Bioaccumulation of Heavy Metals by Aquatic Macrophytes aroundWrocław, Poland

A. SAMECKA-CYMERMAN* AND A. J. KEMPERS†*Department of Ecology and Nature Protection, Wrocław University, ul. Kanonia 6-8, 50-328 Wrocław, 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 aquaticmacrophytes growing in streams and ponds around Wrocław,Poland, partly affected by atmospheric pollution, effluents ofchemical factories, and groundwater contaminated by slagdumpsfrom a smelter and power station. The highest concentrations ofCd, Co, Cr, Cu, Hg, Ni, Pb, and Zn in surface water and aquaticmacrophytes surpass the average values established for back-ground reference sites. Significant positive correlations werefound between Cu contents in water and Cu, Cd, and Zn contentsin plants, between Cu and Cd in plants, between Co and Ni inplants, between Ni contents in water and Ni and Cu contents inplants, between Zn in water and Cu in plants, and between Cdand Ni in plants. Negative correlations were found between Cdcontents in water and Zn contents in plants, between Co in waterand Cd in plants, and between Zn in water and Co in plants.Experiments with the liverwort Scapania undulataoriginatingfrom a clean, forested, mountain stream and cultivated in solu-tions containing 70–100% sewage from a chemical factory dem-onstrated an increase in lead content (85 times in 100% sewageand 58 times in 70% sewage) and in mercury content (40 times in100% sewage and 20 times in 70% sewage), and also an increasein contents of Cd, Cr, Cu, and Ni. Exposure to 70% sewage con-centration during the 14 days of the experiment may be recog-nized as harmless forS. undulata,so this liverwort could be usedin biotechnical purification of water. © 1996 Academic Press

INTRODUCTION

Aquatic macrophytes are known to have great importance,forming a substantial component of the primary production inmany aquatic habitats (Pip, 1990). Investigations concerningtheir role in the cycling of elements, especially heavy metals,is of particular interest. The uptake of trace metals through theroot systems of aquatic plants and subsequent release of metalsduring decomposition of plant material and transmission ofthese metals to organisms of higher trophic levels represents apathway of cycling of trace metals in aquatic ecosystems(McIntoshet al.,1978; Mudroch and Capobianco, 1979). Thedegree of enrichment depended both on the kind of metal andon the species of plant absorbing the metal. The emphasis ofmost studies gradually shifted toward the use of aquatic plantsas monitors for heavy metal water pollution (Mortimer, 1985).

For selection of indicator plants the following criteria wereapplied. The plant should: (1) be representative of the area, (2)be ubiquitous and easily collected, (3) be easy identified un-equivocally, and (4) have a high tolerance for metals and a highconcentration factor (Franzin and McFarlane, 1980). Among10 plant species utilized for control of heavy metal levels inrivers of Great Britain (Whittonet al., 1981), CladophoraglomerataandPotamogeton pectinatuswere selected for thisinvestigation.The aim of this paper was to investigate concentrations of

heavy metals in water and plants collected in streams andponds affected by atmospheric pollution, by the effluents of achemical factory, and (in the area of drinking water supply forthe 0.7 million inhabitants of Wrocław) by groundwater con-taminated by slagdumps from a power station and a formersmelter.

MATERIALS AND METHODS

Fourteen sampling sites (Fig. 1) were selected for this in-vestigation. Sampling sites 1–5 are situated in the drinkingwater supply area southeast of Wrocław, and sampling sites6–14 are situated in the area around a chemical factory north-west of Wrocław. At each site water samples as well as allavailable species of aquatic macrophytes were collected in trip-licate. Species collected were:Batrachium aquatile, Callitricheverna, Ceratophyllum demersum, C. glomerata, Hydrocharismorsus ranae, Lemna minor, Myriophyllum verticillatum,Nuphar luteum, Polygonum amphibium, Potamogeton crispus,Potamogeton lucens, P. pectinatus, Riccia fluitans, Spirodelapolyrhiza, Veronica beccabunga,andZanichellia palustris.

Chemical Analyses

Plants were washed thoroughly and dried at 60°C. Plantmaterial (200 mg in triplicate) was digested with nitric acid andhydrogen peroxide during which temperatures were raised toabout 95°C until evolution of nitrous gas stopped and the di-gest became clear. After proper dilution the digest was ana-lyzed in triplicate for Cd, Co, Cr, Cu, Ni, and Zn by ICPES, Pbby FAAS, and Hg by Cold Vapor Atomic Absorption Spec-trophotometry. The same elements were determined in watersamples by FAAS (with the exception of Cr and Hg).

