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Published online 27 June 2007
Published in J Environ Qual 36:1145-1153 (2007)
DOI: 10.2134/jeq2006.0319
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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Remediation of Heavy Metal–Contaminated Forest Soil Using Recycled Organic Matter and Native Woody Plants

H.-S. Helmisaaria,*, M. Salemaaa, J. Deromeb, O. Kiikkiläa, C. Uhligc and T. M. Nieminena

a Finnish Forest Research Inst., Vantaa Research Unit, P.O. Box 18, FI-01301 Vantaa, Finland
b Finnish Forest Research Inst., Rovaniemi Research Unit, P.O. Box 16, FI-96301 Rovaniemi, Finland
c Bioforsk Nord Holt, The Norwegian Institute for Agricultural and Environmental Research, N-9292 Tromsø, Norway

* Corresponding author (helja-sisko.helmisaari{at}metla.fi)

Received for publication August 16, 2006.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The main aim of this study was to determine how the application of a mulch cover (a mixture of household biocompost and woodchips) onto heavy metal–polluted forest soil affects (i) long-term survival and growth of planted dwarf shrubs and tree seedlings and (ii) natural revegetation. Native woody plants (Pinus sylvestris, Betula pubescens, Empetrum nigrum, and Arctostaphylos uva-ursi) were planted in mulch pockets on mulch-covered and uncovered plots in summer 1996 in a highly polluted Scots pine stand in southwest Finland. Spreading a mulch layer on the soil surface was essential for the recolonization of natural vegetation and increased dwarf shrub survival, partly through protection against drought. Despite initial mortality, transplant establishment was relatively successful during the following 10 yr. Tree species had higher survival rates, but the dwarf shrubs covered a larger area of the soil surface during the experiment. Especially E. nigrum and P. sylvestris proved to be suitable for revegetating heavy metal–polluted and degraded forests. Natural recolonization of pioneer species (e.g., Epilobium angustifolium, Taraxacum coll., and grasses) and tree seedlings (P. sylvestris, Betula sp., and Salix sp.) was strongly enhanced on the mulched plots, whereas there was no natural vegetation on the untreated plots. These results indicate that a heavy metal–polluted site can be ecologically remediated without having to remove the soil. Household compost and woodchips are low-cost mulching materials that are suitable for restoring heavy metal–polluted soil.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
THERE ARE SEVERAL forested areas in the boreal region that have become so polluted by heavy metals and other pollutants that understorey vegetation cannot be sustained on the site. The absence of understorey vegetation can be caused by poor growing conditions, by phytotoxicity, or by a combination of the two. Removing the polluted topsoil and replacing it with unpolluted soil is the most widely used remediation measure on such sites. However, removing polluted soil is expensive and possible only at small, high-value sites (e.g., in housing development areas). Removal also destroys the soil structure and function.

Two possibilities, used alone or in combination, are available for remediating heavy metal–polluted forest soils without having to remove the soil: (i) the application of soil additives to immobilize the metals and provide mineral plant nutrients and (ii) the use of plant species sufficiently tolerant to heavy metals, episodic drought, and/or low nutrient availability (Schat and Verkleij, 1998). However, even if conventional soil amendments, such as fertilization and especially liming, have been shown to reduce heavy metal mobility and increase tree growth (Mälkönen et al., 1999), they have not resulted in recovery of the understorey vegetation without sowing new seeds. In areas where vegetation has been absent for decades, the shortage of propagules (e.g., seeds, spores, buds, rhizomes, or roots) may be a factor limiting revegetation (Moore and Wein, 1977).

Phytoremediation can be defined as an in situ remediation strategy that uses vegetation and associated microbiota, soil amendments, and agronomic techniques to remove, contain, or render environmental contaminants harmless (Cunningham and Ow, 1996). Re-establishing a normally functioning organic layer and vegetation cover aims to decrease the concentrations and mobility of heavy metals and dust circulation through the phytostabilization of soils, thereby increasing biodiversity, promoting natural nutrient cycling, and increasing the recreational and scenic value of the site.

