cr Fe Mn Pb Sr
Leccinum aurantiacum
2348038133
1112222158
69221513490.060.130.252.049201.40.9
75139311440.150.150.301.043222.60.3
351811010490.110.07-0.2394-2.11.2
86471999370.030.090.170.887491.62.6
628024512450.13.0.220.450.461-'2.31.3
1427477320.030.100.121.040261.70.8
1550454540.030.110.200.957310.81.0
88832952321.30.080.120.6170-0.91.3
Leccinum scabrum
43141902828
22001737
864719913290.100.090.210.557132.30.3
73264511230.100.070.180.559-2.20.5
68222712270.100.100.150.653562.01.5
9617708160.160.080.120.548155.20.6
2610856180.120.100.210.471282.20.9
85391986160.070.060.180.539-2.40.3
6922154220.60.050.070.595-1.10.2
1550453170.060.070.130.635-1.70.2
57100190314


Table VII
Metal concentration in mushrooms
Plot
¹/¹		 Plot position
in relation to Smelter		 Concentration,
ppm d.w.
Distance
km		 Azimuth
degrees		 Ni Cu As Cd Co Cr Fe Mn Pb Sr
Xerocomus subtomentosus
13203318340.030.320.470.3--1.70.4
38 1912719440.110.180.180.52027553.15,5a
5 162011230.050.140.120.31080523.00.7
28119013390.070.100.240.51662511.70.4
1427478220.060.100.090.51530541.81.0
7326453320.050.140.180.61932-1.31.3
62802455250.100.060.10-2008-2.41.4
921652955250.090.070.110.21336-2.70.2
Suilus luteus
69 221510230.060.090.120.437212.31.2
68 222711300.040.120.160.456-2.01.4
87 5020310250.050.080.130.470-2.11.9
16 3047721
21 6075217
21 6075217
61 53220323
63 80247420


12. Discussion and Conclusion


The changes of nickel and copper concentrations in soils and berries away from the emission source are similar (Figures 2 and 3). The conjugation of two relations, viz 'distance-metal concentration in soil' and 'distance-metal concentration in berries' results the directly proportional relation between metal concentrations in soil and berries - see Figure 6. It seems to be obvious that metal absorption by berries is caused by its absorption in soils, for the mineral nutrition of plants is realized by roots. Sedimentation of dust particles on a leaf plate, the subsequent ionization of metal and absorbtion of ions through the stomata, as well as an irrigation of leaves by rains or thawing snow, containing heavy metals, are also possible.

But direct absorption of metals by berries seem to be impossible, because berries are protected from external impact much better than leaves. The same consideration concerning nickel is correct for mushrooms as well, but copper is absorbed by mushrooms super-proportionally, i.e. if the copper content in soil in equal to mickel or less, the copper content in mushrooms is 2-3 times more than that of nickel. Perhaps, this is a physiological property of mushrooms, analogous to what has been mentioned concerning other mushroom species (Byrne and Ravnik, 1976). None of the other metals determined (chromium, lead, arsenic, strontium, cadmium and cobalt) displayed any correlation between the berry and mushroom accumulation level and the soil level of these metals, because the Smelter Complex is not an essential emission source of them. The source of strontium contamination was identified - dust from the apatite concentrate during transporation by rail. The pollution of berries and mushrooms by heavy metals shows that there is a serious environmental pollution by these metals in the region.





This is an extremely important finding because these plants are an essential source of food for people in Northern Russia. Forest berries and mushrooms are also essential sources of food for many species of animals. A Joint FAO/WHO Expert Comittee on Food Additives recomended for the control of some metals intake a Provisional Tolerable Weekly Intake (PTWI) of them, expressed in terms of intake per kg of body weight. This quantity includes the intake from all sources - inhalation, water and food. This is justified from the point of view of medical science, but is not very useful for physicians and control bodies. More convenient is the system of Maximum Tolerable Concentrations (MTC) accepted in Russia. The values of MTC are calculated proceeding from the share of given food in the food allowance, assuming that the volumes of consumed water and inhalation are constant. The calculated daily intake of some metals with berries and mushrooms, gathered in a radius of 30 km around the town of Monchegorsk, is shown in Table IX. From these foods the nickel daily intake doubles in comparison with the level 165 mg, which is the ordinary one in nonpolluted areas (Myron et al., 1978). It should be noted that cultivated plants in the studied area are also contaminated by crops (oats, rye and grass) on fields situated under the emission plume was 5-10 time more than MTC. Vegetables from the market hothouse near Monchegorsk contained nickel and copper (ppm w.w.): cucumbers 12 and 17, spring onions -26 and 36 and lettuce 419 (1) and 269 (!) respectively (Evdockimova unpublished). We have found nickel up to 5 ppm w.w. in potatoes from private kitchen-gardens situated under the emission plume, i.e. 10 times more than MTC.

