ECOTOXICOLOGY AND ENVIRONMENTAL SAFETY ARTICLE NO.

0106

35, 242247 (1996)

Bioaccumulation of Heavy Metals by Aquatic Macrophytes around Wrocaw, Poland

A. SAMECKA-CYMERMAN*
AND

A. J. KEMPERS

*Department of Ecology and Nature Protection, Wrocaw University, ul. Kanonia 6-8, 50-328 Wrocaw, Poland; and Department of Aquatic Ecology and Biogeology, University of Nijmegen, Toernooiveld, 6525 ED Nijmegen, The Netherlands Received December 15, 1995

Studies were made of heavy metal accumulation in aquatic macrophytes growing in streams and ponds around Wrocaw, Poland, partly affected by atmospheric pollution, effluents of chemical factories, and groundwater contaminated by slagdumps from a smelter and power station. The highest concentrations of Cd, Co, Cr, Cu, Hg, Ni, Pb, and Zn in surface water and aquatic macrophytes surpass the average values established for background reference sites. Significant positive correlations were found between Cu contents in water and Cu, Cd, and Zn contents in plants, between Cu and Cd in plants, between Co and Ni in plants, between Ni contents in water and Ni and Cu contents in plants, between Zn in water and Cu in plants, and between Cd and Ni in plants. Negative correlations were found between Cd contents in water and Zn contents in plants, between Co in water and Cd in plants, and between Zn in water and Co in plants. Experiments with the liverwort Scapania undulata originating from a clean, forested, mountain stream and cultivated in solutions containing 70100% sewage from a chemical factory demonstrated an increase in lead content (85 times in 100% sewage and 58 times in 70% sewage) and in mercury content (40 times in 100% sewage and 20 times in 70% sewage), and also an increase in contents of Cd, Cr, Cu, and Ni. Exposure to 70% sewage concentration during the 14 days of the experiment may be recognized as harmless for S. undulata, so this liverwort could be used in biotechnical purification of water. 1996 Academic Press INTRODUCTION

For selection of indicator plants the following criteria were applied. The plant should: (1) be representative of the area, (2) be ubiquitous and easily collected, (3) be easy identified unequivocally, and (4) have a high tolerance for metals and a high concentration factor (Franzin and McFarlane, 1980). Among 10 plant species utilized for control of heavy metal levels in rivers of Great Britain (Whitton et al., 1981), Cladophora glomerata and Potamogeton pectinatus were selected for this investigation. The aim of this paper was to investigate concentrations of heavy metals in water and plants collected in streams and ponds affected by atmospheric pollution, by the effluents of a chemical factory, and (in the area of drinking water supply for the 0.7 million inhabitants of Wrocaw) by groundwater contaminated by slagdumps from a power station and a former smelter.
MATERIALS AND METHODS

Aquatic macrophytes are known to have great importance, forming a substantial component of the primary production in many aquatic habitats (Pip, 1990). Investigations concerning their role in the cycling of elements, especially heavy metals, is of particular interest. The uptake of trace metals through the root systems of aquatic plants and subsequent release of metals during decomposition of plant material and transmission of these metals to organisms of higher trophic levels represents a pathway of cycling of trace metals in aquatic ecosystems (McIntosh et al., 1978; Mudroch and Capobianco, 1979). The degree of enrichment depended both on the kind of metal and on the species of plant absorbing the metal. The emphasis of most studies gradually shifted toward the use of aquatic plants as monitors for heavy metal water pollution (Mortimer, 1985).
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0147-6513/96 $18.00 Copyright 1996 by Academic Press All rights of reproduction in any form reserved.

Fourteen sampling sites (Fig. 1) were selected for this investigation. Sampling sites 15 are situated in the drinking water supply area southeast of Wrocaw, and sampling sites 614 are situated in the area around a chemical factory northwest of Wrocaw. At each site water samples as well as all available species of aquatic macrophytes were collected in triplicate. Species collected were: Batrachium aquatile, Callitriche verna, Ceratophyllum demersum, C. glomerata, Hydrocharis morsus ranae, Lemna minor, Myriophyllum verticillatum, Nuphar luteum, Polygonum amphibium, Potamogeton crispus, Potamogeton lucens, P. pectinatus, Riccia fluitans, Spirodela polyrhiza, Veronica beccabunga, and Zanichellia palustris. Chemical Analyses Plants were washed thoroughly and dried at 60C. Plant material (200 mg in triplicate) was digested with nitric acid and hydrogen peroxide during which temperatures were raised to about 95C until evolution of nitrous gas stopped and the digest became clear. After proper dilution the digest was analyzed in triplicate for Cd, Co, Cr, Cu, Ni, and Zn by ICPES, Pb by FAAS, and Hg by Cold Vapor Atomic Absorption Spectrophotometry. The same elements were determined in water samples by FAAS (with the exception of Cr and Hg).