Although a number of studies have been performed in the field of forest restoration, the large-scale and long-term practical application of the results of these studies to boreal and temperate forests damaged by pollution is restricted to a few areas (Kozlov et al., 2000), the Sudbury area (Winterhalder, 2000) being the largest and most well known example.

The value of native woody plants has been recently recognized in remediation programs (Pulford and Dickinson, 2005) because hyperaccumulating plants for metals are rare (Brooks, 1998) and because the success of hyperaccumulating plants remains far below expectations (Karczewska et al., 2005). Also, most hyperaccumulating plants are small annuals and cannot compete with other plants over the long term. Native trees and shrubs are long-lived woody plants that are able to adapt to increasing heavy metal loads and have a potential to isolate metals in perennial tissues that are slow to enter the decomposition cycle (Lepp and Dickinson, 1998). Perennial dwarf shrubs in the order Ericales can survive in substrates with naturally elevated metal concentrations (e.g., serpentine [Marrs and Bannister, 1978] and polluted soils [Salemaa et al., 2001]). It has been suggested that part of the heavy metal resistance of the dwarf shrubs is derived from their general ability to grow in acidic, nutrient-poor soil where metal availability is high (Bradley et al., 1981; Meharg and Cairney, 2000).

The general aim of our project was to promote a long-term recovery of a heavy metal–polluted forest ecosystem through the establishment of a functioning organic layer and through revegetation using seedlings of native trees and dwarf shrubs. The successful restoration of the ecosystem consists of the following stages: (i) survival of the planted trees and shrubs growing in pockets of unpolluted soil; (ii) recovery of litter production and improvement in litter quality; (iii) a reduction in the bioavailability, mobility, and leaching of heavy metals; and (iv) recovery of overall nutrient cycling in the whole ecosystem.

The specific aim of this study was to determine how the application of a mulch cover (a mixture of composted biowaste and woodchips) onto heavy metal–polluted soil affects (i) survival and growth of planted dwarf shrubs and tree seedlings and (ii) natural revegetation. We also studied the effect of mulch and the established transplants on metal concentrations in the soil.


   MATERIAL AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study area
The Harjavalta area (61°19' N, 22°9' E) in southwestern Finland is one of the areas most polluted by heavy metals in Finland. Copper smelting started in 1945, and nickel smelting started in 1959. The smelted ore concentrates contain sulfur, heavy metals, and arsenic. Although emissions of SO2 and heavy metals from the smelters have been strongly reduced in recent years (Fig. 1), the topsoil of the nearby forested sites contains over 50 yr of accumulation of a wide range of heavy metals (Derome, 1999). The mean total concentrations of heavy metals in the soil organic layer in 1992 at 0.5 km distance from the smelter were: Cu 5799, Ni 462, Fe 18617, Zn 516, and Pb 314 mg kg–1 (Derome and Lindroos, 1998). The exchangeable Cu and Ni concentrations were more than 3000 and 250 mg kg–1, respectively (Derome and Lindroos, 1998). Microbial activity and litter mineralization are strongly retarded (Fritze et al., 1996), the Scots pine trees are suffering from serious defoliation and growth retardation (Nieminen, 1998, 2003; Nieminen et al., 1999, 2000), and fine root mortality is high (Helmisaari et al., 1999). The understorey vegetation is almost completely degraded (Salemaa et al., 2001, 2004). This enhances the wind erosion of metal-contaminated particles, decreases the water-holding capacity of the soil, and may facilitate the leaching of heavy metals (Derome and Nieminen, 1998) into the groundwater. Even though viable seeds have been found in forest soil close to the smelter, high concentrations of heavy metals and drought inhibit seedling rooting (Salemaa and Uotila, 2001). The thick, relatively undecomposed litter layer (McEnroe and Helmisaari, 2001), the shortage of mineral nutrients (Derome and Lindroos, 1998), and the extremely dry conditions disturb nutrient cycling (Helmisaari et al., 1995; Nieminen and Helmisaari, 1996) and make natural revegetation problematic.


