Heavy Metals Uptake and Accumulation by the Hybrid Aspenin Alkalised Soil

Malle Mandre

Received: 23 July 2013 /Accepted: 7 November 2013 /Published online: 29 November 2013# Springer Science+Business Media Dordrecht 2013

Abstract Alkalisation of soil by dust pollution from acement plant was assumed to be the principal cause ofchanges in heavy metal uptake and allocation betweenhybrid aspen (Populus tremula × Populus tremuloidesMichx.) compartments. Emission of over 40 years ofalkaline dust (pH 12.3–12.6) into the atmosphere hadresulted in an increase of pH and an elevated concentra-tion of total heavy metals in the upper layer of the soil(0–30 cm), which is considerable even 14 years afterdust pollution has stopped. The accumulation and allo-cation of heavy metals in stem, shoot and leaves variedbetween themselves and between the trees from pollutedand unpolluted plantations depending more on themobility of elements and pH than element concentra-tions in the alkaline soil. High levels of heavy metalsin the soil do not mean similar concentrations andratios in plants growing in contaminated soil.

Keywords Hybridaspen .Alkalisedsoil .Heavymetals .

Uptake . Allocation

1 Introduction

Hybrid aspen (Populus tremula × Populus tremuloidesMichx.) is considered to be the most promising forshort-rotation forestry in boreal areas (Rytter 2006;Rytter and Stener 2005), for afforestation large areas of

industrially degraded territories or abandoned agricul-tural lands (Tullus 2010) and to use biomass productionfor the forest industry (Yu and Pulkkinen 2003).Recently, the forest industry has shown a renewed in-terest in utilising aspen not only for pulp and paperproduction but also for bioenergy production. That iswhy the interest in plantations has been increasing andthe establishment of short-rotation forest plantations iswidely recommended at present (Hynynen and Karlsson2002; Rytter 2006; Rytter and Stener 2005).

Hybrid aspen has very modest requirements for cli-matic conditions and has proved to be a fast-growing treespecies even under extreme environmental conditions,including on areas severely contaminated by industrialemissions or agricultural activity. Some hybrid aspenclones are capable of growing well in reclaimed surfacemines, reclaimed opencast oil–shale mines (Casselmanet al. 2005; McGill et al. 2004; Tullus et al. 2008), as wellas under the impact of elevated concentrations of O3, SO2

or industrial fly ash (Karnosky 1977; Maňkovská et al.1998). Fast-growing hybrid aspen can accumulate envi-ronmental pollutants and thus may be used even forremediation of contaminated soils (Dix et al. 1997;Malá et al. 2007; Monsant et al. 2008).

A large part of abandoned agricultural lands in NorthEstonia are located in industrially damaged territories,where soils are predominantly alkalised and their chemicalcomposition is unbalanced due to the long-time impactof alkaline dust and ash pollution from building mate-rial production, oil–shale mining, and processing andenergy production. It is known that many tree speciesare relatively sensitive to alkalisation of soil and toalkaline air pollution (Farmer 1993; Klõšeiko 2005;Lukjanova and Mandre 2010; Mandre 2009).

Water Air Soil Pollut (2014) 225:1808DOI 10.1007/s11270-013-1808-6

M. Mandre (*)Department of Ecophysiology, Institute of Forestry and RuralEngineering, Estonian University of Life Sciences,Viljandi mnt. 18B, Tallinn 11216, Estoniae-mail: malle.mandre@emu.ee

As plantation forestry with aspens is still quite a newpractice in northern Europe, aspen’s response to differ-ent environmental conditions is an important topic. Ourprevious studies in the vicinity of a cement plant onhybrid aspen demonstrated that alkalisation and highconcentrations of base cations in soil cause stress tohybrid aspen, resulting in retarded height, diameter,and dimensions of leaves and reduction of photosyn-thetic and transpiration rates (Mandre et al. 2012).

The dust emitted from the cement plant includes acertain amount of heavy metals and the response ofhybrid aspen to the increased content of heavy metalsin soil should be understood. Although higher plantsare believed not to tolerate increased concentrationsof heavy metals well, they are also widely known toaccumulate these elements and to survive on soilscontaminated by large quantities of various heavymetals. Cripps (2001) showed that aspen is apparentlysustainable in areas where soils are high in heavymetals due to mutualistic relationships with mycorrhizalfungi. Malá et al. (2007) found in hydroponic conditiondifferences in the accumulation of heavy metals in dif-ferent compartments of hybrid aspen: Cd and Pb aremuch higher in the roots than in the shoots and theamounts of Mn in roots are significantly lower than inthe aboveground parts. The concentration of heavymetals in trees depends on the pH of the soil solution(Kahle 1993). It is important to consider the optimumsoil pH for the growth of aspens, which, according to theliterature, is in the range of 6 to 6.5 (7) (DesRocherset al. 2003; Stanturf 2001).