ECOTOXICOLOGY AND ENVIRONMENTAL SAFETY35, 242–247 (1996)ARTICLE NO. 0106

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0147-6513/96 $18.00Copyright © 1996 by Academic PressAll rights of reproduction in any form reserved.

Experimental

Sewage samples of the ‘‘Rokita’’ pesticide-producing fac-tory in Brzeg Dolny were collected where the effluents enteredthe Odra river. Experimental solutions containing 100, 90, 80,and 70% of these sewages (in five replications, in two series)were prepared. Gametophyte stems ofScapania undulatawithintact growing points originating from a clean mountain streamwere placed in each solution. The experiment was run for 14days. 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 signifi-cance of difference was checked with a SnedecorF test with aprobability level of 0.05. The least significant difference wasestablished (Parker, 1983). Examined plants were divided intofive groups: (A) floating, (B) submersed and not attached to thebottom, (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 werecalculated. All calculations were done with the program CSS(Statistica).

RESULTS AND DISCUSSION

The results of the analyses are given in Tables 1 and 2. Thehighest concentrations of the examined elements in water sur-pass the average values established for background referencesites by Kabata-Pendias and Pendias (1993). The most pollutedis the water of sampling site 12 in the vicinity of the Rokitapesticide-producing factory in Brzeg Dolny. The banks of theOdra where the effluents of the factory reach the river arecharacterized 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 absorptionby the loamy fraction of sediments and biological sorption)rarely exceeds 21–35 ppb (Kabata-Pendias and Pendias, 1993).In this investigation the highest concentration of Pb in wateramounts to 296 ppb in sampling site 8, indicating a high leadpollution.

FIG. 1. Location of the sampling sites in and around Wrocław.

BIOACCUMULATION OF HEAVY METALS BY AQUATIC MACROPHYTES 243

Comparison of concentrations of microelements in the ex-amined aquatic macrophytes with average values establishedfor background concentrations in plants by Kabata-Pendias andPendias (1993) and Markert (1992) proves that onlyR. fluitansfrom sampling site 14 contains Cu in amounts higher than thebackground values (Tables 2 and 3). This means that all otherexamined macrophytes do not reveal pollution of the investi-gated habitats with Cu.Most of the plants collected in the drinking water area (sam-

pling sites 1–5) and the area around the chemical factory inBrzeg Dolny (sampling sites 6–14) contain much higher con-centrations of Ni than background values. The highest concen-tration of Ni established forL. minorof sampling site 8 attainsa Ni concentration in tissue far in excess (75–300 times) of thebackground 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 mod-est (according to Markert) concentrations inS. polyrhizafromsampling site 2, all plants from site 3,C. demersumandH.morsus ranaeof sampling site 4, andL. minorof sampling site

TABLE 1Chemical Composition of Water (µg/liter) of 14

Investigated Microhabitats

Ss Cu Ni Co Cd Zn Pb

1 6 <4 10 <4 46 4.12 21 21 24 18 95 793 8 <2 26 21 23 154 7 <2 15 18 50 375 8 8 12 <2 49 556 <2 4 26 6 54 1.77 3 <2 28 4 12 138 3 <2 20 9 69 2969 7 2 19 5 34 1710 2 16 10 11 42 611 15 2 22 7 87 2712 31 19 50 33 248 4313 13 8 12 5 13 1214 29 4 1 10 35 12Bg 0.9 5 1 <0.1 1–90 <0.03

Note.RSD < 3%,n 4 3. Ss, sampling site; Bg, background.

TABLE 2Elemental Composition of Aquatic Macrophytes (mgz kg−1 dry wt)