Figure 1
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  		Fig. 1. Cu and Ni (bars) and SO2 (line) emissions (t/yr) from the Harjavalta smelter from 1985 through 2005. From Outokumpu Harjavalta Metals Oy and Boliden Harjavalta.

 
Remediation Experiment
We established a remediation experiment in summer 1996 in a damaged Scots pine stand in the immediate vicinity (at a distance of 500 m of the main stack) of the Harjavalta smelter. The site is situated in the southern boreal coniferous zone on a forested esker. At establishment, the understorey was almost completely absent (Salemaa et al., 2004), and the growth of the mature Scots pines was extremely poor (Mälkönen et al., 1999). In 1991, 5 yr before the establishment of the remediation experiment, the volume increment of the 49-yr-old Scots pine stand (number of trees, 1008 ha–1) was 0.3 m3 ha–1 yr–1. The stand also suffered from severe needle loss (Nieminen et al., 1999). The long-term mean annual temperature at a nearby weather station (Pori Airport) of the Finnish Meteorological Institute is 4.0°C, and the annual precipitation 558 mm. The mean annual temperature and annual precipitation during the study period (1996–2005) were 5.3 ± 0.6°C and 591 ± 62 mm, respectively.

A total of 36 plots, each 5 x 5 m in size including 1-m-wide buffer zones, were placed in the openings of the stand. Partial shading of mature trees could not be excluded. Twelve treatments were established using a completely randomized design (Table 1). A 5-cm-thick layer of mulch was added in May-June 1996 to 18 of the 36 plots to provide a new, unpolluted organic layer. The other 18 plots were not covered. The mulch was spread directly over the layer of undecomposed plant litter on the forest floor. Seedlings of two native tree species, Betula pubescens Ehrh. and Pinus silvestris L., and cuttings of two native dwarf shrub species, Arctostaphylos uva-ursi L. and Empetrum nigrum L. (subsequently referred to by their generic names), were planted on six replicate plots each: Three of the plots were covered with mulch, and three were left uncovered. Forty-nine transplants were systematically planted in a 7 x 7 design on each plot. The total number of transplants was 294 per species. All the transplants were planted in pockets (2 L, depth about 20 cm) containing mulch. Planting the cuttings and seedlings in mulch pockets penetrating down into the less-contaminated soil was considered to be essential for their initial survival. Control mulch pockets without transplants (three mulch-covered and three uncovered plots) were made in the soil. Three mulch-covered plots (without mulch pockets) and three plots without mulch cover or pockets (untreated controls) were established (Table 1). Some of the plots were destroyed in 2005 during the expansion of the nearby slag cooling area of the smelters.


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  		Table 1. Experimental design and number of replicates for the studied variables. Spontaneous seedlings were counted and soil samples taken from plots not affected by the expansion of the slag cooling area.

 
The mulch consisted of a mixture of household biocompost and woodchips (saw mill waste). The biocompost was 14 mo old and had been produced in outdoor windrows at the Ämmässuo Waste Handling Centre, Espoo, Finland by mixing kitchen and garden waste from the Greater Helsinki area and coarse woodchips (diameter ~50 mm). The average Cu and Ni concentrations in the Ämmässuo biocompost were 60 and 3 mg kg–1 per dry weight, respectively (Kiikkilä et al., 2001). The biocompost was spread on the plots at a dose of 5.4 kg m–2 (dry weight).

Smaller woodchips (diameter <20 mm) of Scots pine and Norway spruce stemwood were added to the biocompost before application to increase the amount of slow-release C available for microbiota, especially for fungi, because the biomass of fungi is strongly decreased in heavy metal–polluted soils (Pennanen et al., 1996). The mulch was prepared 1 wk before spreading. The pH of the mulch was 6.3, and the C to N ratio was 16:1. The input of C through mulching was 2 kg m–2 (Kiikkila et al., 2001). The original, polluted podzolic soil had pH 4.1 in the organic layer and mineral soil (fine sand) down to 20 cm.