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FIG. 1.

Location of the sampling sites in and around Wrocaw.

Experimental Sewage samples of the Rokita pesticide-producing factory in Brzeg Dolny were collected where the effluents entered the Odra river. Experimental solutions containing 100, 90, 80, and 70% of these sewages (in five replications, in two series) were prepared. Gametophyte stems of Scapania undulata with intact growing points originating from a clean mountain stream were placed in each solution. The experiment was run for 14 days. Before and after the experiment the amount of Cd, Co, Cr, Cu, Hg, Ni, Pb, and Zn was determined. Statistical Methods Analysis of variance was applied to the results. The significance of difference was checked with a Snedecor F test with a probability level of 0.05. The least significant difference was established (Parker, 1983). Examined plants were divided into five groups: (A) floating, (B) submersed and not attached to the bottom, (C) submersed with roots attached to the bottom, (D) with roots attached to the bottom and floating leaves, and (E) amphibious. Pearson Correlations (Parker, 1983) between con-

centration of elements in water and each group of plants were calculated. All calculations were done with the program CSS (Statistica).
RESULTS AND DISCUSSION

The results of the analyses are given in Tables 1 and 2. The highest concentrations of the examined elements in water surpass the average values established for background reference sites by Kabata-Pendias and Pendias (1993). The most polluted is the water of sampling site 12 in the vicinity of the Rokita pesticide-producing factory in Brzeg Dolny. The banks of the Odra where the effluents of the factory reach the river are characterized by bare soils without any cover of vegetation. The contamination of water is caused by Cd, Co, Cu, Ni, Pb, and Zn. The concentration of Pb (because of its easy absorption by the loamy fraction of sediments and biological sorption) rarely exceeds 2135 ppb (Kabata-Pendias and Pendias, 1993). In this investigation the highest concentration of Pb in water amounts to 296 ppb in sampling site 8, indicating a high lead pollution.

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TABLE 1 Chemical Composition of Water (g/liter) of 14 Investigated Microhabitats

Ss 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Bg Cu 6 21 8 7 8 <2 3 3 7 2 15 31 13 29 0.9 Ni <4 21 <2 <2 8 4 <2 <2 2 16 2 19 8 4 5 Co 10 24 26 15 12 26 28 20 19 10 22 50 12 1 1 Cd <4 18 21 18 <2 6 4 9 5 11 7 33 5 10 <0.1 Zn 46 95 23 50 49 54 12 69 34 42 87 248 13 35 190 Pb 4.1 79 15 37 55 1.7 13 296 17 6 27 43 12 12 <0.03

Note. RSD < 3%, n

3. Ss, sampling site; Bg, background.

Comparison of concentrations of microelements in the examined aquatic macrophytes with average values established for background concentrations in plants by Kabata-Pendias and Pendias (1993) and Markert (1992) proves that only R. fluitans from sampling site 14 contains Cu in amounts higher than the background values (Tables 2 and 3). This means that all other examined macrophytes do not reveal pollution of the investigated habitats with Cu. Most of the plants collected in the drinking water area (sampling sites 15) and the area around the chemical factory in Brzeg Dolny (sampling sites 614) contain much higher concentrations of Ni than background values. The highest concentration of Ni established for L. minor of sampling site 8 attains a Ni concentration in tissue far in excess (75300 times) of the background values (Tables 2 and 3). Concentration of Co in the examined aquatic plants is much higher than the background value (<1 mg/kg) except for modest (according to Markert) concentrations in S. polyrhiza from sampling site 2, all plants from site 3, C. demersum and H. morsus ranae of sampling site 4, and L. minor of sampling site

TABLE 2 Elemental Composition of Aquatic Macrophytes (mg kg1 dry wt)