Measurements of the influx of cement dust indicateconsiderable concentrations of Pb, Zn, Cu, Cr, Cd, Fe,Al, etc. (Enel 2003; Pets 1997), which are dangerouspollutants due to their ability to form complexes withorganic compounds. In small amounts, they are indis-pensable for life, being active centres of enzymes andcatalysing metabolism. Elevated concentrations oftrace elements may negatively affect the growth,development, and health of plant organisms. ElevatedCd contents in plants retard the growth and root devel-opment, Cu induces chlorosis of leaves and root malfor-mation, toxic effects of Pb are related mainly to distur-bance of fundamental processes of photosynthesis,growth, mitosis, etc. (Kabata-Pendias and Pendias1992). Co-occurrence of some metals (Ni and Zn, Cuand Cd) may be more toxic than the simple sum ofeffects would suggest (Pasternak and Reczyńska-Dutka 1984). Heavy metals in cement dust may be one

of the factors that retard tree growth and biomass for-mation in cement dust-contaminated alkalised soil(Mandre et al. 2011).

On the other hand, the accumulation of heavy metals(Mn, Fe, Cu, etc.) in aspen wood is a factor that influ-ences pulp and paper quality and may affect the perma-nence of paper or interfere with the paper manufacturingprocess (Malá et al. 2007). The following metals areoften found in the wood from which pulp is made: Fe,Mn, Cu, Al, Ca, Mg, Zn, Co and Ba (McCrady 1996).Hydroxides/oxides of Fe, Cu and Mn catalyse cellulosehydrolysis (Banik and Ponahlo 1981; Lindström 1989).Zhuang and Biermann (1993) hypothesise that Feions are effective on the darkness of unbleached ormechanical pulp papers. Unfortunately, informationon the accumulation of metals by aspens and theinfluence of alkalisation of the environment on metalconcentrations in trees is, up to now, relatively scarce.

The aim of the study was to clarify heavymetal (HM)accumulation by hybrid aspen planted on former arablelands on an unpolluted area and on an area influencedfor a long time by cement dust pollution in NorthEstonia 14 years after dust emission stopped. Attentionis paid to the accumulation and partitioning of HM in thedifferent compartments of trees for understanding thetranslocation of HM in trees growing in extremely alka-line soil. The overall aim was to investigate theinteracting controls of hybrid aspen by HM availabilityand soil alkalisation level. The findings help understandthe changes in the system–tree growth environment,prognosticate possibilities of using hybrid aspen forafforestation of industrially destroyed lands in North-East Estonian alkalised territories, and estimate the qual-ity of wood for paper manufacturing.

2 Materials and Methods

2.1 Study Area

About 700 ha of industrial hybrid aspen plantationshave been established since 1999 on abandonedagricultural lands in Estonia (Tullus et al. 2007).This study was conducted with hybrid aspens P.tremula × P. tremuloides Michx. growing in twoplantations on former agricultural lands in NorthEstonia. The plantations were established with 1-year-old micropropagated plants with an average rate of 1,300 trees ha−1. The most abundantly used clones were

1808, Page 2 of 9 Water Air Soil Pollut (2014) 225:1808

C05–99–10 and C05–99–34 (clone identification num-bers according to the Finnish Plant Production InspectionCentre).

The soils in both plantations are well-drained gravel-ly mineral soils that have developed on stony calcareoustill on Ordovician limestone (Tullus 2010). The meanannual temperature in the studied area is 4.9 °C, annualamount of precipitation 534 mm and dominating windsblow from the south and south-west at a mean velocityof 5.2 m s−1 (data from the Estonian Meteorological andHydrological Institute).

The plantation at Kunda (59°29′ N, 26°34′ E) with asize of 8.2 ha was established (1999) on a territoryinfluenced over 40 years by a cement plant in thevicinity of the town of Kunda, North Estonia. Theplantation is located at a distance of 3 km E of theemission centre. The emission from the cement plantcontained 87–91 % technological dust and 9–13 %gaseous pollutants (SO2, NOx, CO, etc.). The dustemitted from cement production contained 40–50 %CaO, 12–17 % SiO2, 6–9 % K2O, 2–4 % MgO, 4–8 %SO3, 2–3 % Fe2O3, 3–5 % Al2O3, 0.034 % MnO,0.13 % P, 0.1 % Na, 0.007 % Pb, 0.012 % Zn, 0.004 %Cu, 0.0001%Cd, 0.001%Co, 0.005%Cr, etc. accordingto the analyses by the laboratories of Kunda cement plantand the Estonian Environmental Research Centre, Pets(1997) and Enel (2003).

The water solution of dust from electric filters had pHvalues from 12.3–13.0 in 1:5 dust/water, w/w (Mandre2000). The dust emission from the cement plant wasextremely high in 1990–1992 being 80–100 Mt per year(Estonian Environment 19911991; Estonian Environment1995 1996). In 1996, the emission of cement dustfrom the plant decreased notably thanks to the instal-lation of efficient filters and at present it is lower thanthe permitted quantity (421 t year−1) (EnvironmentalReview 2007). By the time of the establishment of theplantation, the emission of dust from the cement planthad practically stopped (Fig. 1).

In the region of the plantation, the typical soils werecalcaric cambisols according to the World reference basefor soil resources. The plantation at Rapla (58°53′ N,24°41′ E) with a size of 7.4 ha was established (2000)in similar climatic and edaphic conditions on an unpol-luted area at a distance of about 120 km Wof the Kundaplantation. It served as the control for the Kunda planta-tion established on a polluted territory. The soils in thearea of this plantation were chromic cambisol accordingto the world reference base for soil resources.