The Arctostaphylos cuttings originated from the Harjavalta area and were rooted in a commercial nursery. The Arctostaphylos cuttings were relatively small (10–15 cm) when planted and had only two annual growth segments. The Empetrum cuttings were purchased from a commercial nursery, and their origin was from western Finland. The cuttings had plenty of branches, with four to five annual segments. The tree seedlings were containerized in peat containers. They were obtained from the Suonenjoki nursery and were of southern Finland origin. The Betula seedlings were 1 yr old at planting, and the Pinus seedlings were 2 yr old at planting.

Vegetation Measurements
The survivorship and mortality of the tree seedlings and dwarf shrub cuttings planted on the plots were recorded every spring (May–June) and autumn (August–September) during the study period (1996–2005) (Table 1). Cumulative death rate curves over time were calculated separately for the mulch-covered and uncovered plots by combining the replicates. The final species-specific average mortality was compared between the treatments using the t test. Shoot elongation of Arctostaphylos and Empetrum was measured annually on five randomly selected plants per plot at the end of the growing season. Five naturally regenerated clones growing in the vicinity of the experimental area were selected to act as the reference level for both species. Average annual shoot growth was compared between the mulch-covered and uncovered plots using the t test.

The spontaneously spread nonwoody plant species (grasses and herbs) were recorded in June 2002. Naturally recolonized birches, pines, and other tree seedlings were counted on the remaining plots in August 2005 (Table 1).

Soil Sampling and Analysis
Soil samples were taken in August 2005 using a soil corer with a diameter of 58 mm. On the plots with mulch pockets, soil cores were taken from randomly chosen mulch pockets and the uppermost 5-cm mineral soil layer beneath the pockets. Each soil core was divided into an organic (litter layer formed during the experiment + mulch) and a mineral soil sample. In addition, samples were taken from the mulch-covered plots without mulch pockets and from the untreated plots. The organic soil sample of the mulch-covered plots consisted of the litter layer formed during the experiment + added mulch cover + original organic layer, whereas that of the untreated plots consisted only of the litter layer formed during the experiment + the original organic layer. Mineral soil samples were taken from these plots to act as references for the samples taken from the plots with mulch pockets. Hence, they were taken from approximately the same depth (10–15 cm) as the soil layer beneath the mulch pockets (Fig. 4).


Figure 4
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  		Fig. 4. Exchangeable Cu and Ni concentrations in the organic soil (A) and in the mineral soil (B) in four treatments. (a) Mulch pocket with transplant; (b) mulch pocket without transplant; (c) mulch cover without pocket; and (d) untreated soil.

 
In the case of the plots with mulch pockets, samples were taken from seven replicate plots with transplants (from three plots planted with Empetrum, three plots planted with Pinus, and one plot planted with Betula) and from two replicate plots with no transplants (only mulch pockets). On the plots without mulch pockets, samples were taken from two remaining mulch-covered plots and from three untreated plots (Table 1). Three randomly chosen soil cores were taken from each plot, and these replicate samples were combined to give one composite sample of organic and one composite sample of mineral soil per plot.

Exchangeable Cu and Ni were determined by extraction with 0.1 M BaCl2 + 2% EDTA (7.5 g of mulch or 15 g of mineral soil/150 mL extractant, shaking for 2 h) followed by filtration and analysis by inductively coupled plasma–atomic emission spectrometry. This extraction was chosen for comparability with earlier studies on the site (Derome and Lindroos, 1998).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Survival of the Transplants
Survival varied between the plant species and treatments. The mortality rate of Betula and Arctostaphylos was high during the first 2 yr. After the initial high mortality period, the remaining transplants of all species became successfully established during the 10 yr of the experiment (Fig. 2).


Figure 2
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  		Fig. 2. Cumulative mortality percentages of the seedlings of (a) Betula pubescens and (b) Pinus sylvestris and cuttings of (c) Arctostaphylos uva-ursi and (d) Empetrum nigrum. The death rate of the transplants was recorded every spring and autumn from 1996 through 2005. The first inventory was performed in autumn 1996. The curves have been calculated separately for mulch-covered (n = 3) and uncovered (n = 3) plots.