Ss Species Cu Ni Co Cr Cd Hg Zn Pb

1 C. glomerata 12.8\14 5.3\23 7.7\13 <0.004 0.23\26 0.22\23 436\1 9.8\81 Lemna minor 10.3\1 25.7\24 1.8\61 <0.004 0.15\7 0.09\11 814\1 3.5\112 L. minor 7.3\4 8.9\3 1.7\2 0.28\18 0.25\12 0.10\4 74.5\4 3.1\62 H. morsus r. 10.9\2 18.1\2 4.7\1 0.91\1 0.54\6 0.27\4 133\2 4.3\72 S. polyrhiza 6.2\5 4.9\2 0.80\2 <0.004 <0.002 0.07\11 126\4 5.5\42 C. demersum 10.3\9 36.1\9 7.2\1 <0.004 0.65\14 0.14\6 180\10 5.8\73 P. lucens 4.7\4 3.6\6 0.90\8 0.80\12 0.15\40 0.07\6 26.7\1 3.2\63 M. verticillatum 3.4\1 5.6\4 0.95\8 0.79\5 0.10\30 0.14\36 29.7\6 4.6\43 P. amphibium 3.4\1 1.2\2 0.98\8 0.10\20 0.08\25 0.17\5 36.6\1 3.5\34 C. demersum 1.9\2 4.4\5 0.71\15 0.19\16 <0.002 0.03\23 814\1 3.5\114 H. morsus r. 4.3\5 5.3\17 0.68\12 <0.004 <0.002 0.11\9 35.7\3 4.6\24 C. verna 18.5\10 3.3\3 2.1\7 <0.004 0.11\36 0.09\2 114\4 5.5\14 L. minor 10.3\4 13.8\11 1.4\11 <0.004 1.43\10 0.09\3 74.5\4 3.1\65 Nuphar luteum 3.8\15 5.8\22 1.4\36 0.20\55 0.9\78 0.39\8 49.3\5 2.7\75 M. verticillatum 9.6\12 14.3\3 5.9\25 0.62\15 0.58\31 0.50\10 215\2 12.2\46 Z. palustris 6.3\17 20.3\18 16.7\5 <0.004 1.10\7 0.13\1 95.5\5 1.2\27 C. verna 5.8\7 15.1\10 37.8\6 11.2\16 0.13\77 0.13\1 173\0.5 2.6\27 L. minor 8.9\4 2.1\10 0.45\2 2.6\4 0.30\7 0.13\8 65.6\2 8.5\67 V. beccabunga 9.0\0.5 24.5\1 55.5\3 1.6\19 0.56\7 0.12\33 109\0.5 2.4\0.57 Z. palustris 7.9\2 93.6\11 131\8 2.5\4 1.40\5 0.13\77 286\0.5 7.6\38 L. minor 4.2\4 305\8 16.6\13 0.38\13 0.28\32 0.07\7 56.2\0.1 6.9\18 P. pectinatus 5.8\12 27.2\5 23.7\12 1.2\25 0.65\31 0.09\6 55.2\0.2 11.5\19 M. verticillatum 3.3\7 31.1\3 4.7\18 1.9\8 0.34\3 0.05\16 49.4\7 3.3\310 M. verticillatum 5.3\2 45.9\2 6.9\2 <0.004 0.35\11 0.07\4 81.9\1 2.8\711 P. amphibium 8.2\3 4.4\9 1.6\12 1.0\11 0.28\14 0.44\0.5 102\5 3.7\812 P. amphibium 4.9\2 2.6\12 1.4\19 2.3\10 0.38\21 0.24\12 156\5 2.6\413 B. aquatile 7.1\1 9.5\15 25.9\7 2.4\27 0.63\14 0.16\4 101\0.1 1.6\613 N. luteum 2.9\3 2.1\19 4.3\13 0.05\2 0.04\25 0.15\13 25.2\8 0.83\1213 L. minor 8.1\7 15.7\10 13.5\14 <0.004 0.10\40 0.07\1 60\4 1.2\814 L. minor 5.5\5 15.3\3 3.9\3 0.28\32 0.90\13 0.16\6 168\3 3.2\314 P. crispus 1.3\2 3.9\15 9.5\3 <0.004 2.3\0.5 0.11\9 57.1\5 1.2\814 Riccia fluitans 29.1\2 3.2\0.5 5.2\5 <0.004 5.2\8 0.15\7 50.6\2 2.3\9

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

SAMECKA-CYMERMAN AND KEMPERS244

7. The amounts of chromium in almost all plants from sam-pling sites 7–13 indicate pollution of their habitats with thiselement.Lemna minorof sampling site 4,Z. palustrisof sampling site