Table VIII
Metal concentration in mushrooms
Plot
¹/¹		 Plot position
in relation to Smelter		 Concentration,
ppm d.w.
Distance
km		 Azimuth
degrees		 Ni Cu As Cd Co Cr Fe Mn Pb Sr
Lactarius trivialis
67173061640.120.210.150.756242.41.1
68222744330.060.250.250.473191.10.8
69221533320.080.120.210.257201.30.9
46321852429––––––––
76207024400.090.110.220.566313.12.9
33131252045––––––k––
26108519400.070.130.220.587393.01.3
15504516310.040.160.270.695311.50.3
Lactarius torminosus
6573019410.060.150.190.573242.21.3
32121251423––––––––
26108511420.150.130.280.4181462.41.2
14274712270.090.100.140.291113.11.3
163047717––––––––
61532201021––––––––
1550455290.040.090.150.291120.61.8
62802458230.030.120.140.3136373.53.0
Russula vesca
1010201271330.330.150.310.493412.70.9
1112226963––––––––
966028731.00.190.240.580373.41.1
45231803983––––––––
69221517580.130.200.270.560192.41.1
1550459280.080.080.120.350431.31.1
56332139500.200.070.130.394671.22.4
22100753500.060.060.21–43131.10.3
62802453480.050.050.121.449242.11.8


Table IX
The metal human daily intake with berries and mushrooms, mg day-1 per person
Ni Cr Pb As Cd
Daily Total Maximum Tolerable Intake
by WHO recommendations
(food + inhalation + water)		 - - 500 - 65
Daily Total Intake valuated in fact
in unpolluted regions
(food + inhalation + water)		 165 100 - 300 -
Concentrations, accepted in Russia,
for the consumption level of berries 15 kg
and of mushrooms 20 kg per person per annum 		50 10 40 35 7
Daily Intake in fact with the same consumption
level when the plants gathered
in the radius 30 km around the town of Monchegorsk		 200 5 20 1 1

The annualy consumption of enumerated green vegetable species was about (kg; óåar per body): cucumbers - 4, spring onions - 3, lettuce - 2, and potatoes - 100. The total in unpolluted areas. Accordingly the official information of town's adrministration he area under kitchen-gardens has increased hundred times recently, exclusively for the cultivation of potatoes. It is appropriate to mention here a maximum tolerable concentration of the unhealthy admixture is not always a safe concentration. For example, the consumption of 100 kg day-1 potatoes containing 0.5 ppm Ni w.w. will provide the nickel intake 135 mg day-1 per body, besides other sources, such as water, air, other foods, etc. Therefore the safety level is 10-20% MTC, mean -20-50%, elevated - 50-70%, but 70-100% MTC is dangerous, with a high level of harmful admixtures. The main objective of this paper was to attract attention to the danger of long-term, low-level exposure of human population to toxic metals. The whole of population, i.e one hundred thousand persons are suffering from subclinical metal poisoning in the vicinity of Severonickel Smelter Complex. The urban areas of the towns of Monchegorsk and Olenegorsk at the Kola Peninsula have become hot spots of metal pollution. The contamination of berries and mushrooms by toxic metals is dangerous by itself, but it is not yet a calamity - it is ah indication of calamity, the disastrous pollution of environment.



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Water, Air, and Soil Pollution 103: 173-195,1998.

© 1998 Kluwer Academic Publishers. Printed in the Netherlands.