 
At the end of the experiment, the average mortality (±SD, n = 3 replicate plots) of Empetrum cuttings was 3.5 ± 6.1% on the mulch-covered plots and 48 ± 37% on the uncovered plots (Fig. 2). Arctostaphylos also had a higher mortality on the uncovered (72 ± 22%) than on the mulch-covered plots (57 ± 12%). The mortality of tree seedlings was higher on the mulch-covered plots (Betula 48 ± 14% and Pinus 11 ± 7%) than on the uncovered plots (Betula 17 ± 14% and Pinus 3.9 ± 4.5%). Owing to the low number of replicates, the differences between the treatments were statistically significant only for Betula (t = 2.66; df = 4; p = 0.05).

The final mortality rate of the dwarf shrub species together tended to be higher on the uncovered than on the mulch-covered plots (t = 1.88; df = 10; p = 0.09), but the opposite was true for the tree seedlings (t = 2.04; df = 10; p = 0.07). The dry summers in 1997 and 2003 seemed to have increased transplant mortality. This was especially clear for Empetrum: The large established clones started to die on the uncovered plots (Fig. 2d) after the hot summer in 2003 (temperature in Fig. 3a).


Figure 3
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  		Fig. 3. Average annual elongation of the shoots (bars) of (a) Arctostaphylos uva-ursi and (b) Empetrum nigrum. The data consist of 3 plots x 5 plants for the two treatments (mulch-covered and uncovered plots). The reference represents 10-yr (1996–2005) average elongation measured on five natural clones per species. Standard deviation is marked. Statistically significant differences between the treatments: *p < 0.05; **p < 0.01; ***p < 0.001 (t test). Average July temperature is marked with a line in (a).

 
Shoot Elongation of Dwarf Shrubs
Shoot elongation of Arctostaphylos did not differ between the mulch-covered and uncovered plots during the first few years of the experiment. During the last 5 yr (2001–2005), elongation was higher on the uncovered plots (Fig. 3a). Shoot elongation of Empetrum was higher on the mulch-covered than on the uncovered plots throughout the study (Fig. 3b). The growth difference increased during the last 2 yr (2004–2005): The annual growth was over 5 cm higher on the mulch-covered than on the uncovered plots. The elongation of Arctostaphylos and Empetrum on the mulch-covered plots was positively correlated with the average July temperature (r = 0.742; p = 0.022 for both species; n = 10 yr) (Fig. 3a). Compared with the reference clones growing near the experiment area, Arctostaphylos had higher elongation on the uncovered plots, and Empetrum grew better in both treatments.

Natural Recolonization
No vegetation developed on the untreated plots, whereas spontaneous recolonization of tree seedlings and other plants (pioneer mosses, grasses, and herbs) occurred on the plots that received a mulch cover and/or soil pockets. After 10 yr, the plots without a mulch cover had between 1 and 25 tree seedlings per plot growing directly on the mulch pockets. The mulch-covered plots had a large number (112–545 individuals per plot) of naturally regenerated tree seedlings growing over the whole plot area (Table 2). The naturally recolonized tree seedlings were mostly Pinus sylvestris and Betula sp. Other species frequently found on the mulch cover or pockets are listed in Table 3.


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  		Table 2. Average number of naturally established tree seedlings per plot with and without mulch cover in the Harjavalta remediation experiment in August 2005. Planted trees are not included. n = number of replicate plots in 2005 (originally three in each treatment).

 

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  		Table 3. Spontaneously recolonized plant species (other than tree seedlings) found on mulch-covered plots or on mulch pockets in the Harjavalta remediation experiment in June 2002.