Ss 1 1 2 2 2 2 3 3 3 4 4 4 4 5 5 6 7 7 7 7 8 8 9 10 11 12 13 13 13 14 14 14 Species C. glomerata Lemna minor L. minor H. morsus r. S. polyrhiza C. demersum P. lucens M. verticillatum P. amphibium C. demersum H. morsus r. C. verna L. minor Nuphar luteum M. verticillatum Z. palustris C. verna L. minor V. beccabunga Z. palustris L. minor P. pectinatus M. verticillatum M. verticillatum P. amphibium P. amphibium B. aquatile N. luteum L. minor L. minor P. crispus Riccia fluitans Cu 12.8 14 10.3 1 7.3 4 10.9 2 6.2 5 10.3 9 4.7 4 3.4 1 3.4 1 1.9 2 4.3 5 18.5 10 10.3 4 3.8 15 9.6 12 6.3 17 5.8 7 8.9 4 9.0 0.5 7.9 2 4.2 4 5.8 12 3.3 7 5.3 2 8.2 3 4.9 2 7.1 1 2.9 3 8.1 7 5.5 5 1.3 2 29.1 2 Ni 5.3 23 25.7 24 8.9 3 18.1 2 4.9 2 36.1 9 3.6 6 5.6 4 1.2 2 4.4 5 5.3 17 3.3 3 13.8 11 5.8 22 14.3 3 20.3 18 15.1 10 2.1 10 24.5 1 93.6 11 305 8 27.2 5 31.1 3 45.9 2 4.4 9 2.6 12 9.5 15 2.1 19 15.7 10 15.3 3 3.9 15 3.2 0.5 Co 7.7 13 1.8 61 1.7 2 4.7 1 0.80 2 7.2 1 0.90 8 0.95 8 0.98 8 0.71 15 0.68 12 2.1 7 1.4 11 1.4 36 5.9 25 16.7 5 37.8 6 0.45 2 55.5 3 131 8 16.6 13 23.7 12 4.7 18 6.9 2 1.6 12 1.4 19 25.9 7 4.3 13 13.5 14 3.9 3 9.5 3 5.2 5 Cr <0.004 <0.004 0.28 18 0.91 1 <0.004 <0.004 0.80 12 0.79 5 0.10 20 0.19 16 <0.004 <0.004 <0.004 0.20 55 0.62 15 <0.004 11.2 16 2.6 4 1.6 19 2.5 4 0.38 13 1.2 25 1.9 8 <0.004 1.0 11 2.3 10 2.4 27 0.05 2 <0.004 0.28 32 <0.004 <0.004 Cd 0.23 26 0.15 7 0.25 12 0.54 6 <0.002 0.65 14 0.15 40 0.10 30 0.08 25 <0.002 <0.002 0.11 36 1.43 10 0.9 78 0.58 31 1.10 7 0.13 77 0.30 7 0.56 7 1.40 5 0.28 32 0.65 31 0.34 3 0.35 11 0.28 14 0.38 21 0.63 14 0.04 25 0.10 40 0.90 13 2.3 0.5 5.2 8 Hg 0.22 23 0.09 11 0.10 4 0.27 4 0.07 11 0.14 6 0.07 6 0.14 36 0.17 5 0.03 23 0.11 9 0.09 2 0.09 3 0.39 8 0.50 10 0.13 1 0.13 1 0.13 8 0.12 33 0.13 77 0.07 7 0.09 6 0.05 16 0.07 4 0.44 0.5 0.24 12 0.16 4 0.15 13 0.07 1 0.16 6 0.11 9 0.15 7 Zn 436 1 814 1 74.5 4 133 2 126 4 180 10 26.7 1 29.7 6 36.6 1 814 1 35.7 3 114 4 74.5 4 49.3 5 215 2 95.5 5 173 0.5 65.6 2 109 0.5 286 0.5 56.2 0.1 55.2 0.2 49.4 7 81.9 1 102 5 156 5 101 0.1 25.2 8 60 4 168 3 57.1 5 50.6 2 Pb 9.8 8 3.5 11 3.1 6 4.3 7 5.5 4 5.8 7 3.2 6 4.6 4 3.5 3 3.5 11 4.6 2 5.5 1 3.1 6 2.7 7 12.2 4 1.2 2 2.6 2 8.5 6 2.4 0.5 7.6 3 6.9 1 11.5 1 3.3 3 2.8 7 3.7 8 2.6 4 1.6 6 0.83 12 1.2 8 3.2 3 1.2 8 2.3 9

Note. RSD is indicated after the backslash ( ). Ss, sampling site.