2.2 Chemical Analysis of Soil

Taking into account that approximately 80 % of theroots of trees actively engage in the uptake of waterand nutrients are located in the layer of 0–30 cm fromthe surface (Barnes et al. 1998; Eissenstat and van Rees1994), soil samples were collected from a depth of30 cm. Soil samples were taken in August andSeptember 2010 in six replications per plantation. Soilsamples were dried and sieved through a sieve withmesh size of 2 mm. One composite sample for theplantation was formed for analysis using an equal quan-tity of soil from each replication.

The concentrations of Mn, Cu, Fe, Zn Pb, Cd and Cr(milligram per kilogram) in soil were determined byusing inductively coupled plasma atomic emission spec-troscopy (ICP-OES) after wet digestion in a microwaveoven. Digestion was carried out by heating withsmall amounts of conc. HNO3 according to ISO/11885 method (1999). Analyses were performed bythe Laboratory of Environmental Chemistry of theEstonian Environmental Research Centre. The soil pHwas determined potentiometrically from 1-M KCl sus-pensions in the ratio 10 g: 25 ml (ISO/10390 1994).

2.3 Plant Material Analyses

The study was conducted within the network of perma-nent experimental plots in 11–12-year-old hybrid aspen(P. tremula L. × P. tremuloides Michx.) plantationsestablished for the afforestation of abandoned agricul-tural lands in Estonia. Investigations were carried out inAugust 2010, when shoot growth had ceased and leaveswere fully expanded. Six visually average in heightmodel trees were selected from both plantations andfelled for morphological measurements and forcollecting samples for chemical analyses. The averagestem diameter at breast height (DBH, centimetre) andheight (H, metre) of trees within the plantation weremeasured (Mandre et al. 2012).

The leaves and branches, collected evenly throughthe crown, and stem wood discs (10 cm in length) weretaken from 1.3-m height. Only last year, parts frombranches, which are later called shoots, were used foranalysis. The bark was separated from the wood. Thesamples were dried at +70 °C and ground in a laboratorymill (Tecator Cyclotec) with a screen that yielded parti-cle size <0.5 mm. After grinding, 1–2 g of dried plantmaterial were digested in a microwave by a wet ashing

Water Air Soil Pollut (2014) 225:1808 Page 3 of 9, 1808

procedure with concentrated HNO3 according to ISO/11885 (1999) method and the total concentration of HMwere determined using ICP-OES. Analyses were per-formed by the Laboratory of Environmental Chemistryof the Estonian Environmental Research Centre.

2.4 Statistical Analyses

Average hybrid aspen HM concentrations and soil chem-ical variables were compared between the studied planta-tions. To compare the HM contents in soil upper horizonsin the plantations, t tests were employed. To establish thedifferences between HM concentrations in soil and intrees in the plantations, t tests were conducted with theassumption of unequal variances with the averages ofeach single tree. The t tests were considered significantat p<0.01, <0.05 and <0.001. For finding statistical dif-ferences (t test) the programmes Statgraphics 5.0, Systat10 and MS Excel 2003 were used.

For the detection of relationships between treegrowth variables and HM accumulation variables,Pearson’s correlations (r) at p<0.05 were performed inMS Excel 2003 software for Windows.

3 Results

3.1 Soil in the Plantations

The results of soil analysis showed significant differencesbetween the studied plantations in pH and chemicalcomposition (Table 1). Although the soils had similartexture, the chemical composition of the soil in theKunda plantation was significantly affected by the long-term dust pollution emitted from the cement plant. AtKunda, the average soil pH was 7.3–7.5, and in the

unpolluted plantation at Rapla, 6.5–7.0. The averageconcentration of HM in the soil of the Kunda plantationwas higher than in the Rapla soil (Table 1). There was apositive correlation between average concentrations ofHM in soil and the average dust emission for 1992–2003(r=0.69 and p<0.05). An especially high concentrationof Mn had accumulated in the upper layer of soil atKunda; it was over six times as high as in the unpollutedRapla plantation. The concentrations of Cd, Fe and Cuwere over two times higher than in the soil at Rapla.Although the cement dust contained a relatively lowamount of Cd, its concentration at Kunda differedsignificantly from the control (Table 1). No significantdifferences from the control were observed for Cr andPb concentrations and the Zn concentration was evenlower than the control.

3.2 Partitioning of HM in Different Organs of HybridAspen

Results of analyses show only 14 % differences in theaverage concentration of HM in the aboveground parts ofhybrid aspen between the plantations; the average con-centrations of Cr, Pb, Fe and Cu were much higher in thetrees at Kunda while those of Cd, Mn and Zn were lowerthan the relevant values of control trees at Rapla. Essentialdifferences in the allocation of HM into different com-partments of trees were found (Table 2). In leaves andshoots, the average concentrations of HM were 15 and9 % lower, respectively, but in stems, 55 % higher thanthe control. Significant differences in bark between thetwo plantations were found for Cd, Pb and Mn (Table 2).