 
Soil Cu and Ni Concentrations
Although the exchangeable Cu and Ni concentrations of the mulch strongly increased during the 10-yr experiment from the original concentrations, they remained lower than those in the organic layer of the untreated plots (Fig. 4). The mulch cover, which included the original polluted organic layer (average thickness, 3 cm), had lower exchangeable Cu and Ni concentrations than the organic layer of the untreated plots due to the dilution effect of the added "clean" mulch. The exchangeable Cu and Ni concentrations tended to be lower in the mulch of pockets containing transplants than in those without. In the mineral soil, the exchangeable Cu and Ni concentrations were relatively low, and there was a considerable spatial variation between plots.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Survival and Shoot Elongation of the Transplants
Overall, planting the cuttings and seedlings in mulch pockets on the mulch-covered and uncovered plots was relatively successful. This was especially true for Pinus, which had less than 12% mortality rate in both treatments. In general, the tree species had higher survival rates, but the dwarf shrubs covered a larger area of the soil surface during the 10 yr experiment. In addition to heavy metals, episodic events (e.g., animal herbivory and drought) seemed to disturb the transplant establishment. For instance, the mortality rate of the Betula seedlings on the mulched plots was higher than that on the control plots because of hare damage immediately after planting. This indirectly reflected a feeding preference of hares for the birch seedlings on the mulch-covered plots (more leaves, higher palatability).

After the initial period of mortality, the survived dwarf shrubs spread out over a wide area. At maximum, they covered 50 to 100% of the plot surface. Almost all (96%) of the Empetrum cuttings survived on the mulch-covered plots, whereas the mortality on the uncovered plots increased sharply after the hot, dry summer in 2003. There was a similar increase in the mortality of Arctostaphylos after the hot summer in 1997, when the long drought period killed the transplants with small roots on the uncovered plots especially. Spreading the mulch over the whole plot surface reduced the loss of moisture from the soil, thus ensuring that the transplants had a better water supply; this was reflected as a higher survival rate. Better moisture conditions may also explain the higher shoot elongation of Empetrum on mulch-covered plots.

The roots of the dwarf shrubs and trees grew out from the clean mulch pockets to the polluted mineral soil within the 10 yr. All species suffered from a range of disturbances in their shoots: Discoloration of the leaves and dead branches are common and indicate detrimental effects of heavy metals, SO2, and drought. Although the surface soil was toxic to plant establishment from the soil seed bank (Salemaa and Uotila, 2001), all planted species seemed to tolerate the heavy metal levels in the soil under the mulch pocket (exchangeable Cu, 13–37 mg kg–1; exchangeable Ni, 1.5–3.5 mg kg–1). Thus, the mulch pocket gave protection and promoted the root growth to deeper horizons and stabilization of the soil. On the other hand, the high pH of mulch may have been detrimental especially to Arctostaphylos adapted to acid substrate.

Dwarf shrubs seem to be suitable for revegetation because of their clonal growth habit and good regrowth potential (activation of dormant buds after the death of the apical bud) that facilitates rapid spreading and coverage of the forest floor (Salemaa et al., 1999; Salemaa and Sievänen, 2002). Empetrum and Arctostaphylos have the ability to accumulate high amounts of Cu in the stems and prevent its access to leaves. Empetrum has proved to be more resistant than Arctostaphylos in experimental Cu exposures (Monni et al., 2000; Salemaa and Monni, 2003). In greenhouse experiments, Pinus tended to accumulate Cu and Ni in roots (Nieminen, 2004). Pinus sylvestris and Betula pubescens were among the most resistant plant species in other studies in severely heavy metal–polluted environments (e.g., close to the huge Severonikel Cu-Ni smelter complexes in Monchegorsk in northwestern Russia) (Kryuchkov, 1993; Rigina and Kozlov, 2000; Lukina and Nikonov, 2001). The preliminary results have shown that all used dwarf shrub and tree species were mycorrhizal, which may also promote resistance to heavy metals (Meharg and Cairney, 2000).