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TABLE 3 Elemental Composition (mg/kg dry wt) of Aquatic Macrophytes Obtained in This Study (1) Compared with Data from Literature (211)
Pb 1 2 3 4 5 6 7 8 9 10 11 12 1.29.8 0.10.9 6170 <4.0 3.345 590 1020 227 401536 233 7.7 Cu 1.929.1 520 220 72000 111.5 Ni 1.2305 <1 0.44 51200 Co 0.45131 <1 0.020.5 Cr <0.00411.2 0.021.0 0.21.0 Cd <0.0025.2 1 0.030.5 0.416 1.95.5 Zn 25.2814 1580 25390 Hg 0.030.50 0.0050.03

766 537 8.2 4169 7.6 4860 <1.5 2.58.8 0.9

0.614 0.556.84 0.23.4 60200 2.9

2741640 210563 1292 600018,000

0.650.88

Note. 1, Results of this investigation. 2, Background values by Kabata-Pendias and Pendias (1993). 3, Background values by Market (1992). 4, Miller et al. (1983), lakes receiving high amounts of sewages with heavy metals, Eleocharis acicularis, Eriocaulon septangulare. 5, Pip (1990), Potamogeton richardsoni, P. gramineus, Najas flexilis, Elodea canadensis, Shoal Lake (Canada). 6, Reimer (1989), Potamogeton gramineus, Shoal Lake (Canada). 7, Denny (1981), Myriophyllum alterniflorum from lead mining area (higher values) and from polluted areas (lower value). 8, Franzin and MacFarlane (1980), Myriophyllum exalbescens, Nuphar variegatum, Utricularia vulgaris, Sparganium sp., water reservoir in vicinity of lead smelter. 9, Sprenger and McIntosh (1989), Nymphaea sp., Potamogeton sp., water reservoir in vicinity of steelwork, 10, Mudroch and Capobianco (1979), Myriophyllum verticillatum, Nymphaea odorata mining waters. 11, Mouvet (1992), aquatic bryophytes examined after discharge of sewages. 12, Wiersma et al. (1990), aquatic moss Vittia pachyloma from remote forest in South Chile, background values.

7. The amounts of chromium in almost all plants from sampling sites 713 indicate pollution of their habitats with this element. Lemna minor of sampling site 4, Z. palustris of sampling site 6, C. verna and Z. palustris of sampling site 7, and R. fluitans and P. crispus of sampling site 14 contain Cd in amounts which prove pollution of its habitats. Concentration of Hg ranges from 0.03 in C. demersum (sampling site 4) to 0.39 and 0.5 mg/kg dry wt in N. luteum and M. verticillatum (respectively) from sampling site 5 in the Oawa river. Water of this river, together with groundwater in this area, is also a source of drinking water for Wrocaw and is polluted partly by the presence of the remnants of a former metal smelter, the remnants of waste products of this smelter in a dump, and a power station (using coal as energy source), all situated southeast of Wrocaw in Siechnice (Fig. 1). Groundwater under the power station and the former smelter aliments the river Oawa and ponds in the drinking water supply area and contains increased concentrations of a.o. chromium, zinc, and mercury (Poprawski and Bednarek, 1986). Also, atmospheric pollution in the past and present has contributed to the contamination of this area. Polygonium amphibium from sampling site 11 (under influence of the effluents and atmospheric pollution of a chemical factory in Brzeg Dolny) contains 0.44 mg Hg/kg dry wt. According to Mouvet et al. (1992), the concentration of Hg in aquatic bryophytes measured after discharge of sewage containing mercury ranges from 0.65 to 0.88 mg/kg dry wt. The high concentration of mercury in aquatic plants of sampling site 5 proves the existence of pollution of the Oawa river.