Most analysed HM accumulated in the stem, exceptCd, whose concentration in the stem was nearly 66 %lower than that in the control trees, and Pb, which didnot show any significant difference between the two

0

10

20

30

40

50

60

70

80

90

1992

1993

1994

1995

1996

1997

1998

1999

2000

2001

2002

2003

2004

2005

2006

2007

0

200

400

600

800

1000

1200

Cem

ent p

rodu

ctio

n, th

ousa

nd to

ns y

r –1

Dust emission Cement production

Dus

t em

issi

on, t

hous

and

tons

yr–1

Fig. 1 Emission of dust intothe atmosphere from thecement plant in Kunda(Estonia) and cement pro-duction during 1992–2007(Environmental Review2008)

1808, Page 4 of 9 Water Air Soil Pollut (2014) 225:1808

plantations. If we take the HMconcentration in the trees atRapla as 100 %, then we can see that Cu and Cr accumu-lated, relatively, intensively in the stem in the pollutedplantation: their concentrations at Kunda were by 206 and137 % higher, respectively, and Mn, Zn and Fe were by20, 33 and 45 % higher than the relevant figures at Rapla.In the leaves and shoots of hybrid aspen, the concentra-tions of Cr, Pb and Fe showed significantly elevated levelsin the Kunda plantation while much lower concentrationswere established forMn (77% of the control in leaves and66 % in shoots), Zn (80 and 90 %, respectively) and Cu(83 and 92 %) (Fig. 2). The leaves and shoots showedespecially low concentrations of Cd; only 29 % of thecontrol in the leaves and 41 % in the shoots.

The trees growing in the studied plantations differedsignificantly in height growth (Fig. 3). After 11–12 yearsof growth the mean H at Kunda was about 32 % andDBH about 42 % lower than at Rapla, and the t testrevealed significant differences between trees in theplantations studied (Fig. 3) (Mandre et al. 2012). TheH and DBH scaled negatively and significantly with theaverage Cr in leaves, shoots and stems of trees fromthe Kunda plantation (H r=−0.8668, p=0.0061; DBHr=−0.6745, p=0.0144) while the relationships with theaverage concentrations of Cd andMn in the abovegroundcompartments of trees were positive (H rCd=0.7231,p=0.0057; rMn=0.7893, p=0.0163; DBH rCd=0.6431,p=0.0257; rMn=0.6124, p=0.0114).

Table 1 Average concentration of heavy metals and pH (±SD) in soils of unpolluted Rapla and in polluted Kunda plantations (n=6) in 2010

pHKCl Cd Cr Mn Pb Fe Zn Cu

mg kg−1

Rapla 6.817 1.14 16.40 466.00 13.90 12,500.00 71.60 6.82

±0.204 ±0.110 ±1.600 ±22.000 ±1.290 ±301.000 ±3.72 ±0.213

Kunda 7.317 2.32 20.80 2,790.00 19.50 25,400.00 49.10 15.00

±0.098 ±0.297 ±0.740 ±84.000 ±0.870 ±125.000 ±4.110 ±0.322

p 0.0009 0.004 0.09 2.40E-03 0.0564 1.30E-06 0.009 2.10E-03

Differences (t test) of soils between plantations and p values was conducted based on the assumption of unequal variances

Table 2 Concentration of heavy metals (±SD) in different compartments of hybrid aspen in 2010

Compartment Cd Cr Pb Mn Fe Zn Cu

mg kg−1

Rapla Leaf 1.14±0.07 0.15±0.01 0.12±0.01 55.85±4.58 38.57±3.33 223.33±16.14 6.65±0.42

Shoot 0.75±0.01 0.15±0.01 0.22±0.01 6.98±0.61 12.46±0.99 45.30±4.24 7.07±0.07

Stem 0.29±0.00 0.24±0.02 0.08±0.01 1.41±0.01 7.23±0.75 11.08±1.10 2.87±0.15

Bark 1.10±0.01 0.22±0.02 0.11±0.01 11.16±0.98 10.83±0.86 105.33±9.54 3.72±0.29

Kunda Leaf 0.33±0.00 0.29±0.02 0.14±0.01 42.80±2.16 54.80±5.13 179.00±13.12 5.50±0.54

Shoot 0.31±0.01 0.41±0.02 0.30±0.01 4.63±0.39 13.28±1.01 40.70±2.79 6.48±0.43

Stem 0.10±0.00 0.56±0.03 0.09±0.00 1.70±0.01 10.10±0.92 14.70±1.32 8.80±0.81

Bark 0.61±0.01 0.19±0.01 0.26±0.01 7.94±0.62 13.08±1.11 103.17±10.00 3.75±0.17

p Leaf 0.0001 0.021 0.563 0.014 1.16E-05 0.001 0.036

Shoot 0.0006 0.002 0.048 0.007 0.252 0.124 0.653

Stem 3.47E-05 0.005 0.902 0.051 0.017 0.018 1.17E-06

Bark 0.001 0.217 1.10E-06 0.002 0.219 0.767 0.936

Differences (t test) of heavy metal concentrations between plantations and p values was conducted based on the assumption of unequalvariances. Average concentration was calculated for above ground compartments