6,C. vernaandZ. palustrisof sampling site 7, andR. fluitansand P. crispusof sampling site 14 contain Cd in amountswhich prove pollution of its habitats. Concentration of Hgranges from 0.03 inC. demersum(sampling site 4) to 0.39 and0.5 mg/kg dry wt inN. luteumandM. verticillatum (respec-tively) from sampling site 5 in the Oława river. Water of thisriver, together with groundwater in this area, is also a source ofdrinking water for Wrocław and is polluted partly by the pres-ence of the remnants of a former metal smelter, the remnants ofwaste products of this smelter in a dump, and a power station(using coal as energy source), all situated southeast ofWrocław in Siechnice (Fig. 1). Groundwater under the powerstation and the former smelter aliments the river Oława andponds in the drinking water supply area and contains increasedconcentrations of a.o. chromium, zinc, and mercury (Popraw-ski and Bednarek, 1986). Also, atmospheric pollution in thepast and present has contributed to the contamination of thisarea.Polygonium amphibiumfrom sampling site 11 (underinfluence of the effluents and atmospheric pollution of achemical factory in Brzeg Dolny) contains 0.44 mg Hg/kg drywt. According to Mouvetet al. (1992), the concentration of Hgin aquatic bryophytes measured after discharge of sewage con-taining mercury ranges from 0.65 to 0.88 mg/kg dry wt. Thehigh concentration of mercury in aquatic plants of samplingsite 5 proves the existence of pollution of the Oława river.

Most of the plants from sampling sites 1–2, 4–7, and 11–14contain concentrations of Zn pointing to contamination of theaquatic environment with this element. Elevated concentra-tions of several heavy metals in plants collected from the drink-ing water supply area of Wrocław prove (in comparison withbackground values) the existence of pollution of this area withCo, Hg, Zn, and Ni (Table 2). Background concentration of Hgis <0.03 mg/kg dry wt for plants (Kabata-Pendias and Pendias,1993) and 0.005 mg/kg forE. densa(Maury-Brachetet al.,1990).Myriophyllum verticillatumfrom the Oława river (sampling

site 5) characterizes the highest concentration of mercury (0.5mg/kg) together with high concentrations of Co, Ni, Pb, andZn. Guilizzoni (1991) proved thatM. sp. andC. demersumaretwo of the best monitors of water pollution with heavy metals.Nuphar luteumof the same sampling site (No. 5) contains

lower amounts of these elements, which is in agreement withthe results of Mannyet al. (1991) that plants with floatingleaves accumulate lower levels of heavy metals (e.g., Cd, Pb,or Zn) than submersed plants. Aquatic macrophytes growing inthe vicinity of the Rokita organo-chemical factory contain el-evated levels of Cd, Co, Hg, Ni, and Zn (Table 2).Comparison of levels of elements in each of the examined

groups of plants (A–D) proved that the highest concentrationsof Co, Cu, and Zn are found in submersed plants (group C), thehighest concentrations of Cr, Pb, and Ni in floating plants(group A), and the highest concentrations of Cd and Hg inplants with floating leaves (group D).Significant positive correlations calculated between concen-

TABLE 3Elemental Composition (mg/kg dry wt) of Aquatic Macrophytes Obtained in This Study (1) Compared with Data from

Literature (2–11)

Pb Cu Ni Co Cr Cd Zn Hg

1 1.2–9.8 1.9–29.1 1.2–305 0.45–131 <0.004–11.2 <0.002–5.2 25.2–814 0.03–0.502 0.1–0.9 5–20 <1 <1 0.02–1.0 1 15–80 0.005–0.033 2–20 0.4–4 0.02–0.5 0.2–1.0 0.03–0.54 6–170 7–2000 5–1200 0.4–16 25–3905 <4.0 1–11.5 1.9–5.56 3.3–457 590

10–208 2–27 7–66 0.6–14 274–16409 401–536 0.55–6.84 210–56310 2–33 5–37 4–169 4–860 2.5–8.8 0.2–3.4 12–9211 60–200 6000–18,000 0.65–0.8812 7.7 8.2 7.6 <1.5 0.9 2.9

Note.1, Results of this investigation. 2, Background values by Kabata-Pendias and Pendias (1993). 3, Background values by Market (1992). 4, Milleret 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 alterniflorumfrom lead mining area (higher values) and from polluted areas (lower value). 8, Franzin and MacFarlane (1980),Myriophyllumexalbescens, Nuphar variegatum, Utricularia vulgaris, Sparganiumsp., water reservoir in vicinity of lead smelter. 9, Sprenger and McIntosh (1989),Nymphaeasp.,Potamogetonsp., water reservoir in vicinity of steelwork, 10, Mudroch and Capobianco (1979),Myriophyllum verticillatum, Nymphaea odorataminingwaters. 11, Mouvet (1992), aquatic bryophytes examined after discharge of sewages. 12, Wiersmaet al.(1990), aquatic mossVittia pachylomafrom remote forestin South Chile, background values.