Natural Recolonization
Natural recolonization of pioneer species (e.g., Epilobium angustifolium, Taraxacum coll., and grasses) and tree seedlings (P. sylvestris, Betula sp., and Salix sp.) was greatly enhanced on the mulched plots. Natural vegetation has only become established on the plots that had a mulch cover or soil pockets containing mulch. Relatively few natural tree seedlings were growing on plots with only mulch pockets, whereas there were large numbers on the mulch-covered plots. It is probable that most of the Pinus and Betula seedlings were from seeds of the local or neighboring tree stands. Without a mulch cover, the initial development of the young seedlings would fail as a result of the phytotoxicity of heavy metals (Nieminen, 2004). The mulch cover also protected the plant roots from drought in a number of dry summers during the study period and provided a source of nutrients. Our results on effective revegetation with a mulch cover are in agreement with those of Tejada et al. (2006), who reported natural colonization of vegetation on semiarid plots amended with organic waste.

Slightly more natural tree seedlings became established on plots planted with Betula and Pinus than on those with dwarf shrubs. This may be related to the growth form of the species. On the mulch-covered plots, the planted dwarf shrubs covered a larger area of the soil surface than the trees, leaving less space for natural recolonization. Trees were able to recolonize also through natural seeding, whereas the establishment of the native dwarf shrubs required planting.

Soil Cu and Ni Concentrations
Atmospheric deposition of Cu and Ni is the most probable explanation for the strong enrichment of these metals in the mulch of the soil pockets during the experiment. Nieminen and Saarsalmi (2002) estimated the annual deposition of Cu and Ni at the same site in 1993. According to these investigators, 380 mg Cu m–2 was deposited as stand throughfall and 612 mg Cu m–2 as litterfall, whereas the corresponding values for Ni were 70 mg m–2 and 95 mg m–2. Although there has been a drastic decrease in overall emissions from the smelter during the last decades, no decreasing trend in the stand throughfall deposition of Cu during 1992 through 1998 was found in a study performed at the same site, and for Ni a strong increase was found from 1997 to 1998 (Nieminen et al., 2004). The wind-borne dust from polluted barren forest floor and slag heaps surrounding the experimental area is an important source of Cu and Ni deposition (Nieminen et al., 1999). The general enrichment of elements is also partly due to decomposition of the mulch during the 10 yr of the experiment.

The somewhat lower exchangeable Cu and Ni concentrations in the mulch pockets with transplants compared with those without transplants may suggest that the plant has increased metal mobility and downward leaching or immobilization of Cu and Ni. Low-molecular-root exudates may enhance metal mobilization from nonlabile soil pools (Mench et al., 1988; Zhang et al., 1991). According to Ruttens et al. (2006), the formation of original metal complexes may decrease the exchangeable metal concentrations. However, because of the small number of replicate plots, the differences may be related to spatial variation, and root uptake could have affected exchangeable Cu and Ni concentrations in mulch.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The reduction in emissions has opened new possibilities for remediation of the forest ecosystems close to Harjavalta smelter. The results from our study showed that, in a heavy metal–polluted forest without a natural understorey, the addition of unpolluted organic material was essential for the establishment of vegetation. Spreading a mulch layer on the soil surface gave the best results for the recolonization of natural vegetation and increased dwarf shrub survival, partly through protection against drought. The use of native woody species was successful for creating a green, continuous vegetation cover. Especially E. nigrum and P. sylvestris proved to be suitable for revegetating heavy metal–polluted and degraded forests. Establishment of a natural understorey is essential for the long-term improvement of nutrient cycling and for the reduction of soil erosion and dust circulation, which are potentially harmful to human health. Native plants and mulch consisting of household compost and woody chips are inexpensive and can thus be used for remediating even extensive heavy metal–polluted areas.


   ACKNOWLEDGMENTS
 
The present study formed a part of the research project "Recovery of boreal forest ecosystem from long-term heavy-metal pollution" carried out at the Finnish Forest Research Institute and was partly financed by the Academy of Finland. The authors are grateful to the personnel of the Finnish Forest Research Institute for assistance in field sampling and measurements. We are especially grateful to Leena Hamberg, Satu Lyyra, and Ilkka Vanha-Majamaa for assistance in different phases of the study.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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The SCI Journals Agronomy Journal Crop Science
Journal of Natural Resources
and Life Sciences Education		 Vadose Zone Journal
Soil Science Society of America Journal Journal of Plant Registrations The Plant Genome