Water Air Soil Pollut (2014) 225:1808 Page 5 of 9, 1808

4 Discussion

For a long time, the main damaging factor to trees in theinvestigation area was apparently the high level of alka-line dust emissions from the cement plant, which hasbrought about alkalisation and serious changes in thechemical composition of the soil in the Kunda area,which are still evident (Annuka and Mandre 1995;Mandre and Ots 2012). Although the soils in our hybridaspen plantations had similar textures and have devel-oped both on stony calcareous till on Ordovician lime-stone, the chemical composition of soil in the Kundaplantation was significantly affected by over 40 years ofalkaline dust pollution. In the polluted soil, the averagepH was 0.5 units higher than in the unpolluted planta-tion at Rapla. According to DesRochers et al. (2007), theoptimum soil pH for the growth of aspen is in the range

from 6 to 7. Thus, the pH of the soil in the Raplaplantation should be optimum for hybrid aspen.

It appears that the effect of cement dust pollution onHM concentration levels is considerable. It should bestressed that the ratios of HM in soil are not analogous totheir ratios in cement dust. Different solubility andmobility of elements causes their different accumula-tion, concentrations and ratios in the upper layers ofsoil. It is known that the relatively large differences inthe pH values have a strong effect on the dissolvingcapacity of HM (Rademacher 2003). The solubility ofMn in soils is known to depend on the pH andincreased mobility of Mn is indicated in soils with pHlevels below 5.5 (Kabata-Pendias and Pendias 1992;Marschner 2002). In alkaline soils, Mn2+ oxidises intoMn3+ or Mn4+, which have a very low solubility(Marschner 2002). This explains the very high

0

50

100

150

200

250

300

350

Leaf Shoot Stem Bark

Cd Cr Pb Mn Fe Zn Cu

% o

f con

trol

Fig. 2 Accumulation ofheavy metals in differentcompartments of hybrid as-pen growing in Kunda plan-tation as percentage of theunpolluted plantation atRapla

0

1

2

3

4

5

6

7

8

9

10

1 5 7 12

Rapla Kunda

H, m

Age of trees, yr

a

0

1

2

3

4

5

6

7

8

9

10

5 7 13Age of trees, yr

DB

H, c

m

bFig. 3 Average height (±SD)(a) and diameter at breastheight (±SD) (b) of hybridaspen on abandoned agricul-tural lands at unpolluted(Rapla) and polluted (Kunda)plantations. The height of1-year-old seedlings is fromVares et al. (2003), height anddiameter of 5- and 7-year-oldtrees based on about 100measurements at both sitesfrom Tullus (2010), andthe height and diameter of11- and 12-year-old modeltrees (n=6) from Mandreet al.(2012)

1808, Page 6 of 9 Water Air Soil Pollut (2014) 225:1808

concentration of total Mn in the upper soil horizon at theKunda plantation. Also, the soluble Fe level reaches aminimum in the alkaline range of soils and Fe present incement dust accumulates in the upper layer of soil innon-soluble forms (Marschner 2002). The long-termemission of cement dust has also brought about anincrease in the total concentrations of Cd, Cu, Pb andCr in the soil in the vicinity of the cement plant com-pared with the control plantation at Rapla. However,high levels of HM in soil do not mean similar concen-trations and ratios in plants growing in contaminatedsoils (Kabata-Pendias and Pendias 1992; Mandre andOts 2012; Marschner 2002).

Fast-growing trees such as hybrid aspen could have ahigh capability to uptake and accumulate toxic com-pounds in industrially contaminated areas (Lombi et al.2001). We compared the uptake capability of hybridaspen for several toxic metals and found remarkabledifferences in the accumulation and partitioning ofthe HM in the aboveground compartments of trees.Although the total Mn content is high in the soil inthe area affected by cement dust pollution, its uptakefrom soil is hindered by the high soil pH (Kabata andKabata-Pendias 1992). However, Mala et al. (2007)found in hydroponic experiments that Mn may accu-mulate significantly less in roots and predominantlyinto all aboveground parts of hybrid aspen. Our studyshowed that on the unpolluted area at Rapla, Mnaccumulated more into leaves and bark than intoother aboveground organs. In the alkalised growthenvironment at Kunda, the Mn concentration inleaves shoots and bark were significantly lower than inthe control trees at Rapla but a somewhat higher Mnlevel than in the control trees was observed in the stem.

The concentration of Cd was suppressed in all com-partments of hybrid aspen in the Kunda plantation.However, the concentration of Cr was higher than con-trol in the leaves, shoots and stem, and the concentra-tions of Fe and Pb were somewhat higher in all studiedorgans of hybrid aspen. While the concentrations of Znand Cu in the trees growing at Kunda were lower inleaves and shoots than in the stems, these elements,especially Cu, had accumulated in significantly higherconcentrations.

The accumulation capacity for HM of hybrid aspenvaried between compartments depending on the mobilityof HM in alkaline soil. Pollution of soils and its hazard-ousness depend also on individual properties of the soilconcerned (tolerance, self-purification capability, etc.).