Most of the plants from sampling sites 12, 47, and 1114 contain concentrations of Zn pointing to contamination of the aquatic environment with this element. Elevated concentrations of several heavy metals in plants collected from the drinking water supply area of Wrocaw prove (in comparison with background values) the existence of pollution of this area with Co, Hg, Zn, and Ni (Table 2). Background concentration of Hg is <0.03 mg/kg dry wt for plants (Kabata-Pendias and Pendias, 1993) and 0.005 mg/kg for E. densa (Maury-Brachet et al., 1990). Myriophyllum verticillatum from the Oawa river (sampling site 5) characterizes the highest concentration of mercury (0.5 mg/kg) together with high concentrations of Co, Ni, Pb, and Zn. Guilizzoni (1991) proved that M. sp. and C. demersum are two of the best monitors of water pollution with heavy metals. Nuphar luteum of the same sampling site (No. 5) contains lower amounts of these elements, which is in agreement with the results of Manny et al. (1991) that plants with floating leaves accumulate lower levels of heavy metals (e.g., Cd, Pb, or Zn) than submersed plants. Aquatic macrophytes growing in the vicinity of the Rokita organo-chemical factory contain elevated levels of Cd, Co, Hg, Ni, and Zn (Table 2). Comparison of levels of elements in each of the examined groups of plants (AD) proved that the highest concentrations of Co, Cu, and Zn are found in submersed plants (group C), the highest concentrations of Cr, Pb, and Ni in floating plants (group A), and the highest concentrations of Cd and Hg in plants with floating leaves (group D). Significant positive correlations calculated between concen-

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TABLE 4 Correlations between Chemical Characteristics of Water and Each Group of Plants (AD)
Significance level of correlation coefficient

Relations Cu Cu Cd Cu Co in in in in in

Floating plants (A) water and Cd in plants 0.0256 (+) water and Cu in plants 0.0368 (+) water and Zn in plants 0.0394 () plants and Cd in plants 0.0041 (+) plants and Ni in plants 0.0067 (+) Plants submersed and nonattached to the bottom (B) Ni in water and Cu in plants 0.463 (+) Ni in water and Ni in plants 0.262 (+) Zn in water and Cu in plants 0.0375 (+) Cu in water and Cd in plants 0.0071 (+) Co in water and Cd in plants 0.0419 () Plants submersed with roots attached to the bottom (C) Zn in water and Co in plants 0.0439 () Co in plants and Ni in plants 0.0168 (+) Plants with roots attached to the bottom and floating leaves (D) Cu in water and Zn in plants 0.0166 (+) Cd in plants and Ni in plants 0.0237 (+)

and plants, probably because of the decreasing influence of riverwater on these types of plants. Scapania undulata cultivated in solutions containing 80 100% sewage died within 46 days, but that cultivated in solution containing 70% sewage survived the whole period of the experiment (14 days). Concentrations of elements in S. undulata before and after the experiment are presented in Table 5. Elevated levels of some elements proved that sewage of the Rokita factory contains mainly lead (the amount of this element increased 85 times in 100% sewage compared to the control, or 58 times in 70% sewage) and mercury (the amount of this element increased 45 times in 100% sewage or 21 times in 70% sewage). Concentration of mercury in plants of 1.444.32 mg/kg dry wt is recognized as a symptom of heavy pollution of water of their habitats (Mouvet et al., 1992). After completion of the bioassay, S. undulata contained 1.62.4 mg Hg/kg (Table 5). Also, elevated concentration of lead in S. undulata after completion of the experiment is typical for plants originating from strongly polluted environments (Table 3). Because S. undulata survived without any harmful effect on cultivation in 70% sewage, thereby increasing significant concentrations of heavy metals in its tissues, it can be assumed that this species could be very useful in biotechnical purification of water.
CONCLUSIONS

trations of the examined elements in water and plants are presented in Table 4. According to Kabata-Pendias and Pendias (1993), an increase in the concentration of Zn in water decreases the accumulation of Cd by plants. Antagonism between these elements is probably caused by their chemical affinity to the same organicmineral compounds. This antagonism is proved by the significant, negative correlation between concentrations of Cd in water and Zn in floating plants (Table 4). The influence of Ni on the accumulation of other heavy metals is not very clear. Kabata-Pendias and Pendias (1993) indicated that Cd and Ni exhibit synergism, but in this investigation a significant positive correlation between Cd and Ni in plants with floating leaves was calculated. All other correlations (Table 4) are in contradiction with those of KabataPendias and Pendias (1993), proving that Cu and Zn, Cu and Cd, and Cd and Co are characterized by a strong antagonism. No correlations were found within the amphibious group of plants (group E) between the measured heavy metals in water