BIOACCUMULATION OF HEAVY METALS BY AQUATIC MACROPHYTES 245

trations of the examined elements in water and plants are pre-sented in Table 4. According to Kabata-Pendias and Pendias(1993), an increase in the concentration of Zn in water de-creases the accumulation of Cd by plants. Antagonism betweenthese elements is probably caused by their chemical affinity tothe same organic–mineral compounds. This antagonism isproved by the significant, negative correlation between con-centrations 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 inves-tigation a significant positive correlation between Cd and Ni inplants with floating leaves was calculated. All other correla-tions (Table 4) are in contradiction with those of Kabata-Pendias and Pendias (1993), proving that Cu and Zn, Cu andCd, and Cd and Co are characterized by a strong antagonism.No correlations were found within the amphibious group ofplants (group E) between the measured heavy metals in water

and plants, probably because of the decreasing influence ofriverwater on these types of plants.Scapania undulatacultivated in solutions containing 80–

100% sewage died within 4–6 days, but that cultivated in so-lution containing 70% sewage survived the whole period of theexperiment (14 days). Concentrations of elements inS. undu-lata before and after the experiment are presented in Table 5.Elevated levels of some elements proved that sewage of theRokita factory contains mainly lead (the amount of this ele-ment increased 85 times in 100% sewage compared to thecontrol, or 58 times in 70% sewage) and mercury (the amountof this element increased 45 times in 100% sewage or 21 timesin 70% sewage).Concentration of mercury in plants of 1.44–4.32 mg/kg dry

wt is recognized as a symptom of heavy pollution of water oftheir habitats (Mouvetet al., 1992). After completion of thebioassay,S. undulatacontained 1.6–2.4 mg Hg/kg (Table 5).Also, elevated concentration of lead inS. undulataaftercompletion of the experiment is typical for plants originatingfrom strongly polluted environments (Table 3). BecauseS.undulatasurvived without any harmful effect on cultivation in70% sewage, thereby increasing significant concentrations ofheavy metals in its tissues, it can be assumed that this speciescould be very useful in biotechnical purification of water.

CONCLUSIONS

The highest concentrations of the examined elements in wa-ter and aquatic bryophytes near the Rokita pesticide-producingfactory in Brzeg Dolny and the slagdumps from a power stationand former smelter in the drinking water supply area ofWrocław surpass the average values established for back-ground 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 concen-trations of Cr, Pb, and Ni in floating plants, and the highestconcentrations 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, be-tween 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 4Correlations between Chemical Characteristics of Water and

Each Group of Plants (A–D)

Relations

Significancelevel of

correlationcoefficient

Floating plants (A)Cu in water and Cd in plants 0.0256 (+)Cu in water and Cu in plants 0.0368 (+)Cd in water and Zn in plants 0.0394 (−)Cu in plants and Cd in plants 0.0041 (+)Co in 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 andfloating leaves (D)

Cu in water and Zn in plants 0.0166 (+)Cd in plants and Ni in plants 0.0237 (+)

TABLE 5Concentration of Elements inScapania undulata(mg/kg dry wt) before and after Bioassay

Hg Cu Ni Co Cr Cd Zn Pb

Before 0.05 2.33 0.83 0.75 <0.004 <0.002 37.7 1.5After100% sewage 2.4 14.9 6.37 0.74 0.31 2.17 181 12870% sewage 1.6 12.2 4.97 0.68 0.19 0.74 112 87

LSD 0.23 0.19 0.45 0.2 0.13 0.5 2.52 1.37

Note.LSD, least significant difference.

SAMECKA-CYMERMAN AND KEMPERS246

in plants. Negative correlations were found between Cd con-tents in water and Zn contents in plants, between Co in waterand Cd in plants, and between Zn in water and Co in plants.Experiments with the liverwortS. undulataoriginating from

a clean, forested, mountain stream and cultivated in solutionscontaining 70–100% sewage from a chemical factory indicatedan increase in lead content (85 times in 100% sewage and 58times in 70% sewage) and in mercury content (40 times in100% sewage and 20 times in 70% sewage), and also an in-crease in Cd, Cr, Cu, and Ni contents. Exposure to 70% sewageduring the 14 days of the experiment may be recognized asharmless forS. undulata,so this liverwort could be used inbiotechnical purification of water.

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