Although the higher plants are believed to be less tolerantof increased concentrations of HM, they are also widelyknown to accumulate these elements and to survive insoil contaminated by large quantities of various HM.High levels of HM in the soil do not always indicatesimilar high concentrations in plants. Several studiessupport the suggestion that at the concentration generallypresent in the soil solution, the absorption of HMby plantroots is controlled by metabolic processes within theplant (Turcsanyi 1992), which finally influences thegrowth, development and cold-hardiness and drought-resistance of plants (Lee et al. 2002).

A good understanding of plant responses to high con-centrations of HM can be of great significance in mor-phological studies. Our earlier investigations showed thatthe average height and diameter at breast height of hybridaspens in the Kunda plantation are generally depressed(Mandre et al. 2012). One of the reasons of this may bethe relatively high concentration of Cr, which influencesDNA and protein compound systems (Tobin et al. 1984),and of Pb, which impacts on photosynthesis, mitosis andwater absorption (Kabata-Pendias and Pendias 1992). Onthe other hand, the deficit of Mn, Cd and Zn in theorganism of hybrid aspens and serious misbalances ofthese elements in the tree organism may inhibit hybridaspen development. As Mn and Zn activate a relativelylarge number of enzymes, their deficit may affect protein,carbohydrates and lipids metabolism, etc. (Marschner2002). The growth of Mn-deficient plants is retarded,the turgor is reduced and the affected leaves break.Chloroplasts are the most sensitive of all cell componentsto Mn deficiency and react by showing structural impair-ment (Boardman 1975; Malá et al. 2007). In contrast, Cdis considered to be a nonessential element for plant met-abolic processes and there are no known enzymes thatdepend on Cd for their normal activity (Kabata-Pendiasand Pendias 1992). We can find information that elevatedCd content in plants causes growth retardation and rootdamage, chlorosis of leaves and decrease of activity ofphotosynthesis (Kabata-Pendias and Pendias 1992), butthere is no information about the influence of a low levelor deficiency of Cd on plant physiology. Most often,the integrated effects of Cd with other HM have beendescribed (Babich and Stotzky 1978).

In conclusion, this study showed that alkalisation ofsoil changed the HM accumulation by hybrid aspen. Themost important factor affecting the accumulation of HMfrom soil and their allocation in tree compartments wassoil pH. However, high levels of HM in the soil did not

Water Air Soil Pollut (2014) 225:1808 Page 7 of 9, 1808

mean similar concentrations and their ratios in plantsgrowing in contaminated soils. Accumulation of HM intotissues had caused various physiological disturbancesand resulted to a lowered bioproductivity of trees.

Acknowledgments The study was supported by the EstonianMinistry of Education and Research (project No. 0170021 s08)and the Kunda Nordic Tsement AS. I would like to thank ArvoTullus, Henn Pärn and Kersti Poom for their technical assistance inthe collection and preparation of samples for laboratory analyses.

References

Annuka, E., & Mandre, M. (1995). Soil responses to alkaline dustpollution. In M. Mandre (Ed.), Dust pollution and forestecosystems. A study of conifers in an alkalized environment(Vol. 3, pp. 356–344). Tallinn: Institute of Ecology.

Babich, H., & Stotzky, G. (1978). Effects of cadmium on the biota:influence of environmental factors. Advances in AppliedMicrobiology, 23, 55–117. doi:10.1016/S0065-2164(08)70065-0.

Banik, G., & Ponahlo, J. (1981). Some aspects concerning degra-dation phenomena of paper caused by green copper containingpigments. 6th Triennal Meeting. Paper 81/14/1 (pp. 1–14).Ottawa: ICOM Committee for Conservation.

Barnes, B. V., Zak, D. R., Denton, S. R., & Spurr, S. H. (1998).Forest ecology (4th ed.). New York: John Wiley & Sons.

Boardman, N. K. (1975). Trace elements in photosynthesis. InP. J. D. Nicholas & A. R. Egan (Eds.), Trace elements insoil–plant–animal systems (pp. 199–212). New York:Academic.

Casselman, C.N., Fox, T.R., Burger, J.A., & Jones, A.T. (2005).First year seedling response to three levels of silviculturalinput on post-SMCRA reclaimed lands. In Proceedings ofJoint Conference of American Society of Mining andReclamation 22nd Annual National Conference (pp. 191–210). Breckenridge, Colorado, June 19–23, 2005

Cripps, C. L. (2001). Mycorrhizae of aspen forests: ecology andpotential application. In: Sustaining aspen in western land-scapes. Proceedings of the Symposium on Western AspenForests (pp. 285–298). Grand Junction, CO, June 2000.

DesRochers, A., van den Driessche, R., & Thomas, B. R. (2003).Nitrogen fertilization of trembling aspen seedlings on soil ofdifferent pH. Canadian Journal of Forest Research, 33(4),552–560. doi:10.1139/X02-191.

DesRochers, A., van den Driessche, R., & Thomas, B. R. (2007).The interaction between nitrogen source, soil pH, anddrought in the growth and physiology of three poplar clones.Canadian Journal of Botany, 85, 1046–1057. doi:10.1139/BO7-062.