The highest concentrations of the examined elements in water and aquatic bryophytes near the Rokita pesticide-producing factory in Brzeg Dolny and the slagdumps from a power station and former smelter in the drinking water supply area of Wrocaw surpass the average values established for background reference sites. Comparison of levels of elements in each of the examined groups of plants proved that the highest concentrations of Co, Cu, and Zn are found in submersed plants, the highest concentrations of Cr, Pb, and Ni in floating plants, and the highest concentrations of Cd and Hg in plants with floating leaves. Significant positive correlations were found between Cu contents in water and Cu, Cd, and Zn contents in plants, between Cu and Cd in plants, between Co and Ni in plants, between Ni contents in water and Ni and Cu contents in plants, between Zn in water and Cu in plants, and between Cd and Ni

TABLE 5 Concentration of Elements in Scapania undulata (mg/kg dry wt) before and after Bioassay
Hg Before After 100% sewage 70% sewage LSD 0.05 2.4 1.6 0.23 Cu 2.33 14.9 12.2 0.19 Ni 0.83 6.37 4.97 0.45 Co 0.75 0.74 0.68 0.2 Cr <0.004 0.31 0.19 0.13 Cd <0.002 2.17 0.74 0.5 Zn 37.7 181 112 2.52 Pb 1.5 128 87 1.37

Note. LSD, least significant difference.

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in plants. Negative correlations were found between Cd contents in water and Zn contents in plants, between Co in water and Cd in plants, and between Zn in water and Co in plants. Experiments with the liverwort S. undulata originating from a clean, forested, mountain stream and cultivated in solutions containing 70100% sewage from a chemical factory indicated an increase in lead content (85 times in 100% sewage and 58 times in 70% sewage) and in mercury content (40 times in 100% sewage and 20 times in 70% sewage), and also an increase in Cd, Cr, Cu, and Ni contents. Exposure to 70% sewage during the 14 days of the experiment may be recognized as harmless for S. undulata, so this liverwort could be used in biotechnical purification of water.
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Maury-Brachet, R., Ribeyre, F., and Boudou, A. (1990). Actions and interactions of temperature and photoperiod on mercury accumulation by Elodea densa from sediment source. Ecotoxicol. Environ. Safety 20, 141155. McIntosh, A. W., Shephard, B. K., Mayes, R. A., Atchison, G. J., and Nelson, D. W. (1978). Some aspects of sediment distribution and macrophyte cycling of heavy metals in a contaminated lake. J. Environ. Qual. 7, 301305. Miller, G. E., Wile, I., and Hitchin, G. G. (1983). Patterns of accumulation of selected metals in members of the soft-water macrophyte flora of central Ontario Lakes. Aquatic Botany 15, 5364. Mortimer, D. C. (1985). Freshwater aquatic macrophytes as heavy metal monitorsThe Ottawa River experience. Environ. Monitoring Assessment 5, 311323. Mouvet, C., Morhain, E., Sutter, C., and Couturieux, N. (1992). Aquatic mosses for the detection and follow-up of accidental discharges in surface waters. Water Air Soil Pollut. 239, 111. Mudroch, A., and Capobianco, J. A. (1979). Effects of mine effluent on uptake of Co, Ni, Cu, As, Zn, Cd, Cr and Pb by aquatic macrophytes. Hydrobiologia 64, 223231. Parker, R. E. (1983). Introductory Statistics for Biology. Edward Arnold, London. Pip, E. (1990). Cadmium, copper and lead in aquatic macrophytes in Shoal Lake (Manitoba-Ontario). Hydrobiologia 208, 253260. Poprawski, L., and Bednarek, Z. (1986). Huta cry wodociggi. Aure 3, 2627. Reimer, P. (1989). Concentrations of lead in aquatic macrophytes from Shoal Lake (Manitoba) Canada. Environ. Pollution 56, 7784. Sprenger, M., and McIntosh, A. (1989). Relationship between concentrations of aluminium, cadmium, lead and zinc in water, sediments and aquatic macrophytes in six acidic lakes. Arch. Environ. Contam. Toxicol. 18, 225 231. Whitton, B. A., Say, P. J., and Wehr, J. D. (1981). Use of plants to monitor heavy metals in rivers. In Heavy Metals in Northern England: Environmental and Biological Aspects (P. J. Say and B. A. Whitton, Eds.), pp. 135145. University of Durham, UK. Wiersma, G. B., Bruns, D. A., Boelcke, C., Whitworth, C., and McAnulty, L. (1990). Elemental composition of mosses from remote Nothofagus forest site in southern Chile. Chemisphere 20, 569583.