Dix, M. E., Klopfenstein, N. B., Zhang, J. W., & Kim, M. S.(1997). Potential use of Populus phytoremediation of envi-ronmental pollution in riparian zone. In N. B. Klopfenstein,Y. W. Chun, M. S. Kim, & M. R. Ahuja (Eds.),Micropopagation, genetic engineering, and molecular biol-ogy of Populus (pp. 206–211). Fort Collins: RockyMountainForest and Range Experimental Station.

Eissenstat, D. M., & van Rees, K. C. J. (1994). The growthand function of pine roots. In H. L. Gholz, S. Linder, &R. E. McMurtrie (Eds.), Environmental constraints on thestructure and productivity of pine forest ecosystems. A com-parative analysis (pp. 76–91). Copenhagen: EcologicalBulletin. 43.

Enel, M. (2003). Distribution of heavy metals in plants and theirhabitats in the outcrop area of Dictyonema shale. Oil Shale,20, 459–476.

Environmental Review No. 16. (2007). Kunda: Kunda NordicHeidelberg Cement Group.

Environmental Review No. 17. (2008). Kunda: Kunda NordicHeidelberg Cement Group.

Estonian Environment 1991 (1991). Environmental Report 4.Helsinki: Environment Data Centre, National Board ofWaters and the Environment.

Estonian Environment 1995 (1996). Tallinn: Ministry of theEnvironment of Estonia, Environmental Information Centre.

Farmer, A. M. (1993). The effect of dust on vegetation—a review.Environmental Pollution, 79(1), 63–75. doi:10.1016/0269-7491(93)90179-R.

Hynynen, J., & Karlsson, K. (2002). Intensive management ofhybrid aspen in Finland. In J. Hynynen, & A. Sanaslahti(Eds.), Proceedings of Workshop Management andUtilization of Broadleaved Tree Species in Nordic and BalticCountries – Birch, Aspen and Alder. (pp. 99–100). Vantaa,Finland, May 16–18, 2001

Kabata-Pendias, A., & Pendias, H. (1992). Trace elements in soiland plants (2nd ed.). Boca Raton: CRC Press.

Kahle, H. (1993). Response of roots of trees to heavy metals.Environmental and Experimental Botany, 33(1), 99–119.doi:10.1016/0098-8472(93)90059-O.

Karnosky, D. F. (1977). Evidence for genetic control of responseto sulfur dioxide and ozone in Populus tremuloides.Canadian Journal of Forest Research, 7(3), 437–440. doi:10.1139/x77-056.

Klõšeiko, J. (2005). Concentration of carbohydrates in coniferneedles near Kunda cement plant, Estonia, nine years afterreduced dust pollution. Metsanduslikud Uurimused/ForStud, 42, 87–94.

Lee, I.-S., Kim, O. K., Chang, Y. Y., Bae, B., Kim, H. H., & Baek,K. H. (2002). Heavy metal concentrations and enzyme activ-ities in soil from a contaminated Korean shooting range. JBiosci Bioeng, 94(5), 406–411.

Lindström, T. (1989). Effect of metal ions. In C. Fellers, T.Iversen, T. Lindström, T. Nilsson, & M. Rigdahl (Eds.),Ageing/degradation of paper. A literature survey. ReportNo. 1E (pp. 108–111). Stockholm: FoU-projektet förpapperskonservering.

Lombi, E., Zhao, F. J., Dunham, S. J., & McGrath, S. P. (2001).Phytoremidiation of heavy metal-contaminated soils:natural hyperaccumulation versus chemically enhancedphytoextraction. Journal of Environmental Quality, 30(6),1919–1926.

Lukjanova, A., &Mandre,M. (2010). Effects of alkalization of theenvironment on the anatomy of Scots pine (Pinus sylvestris)needles.Water, Air, and Soil Pollution, 206(1–4), 13–22. doi:10.1007/s11270-009.0080-2.

Malá, J., Máchová, P., Cvrčková, H., & Vaněk, T. (2007). Heavymetals uptake by hybrid aspen and rowan-tree clones.Journal of Forest Science, 53(11), 491–497.

1808, Page 8 of 9 Water Air Soil Pollut (2014) 225:1808

Mandre, M. (2000). Stress induced changes in lignin and nutrientpartitioning in Picea abies (L.) Karst. Baltic Forestry, 6(1),30–36.

Mandre, M. (2009). Vertical gradients of mineral elements inPinus sylvestris crown in alkalised soil. EnvironmentalMonitoring and Assessment, 159(1–4), 111–124. doi:10.1007/s10661-008-0616-8.

Mandre, M., & Ots, K. (2012). Monitoring of heavy metals uptakeand allocation in Pinus sylvestris organs in alkalised soil.Environmental Monitoring and Assessment, 184(12), 7689–7689. doi:10.1007/s10661-012-2878-4.

Mandre, M., Tullus, A., Klõšeiko, J., Lukjanova, A., & Tullus, H.(2011). Variation of carbohydrates and lignin in hybrid aspen(Populus tremula × P. tremuloides) on alkaline soil.CelluloseChemistry and Technology, 45(5–6), 299–311.

Mandre, M., Kloseiko, J., Lukjanova, A., & Tullus, A. (2012).Hybrid aspens responses to alkalisation of soil: growth, leafstructure, photosynthetic rate and carbohydrates. Trees, 26,1847–1858. doi:10.1007/s 00468-012-0754-z.

Maňkovská, B., Percy, K., & Karnosky, D. F. (1998). Impact ofambient tropospheric O3, CO2 and particulates on the epicu-ticular waxes of aspen clones differing in O3 tolerance.Ekológia (Bratislava), 18(2), 200–210.

Marschner, H. (2002).Mineral nutrition of higher plants. London:Academic.

McCrady, E. (1996). Effect of metals on paper: a literature review.Alkaline Paper Advocate, 9(1). http://cool.conservation-us.org/byorg/abbey/ap/ap09/ap09-1/ap09-109.html

McGill, D. W., Ford, V. L., & McNeel, J. F. (2004). Earlydevelopment of a species test established on surface minesthirty years post-reclamation. In Proceedings of JointConference of 21st Annual Meeting of the American Societyof Mining and Reclamation, 25th West Virginia Surface MinDrainage Task Force Symposium (pp. 1227–1238).Morgantown, WV, April 18–24, 2004.

Monsant, A. C., Tang, C., & Baker, A. J. M. (2008). The effect ofnitrogen form on rhizosphere soil pH and zinc phytoextractionby Thlaspi caerulescens. Chemosphere, 73(5), 635–642.doi:10.1016/j.chemosphere.2008.07.034.

Pasternak, K., & Reczyńska-Dutka, M. (1984). Outflow and accu-mulation of heavymetals in streams of the Niepołomice forest.In W. Grodziński, J. Weiner, & P. F. Maycock (Eds.), Forestecosystems in industrial regions. Studies on the cycling ofenergy, nutrients, and pollutants in the Niepołomice Forest,southern Poland (pp. 193–203). Berlin: Springer.

Pets, L. (1997). Depositions of macro- and microelements fromatmospheric emission of oil shale ashes in NortheasternEstonia. Oil Shale, 14(2), 163–170.

Rademacher, P. (2003). Atmospheric heavy metals and forestecosystems. Hamburg: Federal Research Centre forForestry and Forest Products. http://www.bfafth.de/bibl/pdf/i_03_12.pdf

Rytter, L. (2006). A management regime for hybrid aspen standscombining conventional forestry techniques with early bio-mass harvests to exploit their rapid early growth. ForestEcology and Management, 236(2–3), 422–426. doi:10.1016/j.foreco.2006.09.055.

Rytter, L., & Stener, L.-G. (2005). Productivity and thinningeffects in hybrid aspen (Populus tremula L. × P. tremuloidesMichx.) stands in southern Sweden. Forestry, 78(3), 285–295. doi:10.1093/forestry/cpi026.

Stanturf, J. A., van Oosten, C., Netzer, D. A., Coleman, M. D., &Portwood, C. J. (2001). Ecology and silviculture of poplarplantations. In D. I. Dickmann, J. G. Isebrands, J. E.Eckenwalder, & J. Richardson (Eds.), Poplar culture inNorth America (pp. 153–206). Ottawa: NRC Research Press.

Tobin, J. M., Cooper, D. G., & Neufeld, R. J. (1984). Uptake ofmetal ions by Rhizopus arrhizus biomass. Applied andEnvironmental Microbiology, 47(4), 821–824.

Tullus, A. (2010). Tree growth and the factors affectingit in younghybrid aspen plantations. PhD Thesis. Estonian University ofLife Sciences.

Tullus, A., Tullus, H., Vares, A., & Kanal, A. (2007). Earlygrowth of hybrid aspen (Populus × wettsteinii Hämet-Ahti) plantations on former agricultural lands in Estonia.For Ecol Manag, 245, 118–129. doi:10.1016/j.foreco.2007.04.006.

Tullus, A., Soo, T., Tullus, H., Vares, A., Kanal, A., & Roosaluste,E. (2008). Early growth and floristic diversity of hybrid aspen(Populus × wettsteinii Hämet-Ahti) plantations on areclaimed opencast oil shale quarry in North-East Estonia.Oil Shale, 25(1), 57–74. doi:10.3176/oil.2008.1.07.

Turcsanyi, G. (1992). Plant cells and tissues as indicators ofenvironmental pollution. In M. Kovács (Ed.), Biologicalindicators in environmental protection (pp. 131–168). NewYork: Ellis Horwood.

Vares, A., Uri, V., Tullus, H., & Kanal, A. (2003). Heightgrowth of four fast-growing deciduous tree species onformer agricultural lands in Estonia. Baltic Forestry, 9(1), 2–8.

Yu, Q., & Pulkkinen, P. (2003). Genotype-environment interactionand stability in growth of aspen hybrid clones. For EcolManag, 173, 25–35. doi:10.1016/S0378-1127(01)00819-2.

Zhuang, J. F., & Biermann, C. J. (1993). Rosin soap sizing withferric and ferrous-ions as mordants. Tappi Journal, 76(12),141–147.

Water Air Soil Pollut (2014) 225:1808 Page 9 of 9, 1808